Impact and Recovery of VHA Epilepsy Care Services During the COVID-19 Pandemic

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The COVID-19 pandemic affected diverse workplaces globally, leading to temporary and permanent changes across the health care landscape. Included among the impacted areas of care were epilepsy and electroencephalogram (EEG) clinicians and services. Surveys among epilepsy specialists and neurophysiologists conducted at the onset of the pandemic to evaluate working conditions include analyses from the American Epilepsy Society (AES), the National Association of Epilepsy Centers (NAEC), the International League Against Epilepsy, and an Italian national survey.1-4 These investigations revealed reductions in epilepsy monitoring unit (EMU) admissions (23% decline), epilepsy surgery (6% decline), inpatient EEG (22% of respondents reported decline), and patients having difficulty accessing epilepsy professionals (28% of respondents reported decline) or obtaining medications (20% of respondents reported decline).1-3

While such research provided evidence for changes to epilepsy care in 2020, there are limited data on subsequent adaptations during the pandemic. These studies did not incorporate data on the spread of COVID-19 or administrative workload numbers to analyze service delivery beyond self reports. This study aimed to address this gap in the literature by highlighting results from longitudinal national surveys conducted at the Epilepsy Centers of Excellence (ECoE), a specialty care service within the Veterans Health Administration (VHA), which annually serves > 9 million veterans.5 The ECoE represents epileptologists and neurophysiologists across the United States at the 17 primary facilities that were established at the time of this survey (2 ECoEs have been added since survey completion) in 4 geographical regions and for which other regional facilities refer patients for diagnostic services or specialty care.6

National surveys were conducted among the ECoE directors regarding adaptations made from May 2020 to June 2022 to provide a comprehensive account of limitations they experienced and how adjustments have been made to improve patient care. Survey responses were compared to administrative workload numbers and COVID-19 spread data from the Centers for Disease Control and Prevention (CDC) to provide a comprehensive analysis of performance during the pandemic.

METHODS

Data were collected as part of a quality improvement initiative by the VHA ECoE; institutional review board approval was not required. An 18-item survey covering 5 broad domains was sent to ECoE directors 4 separate times to accumulate data from 4 time periods: May to June 2020 (T1); December 2020 to February 2021 (T2); July to August 2021 (T3); and June to July 2022 (T4). These periods correspond to the following phases of the pandemic: T1, onset of pandemic; T2, vaccine availability; T3, Delta variant predominant; T4, Omicron variant predominant.

table 1

Data on the spread of COVID-19 were collected from the CDC archived dataset, US COVID-19 County Level of Community Transmission Historical Changes (Table 1).7 Administrative workload (patient counts) for EEG, EMU, and outpatient clinics were extracted from VHA administrative databases for the participating sites for the months prior to each survey: T1, April 2020; T2, November 2020; T3, June 2021; and T4, May 2022 (Table 2).

table 2

Survey Structure and Content

The survey was developed by the ECoE and was not validated prior to its use due to the time-sensitive nature of gathering information during the pandemic. The first survey (T1) was an emailed spreadsheet with open-ended questions to gauge availability of services (ie, outpatient clinic, EEG, EMU), assess whether safety precautions were being introduced, and understand whether national or local guidelines were thought to be helpful. Responses from this and subsequent surveys were standardized into yes/no and multiple choice formats. Subsequent surveys were administered online using a Research Electronic Data Capture tool.8,9

Availability of outpatient epilepsy services across the 4 time periods were categorized as unlimited (in-person with no restrictions), limited (in-person with restrictions), planned (not currently performed but scheduled for the near future), and unavailable (no in-person services offered) (eAppendices 1-6, available in article PDF).

Statistical Analyses

Analyses were performed to compare survey responses to workload and CDC data on COVID-19 community spread. The following associations were examined: (1) CDC COVID-19 spread vs respondents’ perception of spread; (2) respondents’ perception of spread vs availability of services; (3) CDC COVID-19 spread vs availability of services; (4) respondents’ perception of spread vs workload; and (5) CDC COVID-19 spread vs workload. Availability of services was dichotomized for analyses, with limited or fully available services classified as available. As services were mostly open at T3 regardless of the spread of the virus, and the CDC COVID-19 spread classification for all sites was severe or high at T2 and T4, corresponding associations were not tested at these time points. For associations 1 through 3, Fisher exact tests were used; for associations 4 and 5, Mann-Whitney U tests (where the COVID-19 spread fell into 2 categories) and Kruskal-Wallis tests (for 3 categories of COVID-19 spread) were performed. All tests were 2-tailed and performed at 0.05 error rate. Bonferroni corrections were applied to adjust P values for multiple hypotheses tests.

RESULTS

From the 17 sites invited, responses at each time point were obtained from 13 (T1),17 (T2), 15 (T3), and 16 (T4) centers. There was no significant association between self-reported COVID-19 spread and CDC classification of COVID spread. There were no associations between COVID-19 community spread (respondent reported or CDC severity level) and outpatient clinic availability (self-reported or workload captured). At T3, a positive association was found between the CDC spread level and workload (P = .008), but this was not significant after Bonferroni correction (P = .06).

EEG availability surpassed EMU availability at all time points, although EMU services made some recovery at T3 and T4. No associations were found between COVID-19 community spread (self-reported or CDC severity level) and outpatient EEG or EMU availability (self-reported or workload captured). At T3, there was a positive association between EEG workload and CDC COVID-19 severity level (P = .04), but this was not significant after Bonferroni correction (P = .30). 

For outpatient EEG, staff and patient mask use were universally implemented by T2, while the use of full personal protective equipment (PPE) occurred at a subset of sites (T2, 6/17 [35%]; T3, 3/15 [20%]; T4: 4/16 [25%]). COVID-19 testing was rarely implemented prior to outpatient EEG (T1, 0 sites; T2, 1 site; T3, 1 site; T4, 0 sites). Within the EMU, safety precautions including COVID-19 testing, patient mask usage, staff mask usage, and aerosolization demonstrated a sustained majority usage across the 4 surveys.

National and Local Guidelines

The open-ended survey at T1 asked site directors, “Should there be national recommendations on how EEGs and related procedures should be done during the pandemic or should this be left to local conditions?” Responses were mixed, with 5 respondents desiring a national standard, 4 respondents favoring a local response, and 4 respondents believing a national standard should be in place but with modifications based on local outbreak levels and needs.

Surveys performed at T2 through T4 asked, “Which of the following do you feel was/will be helpful in adapting to COVID-19–related changes?” Overall, there was substantial agreement that guidelines were helpful. Most sites anticipated permanent changes in enhanced safety precautions and telehealth.

DISCUSSION

This longitudinal study across 4 time points describes how epilepsy services within the VHA and ECoE adapted to the COVID-19 pandemic. The first survey, conducted 2 months after COVID-19 was declared a pandemic, allowed a comparison with other concurrent US national surveys.1,2,10 The subsequent surveys describe longitudinal adaptations to balance patient and staff safety with service availability and is a unique feature of the current report. Results demonstrate flexibility and adaptability by the ECoEs surveyed, which surprisingly did not show significant associations between CDC COVID-19 spread data and administrative workload data.

Trends in Availability of Services

The most significant impact of COVID-19 restrictions was during T1. There were no significant relationships between service availability/workload and objective CDC COVID-19 spread levels or subjective self-reported COVID-19 spread. Respondents’ perceptions of local COVID-19 spread showed no association with CDC COVID-19 spread data. It appears that subjective perception of spread may be unreliable and factors other than actual or perceived COVID-19 spread were likely driving patterns for service availability.

In-person outpatient visits were most impacted at T1, similar to other civilian surveys, with only 1 site reporting in-person outpatient visits without limitations.1,2 These numbers significantly changed by T2, with all sites offering either limited or unlimited in-person visits. While the surveys did not evaluate factors leading to this rapid recovery, it may be related to the availability of COVID-19 vaccinations within the VHA during this time.11 The US Department of Veterans Affairs was the first federal agency to mandate employee vaccination.12 By the most recent time point (T4), all responding sites offered outpatient visits. Outpatient EEGs followed a similar trend, with T1 being the most restrictive and full, unrestricted outpatient EEGs available by T3. 

Fiscal year (FY) trends from ECoE annual reports suggest that encounters slowly recovered over the course of the pandemic. In FY 2019 there were 13,143 outpatient encounters and 6394 EEGs, which dropped to 8097 outpatient encounters and 4432 EEGs in FY 2020 before rising to 8489 outpatient encounters and 5604 EEGs in FY 2021 and 9772 outpatient encounters and 5062 EEGs in FY 2022. Thus, while clinicians described availability of services, patients may have remained hesitant or were otherwise unable to fulfill in-person appointments. The increased availability of home EEG (145 encounter days in 2021 and 436 encounter days in 2022) may be filling this gap. 

In contrast to outpatient clinics and EEG, EMU availability showed relatively slower reimplementation. In the last survey, about 30% of sites were still not offering EMU or had limited services. Early trends regarding reduced staffing and patient reluctance for elective admission cited in other surveys may have also affected EMU availability within the VHA.2,13 Consistent with trends in availability, ECoE annual report data suggest EMU patient participation was about one-half of prepandemic rates: 3069 encounters in FY 2019 dropped to 1614 encounters in 2020. By 2021, rates were about two-thirds of prepandemic rates with 2058 encounters in 2021 and 2101 encounters in 2022.

Early survey results (T1) from this study echo trends from other surveys. In the AES survey (April to June 2020), about a quarter of respondents (22%) reported doing fewer EEG studies than usual. The Italian national survey (April 2020) revealed reduced presurgical evaluations (81%), ambulatory EEG (78%), standard EEG (5%) and long-term EEG (32%).4 In the NAEC survey (end of 2020)—which roughly corresponded to T2—outpatient EEGs were still < 75% of pre-COVID levels in one-half of the centers.

National and Local Guidelines

Both national and local guidelines were perceived as useful by most respondents, with national guidelines being more beneficial. This aligns with the NAEC survey, where there was a perceived need for detailed recommendations for PPE and COVID-19 testing of patients, visitors, and staff. Based on national and local guidelines, ECoE implemented safety procedures, as reflected in responses. Staff masking procedures appeared to be the most widely adopted for all services, while the use of full PPE waned as the pandemic progressed. COVID-19 testing was rarely used for routine outpatient visits but common in EMU admissions. This is similar to a survey conducted by the American Academy of Neurology which found full PPE implementation intermittently in outpatient settings and more frequently in inpatient settings.14

Telehealth Attitudes

While most sites anticipated permanent implementation of safety precautions and telehealth, the latter was consistently reported as more likely to be sustained. The VHA had a large and well-developed system of telehealth services that considerably predated the pandemic.15,16 Through this established infrastructure, remote services were quickly increased across the VHA.17-19 This telehealth structure was supplemented by the ability of VHA clinicians to practice across state lines, following a 2018 federal rule.20 The AES survey noted the VHA ECoE's longstanding experience with telehealth as a model for telemedicine use in providing direct patient care, remote EEG analysis, and clinician-to-clinician consultation.1

Trends in the number of telehealth patients seen, observed through patterns in ECoE annual reports are consistent with positive views toward this method of service provision. Specifically, these annual reports capture trends in Video Telehealth Clinic (local station), Video Telehealth Clinic (different station), Home Video Telehealth, Telephone Clinic, and eConsults. Though video telehealth at in-person stations had a precipitous drop in 2020 that continued to wane in subsequent years (898 encounters in 2019; 455 encounters in 2020; 90 encounters in 2021; 88 encounters in 2022), use of home video telehealth rose over time (143 encounters in 2019; 1003 encounters in 2020; 3206 encounters in 2021; 3315 encounters in 2022). Use of telephone services rose drastically in 2020 but has since become a less frequently used service method (2636 in 2019; 5923 in 2020; 5319 in 2021; 3704 in 2022).

Limitations

While the survey encouraged a high response rate, this limited its scope and interpretability. While the availability of services was evaluated, the underlying reasons were not queried. Follow-up questions about barriers to reopening may have allowed for a better understanding of why some services, such as EMU, continued to operate suboptimally later in the pandemic. Similarly, asking about unique strategies or barriers for telehealth would have allowed for a better understanding of its current and future use. We hypothesize that staffing changes during the pandemic may have influenced the availability of services, but changes to staffing were not assessed via the survey and were not readily available via other sources (eg, ECoE annual reports) at the time of publication. An additional limitation is the lack of comparable surveys in the literature for time points T2 to T4, as most analogous surveys were performed early in 2020.

Conclusions

This longitudinal study performed at 4 time points during the COVID-19 pandemic is the first to offer a comprehensive picture of changes to epilepsy and EEG services over time, given that other similar surveys lacked follow-up. Results reveal a significant limitation of services at VHA ECoE shortly after the onset of the pandemic, with return to near-complete operational status 2 years later. While safety precautions and telehealth are predicted to continue, telehealth is perceived as a more permanent change in services.

References
  1. Albert DVF, Das RR, Acharya JN, et al. The impact of COVID-19 on epilepsy care: a survey of the American Epilepsy Society membership. Epilepsy Curr. 2020;20(5):316-324. doi:10.1177/1535759720956994

  2. Ahrens SM, Ostendorf AP, Lado FA, et al. Impact of the COVID-19 pandemic on epilepsy center practice in the United States. Neurology. 2022;98(19):e1893-e1901. doi:10.1212/WNL.0000000000200285

  3. Cross JH, Kwon CS, Asadi-Pooya AA, et al. Epilepsy care during the COVID-19 pandemic. Epilepsia. 2021;62(10):2322-2332. doi:10.1111/epi.17045

  4. Assenza G, Lanzone J, Ricci L, et al. Electroencephalography at the time of Covid-19 pandemic in Italy. Neurol Sci. 2020;41(8):1999-2004. doi:10.1007/s10072-020-04546-8

  5. US Department of Veterans Affairs. National Center for Veterans Analysis and Statistics. Veteran population. Updated September 7, 2022. Accessed October 25, 2024. https://www.va.gov/vetdata/veteran_population.asp

  6. US Department of Veterans Affairs, Veterans Health Administration. Epilepsy Centers of Excellence (ECoE). Annual report fiscal year 2019. Accessed October 25, 2024. https://www.epilepsy.va.gov/docs/FY19AnnualReport-VHAEpilepsyCentersofExcellence.pdf

  7. Centers for Disease Control and Prevention. United States COVID-19 county level of community transmission historical changes – ARCHIVED. Updated February 20, 2024. Accessed October 25, 2024. https://data.cdc.gov/Public-Health-Surveillance/United-States-COVID-19-County-Level-of-Community-T/nra9-vzzn

  8. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010

  9. Harris PA, Taylor R, Minor BL, et al. The REDCap consortium: building an international community of software platform partners. J Biomed Inform. 2019;95:103208. doi:10.1016/j.jbi.2019.103208

  10. World Health Organization. Rolling updates on coronavirus disease (COVID-19). Updated July 31, 2020. Accessed October 25, 2024. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/events-as-they-happen

  11. US Department of Veterans Affairs. VA announces initial plans for COVID-19 vaccine distribution. News release. December 10, 2020. Accessed October 25, 2024. https://www.va.gov/opa/pressrel/pressrelease.cfm?id=5580

  12. Steinhauer J. V.A. Issues Vaccine Mandate for Health Care Workers, a First for a Federal Agency. The New York Times. August 16, 2021. Accessed October 25, 2024. https://www.nytimes.com/2021/07/26/us/politics/veterans-affairs-coronavirus-covid-19.html

  13. Zafar SF, Khozein RJ, LaRoche SM, Westover MB, Gilmore EJ. Impact of the COVID-19 pandemic on continuous EEG utilization. J Clin Neurophysiol. 2022;39(7):567-574. doi:10.1097/WNP.0000000000000802

  14. Qureshi AI, Rheaume C, Huang W, et al. COVID-19 exposure during neurology practice. Neurologist. 2021;26(6):225-230. doi:10.1097/NRL.0000000000000346

  15. Darkins A, Cruise C, Armstrong M, Peters J, Finn M. Enhancing access of combat-wounded veterans to specialist rehabilitation services: the VA Polytrauma Telehealth Network. Arch Phys Med Rehabil. 2008;89(1):182-187. doi:10.1016/j.apmr.2007.07.027

  16. Darkins A, Ryan P, Kobb R, et al. Care coordination/home telehealth: the systematic implementation of health informatics, home telehealth, and disease management to support the care of veteran patients with chronic conditions. Telemed J E Health. 2008;14(10):1118-1126. doi:10.1089/tmj.2008.0021

  17. Gentry MT, Puspitasari AJ, McKean AJ, et al. Clinician satisfaction with rapid adoption and implementation of telehealth services during the COVID-19 pandemic. Telemed J E Health. 2021;27(12):1385-1392. doi:10.1089/tmj.2020.0575

  18. Connolly SL, Stolzmann KL, Heyworth L, et al. Patient and provider predictors of telemental health use prior to and during the COVID-19 pandemic within the Department of Veterans Affairs. Am Psychol. 2022;77(2):249-261. doi:10.1037/amp0000895

  19. Shelton CJ, Kim A, Hassan AM, Bhat A, Barnello J, Castro CA. System-wide implementation of telehealth to support military veterans and their families in response to COVID-19: a paradigm shift. J Mil Veteran Fam Health. 2020;6(S2):50-57. doi:10.3138/jmvfh-CO19-0003

  20. VA expands telehealth by allowing health care providers to treat patients across state lines. News release. US Dept of Veterans Affairs. May 11, 2018. Accessed October 25, 2024. https://news.va.gov/press-room/va-expands-telehealth-by-allowing-health-care-providers-to-treat-patients-across-state-lines/

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Acknowledgments

The authors would like to acknowledge and thank the Epilepsy Centers of Excellence Directors: James Chen, MD (West Los Angeles), Stephan Eisenschenk, MD (Gainesville), Alfred Frontera, MD (Tampa), Nina Garga, MD (San Francisco), Hamada Hamid, DO, MPH, FAES (West Haven), Stephen Holloway, MD (Minneapolis), John Jones, MD (Madison), Marissa Kellogg, MD, MPH, FAES (Portland), Omar Khan, MD (Baltimore), Maria Lopez, MD (Miami), David McCarthy, MD (Boston), Adetoun Musa, MD (San Antonio), Hae Won Shin, MD (Albuquerque), William Spain, MD (Seattle), and Tung Tran, MD (Durham).

Author affiliations

aMichael E. DeBakey VA Medical Center, Houston, Texas

bBaylor College of Medicine, Houston, Texas

cEpilepsy Centers of Excellence

dDurham VA Medical Center, North Carolina

eHunter Holmes McGuire VA Medical Center, Richmond, Virginia

fVirginia Commonwealth University School of Medicine, RichmondgVeterans Affairs Pittsburgh Healthcare System, Pennsylvania

hUniversity of Pittsburgh, Pennsylvania

iDuke University, Durham, North Carolina

Author disclosures

The authors report no actual or potential conflicts of interest or outside sources of funding with regard to this article.

Disclaimer

The opinions expressed herein are those of the authors and do not necessarily reflect those of Federal Practitioner, Frontline Medical Communications Inc., the US Government, or any of its agencies.

Ethics and consent

Data were collected as part of a quality improvement initiative by the VHA ECoE. IRB approval was not required.

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Acknowledgments

The authors would like to acknowledge and thank the Epilepsy Centers of Excellence Directors: James Chen, MD (West Los Angeles), Stephan Eisenschenk, MD (Gainesville), Alfred Frontera, MD (Tampa), Nina Garga, MD (San Francisco), Hamada Hamid, DO, MPH, FAES (West Haven), Stephen Holloway, MD (Minneapolis), John Jones, MD (Madison), Marissa Kellogg, MD, MPH, FAES (Portland), Omar Khan, MD (Baltimore), Maria Lopez, MD (Miami), David McCarthy, MD (Boston), Adetoun Musa, MD (San Antonio), Hae Won Shin, MD (Albuquerque), William Spain, MD (Seattle), and Tung Tran, MD (Durham).

Author affiliations

aMichael E. DeBakey VA Medical Center, Houston, Texas

bBaylor College of Medicine, Houston, Texas

cEpilepsy Centers of Excellence

dDurham VA Medical Center, North Carolina

eHunter Holmes McGuire VA Medical Center, Richmond, Virginia

fVirginia Commonwealth University School of Medicine, RichmondgVeterans Affairs Pittsburgh Healthcare System, Pennsylvania

hUniversity of Pittsburgh, Pennsylvania

iDuke University, Durham, North Carolina

Author disclosures

The authors report no actual or potential conflicts of interest or outside sources of funding with regard to this article.

Disclaimer

The opinions expressed herein are those of the authors and do not necessarily reflect those of Federal Practitioner, Frontline Medical Communications Inc., the US Government, or any of its agencies.

Ethics and consent

Data were collected as part of a quality improvement initiative by the VHA ECoE. IRB approval was not required.

Author and Disclosure Information

Acknowledgments

The authors would like to acknowledge and thank the Epilepsy Centers of Excellence Directors: James Chen, MD (West Los Angeles), Stephan Eisenschenk, MD (Gainesville), Alfred Frontera, MD (Tampa), Nina Garga, MD (San Francisco), Hamada Hamid, DO, MPH, FAES (West Haven), Stephen Holloway, MD (Minneapolis), John Jones, MD (Madison), Marissa Kellogg, MD, MPH, FAES (Portland), Omar Khan, MD (Baltimore), Maria Lopez, MD (Miami), David McCarthy, MD (Boston), Adetoun Musa, MD (San Antonio), Hae Won Shin, MD (Albuquerque), William Spain, MD (Seattle), and Tung Tran, MD (Durham).

Author affiliations

aMichael E. DeBakey VA Medical Center, Houston, Texas

bBaylor College of Medicine, Houston, Texas

cEpilepsy Centers of Excellence

dDurham VA Medical Center, North Carolina

eHunter Holmes McGuire VA Medical Center, Richmond, Virginia

fVirginia Commonwealth University School of Medicine, RichmondgVeterans Affairs Pittsburgh Healthcare System, Pennsylvania

hUniversity of Pittsburgh, Pennsylvania

iDuke University, Durham, North Carolina

Author disclosures

The authors report no actual or potential conflicts of interest or outside sources of funding with regard to this article.

Disclaimer

The opinions expressed herein are those of the authors and do not necessarily reflect those of Federal Practitioner, Frontline Medical Communications Inc., the US Government, or any of its agencies.

Ethics and consent

Data were collected as part of a quality improvement initiative by the VHA ECoE. IRB approval was not required.

Article PDF
Article PDF

The COVID-19 pandemic affected diverse workplaces globally, leading to temporary and permanent changes across the health care landscape. Included among the impacted areas of care were epilepsy and electroencephalogram (EEG) clinicians and services. Surveys among epilepsy specialists and neurophysiologists conducted at the onset of the pandemic to evaluate working conditions include analyses from the American Epilepsy Society (AES), the National Association of Epilepsy Centers (NAEC), the International League Against Epilepsy, and an Italian national survey.1-4 These investigations revealed reductions in epilepsy monitoring unit (EMU) admissions (23% decline), epilepsy surgery (6% decline), inpatient EEG (22% of respondents reported decline), and patients having difficulty accessing epilepsy professionals (28% of respondents reported decline) or obtaining medications (20% of respondents reported decline).1-3

While such research provided evidence for changes to epilepsy care in 2020, there are limited data on subsequent adaptations during the pandemic. These studies did not incorporate data on the spread of COVID-19 or administrative workload numbers to analyze service delivery beyond self reports. This study aimed to address this gap in the literature by highlighting results from longitudinal national surveys conducted at the Epilepsy Centers of Excellence (ECoE), a specialty care service within the Veterans Health Administration (VHA), which annually serves > 9 million veterans.5 The ECoE represents epileptologists and neurophysiologists across the United States at the 17 primary facilities that were established at the time of this survey (2 ECoEs have been added since survey completion) in 4 geographical regions and for which other regional facilities refer patients for diagnostic services or specialty care.6

National surveys were conducted among the ECoE directors regarding adaptations made from May 2020 to June 2022 to provide a comprehensive account of limitations they experienced and how adjustments have been made to improve patient care. Survey responses were compared to administrative workload numbers and COVID-19 spread data from the Centers for Disease Control and Prevention (CDC) to provide a comprehensive analysis of performance during the pandemic.

METHODS

Data were collected as part of a quality improvement initiative by the VHA ECoE; institutional review board approval was not required. An 18-item survey covering 5 broad domains was sent to ECoE directors 4 separate times to accumulate data from 4 time periods: May to June 2020 (T1); December 2020 to February 2021 (T2); July to August 2021 (T3); and June to July 2022 (T4). These periods correspond to the following phases of the pandemic: T1, onset of pandemic; T2, vaccine availability; T3, Delta variant predominant; T4, Omicron variant predominant.

table 1

Data on the spread of COVID-19 were collected from the CDC archived dataset, US COVID-19 County Level of Community Transmission Historical Changes (Table 1).7 Administrative workload (patient counts) for EEG, EMU, and outpatient clinics were extracted from VHA administrative databases for the participating sites for the months prior to each survey: T1, April 2020; T2, November 2020; T3, June 2021; and T4, May 2022 (Table 2).

table 2

Survey Structure and Content

The survey was developed by the ECoE and was not validated prior to its use due to the time-sensitive nature of gathering information during the pandemic. The first survey (T1) was an emailed spreadsheet with open-ended questions to gauge availability of services (ie, outpatient clinic, EEG, EMU), assess whether safety precautions were being introduced, and understand whether national or local guidelines were thought to be helpful. Responses from this and subsequent surveys were standardized into yes/no and multiple choice formats. Subsequent surveys were administered online using a Research Electronic Data Capture tool.8,9

Availability of outpatient epilepsy services across the 4 time periods were categorized as unlimited (in-person with no restrictions), limited (in-person with restrictions), planned (not currently performed but scheduled for the near future), and unavailable (no in-person services offered) (eAppendices 1-6, available in article PDF).

Statistical Analyses

Analyses were performed to compare survey responses to workload and CDC data on COVID-19 community spread. The following associations were examined: (1) CDC COVID-19 spread vs respondents’ perception of spread; (2) respondents’ perception of spread vs availability of services; (3) CDC COVID-19 spread vs availability of services; (4) respondents’ perception of spread vs workload; and (5) CDC COVID-19 spread vs workload. Availability of services was dichotomized for analyses, with limited or fully available services classified as available. As services were mostly open at T3 regardless of the spread of the virus, and the CDC COVID-19 spread classification for all sites was severe or high at T2 and T4, corresponding associations were not tested at these time points. For associations 1 through 3, Fisher exact tests were used; for associations 4 and 5, Mann-Whitney U tests (where the COVID-19 spread fell into 2 categories) and Kruskal-Wallis tests (for 3 categories of COVID-19 spread) were performed. All tests were 2-tailed and performed at 0.05 error rate. Bonferroni corrections were applied to adjust P values for multiple hypotheses tests.

RESULTS

From the 17 sites invited, responses at each time point were obtained from 13 (T1),17 (T2), 15 (T3), and 16 (T4) centers. There was no significant association between self-reported COVID-19 spread and CDC classification of COVID spread. There were no associations between COVID-19 community spread (respondent reported or CDC severity level) and outpatient clinic availability (self-reported or workload captured). At T3, a positive association was found between the CDC spread level and workload (P = .008), but this was not significant after Bonferroni correction (P = .06).

EEG availability surpassed EMU availability at all time points, although EMU services made some recovery at T3 and T4. No associations were found between COVID-19 community spread (self-reported or CDC severity level) and outpatient EEG or EMU availability (self-reported or workload captured). At T3, there was a positive association between EEG workload and CDC COVID-19 severity level (P = .04), but this was not significant after Bonferroni correction (P = .30). 

For outpatient EEG, staff and patient mask use were universally implemented by T2, while the use of full personal protective equipment (PPE) occurred at a subset of sites (T2, 6/17 [35%]; T3, 3/15 [20%]; T4: 4/16 [25%]). COVID-19 testing was rarely implemented prior to outpatient EEG (T1, 0 sites; T2, 1 site; T3, 1 site; T4, 0 sites). Within the EMU, safety precautions including COVID-19 testing, patient mask usage, staff mask usage, and aerosolization demonstrated a sustained majority usage across the 4 surveys.

National and Local Guidelines

The open-ended survey at T1 asked site directors, “Should there be national recommendations on how EEGs and related procedures should be done during the pandemic or should this be left to local conditions?” Responses were mixed, with 5 respondents desiring a national standard, 4 respondents favoring a local response, and 4 respondents believing a national standard should be in place but with modifications based on local outbreak levels and needs.

Surveys performed at T2 through T4 asked, “Which of the following do you feel was/will be helpful in adapting to COVID-19–related changes?” Overall, there was substantial agreement that guidelines were helpful. Most sites anticipated permanent changes in enhanced safety precautions and telehealth.

DISCUSSION

This longitudinal study across 4 time points describes how epilepsy services within the VHA and ECoE adapted to the COVID-19 pandemic. The first survey, conducted 2 months after COVID-19 was declared a pandemic, allowed a comparison with other concurrent US national surveys.1,2,10 The subsequent surveys describe longitudinal adaptations to balance patient and staff safety with service availability and is a unique feature of the current report. Results demonstrate flexibility and adaptability by the ECoEs surveyed, which surprisingly did not show significant associations between CDC COVID-19 spread data and administrative workload data.

Trends in Availability of Services

The most significant impact of COVID-19 restrictions was during T1. There were no significant relationships between service availability/workload and objective CDC COVID-19 spread levels or subjective self-reported COVID-19 spread. Respondents’ perceptions of local COVID-19 spread showed no association with CDC COVID-19 spread data. It appears that subjective perception of spread may be unreliable and factors other than actual or perceived COVID-19 spread were likely driving patterns for service availability.

In-person outpatient visits were most impacted at T1, similar to other civilian surveys, with only 1 site reporting in-person outpatient visits without limitations.1,2 These numbers significantly changed by T2, with all sites offering either limited or unlimited in-person visits. While the surveys did not evaluate factors leading to this rapid recovery, it may be related to the availability of COVID-19 vaccinations within the VHA during this time.11 The US Department of Veterans Affairs was the first federal agency to mandate employee vaccination.12 By the most recent time point (T4), all responding sites offered outpatient visits. Outpatient EEGs followed a similar trend, with T1 being the most restrictive and full, unrestricted outpatient EEGs available by T3. 

Fiscal year (FY) trends from ECoE annual reports suggest that encounters slowly recovered over the course of the pandemic. In FY 2019 there were 13,143 outpatient encounters and 6394 EEGs, which dropped to 8097 outpatient encounters and 4432 EEGs in FY 2020 before rising to 8489 outpatient encounters and 5604 EEGs in FY 2021 and 9772 outpatient encounters and 5062 EEGs in FY 2022. Thus, while clinicians described availability of services, patients may have remained hesitant or were otherwise unable to fulfill in-person appointments. The increased availability of home EEG (145 encounter days in 2021 and 436 encounter days in 2022) may be filling this gap. 

In contrast to outpatient clinics and EEG, EMU availability showed relatively slower reimplementation. In the last survey, about 30% of sites were still not offering EMU or had limited services. Early trends regarding reduced staffing and patient reluctance for elective admission cited in other surveys may have also affected EMU availability within the VHA.2,13 Consistent with trends in availability, ECoE annual report data suggest EMU patient participation was about one-half of prepandemic rates: 3069 encounters in FY 2019 dropped to 1614 encounters in 2020. By 2021, rates were about two-thirds of prepandemic rates with 2058 encounters in 2021 and 2101 encounters in 2022.

Early survey results (T1) from this study echo trends from other surveys. In the AES survey (April to June 2020), about a quarter of respondents (22%) reported doing fewer EEG studies than usual. The Italian national survey (April 2020) revealed reduced presurgical evaluations (81%), ambulatory EEG (78%), standard EEG (5%) and long-term EEG (32%).4 In the NAEC survey (end of 2020)—which roughly corresponded to T2—outpatient EEGs were still < 75% of pre-COVID levels in one-half of the centers.

National and Local Guidelines

Both national and local guidelines were perceived as useful by most respondents, with national guidelines being more beneficial. This aligns with the NAEC survey, where there was a perceived need for detailed recommendations for PPE and COVID-19 testing of patients, visitors, and staff. Based on national and local guidelines, ECoE implemented safety procedures, as reflected in responses. Staff masking procedures appeared to be the most widely adopted for all services, while the use of full PPE waned as the pandemic progressed. COVID-19 testing was rarely used for routine outpatient visits but common in EMU admissions. This is similar to a survey conducted by the American Academy of Neurology which found full PPE implementation intermittently in outpatient settings and more frequently in inpatient settings.14

Telehealth Attitudes

While most sites anticipated permanent implementation of safety precautions and telehealth, the latter was consistently reported as more likely to be sustained. The VHA had a large and well-developed system of telehealth services that considerably predated the pandemic.15,16 Through this established infrastructure, remote services were quickly increased across the VHA.17-19 This telehealth structure was supplemented by the ability of VHA clinicians to practice across state lines, following a 2018 federal rule.20 The AES survey noted the VHA ECoE's longstanding experience with telehealth as a model for telemedicine use in providing direct patient care, remote EEG analysis, and clinician-to-clinician consultation.1

Trends in the number of telehealth patients seen, observed through patterns in ECoE annual reports are consistent with positive views toward this method of service provision. Specifically, these annual reports capture trends in Video Telehealth Clinic (local station), Video Telehealth Clinic (different station), Home Video Telehealth, Telephone Clinic, and eConsults. Though video telehealth at in-person stations had a precipitous drop in 2020 that continued to wane in subsequent years (898 encounters in 2019; 455 encounters in 2020; 90 encounters in 2021; 88 encounters in 2022), use of home video telehealth rose over time (143 encounters in 2019; 1003 encounters in 2020; 3206 encounters in 2021; 3315 encounters in 2022). Use of telephone services rose drastically in 2020 but has since become a less frequently used service method (2636 in 2019; 5923 in 2020; 5319 in 2021; 3704 in 2022).

Limitations

While the survey encouraged a high response rate, this limited its scope and interpretability. While the availability of services was evaluated, the underlying reasons were not queried. Follow-up questions about barriers to reopening may have allowed for a better understanding of why some services, such as EMU, continued to operate suboptimally later in the pandemic. Similarly, asking about unique strategies or barriers for telehealth would have allowed for a better understanding of its current and future use. We hypothesize that staffing changes during the pandemic may have influenced the availability of services, but changes to staffing were not assessed via the survey and were not readily available via other sources (eg, ECoE annual reports) at the time of publication. An additional limitation is the lack of comparable surveys in the literature for time points T2 to T4, as most analogous surveys were performed early in 2020.

Conclusions

This longitudinal study performed at 4 time points during the COVID-19 pandemic is the first to offer a comprehensive picture of changes to epilepsy and EEG services over time, given that other similar surveys lacked follow-up. Results reveal a significant limitation of services at VHA ECoE shortly after the onset of the pandemic, with return to near-complete operational status 2 years later. While safety precautions and telehealth are predicted to continue, telehealth is perceived as a more permanent change in services.

The COVID-19 pandemic affected diverse workplaces globally, leading to temporary and permanent changes across the health care landscape. Included among the impacted areas of care were epilepsy and electroencephalogram (EEG) clinicians and services. Surveys among epilepsy specialists and neurophysiologists conducted at the onset of the pandemic to evaluate working conditions include analyses from the American Epilepsy Society (AES), the National Association of Epilepsy Centers (NAEC), the International League Against Epilepsy, and an Italian national survey.1-4 These investigations revealed reductions in epilepsy monitoring unit (EMU) admissions (23% decline), epilepsy surgery (6% decline), inpatient EEG (22% of respondents reported decline), and patients having difficulty accessing epilepsy professionals (28% of respondents reported decline) or obtaining medications (20% of respondents reported decline).1-3

While such research provided evidence for changes to epilepsy care in 2020, there are limited data on subsequent adaptations during the pandemic. These studies did not incorporate data on the spread of COVID-19 or administrative workload numbers to analyze service delivery beyond self reports. This study aimed to address this gap in the literature by highlighting results from longitudinal national surveys conducted at the Epilepsy Centers of Excellence (ECoE), a specialty care service within the Veterans Health Administration (VHA), which annually serves > 9 million veterans.5 The ECoE represents epileptologists and neurophysiologists across the United States at the 17 primary facilities that were established at the time of this survey (2 ECoEs have been added since survey completion) in 4 geographical regions and for which other regional facilities refer patients for diagnostic services or specialty care.6

National surveys were conducted among the ECoE directors regarding adaptations made from May 2020 to June 2022 to provide a comprehensive account of limitations they experienced and how adjustments have been made to improve patient care. Survey responses were compared to administrative workload numbers and COVID-19 spread data from the Centers for Disease Control and Prevention (CDC) to provide a comprehensive analysis of performance during the pandemic.

METHODS

Data were collected as part of a quality improvement initiative by the VHA ECoE; institutional review board approval was not required. An 18-item survey covering 5 broad domains was sent to ECoE directors 4 separate times to accumulate data from 4 time periods: May to June 2020 (T1); December 2020 to February 2021 (T2); July to August 2021 (T3); and June to July 2022 (T4). These periods correspond to the following phases of the pandemic: T1, onset of pandemic; T2, vaccine availability; T3, Delta variant predominant; T4, Omicron variant predominant.

table 1

Data on the spread of COVID-19 were collected from the CDC archived dataset, US COVID-19 County Level of Community Transmission Historical Changes (Table 1).7 Administrative workload (patient counts) for EEG, EMU, and outpatient clinics were extracted from VHA administrative databases for the participating sites for the months prior to each survey: T1, April 2020; T2, November 2020; T3, June 2021; and T4, May 2022 (Table 2).

table 2

Survey Structure and Content

The survey was developed by the ECoE and was not validated prior to its use due to the time-sensitive nature of gathering information during the pandemic. The first survey (T1) was an emailed spreadsheet with open-ended questions to gauge availability of services (ie, outpatient clinic, EEG, EMU), assess whether safety precautions were being introduced, and understand whether national or local guidelines were thought to be helpful. Responses from this and subsequent surveys were standardized into yes/no and multiple choice formats. Subsequent surveys were administered online using a Research Electronic Data Capture tool.8,9

Availability of outpatient epilepsy services across the 4 time periods were categorized as unlimited (in-person with no restrictions), limited (in-person with restrictions), planned (not currently performed but scheduled for the near future), and unavailable (no in-person services offered) (eAppendices 1-6, available in article PDF).

Statistical Analyses

Analyses were performed to compare survey responses to workload and CDC data on COVID-19 community spread. The following associations were examined: (1) CDC COVID-19 spread vs respondents’ perception of spread; (2) respondents’ perception of spread vs availability of services; (3) CDC COVID-19 spread vs availability of services; (4) respondents’ perception of spread vs workload; and (5) CDC COVID-19 spread vs workload. Availability of services was dichotomized for analyses, with limited or fully available services classified as available. As services were mostly open at T3 regardless of the spread of the virus, and the CDC COVID-19 spread classification for all sites was severe or high at T2 and T4, corresponding associations were not tested at these time points. For associations 1 through 3, Fisher exact tests were used; for associations 4 and 5, Mann-Whitney U tests (where the COVID-19 spread fell into 2 categories) and Kruskal-Wallis tests (for 3 categories of COVID-19 spread) were performed. All tests were 2-tailed and performed at 0.05 error rate. Bonferroni corrections were applied to adjust P values for multiple hypotheses tests.

RESULTS

From the 17 sites invited, responses at each time point were obtained from 13 (T1),17 (T2), 15 (T3), and 16 (T4) centers. There was no significant association between self-reported COVID-19 spread and CDC classification of COVID spread. There were no associations between COVID-19 community spread (respondent reported or CDC severity level) and outpatient clinic availability (self-reported or workload captured). At T3, a positive association was found between the CDC spread level and workload (P = .008), but this was not significant after Bonferroni correction (P = .06).

EEG availability surpassed EMU availability at all time points, although EMU services made some recovery at T3 and T4. No associations were found between COVID-19 community spread (self-reported or CDC severity level) and outpatient EEG or EMU availability (self-reported or workload captured). At T3, there was a positive association between EEG workload and CDC COVID-19 severity level (P = .04), but this was not significant after Bonferroni correction (P = .30). 

For outpatient EEG, staff and patient mask use were universally implemented by T2, while the use of full personal protective equipment (PPE) occurred at a subset of sites (T2, 6/17 [35%]; T3, 3/15 [20%]; T4: 4/16 [25%]). COVID-19 testing was rarely implemented prior to outpatient EEG (T1, 0 sites; T2, 1 site; T3, 1 site; T4, 0 sites). Within the EMU, safety precautions including COVID-19 testing, patient mask usage, staff mask usage, and aerosolization demonstrated a sustained majority usage across the 4 surveys.

National and Local Guidelines

The open-ended survey at T1 asked site directors, “Should there be national recommendations on how EEGs and related procedures should be done during the pandemic or should this be left to local conditions?” Responses were mixed, with 5 respondents desiring a national standard, 4 respondents favoring a local response, and 4 respondents believing a national standard should be in place but with modifications based on local outbreak levels and needs.

Surveys performed at T2 through T4 asked, “Which of the following do you feel was/will be helpful in adapting to COVID-19–related changes?” Overall, there was substantial agreement that guidelines were helpful. Most sites anticipated permanent changes in enhanced safety precautions and telehealth.

DISCUSSION

This longitudinal study across 4 time points describes how epilepsy services within the VHA and ECoE adapted to the COVID-19 pandemic. The first survey, conducted 2 months after COVID-19 was declared a pandemic, allowed a comparison with other concurrent US national surveys.1,2,10 The subsequent surveys describe longitudinal adaptations to balance patient and staff safety with service availability and is a unique feature of the current report. Results demonstrate flexibility and adaptability by the ECoEs surveyed, which surprisingly did not show significant associations between CDC COVID-19 spread data and administrative workload data.

Trends in Availability of Services

The most significant impact of COVID-19 restrictions was during T1. There were no significant relationships between service availability/workload and objective CDC COVID-19 spread levels or subjective self-reported COVID-19 spread. Respondents’ perceptions of local COVID-19 spread showed no association with CDC COVID-19 spread data. It appears that subjective perception of spread may be unreliable and factors other than actual or perceived COVID-19 spread were likely driving patterns for service availability.

In-person outpatient visits were most impacted at T1, similar to other civilian surveys, with only 1 site reporting in-person outpatient visits without limitations.1,2 These numbers significantly changed by T2, with all sites offering either limited or unlimited in-person visits. While the surveys did not evaluate factors leading to this rapid recovery, it may be related to the availability of COVID-19 vaccinations within the VHA during this time.11 The US Department of Veterans Affairs was the first federal agency to mandate employee vaccination.12 By the most recent time point (T4), all responding sites offered outpatient visits. Outpatient EEGs followed a similar trend, with T1 being the most restrictive and full, unrestricted outpatient EEGs available by T3. 

Fiscal year (FY) trends from ECoE annual reports suggest that encounters slowly recovered over the course of the pandemic. In FY 2019 there were 13,143 outpatient encounters and 6394 EEGs, which dropped to 8097 outpatient encounters and 4432 EEGs in FY 2020 before rising to 8489 outpatient encounters and 5604 EEGs in FY 2021 and 9772 outpatient encounters and 5062 EEGs in FY 2022. Thus, while clinicians described availability of services, patients may have remained hesitant or were otherwise unable to fulfill in-person appointments. The increased availability of home EEG (145 encounter days in 2021 and 436 encounter days in 2022) may be filling this gap. 

In contrast to outpatient clinics and EEG, EMU availability showed relatively slower reimplementation. In the last survey, about 30% of sites were still not offering EMU or had limited services. Early trends regarding reduced staffing and patient reluctance for elective admission cited in other surveys may have also affected EMU availability within the VHA.2,13 Consistent with trends in availability, ECoE annual report data suggest EMU patient participation was about one-half of prepandemic rates: 3069 encounters in FY 2019 dropped to 1614 encounters in 2020. By 2021, rates were about two-thirds of prepandemic rates with 2058 encounters in 2021 and 2101 encounters in 2022.

Early survey results (T1) from this study echo trends from other surveys. In the AES survey (April to June 2020), about a quarter of respondents (22%) reported doing fewer EEG studies than usual. The Italian national survey (April 2020) revealed reduced presurgical evaluations (81%), ambulatory EEG (78%), standard EEG (5%) and long-term EEG (32%).4 In the NAEC survey (end of 2020)—which roughly corresponded to T2—outpatient EEGs were still < 75% of pre-COVID levels in one-half of the centers.

National and Local Guidelines

Both national and local guidelines were perceived as useful by most respondents, with national guidelines being more beneficial. This aligns with the NAEC survey, where there was a perceived need for detailed recommendations for PPE and COVID-19 testing of patients, visitors, and staff. Based on national and local guidelines, ECoE implemented safety procedures, as reflected in responses. Staff masking procedures appeared to be the most widely adopted for all services, while the use of full PPE waned as the pandemic progressed. COVID-19 testing was rarely used for routine outpatient visits but common in EMU admissions. This is similar to a survey conducted by the American Academy of Neurology which found full PPE implementation intermittently in outpatient settings and more frequently in inpatient settings.14

Telehealth Attitudes

While most sites anticipated permanent implementation of safety precautions and telehealth, the latter was consistently reported as more likely to be sustained. The VHA had a large and well-developed system of telehealth services that considerably predated the pandemic.15,16 Through this established infrastructure, remote services were quickly increased across the VHA.17-19 This telehealth structure was supplemented by the ability of VHA clinicians to practice across state lines, following a 2018 federal rule.20 The AES survey noted the VHA ECoE's longstanding experience with telehealth as a model for telemedicine use in providing direct patient care, remote EEG analysis, and clinician-to-clinician consultation.1

Trends in the number of telehealth patients seen, observed through patterns in ECoE annual reports are consistent with positive views toward this method of service provision. Specifically, these annual reports capture trends in Video Telehealth Clinic (local station), Video Telehealth Clinic (different station), Home Video Telehealth, Telephone Clinic, and eConsults. Though video telehealth at in-person stations had a precipitous drop in 2020 that continued to wane in subsequent years (898 encounters in 2019; 455 encounters in 2020; 90 encounters in 2021; 88 encounters in 2022), use of home video telehealth rose over time (143 encounters in 2019; 1003 encounters in 2020; 3206 encounters in 2021; 3315 encounters in 2022). Use of telephone services rose drastically in 2020 but has since become a less frequently used service method (2636 in 2019; 5923 in 2020; 5319 in 2021; 3704 in 2022).

Limitations

While the survey encouraged a high response rate, this limited its scope and interpretability. While the availability of services was evaluated, the underlying reasons were not queried. Follow-up questions about barriers to reopening may have allowed for a better understanding of why some services, such as EMU, continued to operate suboptimally later in the pandemic. Similarly, asking about unique strategies or barriers for telehealth would have allowed for a better understanding of its current and future use. We hypothesize that staffing changes during the pandemic may have influenced the availability of services, but changes to staffing were not assessed via the survey and were not readily available via other sources (eg, ECoE annual reports) at the time of publication. An additional limitation is the lack of comparable surveys in the literature for time points T2 to T4, as most analogous surveys were performed early in 2020.

Conclusions

This longitudinal study performed at 4 time points during the COVID-19 pandemic is the first to offer a comprehensive picture of changes to epilepsy and EEG services over time, given that other similar surveys lacked follow-up. Results reveal a significant limitation of services at VHA ECoE shortly after the onset of the pandemic, with return to near-complete operational status 2 years later. While safety precautions and telehealth are predicted to continue, telehealth is perceived as a more permanent change in services.

References
  1. Albert DVF, Das RR, Acharya JN, et al. The impact of COVID-19 on epilepsy care: a survey of the American Epilepsy Society membership. Epilepsy Curr. 2020;20(5):316-324. doi:10.1177/1535759720956994

  2. Ahrens SM, Ostendorf AP, Lado FA, et al. Impact of the COVID-19 pandemic on epilepsy center practice in the United States. Neurology. 2022;98(19):e1893-e1901. doi:10.1212/WNL.0000000000200285

  3. Cross JH, Kwon CS, Asadi-Pooya AA, et al. Epilepsy care during the COVID-19 pandemic. Epilepsia. 2021;62(10):2322-2332. doi:10.1111/epi.17045

  4. Assenza G, Lanzone J, Ricci L, et al. Electroencephalography at the time of Covid-19 pandemic in Italy. Neurol Sci. 2020;41(8):1999-2004. doi:10.1007/s10072-020-04546-8

  5. US Department of Veterans Affairs. National Center for Veterans Analysis and Statistics. Veteran population. Updated September 7, 2022. Accessed October 25, 2024. https://www.va.gov/vetdata/veteran_population.asp

  6. US Department of Veterans Affairs, Veterans Health Administration. Epilepsy Centers of Excellence (ECoE). Annual report fiscal year 2019. Accessed October 25, 2024. https://www.epilepsy.va.gov/docs/FY19AnnualReport-VHAEpilepsyCentersofExcellence.pdf

  7. Centers for Disease Control and Prevention. United States COVID-19 county level of community transmission historical changes – ARCHIVED. Updated February 20, 2024. Accessed October 25, 2024. https://data.cdc.gov/Public-Health-Surveillance/United-States-COVID-19-County-Level-of-Community-T/nra9-vzzn

  8. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010

  9. Harris PA, Taylor R, Minor BL, et al. The REDCap consortium: building an international community of software platform partners. J Biomed Inform. 2019;95:103208. doi:10.1016/j.jbi.2019.103208

  10. World Health Organization. Rolling updates on coronavirus disease (COVID-19). Updated July 31, 2020. Accessed October 25, 2024. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/events-as-they-happen

  11. US Department of Veterans Affairs. VA announces initial plans for COVID-19 vaccine distribution. News release. December 10, 2020. Accessed October 25, 2024. https://www.va.gov/opa/pressrel/pressrelease.cfm?id=5580

  12. Steinhauer J. V.A. Issues Vaccine Mandate for Health Care Workers, a First for a Federal Agency. The New York Times. August 16, 2021. Accessed October 25, 2024. https://www.nytimes.com/2021/07/26/us/politics/veterans-affairs-coronavirus-covid-19.html

  13. Zafar SF, Khozein RJ, LaRoche SM, Westover MB, Gilmore EJ. Impact of the COVID-19 pandemic on continuous EEG utilization. J Clin Neurophysiol. 2022;39(7):567-574. doi:10.1097/WNP.0000000000000802

  14. Qureshi AI, Rheaume C, Huang W, et al. COVID-19 exposure during neurology practice. Neurologist. 2021;26(6):225-230. doi:10.1097/NRL.0000000000000346

  15. Darkins A, Cruise C, Armstrong M, Peters J, Finn M. Enhancing access of combat-wounded veterans to specialist rehabilitation services: the VA Polytrauma Telehealth Network. Arch Phys Med Rehabil. 2008;89(1):182-187. doi:10.1016/j.apmr.2007.07.027

  16. Darkins A, Ryan P, Kobb R, et al. Care coordination/home telehealth: the systematic implementation of health informatics, home telehealth, and disease management to support the care of veteran patients with chronic conditions. Telemed J E Health. 2008;14(10):1118-1126. doi:10.1089/tmj.2008.0021

  17. Gentry MT, Puspitasari AJ, McKean AJ, et al. Clinician satisfaction with rapid adoption and implementation of telehealth services during the COVID-19 pandemic. Telemed J E Health. 2021;27(12):1385-1392. doi:10.1089/tmj.2020.0575

  18. Connolly SL, Stolzmann KL, Heyworth L, et al. Patient and provider predictors of telemental health use prior to and during the COVID-19 pandemic within the Department of Veterans Affairs. Am Psychol. 2022;77(2):249-261. doi:10.1037/amp0000895

  19. Shelton CJ, Kim A, Hassan AM, Bhat A, Barnello J, Castro CA. System-wide implementation of telehealth to support military veterans and their families in response to COVID-19: a paradigm shift. J Mil Veteran Fam Health. 2020;6(S2):50-57. doi:10.3138/jmvfh-CO19-0003

  20. VA expands telehealth by allowing health care providers to treat patients across state lines. News release. US Dept of Veterans Affairs. May 11, 2018. Accessed October 25, 2024. https://news.va.gov/press-room/va-expands-telehealth-by-allowing-health-care-providers-to-treat-patients-across-state-lines/

References
  1. Albert DVF, Das RR, Acharya JN, et al. The impact of COVID-19 on epilepsy care: a survey of the American Epilepsy Society membership. Epilepsy Curr. 2020;20(5):316-324. doi:10.1177/1535759720956994

  2. Ahrens SM, Ostendorf AP, Lado FA, et al. Impact of the COVID-19 pandemic on epilepsy center practice in the United States. Neurology. 2022;98(19):e1893-e1901. doi:10.1212/WNL.0000000000200285

  3. Cross JH, Kwon CS, Asadi-Pooya AA, et al. Epilepsy care during the COVID-19 pandemic. Epilepsia. 2021;62(10):2322-2332. doi:10.1111/epi.17045

  4. Assenza G, Lanzone J, Ricci L, et al. Electroencephalography at the time of Covid-19 pandemic in Italy. Neurol Sci. 2020;41(8):1999-2004. doi:10.1007/s10072-020-04546-8

  5. US Department of Veterans Affairs. National Center for Veterans Analysis and Statistics. Veteran population. Updated September 7, 2022. Accessed October 25, 2024. https://www.va.gov/vetdata/veteran_population.asp

  6. US Department of Veterans Affairs, Veterans Health Administration. Epilepsy Centers of Excellence (ECoE). Annual report fiscal year 2019. Accessed October 25, 2024. https://www.epilepsy.va.gov/docs/FY19AnnualReport-VHAEpilepsyCentersofExcellence.pdf

  7. Centers for Disease Control and Prevention. United States COVID-19 county level of community transmission historical changes – ARCHIVED. Updated February 20, 2024. Accessed October 25, 2024. https://data.cdc.gov/Public-Health-Surveillance/United-States-COVID-19-County-Level-of-Community-T/nra9-vzzn

  8. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010

  9. Harris PA, Taylor R, Minor BL, et al. The REDCap consortium: building an international community of software platform partners. J Biomed Inform. 2019;95:103208. doi:10.1016/j.jbi.2019.103208

  10. World Health Organization. Rolling updates on coronavirus disease (COVID-19). Updated July 31, 2020. Accessed October 25, 2024. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/events-as-they-happen

  11. US Department of Veterans Affairs. VA announces initial plans for COVID-19 vaccine distribution. News release. December 10, 2020. Accessed October 25, 2024. https://www.va.gov/opa/pressrel/pressrelease.cfm?id=5580

  12. Steinhauer J. V.A. Issues Vaccine Mandate for Health Care Workers, a First for a Federal Agency. The New York Times. August 16, 2021. Accessed October 25, 2024. https://www.nytimes.com/2021/07/26/us/politics/veterans-affairs-coronavirus-covid-19.html

  13. Zafar SF, Khozein RJ, LaRoche SM, Westover MB, Gilmore EJ. Impact of the COVID-19 pandemic on continuous EEG utilization. J Clin Neurophysiol. 2022;39(7):567-574. doi:10.1097/WNP.0000000000000802

  14. Qureshi AI, Rheaume C, Huang W, et al. COVID-19 exposure during neurology practice. Neurologist. 2021;26(6):225-230. doi:10.1097/NRL.0000000000000346

  15. Darkins A, Cruise C, Armstrong M, Peters J, Finn M. Enhancing access of combat-wounded veterans to specialist rehabilitation services: the VA Polytrauma Telehealth Network. Arch Phys Med Rehabil. 2008;89(1):182-187. doi:10.1016/j.apmr.2007.07.027

  16. Darkins A, Ryan P, Kobb R, et al. Care coordination/home telehealth: the systematic implementation of health informatics, home telehealth, and disease management to support the care of veteran patients with chronic conditions. Telemed J E Health. 2008;14(10):1118-1126. doi:10.1089/tmj.2008.0021

  17. Gentry MT, Puspitasari AJ, McKean AJ, et al. Clinician satisfaction with rapid adoption and implementation of telehealth services during the COVID-19 pandemic. Telemed J E Health. 2021;27(12):1385-1392. doi:10.1089/tmj.2020.0575

  18. Connolly SL, Stolzmann KL, Heyworth L, et al. Patient and provider predictors of telemental health use prior to and during the COVID-19 pandemic within the Department of Veterans Affairs. Am Psychol. 2022;77(2):249-261. doi:10.1037/amp0000895

  19. Shelton CJ, Kim A, Hassan AM, Bhat A, Barnello J, Castro CA. System-wide implementation of telehealth to support military veterans and their families in response to COVID-19: a paradigm shift. J Mil Veteran Fam Health. 2020;6(S2):50-57. doi:10.3138/jmvfh-CO19-0003

  20. VA expands telehealth by allowing health care providers to treat patients across state lines. News release. US Dept of Veterans Affairs. May 11, 2018. Accessed October 25, 2024. https://news.va.gov/press-room/va-expands-telehealth-by-allowing-health-care-providers-to-treat-patients-across-state-lines/

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What’s Eating You? Hookworm and Cutaneous Larva Migrans

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What’s Eating You? Hookworm and
Cutaneous Larva Migrans

It is estimated that the prevalence of human hookworm infection is approximately 450 million individuals worldwide, representing a substantial global disease burden.1 The annual global public health burden ranges from approximately 2 million to 4 million disability-adjusted life-years and $10 billion to $140 billion in hookwormrelated costs.2 In this article, we discuss the lifecycle, transmission, and disease burden of cutaneous larva migrans (CLM) as well as prevention and treatment strategies.

Background

The Ancylostomatidae nematode family comprises at least 68 known species of hookworm that infect more than 110 different species of mammals.3 Many of these parasites are able to infect more than 1 primary host species, but from a disease perspective they can be classified as either anthropophilic, with humans as the intended host, or zoonotic, with humans as an incidental host. It is important to make this distinction because, though the lifecycles and biology of hookworm species generally are similar, the manifestations of incidental human infection from zoonotic hookworms are different from those of anthropophilic hookworms. Of the anthropophilic species, Necator americanus and Ancylostoma duodenale predominate. In the instance of zoonotic hookworm, dog-infecting A caninum and cat- and doginfecting A braziliense and Uncinaria stenocephala are common causes of incidental human disease.3

The life cycle of Ancylostomatidae organisms is astounding. Through millions of years of co-evolution with mammals,4 these parasitic worms have developed perhaps one of the most circuitous paths to propagate themselves in the natural world. Hookworms start their arduous journey as eggs deposited in soil, sand, and ground vegetation from the feces of infected animals.5 Approximately 1 day after the eggs are deposited, they hatch and begin the larval stage, during which they become infective 1 to 5 weeks later. At this point, the larvae become sensitive to their environment, responding to rising temperatures, increasing carbon dioxide levels, and vibrations in the soil—all of which suggest the presence of a potential host and contribute to a concordant increase in undulatory movement of the larvae.5,6 Here, the most vulnerable tissues include the uncovered soles, palms, and buttocks of host mammals that come into contact with contaminated soil. In an undulating fashion and guided by temperature cues, the larvae locate the skin of the host and utilize a mixture of enzymes including hyaluronidases, metalloprotease, and other proteases to penetrate the epidermis.7 Anthropophilic hookworms such as N americanus and A duodenale will enter the circulatory system; from there, the hookworms migrate through the right-sided cardiopulmonary circuit and eventually ascend into the pulmonary vasculature.8 They then penetrate the lung capillary beds and parenchyma to reach the alveoli, ascend the respiratory tree, and, with the help of the mucociliary escalator, reach the esophagus, where they are swallowed by the host. In the gastrointestinal tract, adult hookworms consume host blood, mate, and lay eggs over a period of approximately 1 to 3 years if left untreated.9 Eggs are laid into the lower gastrointestinal tract, and the journey begins again in feces contacting ground or soil.

Geographic Distribution

Hookworms are found in almost all regions of the world, with species-specific distributions that highlight tropical and subtropical regions. Necator americanus and A duodenale are the most common hookworm species, with the former found predominantly in Southeast Asia and Latin America and the latter in Asia-Pacific regions.10 The highest prevalence of hookworms is in Southeast Asia followed by Sub-Saharan Africa, and the unique climate and soil composition of a region help determine the best environments for specific species of hookworm to thrive.11 In addition, socioeconomics and social determinants of health play a big role in the spread of hookworms, as hygiene practices (eg, wearing clean shoes and clothing, bathing), infrastructure (eg, clean water and streets), and anthelmintic campaigns help reduce transmission.12 Soil-transmitted helminths were once endemic to the southeastern United States, with some reports of approximately 40% of individuals infected in the south in the early 1900s.13 Anthelmintic campaigns such as water, sanitation, and hygiene programs as well as deworming of humans and livestock have proven effective in reducing the prevalence of helminth disease in industrialized nations.13,14 However, zoonotic infections remain a problem in these regions, and in some parts of the United States more than 40% of sampled cats and dogs harbored species such as A braziliense.15

Clinical Manifestation

Initial hookworm infection often goes unnoticed because symptoms can range in severity, but it is characterized by transient ground itch—a local pruritic, erythematous, and papular eruption that develops in response to epidermal penetration.16 Because the larvae must traverse the host from skin to target organs for reproduction over several weeks, iron-deficiency anemia will manifest much later than signs of the initial penetration. In the case of incidental infection from zoonotic Ancylostomatidae organisms, the misguided larvae result in CLM, an often intensely pruritic skin condition that will self-resolve in 2 to 8 weeks with eventual death of the larvae.5

Diagnosis and Pathology of Disease

Zoonotic Hookworm—The major presenting sign of zoonotic hookworm infection is CLM. The diagnosis of CLM usually is made clinically, as the larvae themselves are 0.5 mm thick to 10 mm long (Figure 1) and usually extend several centimeters beyond the dermal lesion, with dermoscopy having limited utility.17 Patients may begin to experience itching as little as 1 hour after hookworm penetration of the skin.18 Once in contact with the skin, the hookworms’ hyaluronidases and proteases are capable of breaking through the epidermis, but zoonotic hookworms typically are unable to penetrate the basal layer of the human epidermis and remain entombed between the stratum granulosum and stratum corneum. With the exception of rare cases of direct or indirect pulmonary involvement resulting in Löffler syndrome,19 the larvae will die within weeks to months, and symptoms will subsequently resolve.

FIGURE 1. Microscopic image of hookworm larvae.
FIGURE 1. Microscopic image of hookworm larvae.

Although the infection generally is self-limiting, the dermatologic manifestations of CLM can be severe and warrant intervention. The lesions start as small reddish papules at the site of penetration (Figure 2), then the hallmark elevated, migrating, serpiginous, urticarial rash develops (Figure 3). Cutaneous larva migrans generally manifests unilaterally and is both erythematous and intensely pruritic. As the larvae migrate, they leave behind 1- to 5-cm tunneled creeping eruptions in their wake. The lesions, which can manifest with pain or be painless, may develop eczematous, bullous, follicular, or impetiginized appearances.20 Atypical manifestations include folliculitis and urticarial plaques.17

FIGURE 2. Papule from penetration of a hookworm with developing cutaneous larval migrans on the palm.
FIGURE 2. Papule from penetration of a hookworm with developing
cutaneous larval migrans on the palm.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.

Anthropophilic Hookworm—The lifecycles of N americanus and A duodenale are completed in human infection. Dermatologic manifestations are transient with the development of ground itch at the site of epidermal penetration. The hookworms employ collagenases that allow penetration of the basal layer of the skin, and eosinophilia develops as the parasites travel from the skin to the small intestine. Once attached to the gastrointestinal lumen, blood meals and proteolytic enzymes result in iron-deficiency anemia in the host and may lead to weakness, fatigue, and low birth weights in pregnant patients. With prolonged infection or heavy parasitic burden, patients can develop hypoproteinemia, anasarca, and yellowing of the skin known as chlorosis.11 A clinical diagnosis can be made by examining patient stool samples for eggs, and definitive characterization can be made using molecular tools such as polymerase chain reaction.21,22

Common to hookworm infections is the immune reaction, which promotes inflammation with localized eosinophilia and mastocytosis.11 In a clinical biopsy specimen of gut—usually obtained through esophagogastroduodenoscopy— T-helper (Th) 2–type immune (IL-4, IL-5, IL-9 and IL-13), regulatory Th10 (IL-10 and transcription growth factor β), and some evidence of Th1 (interferon gamma and IL-2) cytokines are present, but little evidence of Th17-type immune response was found.23 It is believed that in zoonotic infections, antiparasitic IgE from basophils are somewhat successful at trapping the helminths in the epidermis, but in the anthropophilic species, IgE and Th2 responses are ineffective at clearing the parasite from the gut, and the defeated immune system transitions to a host-tolerance approach of limiting infection.11 It is now believed that this natural armistice can be manipulated into a potential therapy against autoimmune and inflammatory conditions. Intentional infection with zoonotic whipworm or hookworm has been proposed as a mechanism of switching Th1 and Th2 responses to host-tolerant mechanisms in conditions such as Crohn disease and celiac disease,24 and it has even been hypothesized that prior hookworm infection may reduce the chance of developing allergic conditions such as eczema.25

Treatment and Prevention

The World Health Organization and Centers for Disease Control and Prevention recommend a single oral dose of 400 mg albendazole for adults or 10 to 15 mg/kg in children for CLM. A single dose of ivermectin at 12 mg in adults or 150 μg/kg in children can be used as an alternative where albendazole is not available.11 Topical applications of thiabendazole 10% to 15% under occlusion or 3 times daily for 15 days without occlusion also can manage CLM, and pruritus can be treated with topical corticosteroids for symptomatic relief. Oral albendazole 400 mg twice daily or mebendazole 100 mg twice daily for 3 days or a single 500-mg dose, as well as 11 mg/kg (up to a maximum of 1 g) oral pyrantel pamoate once daily for 3 days can be used to treat intestinal hookworm infection, though it should be avoided in pregnancy. Iron deficiency should be managed with supplementation.11

Prevention of hookworm infection is focused around 2 broad public health efforts: mass drug administration programs and the water, sanitation, and hygiene program. In mass drug administration, treatments such as benzimidazoles are given in mass to communities affected by endemic hookworm as a single dose to reduce the burden of disease. Together, these strategies effectively eliminated hookworms in many developed nations, but areas of resurgence are beginning to surface worldwide. With changes in climate, emerging drug resistance, and socioeconomic disparities, particularly affecting the southeast, a resurgence of hookworm has occurred in the United States.26 One recent study demonstrated that almost one-third (19/55) of children sampled in an impoverished area of rural Alabama had hookworm eggs in their stool.27 Furthermore, pets serve not only as zoonotic reservoirs for CLM recurrence but also as vehicles for the evolution of drug-resistant strains, leading some to call for a ban of animals from beaches and playgrounds as well as tightly controlled veterinary programs.5,28 Ubiquitous benzimidazole use in livestock has led to bendazole-resistant strains, and it is likely that with continued and poorly adherent drug use, more zoonotic and anthropophilic drug-resistant strains of hookworm will emerge.29,30

Conclusion

The burden of hookworm infection and CLM is substantial in parts of the United States. Dermatologists play a critical role in the recognition and management of hookworm infection for both treatment of affected patients and the subsequent prevention of its spread. As drug-resistant strains evolve, clinicians, public health officials, and scientists need to continue to work together to prevent and treat hookworm infection.

References
  1. Vos T, Abajobir AA, Abate KH, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390:1211-1259.
  2. Bartsch SM, Hotez PJ, Asti L, et al. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;10:E0004922.
  3. Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Int J Parasitol Parasites Wildl. 2017;6:177-194.
  4. Adams BJ, Peat SM, Dillman AR. Phylogeny and evolution. In: Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts. Brill; 2010:693-733.
  5. Heukelbach J, Feldmeier H. Epidemiological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis. 2008;8:302-309.
  6. Haas W, Haberl B, Idris I, et al. Infective larvae of the human hookworms Necator americanus and Ancylostoma duodenale differ in their orientation behaviour when crawling on surfaces. Parasitol Res. 2005;95:25-29.
  7. Hotez P, Narasimhan S, Haggerty J, et al. Hyaluronidase from infective Ancylostoma hookworm larvae and its possible function as a virulence factor in tissue invasion and in cutaneous larva migrans. Infect Immun. 1992;60:1018-1023.
  8. Brooker S, Bethony J, Hotez PJ. Human hookworm infection in the 21st century. Adv Parasitol. 2004;58:197-288.
  9. Hoagland K, Schad G. Necator americanus and Ancylostoma duodenale: life history parameters and epidemiological implications of two sympatric hookworms of humans. Exp Parasitol. 1978;44:36-49.
  10. Clements ACA, Alene KA. Global distribution of human hookworm species and differences in their morbidity effects: a systematic review. Lancet Microbe. 2022;3:E72-E79.
  11. Loukas A, Hotez PJ, Diemert D, et al. Hookworm infection. Nat Rev Dis Primers. 2016;2:1-18.
  12. Gazzinelli A, Correa-Oliveira R, Yang GJ, et al. A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLoS Negl Trop Dis. 2012;6:E1603.
  13. Starr MC, Montgomery SP. Soil-transmitted helminthiasis in the United States: a systematic review—1940-2010. Am J Trop Med Hyg. 2011;85:680-684.
  14. Strunz EC, Addiss DG, Stocks ME, et al. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and metaanalysis. PLoS Med. 2014;11:E1001620.
  15. Liotta JL, Youn H, Aksel S, et al. Prevalence of Ancylostoma braziliense in dogs from Alachua and Marion Counties, Florida, United States. J Parasitol. 2012;98:1039-1040.
  16. Hotez PJ, Brooker S, Bethony JM, et al. Hookworm infection. N Engl J Med. 2004;351:799-807.
  17. Prickett KA, Ferringer TC. What’s eating you? cutaneous larva migrans. Cutis. 2015;95:126-128.
  18. Feldmeier H, Schuster A. Mini review: hookworm-related cutaneous larva migrans. Eur J Clin Microbiol Infect Dis. 2012;31:915-918.
  19. Tan SK, Liu TT. Cutaneous larva migrans complicated by Löffler syndrome. Arch Dermatol. 2010;146:210-212.
  20. Eksomtramage T, Aiempanakit K. Bullous and pustular cutaneous larva migrans: two case reports and a literature review. IDCases. 2018;12:130-132.
  21. Utzinger J, Rinaldi L, Lohourignon LK, et al. FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg. 2008;102:84-90.
  22. Chidambaram M, Parija SC, Toi PC, et al. Evaluation of the utility of conventional polymerase chain reaction for detection and species differentiation in human hookworm infections. Trop Parasitol. 2017;7:111-116.
  23. Gaze S, McSorley HJ, Daveson J, et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 2012;8:E1002520.
  24. Croese J, O’Neil J, Masson J, et al. A proof of concept study establishing Necator americanus in Crohn’s patients and reservoir donors. Gut. 2006;55:136-137.
  25. Mpairwe H, Amoah AS. Parasites and allergy: observations from Africa. Parasite Immunol. 2019;41:E12589.
  26. Albonico M, Savioli L. Hookworm: a neglected resurgent infection. Editorial. BMJ. 2017;359:j4813.
  27. McKenna ML, McAtee S, Bryan PE, et al. Human intestinal parasite burden and poor sanitation in rural Alabama. Am J Trop Med Hyg. 2017;97:1623-1628.
  28. Traversa D. Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors. 2012;5:1-19.
  29. Geerts S, Gryseels B. Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev. 2000;13:207-222.
  30. Jimenez Castro PD, Howell SB, Schaefer JJ, et al. Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? Parasit Vectors. 2019;12:1-15.
Author and Disclosure Information

Dr. Bloomquist is from the School of Medicine, University of South Carolina, Columbia. Dr. Elston is from the Department of Dermatology & Dermatologic Surgery, Medical University of South Carolina, Charleston.

The authors have no relevant financial disclosures to report. 

Correspondence: Ryan F. Bloomquist, PhD, DMD, MBA, School of Medicine, University of South Carolina, Columbia, SC (ryan.bloomquist@uscmed.sc.edu).

Cutis. 2024 November;14(5):E12-E15. doi:10.12788/cutis.1136

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Author and Disclosure Information

Dr. Bloomquist is from the School of Medicine, University of South Carolina, Columbia. Dr. Elston is from the Department of Dermatology & Dermatologic Surgery, Medical University of South Carolina, Charleston.

The authors have no relevant financial disclosures to report. 

Correspondence: Ryan F. Bloomquist, PhD, DMD, MBA, School of Medicine, University of South Carolina, Columbia, SC (ryan.bloomquist@uscmed.sc.edu).

Cutis. 2024 November;14(5):E12-E15. doi:10.12788/cutis.1136

Author and Disclosure Information

Dr. Bloomquist is from the School of Medicine, University of South Carolina, Columbia. Dr. Elston is from the Department of Dermatology & Dermatologic Surgery, Medical University of South Carolina, Charleston.

The authors have no relevant financial disclosures to report. 

Correspondence: Ryan F. Bloomquist, PhD, DMD, MBA, School of Medicine, University of South Carolina, Columbia, SC (ryan.bloomquist@uscmed.sc.edu).

Cutis. 2024 November;14(5):E12-E15. doi:10.12788/cutis.1136

It is estimated that the prevalence of human hookworm infection is approximately 450 million individuals worldwide, representing a substantial global disease burden.1 The annual global public health burden ranges from approximately 2 million to 4 million disability-adjusted life-years and $10 billion to $140 billion in hookwormrelated costs.2 In this article, we discuss the lifecycle, transmission, and disease burden of cutaneous larva migrans (CLM) as well as prevention and treatment strategies.

Background

The Ancylostomatidae nematode family comprises at least 68 known species of hookworm that infect more than 110 different species of mammals.3 Many of these parasites are able to infect more than 1 primary host species, but from a disease perspective they can be classified as either anthropophilic, with humans as the intended host, or zoonotic, with humans as an incidental host. It is important to make this distinction because, though the lifecycles and biology of hookworm species generally are similar, the manifestations of incidental human infection from zoonotic hookworms are different from those of anthropophilic hookworms. Of the anthropophilic species, Necator americanus and Ancylostoma duodenale predominate. In the instance of zoonotic hookworm, dog-infecting A caninum and cat- and doginfecting A braziliense and Uncinaria stenocephala are common causes of incidental human disease.3

The life cycle of Ancylostomatidae organisms is astounding. Through millions of years of co-evolution with mammals,4 these parasitic worms have developed perhaps one of the most circuitous paths to propagate themselves in the natural world. Hookworms start their arduous journey as eggs deposited in soil, sand, and ground vegetation from the feces of infected animals.5 Approximately 1 day after the eggs are deposited, they hatch and begin the larval stage, during which they become infective 1 to 5 weeks later. At this point, the larvae become sensitive to their environment, responding to rising temperatures, increasing carbon dioxide levels, and vibrations in the soil—all of which suggest the presence of a potential host and contribute to a concordant increase in undulatory movement of the larvae.5,6 Here, the most vulnerable tissues include the uncovered soles, palms, and buttocks of host mammals that come into contact with contaminated soil. In an undulating fashion and guided by temperature cues, the larvae locate the skin of the host and utilize a mixture of enzymes including hyaluronidases, metalloprotease, and other proteases to penetrate the epidermis.7 Anthropophilic hookworms such as N americanus and A duodenale will enter the circulatory system; from there, the hookworms migrate through the right-sided cardiopulmonary circuit and eventually ascend into the pulmonary vasculature.8 They then penetrate the lung capillary beds and parenchyma to reach the alveoli, ascend the respiratory tree, and, with the help of the mucociliary escalator, reach the esophagus, where they are swallowed by the host. In the gastrointestinal tract, adult hookworms consume host blood, mate, and lay eggs over a period of approximately 1 to 3 years if left untreated.9 Eggs are laid into the lower gastrointestinal tract, and the journey begins again in feces contacting ground or soil.

Geographic Distribution

Hookworms are found in almost all regions of the world, with species-specific distributions that highlight tropical and subtropical regions. Necator americanus and A duodenale are the most common hookworm species, with the former found predominantly in Southeast Asia and Latin America and the latter in Asia-Pacific regions.10 The highest prevalence of hookworms is in Southeast Asia followed by Sub-Saharan Africa, and the unique climate and soil composition of a region help determine the best environments for specific species of hookworm to thrive.11 In addition, socioeconomics and social determinants of health play a big role in the spread of hookworms, as hygiene practices (eg, wearing clean shoes and clothing, bathing), infrastructure (eg, clean water and streets), and anthelmintic campaigns help reduce transmission.12 Soil-transmitted helminths were once endemic to the southeastern United States, with some reports of approximately 40% of individuals infected in the south in the early 1900s.13 Anthelmintic campaigns such as water, sanitation, and hygiene programs as well as deworming of humans and livestock have proven effective in reducing the prevalence of helminth disease in industrialized nations.13,14 However, zoonotic infections remain a problem in these regions, and in some parts of the United States more than 40% of sampled cats and dogs harbored species such as A braziliense.15

Clinical Manifestation

Initial hookworm infection often goes unnoticed because symptoms can range in severity, but it is characterized by transient ground itch—a local pruritic, erythematous, and papular eruption that develops in response to epidermal penetration.16 Because the larvae must traverse the host from skin to target organs for reproduction over several weeks, iron-deficiency anemia will manifest much later than signs of the initial penetration. In the case of incidental infection from zoonotic Ancylostomatidae organisms, the misguided larvae result in CLM, an often intensely pruritic skin condition that will self-resolve in 2 to 8 weeks with eventual death of the larvae.5

Diagnosis and Pathology of Disease

Zoonotic Hookworm—The major presenting sign of zoonotic hookworm infection is CLM. The diagnosis of CLM usually is made clinically, as the larvae themselves are 0.5 mm thick to 10 mm long (Figure 1) and usually extend several centimeters beyond the dermal lesion, with dermoscopy having limited utility.17 Patients may begin to experience itching as little as 1 hour after hookworm penetration of the skin.18 Once in contact with the skin, the hookworms’ hyaluronidases and proteases are capable of breaking through the epidermis, but zoonotic hookworms typically are unable to penetrate the basal layer of the human epidermis and remain entombed between the stratum granulosum and stratum corneum. With the exception of rare cases of direct or indirect pulmonary involvement resulting in Löffler syndrome,19 the larvae will die within weeks to months, and symptoms will subsequently resolve.

FIGURE 1. Microscopic image of hookworm larvae.
FIGURE 1. Microscopic image of hookworm larvae.

Although the infection generally is self-limiting, the dermatologic manifestations of CLM can be severe and warrant intervention. The lesions start as small reddish papules at the site of penetration (Figure 2), then the hallmark elevated, migrating, serpiginous, urticarial rash develops (Figure 3). Cutaneous larva migrans generally manifests unilaterally and is both erythematous and intensely pruritic. As the larvae migrate, they leave behind 1- to 5-cm tunneled creeping eruptions in their wake. The lesions, which can manifest with pain or be painless, may develop eczematous, bullous, follicular, or impetiginized appearances.20 Atypical manifestations include folliculitis and urticarial plaques.17

FIGURE 2. Papule from penetration of a hookworm with developing cutaneous larval migrans on the palm.
FIGURE 2. Papule from penetration of a hookworm with developing
cutaneous larval migrans on the palm.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.

Anthropophilic Hookworm—The lifecycles of N americanus and A duodenale are completed in human infection. Dermatologic manifestations are transient with the development of ground itch at the site of epidermal penetration. The hookworms employ collagenases that allow penetration of the basal layer of the skin, and eosinophilia develops as the parasites travel from the skin to the small intestine. Once attached to the gastrointestinal lumen, blood meals and proteolytic enzymes result in iron-deficiency anemia in the host and may lead to weakness, fatigue, and low birth weights in pregnant patients. With prolonged infection or heavy parasitic burden, patients can develop hypoproteinemia, anasarca, and yellowing of the skin known as chlorosis.11 A clinical diagnosis can be made by examining patient stool samples for eggs, and definitive characterization can be made using molecular tools such as polymerase chain reaction.21,22

Common to hookworm infections is the immune reaction, which promotes inflammation with localized eosinophilia and mastocytosis.11 In a clinical biopsy specimen of gut—usually obtained through esophagogastroduodenoscopy— T-helper (Th) 2–type immune (IL-4, IL-5, IL-9 and IL-13), regulatory Th10 (IL-10 and transcription growth factor β), and some evidence of Th1 (interferon gamma and IL-2) cytokines are present, but little evidence of Th17-type immune response was found.23 It is believed that in zoonotic infections, antiparasitic IgE from basophils are somewhat successful at trapping the helminths in the epidermis, but in the anthropophilic species, IgE and Th2 responses are ineffective at clearing the parasite from the gut, and the defeated immune system transitions to a host-tolerance approach of limiting infection.11 It is now believed that this natural armistice can be manipulated into a potential therapy against autoimmune and inflammatory conditions. Intentional infection with zoonotic whipworm or hookworm has been proposed as a mechanism of switching Th1 and Th2 responses to host-tolerant mechanisms in conditions such as Crohn disease and celiac disease,24 and it has even been hypothesized that prior hookworm infection may reduce the chance of developing allergic conditions such as eczema.25

Treatment and Prevention

The World Health Organization and Centers for Disease Control and Prevention recommend a single oral dose of 400 mg albendazole for adults or 10 to 15 mg/kg in children for CLM. A single dose of ivermectin at 12 mg in adults or 150 μg/kg in children can be used as an alternative where albendazole is not available.11 Topical applications of thiabendazole 10% to 15% under occlusion or 3 times daily for 15 days without occlusion also can manage CLM, and pruritus can be treated with topical corticosteroids for symptomatic relief. Oral albendazole 400 mg twice daily or mebendazole 100 mg twice daily for 3 days or a single 500-mg dose, as well as 11 mg/kg (up to a maximum of 1 g) oral pyrantel pamoate once daily for 3 days can be used to treat intestinal hookworm infection, though it should be avoided in pregnancy. Iron deficiency should be managed with supplementation.11

Prevention of hookworm infection is focused around 2 broad public health efforts: mass drug administration programs and the water, sanitation, and hygiene program. In mass drug administration, treatments such as benzimidazoles are given in mass to communities affected by endemic hookworm as a single dose to reduce the burden of disease. Together, these strategies effectively eliminated hookworms in many developed nations, but areas of resurgence are beginning to surface worldwide. With changes in climate, emerging drug resistance, and socioeconomic disparities, particularly affecting the southeast, a resurgence of hookworm has occurred in the United States.26 One recent study demonstrated that almost one-third (19/55) of children sampled in an impoverished area of rural Alabama had hookworm eggs in their stool.27 Furthermore, pets serve not only as zoonotic reservoirs for CLM recurrence but also as vehicles for the evolution of drug-resistant strains, leading some to call for a ban of animals from beaches and playgrounds as well as tightly controlled veterinary programs.5,28 Ubiquitous benzimidazole use in livestock has led to bendazole-resistant strains, and it is likely that with continued and poorly adherent drug use, more zoonotic and anthropophilic drug-resistant strains of hookworm will emerge.29,30

Conclusion

The burden of hookworm infection and CLM is substantial in parts of the United States. Dermatologists play a critical role in the recognition and management of hookworm infection for both treatment of affected patients and the subsequent prevention of its spread. As drug-resistant strains evolve, clinicians, public health officials, and scientists need to continue to work together to prevent and treat hookworm infection.

It is estimated that the prevalence of human hookworm infection is approximately 450 million individuals worldwide, representing a substantial global disease burden.1 The annual global public health burden ranges from approximately 2 million to 4 million disability-adjusted life-years and $10 billion to $140 billion in hookwormrelated costs.2 In this article, we discuss the lifecycle, transmission, and disease burden of cutaneous larva migrans (CLM) as well as prevention and treatment strategies.

Background

The Ancylostomatidae nematode family comprises at least 68 known species of hookworm that infect more than 110 different species of mammals.3 Many of these parasites are able to infect more than 1 primary host species, but from a disease perspective they can be classified as either anthropophilic, with humans as the intended host, or zoonotic, with humans as an incidental host. It is important to make this distinction because, though the lifecycles and biology of hookworm species generally are similar, the manifestations of incidental human infection from zoonotic hookworms are different from those of anthropophilic hookworms. Of the anthropophilic species, Necator americanus and Ancylostoma duodenale predominate. In the instance of zoonotic hookworm, dog-infecting A caninum and cat- and doginfecting A braziliense and Uncinaria stenocephala are common causes of incidental human disease.3

The life cycle of Ancylostomatidae organisms is astounding. Through millions of years of co-evolution with mammals,4 these parasitic worms have developed perhaps one of the most circuitous paths to propagate themselves in the natural world. Hookworms start their arduous journey as eggs deposited in soil, sand, and ground vegetation from the feces of infected animals.5 Approximately 1 day after the eggs are deposited, they hatch and begin the larval stage, during which they become infective 1 to 5 weeks later. At this point, the larvae become sensitive to their environment, responding to rising temperatures, increasing carbon dioxide levels, and vibrations in the soil—all of which suggest the presence of a potential host and contribute to a concordant increase in undulatory movement of the larvae.5,6 Here, the most vulnerable tissues include the uncovered soles, palms, and buttocks of host mammals that come into contact with contaminated soil. In an undulating fashion and guided by temperature cues, the larvae locate the skin of the host and utilize a mixture of enzymes including hyaluronidases, metalloprotease, and other proteases to penetrate the epidermis.7 Anthropophilic hookworms such as N americanus and A duodenale will enter the circulatory system; from there, the hookworms migrate through the right-sided cardiopulmonary circuit and eventually ascend into the pulmonary vasculature.8 They then penetrate the lung capillary beds and parenchyma to reach the alveoli, ascend the respiratory tree, and, with the help of the mucociliary escalator, reach the esophagus, where they are swallowed by the host. In the gastrointestinal tract, adult hookworms consume host blood, mate, and lay eggs over a period of approximately 1 to 3 years if left untreated.9 Eggs are laid into the lower gastrointestinal tract, and the journey begins again in feces contacting ground or soil.

Geographic Distribution

Hookworms are found in almost all regions of the world, with species-specific distributions that highlight tropical and subtropical regions. Necator americanus and A duodenale are the most common hookworm species, with the former found predominantly in Southeast Asia and Latin America and the latter in Asia-Pacific regions.10 The highest prevalence of hookworms is in Southeast Asia followed by Sub-Saharan Africa, and the unique climate and soil composition of a region help determine the best environments for specific species of hookworm to thrive.11 In addition, socioeconomics and social determinants of health play a big role in the spread of hookworms, as hygiene practices (eg, wearing clean shoes and clothing, bathing), infrastructure (eg, clean water and streets), and anthelmintic campaigns help reduce transmission.12 Soil-transmitted helminths were once endemic to the southeastern United States, with some reports of approximately 40% of individuals infected in the south in the early 1900s.13 Anthelmintic campaigns such as water, sanitation, and hygiene programs as well as deworming of humans and livestock have proven effective in reducing the prevalence of helminth disease in industrialized nations.13,14 However, zoonotic infections remain a problem in these regions, and in some parts of the United States more than 40% of sampled cats and dogs harbored species such as A braziliense.15

Clinical Manifestation

Initial hookworm infection often goes unnoticed because symptoms can range in severity, but it is characterized by transient ground itch—a local pruritic, erythematous, and papular eruption that develops in response to epidermal penetration.16 Because the larvae must traverse the host from skin to target organs for reproduction over several weeks, iron-deficiency anemia will manifest much later than signs of the initial penetration. In the case of incidental infection from zoonotic Ancylostomatidae organisms, the misguided larvae result in CLM, an often intensely pruritic skin condition that will self-resolve in 2 to 8 weeks with eventual death of the larvae.5

Diagnosis and Pathology of Disease

Zoonotic Hookworm—The major presenting sign of zoonotic hookworm infection is CLM. The diagnosis of CLM usually is made clinically, as the larvae themselves are 0.5 mm thick to 10 mm long (Figure 1) and usually extend several centimeters beyond the dermal lesion, with dermoscopy having limited utility.17 Patients may begin to experience itching as little as 1 hour after hookworm penetration of the skin.18 Once in contact with the skin, the hookworms’ hyaluronidases and proteases are capable of breaking through the epidermis, but zoonotic hookworms typically are unable to penetrate the basal layer of the human epidermis and remain entombed between the stratum granulosum and stratum corneum. With the exception of rare cases of direct or indirect pulmonary involvement resulting in Löffler syndrome,19 the larvae will die within weeks to months, and symptoms will subsequently resolve.

FIGURE 1. Microscopic image of hookworm larvae.
FIGURE 1. Microscopic image of hookworm larvae.

Although the infection generally is self-limiting, the dermatologic manifestations of CLM can be severe and warrant intervention. The lesions start as small reddish papules at the site of penetration (Figure 2), then the hallmark elevated, migrating, serpiginous, urticarial rash develops (Figure 3). Cutaneous larva migrans generally manifests unilaterally and is both erythematous and intensely pruritic. As the larvae migrate, they leave behind 1- to 5-cm tunneled creeping eruptions in their wake. The lesions, which can manifest with pain or be painless, may develop eczematous, bullous, follicular, or impetiginized appearances.20 Atypical manifestations include folliculitis and urticarial plaques.17

FIGURE 2. Papule from penetration of a hookworm with developing cutaneous larval migrans on the palm.
FIGURE 2. Papule from penetration of a hookworm with developing
cutaneous larval migrans on the palm.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.
FIGURE 3. Developed serpiginous rash of cutaneous larval migrans.

Anthropophilic Hookworm—The lifecycles of N americanus and A duodenale are completed in human infection. Dermatologic manifestations are transient with the development of ground itch at the site of epidermal penetration. The hookworms employ collagenases that allow penetration of the basal layer of the skin, and eosinophilia develops as the parasites travel from the skin to the small intestine. Once attached to the gastrointestinal lumen, blood meals and proteolytic enzymes result in iron-deficiency anemia in the host and may lead to weakness, fatigue, and low birth weights in pregnant patients. With prolonged infection or heavy parasitic burden, patients can develop hypoproteinemia, anasarca, and yellowing of the skin known as chlorosis.11 A clinical diagnosis can be made by examining patient stool samples for eggs, and definitive characterization can be made using molecular tools such as polymerase chain reaction.21,22

Common to hookworm infections is the immune reaction, which promotes inflammation with localized eosinophilia and mastocytosis.11 In a clinical biopsy specimen of gut—usually obtained through esophagogastroduodenoscopy— T-helper (Th) 2–type immune (IL-4, IL-5, IL-9 and IL-13), regulatory Th10 (IL-10 and transcription growth factor β), and some evidence of Th1 (interferon gamma and IL-2) cytokines are present, but little evidence of Th17-type immune response was found.23 It is believed that in zoonotic infections, antiparasitic IgE from basophils are somewhat successful at trapping the helminths in the epidermis, but in the anthropophilic species, IgE and Th2 responses are ineffective at clearing the parasite from the gut, and the defeated immune system transitions to a host-tolerance approach of limiting infection.11 It is now believed that this natural armistice can be manipulated into a potential therapy against autoimmune and inflammatory conditions. Intentional infection with zoonotic whipworm or hookworm has been proposed as a mechanism of switching Th1 and Th2 responses to host-tolerant mechanisms in conditions such as Crohn disease and celiac disease,24 and it has even been hypothesized that prior hookworm infection may reduce the chance of developing allergic conditions such as eczema.25

Treatment and Prevention

The World Health Organization and Centers for Disease Control and Prevention recommend a single oral dose of 400 mg albendazole for adults or 10 to 15 mg/kg in children for CLM. A single dose of ivermectin at 12 mg in adults or 150 μg/kg in children can be used as an alternative where albendazole is not available.11 Topical applications of thiabendazole 10% to 15% under occlusion or 3 times daily for 15 days without occlusion also can manage CLM, and pruritus can be treated with topical corticosteroids for symptomatic relief. Oral albendazole 400 mg twice daily or mebendazole 100 mg twice daily for 3 days or a single 500-mg dose, as well as 11 mg/kg (up to a maximum of 1 g) oral pyrantel pamoate once daily for 3 days can be used to treat intestinal hookworm infection, though it should be avoided in pregnancy. Iron deficiency should be managed with supplementation.11

Prevention of hookworm infection is focused around 2 broad public health efforts: mass drug administration programs and the water, sanitation, and hygiene program. In mass drug administration, treatments such as benzimidazoles are given in mass to communities affected by endemic hookworm as a single dose to reduce the burden of disease. Together, these strategies effectively eliminated hookworms in many developed nations, but areas of resurgence are beginning to surface worldwide. With changes in climate, emerging drug resistance, and socioeconomic disparities, particularly affecting the southeast, a resurgence of hookworm has occurred in the United States.26 One recent study demonstrated that almost one-third (19/55) of children sampled in an impoverished area of rural Alabama had hookworm eggs in their stool.27 Furthermore, pets serve not only as zoonotic reservoirs for CLM recurrence but also as vehicles for the evolution of drug-resistant strains, leading some to call for a ban of animals from beaches and playgrounds as well as tightly controlled veterinary programs.5,28 Ubiquitous benzimidazole use in livestock has led to bendazole-resistant strains, and it is likely that with continued and poorly adherent drug use, more zoonotic and anthropophilic drug-resistant strains of hookworm will emerge.29,30

Conclusion

The burden of hookworm infection and CLM is substantial in parts of the United States. Dermatologists play a critical role in the recognition and management of hookworm infection for both treatment of affected patients and the subsequent prevention of its spread. As drug-resistant strains evolve, clinicians, public health officials, and scientists need to continue to work together to prevent and treat hookworm infection.

References
  1. Vos T, Abajobir AA, Abate KH, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390:1211-1259.
  2. Bartsch SM, Hotez PJ, Asti L, et al. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;10:E0004922.
  3. Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Int J Parasitol Parasites Wildl. 2017;6:177-194.
  4. Adams BJ, Peat SM, Dillman AR. Phylogeny and evolution. In: Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts. Brill; 2010:693-733.
  5. Heukelbach J, Feldmeier H. Epidemiological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis. 2008;8:302-309.
  6. Haas W, Haberl B, Idris I, et al. Infective larvae of the human hookworms Necator americanus and Ancylostoma duodenale differ in their orientation behaviour when crawling on surfaces. Parasitol Res. 2005;95:25-29.
  7. Hotez P, Narasimhan S, Haggerty J, et al. Hyaluronidase from infective Ancylostoma hookworm larvae and its possible function as a virulence factor in tissue invasion and in cutaneous larva migrans. Infect Immun. 1992;60:1018-1023.
  8. Brooker S, Bethony J, Hotez PJ. Human hookworm infection in the 21st century. Adv Parasitol. 2004;58:197-288.
  9. Hoagland K, Schad G. Necator americanus and Ancylostoma duodenale: life history parameters and epidemiological implications of two sympatric hookworms of humans. Exp Parasitol. 1978;44:36-49.
  10. Clements ACA, Alene KA. Global distribution of human hookworm species and differences in their morbidity effects: a systematic review. Lancet Microbe. 2022;3:E72-E79.
  11. Loukas A, Hotez PJ, Diemert D, et al. Hookworm infection. Nat Rev Dis Primers. 2016;2:1-18.
  12. Gazzinelli A, Correa-Oliveira R, Yang GJ, et al. A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLoS Negl Trop Dis. 2012;6:E1603.
  13. Starr MC, Montgomery SP. Soil-transmitted helminthiasis in the United States: a systematic review—1940-2010. Am J Trop Med Hyg. 2011;85:680-684.
  14. Strunz EC, Addiss DG, Stocks ME, et al. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and metaanalysis. PLoS Med. 2014;11:E1001620.
  15. Liotta JL, Youn H, Aksel S, et al. Prevalence of Ancylostoma braziliense in dogs from Alachua and Marion Counties, Florida, United States. J Parasitol. 2012;98:1039-1040.
  16. Hotez PJ, Brooker S, Bethony JM, et al. Hookworm infection. N Engl J Med. 2004;351:799-807.
  17. Prickett KA, Ferringer TC. What’s eating you? cutaneous larva migrans. Cutis. 2015;95:126-128.
  18. Feldmeier H, Schuster A. Mini review: hookworm-related cutaneous larva migrans. Eur J Clin Microbiol Infect Dis. 2012;31:915-918.
  19. Tan SK, Liu TT. Cutaneous larva migrans complicated by Löffler syndrome. Arch Dermatol. 2010;146:210-212.
  20. Eksomtramage T, Aiempanakit K. Bullous and pustular cutaneous larva migrans: two case reports and a literature review. IDCases. 2018;12:130-132.
  21. Utzinger J, Rinaldi L, Lohourignon LK, et al. FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg. 2008;102:84-90.
  22. Chidambaram M, Parija SC, Toi PC, et al. Evaluation of the utility of conventional polymerase chain reaction for detection and species differentiation in human hookworm infections. Trop Parasitol. 2017;7:111-116.
  23. Gaze S, McSorley HJ, Daveson J, et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 2012;8:E1002520.
  24. Croese J, O’Neil J, Masson J, et al. A proof of concept study establishing Necator americanus in Crohn’s patients and reservoir donors. Gut. 2006;55:136-137.
  25. Mpairwe H, Amoah AS. Parasites and allergy: observations from Africa. Parasite Immunol. 2019;41:E12589.
  26. Albonico M, Savioli L. Hookworm: a neglected resurgent infection. Editorial. BMJ. 2017;359:j4813.
  27. McKenna ML, McAtee S, Bryan PE, et al. Human intestinal parasite burden and poor sanitation in rural Alabama. Am J Trop Med Hyg. 2017;97:1623-1628.
  28. Traversa D. Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors. 2012;5:1-19.
  29. Geerts S, Gryseels B. Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev. 2000;13:207-222.
  30. Jimenez Castro PD, Howell SB, Schaefer JJ, et al. Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? Parasit Vectors. 2019;12:1-15.
References
  1. Vos T, Abajobir AA, Abate KH, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390:1211-1259.
  2. Bartsch SM, Hotez PJ, Asti L, et al. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;10:E0004922.
  3. Seguel M, Gottdenker N. The diversity and impact of hookworm infections in wildlife. Int J Parasitol Parasites Wildl. 2017;6:177-194.
  4. Adams BJ, Peat SM, Dillman AR. Phylogeny and evolution. In: Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts. Brill; 2010:693-733.
  5. Heukelbach J, Feldmeier H. Epidemiological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis. 2008;8:302-309.
  6. Haas W, Haberl B, Idris I, et al. Infective larvae of the human hookworms Necator americanus and Ancylostoma duodenale differ in their orientation behaviour when crawling on surfaces. Parasitol Res. 2005;95:25-29.
  7. Hotez P, Narasimhan S, Haggerty J, et al. Hyaluronidase from infective Ancylostoma hookworm larvae and its possible function as a virulence factor in tissue invasion and in cutaneous larva migrans. Infect Immun. 1992;60:1018-1023.
  8. Brooker S, Bethony J, Hotez PJ. Human hookworm infection in the 21st century. Adv Parasitol. 2004;58:197-288.
  9. Hoagland K, Schad G. Necator americanus and Ancylostoma duodenale: life history parameters and epidemiological implications of two sympatric hookworms of humans. Exp Parasitol. 1978;44:36-49.
  10. Clements ACA, Alene KA. Global distribution of human hookworm species and differences in their morbidity effects: a systematic review. Lancet Microbe. 2022;3:E72-E79.
  11. Loukas A, Hotez PJ, Diemert D, et al. Hookworm infection. Nat Rev Dis Primers. 2016;2:1-18.
  12. Gazzinelli A, Correa-Oliveira R, Yang GJ, et al. A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLoS Negl Trop Dis. 2012;6:E1603.
  13. Starr MC, Montgomery SP. Soil-transmitted helminthiasis in the United States: a systematic review—1940-2010. Am J Trop Med Hyg. 2011;85:680-684.
  14. Strunz EC, Addiss DG, Stocks ME, et al. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and metaanalysis. PLoS Med. 2014;11:E1001620.
  15. Liotta JL, Youn H, Aksel S, et al. Prevalence of Ancylostoma braziliense in dogs from Alachua and Marion Counties, Florida, United States. J Parasitol. 2012;98:1039-1040.
  16. Hotez PJ, Brooker S, Bethony JM, et al. Hookworm infection. N Engl J Med. 2004;351:799-807.
  17. Prickett KA, Ferringer TC. What’s eating you? cutaneous larva migrans. Cutis. 2015;95:126-128.
  18. Feldmeier H, Schuster A. Mini review: hookworm-related cutaneous larva migrans. Eur J Clin Microbiol Infect Dis. 2012;31:915-918.
  19. Tan SK, Liu TT. Cutaneous larva migrans complicated by Löffler syndrome. Arch Dermatol. 2010;146:210-212.
  20. Eksomtramage T, Aiempanakit K. Bullous and pustular cutaneous larva migrans: two case reports and a literature review. IDCases. 2018;12:130-132.
  21. Utzinger J, Rinaldi L, Lohourignon LK, et al. FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg. 2008;102:84-90.
  22. Chidambaram M, Parija SC, Toi PC, et al. Evaluation of the utility of conventional polymerase chain reaction for detection and species differentiation in human hookworm infections. Trop Parasitol. 2017;7:111-116.
  23. Gaze S, McSorley HJ, Daveson J, et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 2012;8:E1002520.
  24. Croese J, O’Neil J, Masson J, et al. A proof of concept study establishing Necator americanus in Crohn’s patients and reservoir donors. Gut. 2006;55:136-137.
  25. Mpairwe H, Amoah AS. Parasites and allergy: observations from Africa. Parasite Immunol. 2019;41:E12589.
  26. Albonico M, Savioli L. Hookworm: a neglected resurgent infection. Editorial. BMJ. 2017;359:j4813.
  27. McKenna ML, McAtee S, Bryan PE, et al. Human intestinal parasite burden and poor sanitation in rural Alabama. Am J Trop Med Hyg. 2017;97:1623-1628.
  28. Traversa D. Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors. 2012;5:1-19.
  29. Geerts S, Gryseels B. Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev. 2000;13:207-222.
  30. Jimenez Castro PD, Howell SB, Schaefer JJ, et al. Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? Parasit Vectors. 2019;12:1-15.
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PRACTICE POINTS

  • Anthropophilic hookworm infection should be considered with evidence of either transient ground itch or iron-deficient anemia in individuals who go barefoot, permitting ground-to-skin transmission.
  • Zoonotic hookworm infection manifests as cutaneous larva migrans, an elevated serpiginous rash that, while usually self-resolving, can be intensely pruritic and should be treated accordingly.
  • Considered a neglected tropical disease, hookworm infection still represents an enormous global disease burden. In addition to ongoing afflicted regions, hookworms are making a resurgence in developed nations, and drug-resistant strains have evolved.
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Comparing Patient Care Models at a Local Free Clinic vs an Insurance- Based University Medical Center

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Comparing Patient Care Models at a Local Free Clinic vs an Insurance- Based University Medical Center

Approximately 25% of Americans have at least one skin condition, and 20% are estimated to develop skin cancer during their lifetime.1,2 However, 40% of the US population lives in areas underserved by dermatologists. 3 The severity and mortality of skin cancers such as melanoma and mycosis fungoides have been positively associated with minoritized race, lack of health insurance, and unstable housing status.4-6 Patients who receive health care at free clinics often are of a racial or ethnic minoritized social group, are uninsured, and/or lack stable housing; this underserved group also includes recent immigrants to the United States who have limited English proficiency (LEP).7 Only 25% of free clinics offer specialty care services such as dermatology.7,8

Of the 42 free clinics and Federally Qualified Health Centers in Pittsburgh, Pennsylvania, the Birmingham Free Clinic (BFC) is one of the few that offers specialty care services including dermatology.9 Founded in 1994, the BFC serves as a safety net for Pittsburgh’s medically underserved population, offering primary and acute care, medication access, and social services. From January 2020 to May 2022, the BFC offered 27 dermatology clinics that provided approximately 100 people with comprehensive care including full-body skin examinations, dermatologic diagnoses and treatments, minor procedures, and dermatopathology services.

In this study, we compared the BFC dermatology patient care model with that of the dermatology department at the University of Pittsburgh Medical Center (UPMC), an insurance-based tertiary referral health care system in western Pennsylvania. By analyzing the demographics, dermatologic diagnoses, and management strategies of both the BFC and UPMC, we gained an understanding of how these patient care models differ and how they can be improved to care for diverse patient populations.

Methods

A retrospective chart review of dermatology patients seen in person at the BFC and UPMC during the period from January 2020 to May 2022 was performed. The UPMC group included patients seen by 3 general dermatologists (including A.J.J.) at matched time points. Data were collected from patients’ first in-person visit during the study period. Variables of interest included patient age, sex, race, ethnicity, primary language, zip code, health insurance status, distance to clinic (estimated using Google Maps to calculate the shortest driving distance from the patient’s zip code to the clinic), history of skin cancer, dermatologic diagnoses, and management strategies. These variables were not collected for patients who cancelled or noshowed their first in-person appointments. All patient charts and notes corresponding to the date and visit of interest were accessed through the electronic medical record (EMR). Patient data were de-identified and stored in a password-protected spreadsheet. Comparisons between the BFC and UPMC patient populations were performed using X2 tests of independence, Fisher exact tests, and Mann-Whitney U tests via SPSS software (IBM). Statistical significance was set at P<.05.

Results

Patient Characteristics—Our analysis included 76 initial appointments at the BFC and 322 at UPMC (Table 1). The mean age for patients at the BFC and UPMC was 39.6 years and 47.8 years, respectively (P=.001). Males accounted for 39 (51.3%) and 112 (34.8%) of BFC and UPMC patients, respectively (P=.008); 2 (0.6%) patients from UPMC were transgender. Of the BFC and UPMC patients, 44.7% (34/76) and 0.9% (3/322) were Hispanic, respectively (P<.001). With regard to race, 52.6% (40/76) of BFC patients were White, 19.7% (15/76) were Black, 6.6% (5/76) were Asian/Pacific Islander (Chinese, 1.3% [1/76]; other Asian, 5.3% [4/76]), and 21.1% (16/76) were American Indian/other/unspecified (American Indian, 1.3% [1/76]; other, 13.2% [10/76]; unspecified, 6.6% [5/76]). At UPMC, 61.2% (197/322) of patients were White, 28.0% (90/322) were Black, 5.3% (17/322) were Asian/Pacific Islander (Chinese, 1.2% [4/322]; Indian [Asian], 1.9% [6/322]; Japanese, 0.3% [1/322]; other Asian, 1.6% [5/322]; other Asian/American Indian, 0.3% [1/322]), and 5.6% (18/322) were American Indian/other/ unspecified (American Indian, 0.3% [1/322]; other, 0.3% [1/322]; unspecified, 5.0% [16/322]). Overall, the BFC patient population was more ethnically and racially diverse than that of UPMC (P<.001).

Forty-six percent (35/76) of BFC patients and 4.3% (14/322) of UPMC patients had LEP (P<.001). Primary languages among BFC patients were 53.9% (41/76) English, 40.8% (31/76) Spanish, and 5.2% (4/76) other/ unspecified (Chinese, 1.3% [1/76]; Indonesian, 2.6% [2/76]; unspecified, 1.3% [1/76]). Primary languages among UPMC patients were 95.7% (308/322) English and 4.3% (14/322) other/unspecified (Chinese, 0.6% [2/322]; Nepali, 0.6% [2/322]; Pali, 0.3% [1/322]; Russian, 0.3% [1/322]; unspecified, 2.5% [8/322]). There were notable differences in insurance status at the BFC vs UPMC (P<.001), with more UPMC patients having private insurance (52.8% [170/322] vs 11.8% [9/76]) and more BFC patients being uninsured (52.8% [51/76] vs 1.9% [6/322]). There was no significant difference in distance to clinic between the 2 groups (P=.183). More UPMC patients had a history of skin cancer (P=.003). More patients at the BFC were no-shows for their appointments (P<.001), and UPMC patients more frequently canceled their appointments (P<.001).

Dermatologic Diagnoses—The most commonly diagnosed dermatologic conditions at the BFC were dermatitis (23.7% [18/76]), neoplasm of uncertain behavior (15.8% [12/76]), alopecia (11.8% [9/76]), and acne (10.5% [8/76]) (Table 2). The most commonly diagnosed conditions at UPMC were nevi (26.4% [85/322]), dermatitis (22.7% [73/322]), seborrheic keratosis (21.7% [70/322]), and skin cancer screening (21.4% [70/322]). Neoplasm of uncertain behavior was more common in BFC vs UPMC patients (P=.040), while UPMC patients were more frequently diagnosed with nevi (P<.001), seborrheic keratosis (P<.001), and skin cancer screening (P<.001). There was no significant difference between the incidence of skin cancer diagnoses in the BFC (1.3% [1/76]) and UPMC (0.6% [2/76]) patient populations (P=.471). Among the biopsied neoplasms, there was also no significant difference in malignant (BFC, 50.0% [5/10]; UPMC, 32.0% [8/25]) and benign (BFC, 50.0% [5/10]; UPMC, 36.0% [9/25]) neoplasms diagnosed at each clinic (P=.444).

Management Strategies—Systemic antibiotics were more frequently prescribed (P<.001) and laboratory testing/ imaging were more frequently ordered (P=.005) at the BFC vs UPMC (Table 3). Patients at the BFC also more frequently required emergency insurance (P=.036). Patients at UPMC were more frequently recommended sunscreen (P=.003) and received education about skin cancer signs by review of the ABCDEs of melanoma (P<.001), sun-protective behaviors (P=.001), and skin examination frequency (P<.001). Notes in the EMR for UPMC patients more frequently specified patient followup instructions (P<.001).

Comment

As of 2020, the city of Pittsburgh had an estimated population of nearly 303,000 based on US Census data.10 Its population is predominantly White (62.7%) followed by Black/African American (22.8%) and Asian (6.5%); 5.9% identify as 2 or more races. Approximately 3.8% identify as Hispanic or Latino. More than 11% of the Pittsburgh population aged 5 years and older speaks a language other than English as their primary language, including Spanish (2.3%), other Indo-European languages (3.9%), and Asian and Pacific Island languages (3.5%).11 More than 5% of the Pittsburgh population does not have health insurance.12

The BFC is located in Pittsburgh’s South Side area, while one of UPMC’s primary dermatology clinics is located in the Oakland district; however, most patients who seek care at these clinics live outside these areas. Our study results indicated that the BFC and UPMC serve distinct groups of people within the Pittsburgh population. The BFC patient population was younger with a higher percentage of patients who were male, Hispanic, racially diverse, and with LEP compared with the UPMC patient population. In this clinical setting, the BFC health care team engages with people from diverse backgrounds and requires greater interpreter and medical support services.

The BFC largely is supported by volunteers, UPMC, grants, and philanthropy. Dermatology clinics are staffed by paid and volunteer team members. Paid team members include 1 nurse and 1 access lead who operates the front desk and registration. Volunteer team members include 1 board-certified dermatologist from UPMC (A.J.J.), or an affiliate clinic and 1 or 2 of each of the following: UPMC dermatology residents, medical or undergraduate students from the University of Pittsburgh, AmeriCorps national service members, and student or community medical interpreters. The onsite pharmacy is run by volunteer faculty, resident, and student pharmacists from the University of Pittsburgh. Dermatology clinics are half-day clinics that occur monthly. Volunteers for each clinic are recruited approximately 1 month in advance.

Dermatology patients at the BFC are referred from the BFC general medicine clinic and nearby Federally Qualified Health Center s for simple to complex medical and surgical dermatologic skin conditions. Each BFC dermatology clinic schedules an average of 7 patients per clinic and places other patients on a wait-list unless more urgent triage is needed. Patients are notified when they are scheduled via phone or text message, and they receive a reminder call or text 1 or 2 days prior to their appointment that also asks them to confirm attendance. Patients with LEP are called with an interpreter and also may receive text reminders that can be translated using Google Translate. Patients are instructed to notify the BFC if they need to cancel or reschedule their appointment. At the end of each visit, patients are given an after-visit summary that lists follow-up instructions, medications prescribed during the visit, and upcoming appointments. The BFC offers bus tickets to help patients get to their appointments. In rare cases, the BFC may pay for a car service to drive patients to and from the clinic.

Dermatology clinics at UPMC use scheduling and self-scheduling systems through which patients can make appointments at a location of their choice with any available board-certified dermatologist or physician assistant. Patients receive a reminder phone call 3 days prior to their appointment instructing them to call the office if they are unable to keep their appointment. Patients signed up for the online portal also receive a reminder message and an option to confirm or cancel their appointment. Patients with cell phone numbers in the UPMC system receive a text message approximately 2 days prior to their appointment that allows them to preregister and pay their copayment in advance. They receive another text 20 minutes prior to their appointment with an option for contactless check-in. At the conclusion of their visit, patients can schedule a follow-up appointment and receive a printed copy of their after-visit summary that provides information about follow-up instructions, prescribed medications, and upcoming visits. They may alternatively access this summary via the online patient portal. Patients are not provided transportation to UPMC clinics, but they are offered parking validation.

Among the most common dermatologic diagnoses for each group, BFC patients presented for treatment of more acute dermatologic conditions, while UPMC patients presented for more benign and preventive-care conditions. This difference may be attributable to the BFC’s referral and triage system, wherein patients with more urgent problems are given scheduling priority. This patient care model contrasts with UPMC’s scheduling process in which no known formal triage system is utilized. Interestingly, there was no difference in skin cancer incidence despite a higher percentage of preventive skin cancer screenings at UPMC.

Patients at the BFC more often required emergency insurance for surgical interventions, which is consistent with the higher percentage of uninsured individuals in this population. Patients at UPMC more frequently were recommended sunscreen and were educated about skin cancer, sun protection, and skin examination, in part due to this group’s more extensive history of skin cancer and frequent presentation for skin cancer screenings. At the same time, educational materials for skin care at both the BFC and UPMC are populated into the EMR in English, whereas materials in other languages are less readily available.

Our retrospective study had several limitations. Demographic information that relied on clinic-dependent intake questionnaires may be limited due to variable intake processes and patients opting out of self-reporting. By comparing patient populations between 2 clinics, confounding variables such as location and hours of operation may impact the patient demographics recorded at the BFC vs UPMC. Resources and staff availability may affect the management strategies and follow-up care offered by each clinic. Our study period also was unique in that COVID-19 may have affected resources, staffing, scheduling, and logistics at both clinics.

Based on the aforementioned differences between the BFC and UPMC patient characteristics, care models should be strategically designed to support the needs of diverse populations. The BFC patient care model appropriately focuses on communication skills with patients with LEP by using interpreter services. Providing more skin care education and follow-up instructions in patients’ primary languages will help them develop a better understanding of their skin conditions. Another key asset of the BFC patient care model is its provision of social services such as transportation and insurance assistance.

To improve the UPMC patient care model, providing patients with bus tickets and car services may potentially reduce appointment cancellations. Using interpreter services to call and text appointment reminders, as well as interpreter resources to facilitate patient visits and patient instructions, also can mitigate language barriers for patients with LEP. Implementing a triage system into the UPMC scheduling system may help patients with more urgent skin conditions to be seen in a timely manner.

Other investigators have analyzed costs of care and proven the value of dermatologic services at free clinics to guide allocation of supplies and resources, demonstrating an area for future investigation at the BFC.13 A cost analysis of care provided at the BFC compared to UPMC could inform us about the value of the BFC’s services.

Conclusion

The dermatology clinics at the BFC and UPMC have distinct demographics, diagnoses, and management strategies to provide an inclusive patient care model. The services provided by both clinics are necessary to ensure that people in Pittsburgh have access to dermatologic care regardless of social barriers (eg, lack of health insurance, LEP). To achieve greater accessibility and health equity, dermatologic care at the BFC and UPMC can be improved by strengthening communication with people with LEP, providing skin care education, and offering social and scheduling services.

References
  1. Lim HW, Collins SAB, Resneck JS, et al. The burden of skin disease in the United States. J Am Acad Dermatol. 2017;76:958-972.e2. doi:10.1016/j.jaad.2016.12.043
  2. American Academy of Dermatology. Skin cancer. Accessed October 7, 2024. https://www.aad.org/media/stats-skin-cancer
  3. Suneja T, Smith ED, Chen GJ, et al. Waiting times to see a dermatologist are perceived as too long by dermatologists: implications for the dermatology workforce. Arch Dermatol. 2001;137:1303-1307. doi:10.1001/archderm.137.10.1303
  4. Grossberg AL, Carranza D, Lamp K, et al. Dermatologic care in the homeless and underserved populations: observations from the Venice Family Clinic. Cutis. 2012;89:25-32.
  5. Amini A, Rusthoven CG, Waxweiler TV, et al. Association of health insurance with outcomes in adults ages 18 to 64 years with melanoma in the United States. J Am Acad Dermatol. 2016;74:309-316. doi:10.1016/j.jaad.2015.09.054
  6. Su C, Nguyen KA, Bai HX, et al. Racial disparity in mycosis fungoides: an analysis of 4495 cases from the US National Cancer Database. J Am Acad Dermatol. 2017;77:497-502.e2. doi:10.1016/j.jaad .2017.04.1137
  7. Darnell JS. Free clinics in the United States: a nationwide survey. Arch Intern Med. 2010;170:946-953. doi:10.1001/archinternmed .2010.107
  8. Madray V, Ginjupalli S, Hashmi O, et al. Access to dermatology services at free medical clinics: a nationwide cross-sectional survey. J Am Acad Dermatol. 2019;81:245-246. doi:10.1016/j.jaad.2018.12.011
  9. Pennsylvania free and income-based clinics. Accessed October 7, 2024. https://www.freeclinics.com/sta/pennsylvania
  10. United States Census Bureau. Decennial census. P1: race. Accessed October 7, 2024. https://data.census.gov/table/DECENNIALPL2020.P1?g=160XX00US4261000
  11. United States Census Bureau. American community survey. S1601: language spoken at home. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020S1601?g=160XX00US4261000
  12. United States Census Bureau. S2701: selected characteristics of health insurance coverage in the United States. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020.S2701?g=160XX00US4261000
  13. Lin CP, Loy S, Boothe WD, et al. Value of Dermatology Nights at a student-run free clinic. Proc (Bayl Univ Med Cent). 2020;34:260-261. doi:10.1080/08998280.2020.1834771
Author and Disclosure Information

Alice J. Lin and Li Wang are from the University of Pittsburgh, Pennsylvania. Alice J. Lin is from the School of Medicine, and Li Wang is from the Clinical and Translational Science Institute. Dr. James is from the Department of Dermatology, University of Pittsburgh Medical Center. Alice J. Lin and Li Wang have no relevant financial disclosures to report. Dr. James is a consultant and section editor for EBSCO/DynaMed.

Correspondence: Alice J. Lin, BS, BA, University of Pittsburgh School of Medicine, 3550 Terrace St, Pittsburgh, PA 15213 (all263@pitt.edu).

Cutis. 2024 November;114(5):E6-E11. doi:10.12788/cutis.1138

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Author and Disclosure Information

Alice J. Lin and Li Wang are from the University of Pittsburgh, Pennsylvania. Alice J. Lin is from the School of Medicine, and Li Wang is from the Clinical and Translational Science Institute. Dr. James is from the Department of Dermatology, University of Pittsburgh Medical Center. Alice J. Lin and Li Wang have no relevant financial disclosures to report. Dr. James is a consultant and section editor for EBSCO/DynaMed.

Correspondence: Alice J. Lin, BS, BA, University of Pittsburgh School of Medicine, 3550 Terrace St, Pittsburgh, PA 15213 (all263@pitt.edu).

Cutis. 2024 November;114(5):E6-E11. doi:10.12788/cutis.1138

Author and Disclosure Information

Alice J. Lin and Li Wang are from the University of Pittsburgh, Pennsylvania. Alice J. Lin is from the School of Medicine, and Li Wang is from the Clinical and Translational Science Institute. Dr. James is from the Department of Dermatology, University of Pittsburgh Medical Center. Alice J. Lin and Li Wang have no relevant financial disclosures to report. Dr. James is a consultant and section editor for EBSCO/DynaMed.

Correspondence: Alice J. Lin, BS, BA, University of Pittsburgh School of Medicine, 3550 Terrace St, Pittsburgh, PA 15213 (all263@pitt.edu).

Cutis. 2024 November;114(5):E6-E11. doi:10.12788/cutis.1138

Approximately 25% of Americans have at least one skin condition, and 20% are estimated to develop skin cancer during their lifetime.1,2 However, 40% of the US population lives in areas underserved by dermatologists. 3 The severity and mortality of skin cancers such as melanoma and mycosis fungoides have been positively associated with minoritized race, lack of health insurance, and unstable housing status.4-6 Patients who receive health care at free clinics often are of a racial or ethnic minoritized social group, are uninsured, and/or lack stable housing; this underserved group also includes recent immigrants to the United States who have limited English proficiency (LEP).7 Only 25% of free clinics offer specialty care services such as dermatology.7,8

Of the 42 free clinics and Federally Qualified Health Centers in Pittsburgh, Pennsylvania, the Birmingham Free Clinic (BFC) is one of the few that offers specialty care services including dermatology.9 Founded in 1994, the BFC serves as a safety net for Pittsburgh’s medically underserved population, offering primary and acute care, medication access, and social services. From January 2020 to May 2022, the BFC offered 27 dermatology clinics that provided approximately 100 people with comprehensive care including full-body skin examinations, dermatologic diagnoses and treatments, minor procedures, and dermatopathology services.

In this study, we compared the BFC dermatology patient care model with that of the dermatology department at the University of Pittsburgh Medical Center (UPMC), an insurance-based tertiary referral health care system in western Pennsylvania. By analyzing the demographics, dermatologic diagnoses, and management strategies of both the BFC and UPMC, we gained an understanding of how these patient care models differ and how they can be improved to care for diverse patient populations.

Methods

A retrospective chart review of dermatology patients seen in person at the BFC and UPMC during the period from January 2020 to May 2022 was performed. The UPMC group included patients seen by 3 general dermatologists (including A.J.J.) at matched time points. Data were collected from patients’ first in-person visit during the study period. Variables of interest included patient age, sex, race, ethnicity, primary language, zip code, health insurance status, distance to clinic (estimated using Google Maps to calculate the shortest driving distance from the patient’s zip code to the clinic), history of skin cancer, dermatologic diagnoses, and management strategies. These variables were not collected for patients who cancelled or noshowed their first in-person appointments. All patient charts and notes corresponding to the date and visit of interest were accessed through the electronic medical record (EMR). Patient data were de-identified and stored in a password-protected spreadsheet. Comparisons between the BFC and UPMC patient populations were performed using X2 tests of independence, Fisher exact tests, and Mann-Whitney U tests via SPSS software (IBM). Statistical significance was set at P<.05.

Results

Patient Characteristics—Our analysis included 76 initial appointments at the BFC and 322 at UPMC (Table 1). The mean age for patients at the BFC and UPMC was 39.6 years and 47.8 years, respectively (P=.001). Males accounted for 39 (51.3%) and 112 (34.8%) of BFC and UPMC patients, respectively (P=.008); 2 (0.6%) patients from UPMC were transgender. Of the BFC and UPMC patients, 44.7% (34/76) and 0.9% (3/322) were Hispanic, respectively (P<.001). With regard to race, 52.6% (40/76) of BFC patients were White, 19.7% (15/76) were Black, 6.6% (5/76) were Asian/Pacific Islander (Chinese, 1.3% [1/76]; other Asian, 5.3% [4/76]), and 21.1% (16/76) were American Indian/other/unspecified (American Indian, 1.3% [1/76]; other, 13.2% [10/76]; unspecified, 6.6% [5/76]). At UPMC, 61.2% (197/322) of patients were White, 28.0% (90/322) were Black, 5.3% (17/322) were Asian/Pacific Islander (Chinese, 1.2% [4/322]; Indian [Asian], 1.9% [6/322]; Japanese, 0.3% [1/322]; other Asian, 1.6% [5/322]; other Asian/American Indian, 0.3% [1/322]), and 5.6% (18/322) were American Indian/other/ unspecified (American Indian, 0.3% [1/322]; other, 0.3% [1/322]; unspecified, 5.0% [16/322]). Overall, the BFC patient population was more ethnically and racially diverse than that of UPMC (P<.001).

Forty-six percent (35/76) of BFC patients and 4.3% (14/322) of UPMC patients had LEP (P<.001). Primary languages among BFC patients were 53.9% (41/76) English, 40.8% (31/76) Spanish, and 5.2% (4/76) other/ unspecified (Chinese, 1.3% [1/76]; Indonesian, 2.6% [2/76]; unspecified, 1.3% [1/76]). Primary languages among UPMC patients were 95.7% (308/322) English and 4.3% (14/322) other/unspecified (Chinese, 0.6% [2/322]; Nepali, 0.6% [2/322]; Pali, 0.3% [1/322]; Russian, 0.3% [1/322]; unspecified, 2.5% [8/322]). There were notable differences in insurance status at the BFC vs UPMC (P<.001), with more UPMC patients having private insurance (52.8% [170/322] vs 11.8% [9/76]) and more BFC patients being uninsured (52.8% [51/76] vs 1.9% [6/322]). There was no significant difference in distance to clinic between the 2 groups (P=.183). More UPMC patients had a history of skin cancer (P=.003). More patients at the BFC were no-shows for their appointments (P<.001), and UPMC patients more frequently canceled their appointments (P<.001).

Dermatologic Diagnoses—The most commonly diagnosed dermatologic conditions at the BFC were dermatitis (23.7% [18/76]), neoplasm of uncertain behavior (15.8% [12/76]), alopecia (11.8% [9/76]), and acne (10.5% [8/76]) (Table 2). The most commonly diagnosed conditions at UPMC were nevi (26.4% [85/322]), dermatitis (22.7% [73/322]), seborrheic keratosis (21.7% [70/322]), and skin cancer screening (21.4% [70/322]). Neoplasm of uncertain behavior was more common in BFC vs UPMC patients (P=.040), while UPMC patients were more frequently diagnosed with nevi (P<.001), seborrheic keratosis (P<.001), and skin cancer screening (P<.001). There was no significant difference between the incidence of skin cancer diagnoses in the BFC (1.3% [1/76]) and UPMC (0.6% [2/76]) patient populations (P=.471). Among the biopsied neoplasms, there was also no significant difference in malignant (BFC, 50.0% [5/10]; UPMC, 32.0% [8/25]) and benign (BFC, 50.0% [5/10]; UPMC, 36.0% [9/25]) neoplasms diagnosed at each clinic (P=.444).

Management Strategies—Systemic antibiotics were more frequently prescribed (P<.001) and laboratory testing/ imaging were more frequently ordered (P=.005) at the BFC vs UPMC (Table 3). Patients at the BFC also more frequently required emergency insurance (P=.036). Patients at UPMC were more frequently recommended sunscreen (P=.003) and received education about skin cancer signs by review of the ABCDEs of melanoma (P<.001), sun-protective behaviors (P=.001), and skin examination frequency (P<.001). Notes in the EMR for UPMC patients more frequently specified patient followup instructions (P<.001).

Comment

As of 2020, the city of Pittsburgh had an estimated population of nearly 303,000 based on US Census data.10 Its population is predominantly White (62.7%) followed by Black/African American (22.8%) and Asian (6.5%); 5.9% identify as 2 or more races. Approximately 3.8% identify as Hispanic or Latino. More than 11% of the Pittsburgh population aged 5 years and older speaks a language other than English as their primary language, including Spanish (2.3%), other Indo-European languages (3.9%), and Asian and Pacific Island languages (3.5%).11 More than 5% of the Pittsburgh population does not have health insurance.12

The BFC is located in Pittsburgh’s South Side area, while one of UPMC’s primary dermatology clinics is located in the Oakland district; however, most patients who seek care at these clinics live outside these areas. Our study results indicated that the BFC and UPMC serve distinct groups of people within the Pittsburgh population. The BFC patient population was younger with a higher percentage of patients who were male, Hispanic, racially diverse, and with LEP compared with the UPMC patient population. In this clinical setting, the BFC health care team engages with people from diverse backgrounds and requires greater interpreter and medical support services.

The BFC largely is supported by volunteers, UPMC, grants, and philanthropy. Dermatology clinics are staffed by paid and volunteer team members. Paid team members include 1 nurse and 1 access lead who operates the front desk and registration. Volunteer team members include 1 board-certified dermatologist from UPMC (A.J.J.), or an affiliate clinic and 1 or 2 of each of the following: UPMC dermatology residents, medical or undergraduate students from the University of Pittsburgh, AmeriCorps national service members, and student or community medical interpreters. The onsite pharmacy is run by volunteer faculty, resident, and student pharmacists from the University of Pittsburgh. Dermatology clinics are half-day clinics that occur monthly. Volunteers for each clinic are recruited approximately 1 month in advance.

Dermatology patients at the BFC are referred from the BFC general medicine clinic and nearby Federally Qualified Health Center s for simple to complex medical and surgical dermatologic skin conditions. Each BFC dermatology clinic schedules an average of 7 patients per clinic and places other patients on a wait-list unless more urgent triage is needed. Patients are notified when they are scheduled via phone or text message, and they receive a reminder call or text 1 or 2 days prior to their appointment that also asks them to confirm attendance. Patients with LEP are called with an interpreter and also may receive text reminders that can be translated using Google Translate. Patients are instructed to notify the BFC if they need to cancel or reschedule their appointment. At the end of each visit, patients are given an after-visit summary that lists follow-up instructions, medications prescribed during the visit, and upcoming appointments. The BFC offers bus tickets to help patients get to their appointments. In rare cases, the BFC may pay for a car service to drive patients to and from the clinic.

Dermatology clinics at UPMC use scheduling and self-scheduling systems through which patients can make appointments at a location of their choice with any available board-certified dermatologist or physician assistant. Patients receive a reminder phone call 3 days prior to their appointment instructing them to call the office if they are unable to keep their appointment. Patients signed up for the online portal also receive a reminder message and an option to confirm or cancel their appointment. Patients with cell phone numbers in the UPMC system receive a text message approximately 2 days prior to their appointment that allows them to preregister and pay their copayment in advance. They receive another text 20 minutes prior to their appointment with an option for contactless check-in. At the conclusion of their visit, patients can schedule a follow-up appointment and receive a printed copy of their after-visit summary that provides information about follow-up instructions, prescribed medications, and upcoming visits. They may alternatively access this summary via the online patient portal. Patients are not provided transportation to UPMC clinics, but they are offered parking validation.

Among the most common dermatologic diagnoses for each group, BFC patients presented for treatment of more acute dermatologic conditions, while UPMC patients presented for more benign and preventive-care conditions. This difference may be attributable to the BFC’s referral and triage system, wherein patients with more urgent problems are given scheduling priority. This patient care model contrasts with UPMC’s scheduling process in which no known formal triage system is utilized. Interestingly, there was no difference in skin cancer incidence despite a higher percentage of preventive skin cancer screenings at UPMC.

Patients at the BFC more often required emergency insurance for surgical interventions, which is consistent with the higher percentage of uninsured individuals in this population. Patients at UPMC more frequently were recommended sunscreen and were educated about skin cancer, sun protection, and skin examination, in part due to this group’s more extensive history of skin cancer and frequent presentation for skin cancer screenings. At the same time, educational materials for skin care at both the BFC and UPMC are populated into the EMR in English, whereas materials in other languages are less readily available.

Our retrospective study had several limitations. Demographic information that relied on clinic-dependent intake questionnaires may be limited due to variable intake processes and patients opting out of self-reporting. By comparing patient populations between 2 clinics, confounding variables such as location and hours of operation may impact the patient demographics recorded at the BFC vs UPMC. Resources and staff availability may affect the management strategies and follow-up care offered by each clinic. Our study period also was unique in that COVID-19 may have affected resources, staffing, scheduling, and logistics at both clinics.

Based on the aforementioned differences between the BFC and UPMC patient characteristics, care models should be strategically designed to support the needs of diverse populations. The BFC patient care model appropriately focuses on communication skills with patients with LEP by using interpreter services. Providing more skin care education and follow-up instructions in patients’ primary languages will help them develop a better understanding of their skin conditions. Another key asset of the BFC patient care model is its provision of social services such as transportation and insurance assistance.

To improve the UPMC patient care model, providing patients with bus tickets and car services may potentially reduce appointment cancellations. Using interpreter services to call and text appointment reminders, as well as interpreter resources to facilitate patient visits and patient instructions, also can mitigate language barriers for patients with LEP. Implementing a triage system into the UPMC scheduling system may help patients with more urgent skin conditions to be seen in a timely manner.

Other investigators have analyzed costs of care and proven the value of dermatologic services at free clinics to guide allocation of supplies and resources, demonstrating an area for future investigation at the BFC.13 A cost analysis of care provided at the BFC compared to UPMC could inform us about the value of the BFC’s services.

Conclusion

The dermatology clinics at the BFC and UPMC have distinct demographics, diagnoses, and management strategies to provide an inclusive patient care model. The services provided by both clinics are necessary to ensure that people in Pittsburgh have access to dermatologic care regardless of social barriers (eg, lack of health insurance, LEP). To achieve greater accessibility and health equity, dermatologic care at the BFC and UPMC can be improved by strengthening communication with people with LEP, providing skin care education, and offering social and scheduling services.

Approximately 25% of Americans have at least one skin condition, and 20% are estimated to develop skin cancer during their lifetime.1,2 However, 40% of the US population lives in areas underserved by dermatologists. 3 The severity and mortality of skin cancers such as melanoma and mycosis fungoides have been positively associated with minoritized race, lack of health insurance, and unstable housing status.4-6 Patients who receive health care at free clinics often are of a racial or ethnic minoritized social group, are uninsured, and/or lack stable housing; this underserved group also includes recent immigrants to the United States who have limited English proficiency (LEP).7 Only 25% of free clinics offer specialty care services such as dermatology.7,8

Of the 42 free clinics and Federally Qualified Health Centers in Pittsburgh, Pennsylvania, the Birmingham Free Clinic (BFC) is one of the few that offers specialty care services including dermatology.9 Founded in 1994, the BFC serves as a safety net for Pittsburgh’s medically underserved population, offering primary and acute care, medication access, and social services. From January 2020 to May 2022, the BFC offered 27 dermatology clinics that provided approximately 100 people with comprehensive care including full-body skin examinations, dermatologic diagnoses and treatments, minor procedures, and dermatopathology services.

In this study, we compared the BFC dermatology patient care model with that of the dermatology department at the University of Pittsburgh Medical Center (UPMC), an insurance-based tertiary referral health care system in western Pennsylvania. By analyzing the demographics, dermatologic diagnoses, and management strategies of both the BFC and UPMC, we gained an understanding of how these patient care models differ and how they can be improved to care for diverse patient populations.

Methods

A retrospective chart review of dermatology patients seen in person at the BFC and UPMC during the period from January 2020 to May 2022 was performed. The UPMC group included patients seen by 3 general dermatologists (including A.J.J.) at matched time points. Data were collected from patients’ first in-person visit during the study period. Variables of interest included patient age, sex, race, ethnicity, primary language, zip code, health insurance status, distance to clinic (estimated using Google Maps to calculate the shortest driving distance from the patient’s zip code to the clinic), history of skin cancer, dermatologic diagnoses, and management strategies. These variables were not collected for patients who cancelled or noshowed their first in-person appointments. All patient charts and notes corresponding to the date and visit of interest were accessed through the electronic medical record (EMR). Patient data were de-identified and stored in a password-protected spreadsheet. Comparisons between the BFC and UPMC patient populations were performed using X2 tests of independence, Fisher exact tests, and Mann-Whitney U tests via SPSS software (IBM). Statistical significance was set at P<.05.

Results

Patient Characteristics—Our analysis included 76 initial appointments at the BFC and 322 at UPMC (Table 1). The mean age for patients at the BFC and UPMC was 39.6 years and 47.8 years, respectively (P=.001). Males accounted for 39 (51.3%) and 112 (34.8%) of BFC and UPMC patients, respectively (P=.008); 2 (0.6%) patients from UPMC were transgender. Of the BFC and UPMC patients, 44.7% (34/76) and 0.9% (3/322) were Hispanic, respectively (P<.001). With regard to race, 52.6% (40/76) of BFC patients were White, 19.7% (15/76) were Black, 6.6% (5/76) were Asian/Pacific Islander (Chinese, 1.3% [1/76]; other Asian, 5.3% [4/76]), and 21.1% (16/76) were American Indian/other/unspecified (American Indian, 1.3% [1/76]; other, 13.2% [10/76]; unspecified, 6.6% [5/76]). At UPMC, 61.2% (197/322) of patients were White, 28.0% (90/322) were Black, 5.3% (17/322) were Asian/Pacific Islander (Chinese, 1.2% [4/322]; Indian [Asian], 1.9% [6/322]; Japanese, 0.3% [1/322]; other Asian, 1.6% [5/322]; other Asian/American Indian, 0.3% [1/322]), and 5.6% (18/322) were American Indian/other/ unspecified (American Indian, 0.3% [1/322]; other, 0.3% [1/322]; unspecified, 5.0% [16/322]). Overall, the BFC patient population was more ethnically and racially diverse than that of UPMC (P<.001).

Forty-six percent (35/76) of BFC patients and 4.3% (14/322) of UPMC patients had LEP (P<.001). Primary languages among BFC patients were 53.9% (41/76) English, 40.8% (31/76) Spanish, and 5.2% (4/76) other/ unspecified (Chinese, 1.3% [1/76]; Indonesian, 2.6% [2/76]; unspecified, 1.3% [1/76]). Primary languages among UPMC patients were 95.7% (308/322) English and 4.3% (14/322) other/unspecified (Chinese, 0.6% [2/322]; Nepali, 0.6% [2/322]; Pali, 0.3% [1/322]; Russian, 0.3% [1/322]; unspecified, 2.5% [8/322]). There were notable differences in insurance status at the BFC vs UPMC (P<.001), with more UPMC patients having private insurance (52.8% [170/322] vs 11.8% [9/76]) and more BFC patients being uninsured (52.8% [51/76] vs 1.9% [6/322]). There was no significant difference in distance to clinic between the 2 groups (P=.183). More UPMC patients had a history of skin cancer (P=.003). More patients at the BFC were no-shows for their appointments (P<.001), and UPMC patients more frequently canceled their appointments (P<.001).

Dermatologic Diagnoses—The most commonly diagnosed dermatologic conditions at the BFC were dermatitis (23.7% [18/76]), neoplasm of uncertain behavior (15.8% [12/76]), alopecia (11.8% [9/76]), and acne (10.5% [8/76]) (Table 2). The most commonly diagnosed conditions at UPMC were nevi (26.4% [85/322]), dermatitis (22.7% [73/322]), seborrheic keratosis (21.7% [70/322]), and skin cancer screening (21.4% [70/322]). Neoplasm of uncertain behavior was more common in BFC vs UPMC patients (P=.040), while UPMC patients were more frequently diagnosed with nevi (P<.001), seborrheic keratosis (P<.001), and skin cancer screening (P<.001). There was no significant difference between the incidence of skin cancer diagnoses in the BFC (1.3% [1/76]) and UPMC (0.6% [2/76]) patient populations (P=.471). Among the biopsied neoplasms, there was also no significant difference in malignant (BFC, 50.0% [5/10]; UPMC, 32.0% [8/25]) and benign (BFC, 50.0% [5/10]; UPMC, 36.0% [9/25]) neoplasms diagnosed at each clinic (P=.444).

Management Strategies—Systemic antibiotics were more frequently prescribed (P<.001) and laboratory testing/ imaging were more frequently ordered (P=.005) at the BFC vs UPMC (Table 3). Patients at the BFC also more frequently required emergency insurance (P=.036). Patients at UPMC were more frequently recommended sunscreen (P=.003) and received education about skin cancer signs by review of the ABCDEs of melanoma (P<.001), sun-protective behaviors (P=.001), and skin examination frequency (P<.001). Notes in the EMR for UPMC patients more frequently specified patient followup instructions (P<.001).

Comment

As of 2020, the city of Pittsburgh had an estimated population of nearly 303,000 based on US Census data.10 Its population is predominantly White (62.7%) followed by Black/African American (22.8%) and Asian (6.5%); 5.9% identify as 2 or more races. Approximately 3.8% identify as Hispanic or Latino. More than 11% of the Pittsburgh population aged 5 years and older speaks a language other than English as their primary language, including Spanish (2.3%), other Indo-European languages (3.9%), and Asian and Pacific Island languages (3.5%).11 More than 5% of the Pittsburgh population does not have health insurance.12

The BFC is located in Pittsburgh’s South Side area, while one of UPMC’s primary dermatology clinics is located in the Oakland district; however, most patients who seek care at these clinics live outside these areas. Our study results indicated that the BFC and UPMC serve distinct groups of people within the Pittsburgh population. The BFC patient population was younger with a higher percentage of patients who were male, Hispanic, racially diverse, and with LEP compared with the UPMC patient population. In this clinical setting, the BFC health care team engages with people from diverse backgrounds and requires greater interpreter and medical support services.

The BFC largely is supported by volunteers, UPMC, grants, and philanthropy. Dermatology clinics are staffed by paid and volunteer team members. Paid team members include 1 nurse and 1 access lead who operates the front desk and registration. Volunteer team members include 1 board-certified dermatologist from UPMC (A.J.J.), or an affiliate clinic and 1 or 2 of each of the following: UPMC dermatology residents, medical or undergraduate students from the University of Pittsburgh, AmeriCorps national service members, and student or community medical interpreters. The onsite pharmacy is run by volunteer faculty, resident, and student pharmacists from the University of Pittsburgh. Dermatology clinics are half-day clinics that occur monthly. Volunteers for each clinic are recruited approximately 1 month in advance.

Dermatology patients at the BFC are referred from the BFC general medicine clinic and nearby Federally Qualified Health Center s for simple to complex medical and surgical dermatologic skin conditions. Each BFC dermatology clinic schedules an average of 7 patients per clinic and places other patients on a wait-list unless more urgent triage is needed. Patients are notified when they are scheduled via phone or text message, and they receive a reminder call or text 1 or 2 days prior to their appointment that also asks them to confirm attendance. Patients with LEP are called with an interpreter and also may receive text reminders that can be translated using Google Translate. Patients are instructed to notify the BFC if they need to cancel or reschedule their appointment. At the end of each visit, patients are given an after-visit summary that lists follow-up instructions, medications prescribed during the visit, and upcoming appointments. The BFC offers bus tickets to help patients get to their appointments. In rare cases, the BFC may pay for a car service to drive patients to and from the clinic.

Dermatology clinics at UPMC use scheduling and self-scheduling systems through which patients can make appointments at a location of their choice with any available board-certified dermatologist or physician assistant. Patients receive a reminder phone call 3 days prior to their appointment instructing them to call the office if they are unable to keep their appointment. Patients signed up for the online portal also receive a reminder message and an option to confirm or cancel their appointment. Patients with cell phone numbers in the UPMC system receive a text message approximately 2 days prior to their appointment that allows them to preregister and pay their copayment in advance. They receive another text 20 minutes prior to their appointment with an option for contactless check-in. At the conclusion of their visit, patients can schedule a follow-up appointment and receive a printed copy of their after-visit summary that provides information about follow-up instructions, prescribed medications, and upcoming visits. They may alternatively access this summary via the online patient portal. Patients are not provided transportation to UPMC clinics, but they are offered parking validation.

Among the most common dermatologic diagnoses for each group, BFC patients presented for treatment of more acute dermatologic conditions, while UPMC patients presented for more benign and preventive-care conditions. This difference may be attributable to the BFC’s referral and triage system, wherein patients with more urgent problems are given scheduling priority. This patient care model contrasts with UPMC’s scheduling process in which no known formal triage system is utilized. Interestingly, there was no difference in skin cancer incidence despite a higher percentage of preventive skin cancer screenings at UPMC.

Patients at the BFC more often required emergency insurance for surgical interventions, which is consistent with the higher percentage of uninsured individuals in this population. Patients at UPMC more frequently were recommended sunscreen and were educated about skin cancer, sun protection, and skin examination, in part due to this group’s more extensive history of skin cancer and frequent presentation for skin cancer screenings. At the same time, educational materials for skin care at both the BFC and UPMC are populated into the EMR in English, whereas materials in other languages are less readily available.

Our retrospective study had several limitations. Demographic information that relied on clinic-dependent intake questionnaires may be limited due to variable intake processes and patients opting out of self-reporting. By comparing patient populations between 2 clinics, confounding variables such as location and hours of operation may impact the patient demographics recorded at the BFC vs UPMC. Resources and staff availability may affect the management strategies and follow-up care offered by each clinic. Our study period also was unique in that COVID-19 may have affected resources, staffing, scheduling, and logistics at both clinics.

Based on the aforementioned differences between the BFC and UPMC patient characteristics, care models should be strategically designed to support the needs of diverse populations. The BFC patient care model appropriately focuses on communication skills with patients with LEP by using interpreter services. Providing more skin care education and follow-up instructions in patients’ primary languages will help them develop a better understanding of their skin conditions. Another key asset of the BFC patient care model is its provision of social services such as transportation and insurance assistance.

To improve the UPMC patient care model, providing patients with bus tickets and car services may potentially reduce appointment cancellations. Using interpreter services to call and text appointment reminders, as well as interpreter resources to facilitate patient visits and patient instructions, also can mitigate language barriers for patients with LEP. Implementing a triage system into the UPMC scheduling system may help patients with more urgent skin conditions to be seen in a timely manner.

Other investigators have analyzed costs of care and proven the value of dermatologic services at free clinics to guide allocation of supplies and resources, demonstrating an area for future investigation at the BFC.13 A cost analysis of care provided at the BFC compared to UPMC could inform us about the value of the BFC’s services.

Conclusion

The dermatology clinics at the BFC and UPMC have distinct demographics, diagnoses, and management strategies to provide an inclusive patient care model. The services provided by both clinics are necessary to ensure that people in Pittsburgh have access to dermatologic care regardless of social barriers (eg, lack of health insurance, LEP). To achieve greater accessibility and health equity, dermatologic care at the BFC and UPMC can be improved by strengthening communication with people with LEP, providing skin care education, and offering social and scheduling services.

References
  1. Lim HW, Collins SAB, Resneck JS, et al. The burden of skin disease in the United States. J Am Acad Dermatol. 2017;76:958-972.e2. doi:10.1016/j.jaad.2016.12.043
  2. American Academy of Dermatology. Skin cancer. Accessed October 7, 2024. https://www.aad.org/media/stats-skin-cancer
  3. Suneja T, Smith ED, Chen GJ, et al. Waiting times to see a dermatologist are perceived as too long by dermatologists: implications for the dermatology workforce. Arch Dermatol. 2001;137:1303-1307. doi:10.1001/archderm.137.10.1303
  4. Grossberg AL, Carranza D, Lamp K, et al. Dermatologic care in the homeless and underserved populations: observations from the Venice Family Clinic. Cutis. 2012;89:25-32.
  5. Amini A, Rusthoven CG, Waxweiler TV, et al. Association of health insurance with outcomes in adults ages 18 to 64 years with melanoma in the United States. J Am Acad Dermatol. 2016;74:309-316. doi:10.1016/j.jaad.2015.09.054
  6. Su C, Nguyen KA, Bai HX, et al. Racial disparity in mycosis fungoides: an analysis of 4495 cases from the US National Cancer Database. J Am Acad Dermatol. 2017;77:497-502.e2. doi:10.1016/j.jaad .2017.04.1137
  7. Darnell JS. Free clinics in the United States: a nationwide survey. Arch Intern Med. 2010;170:946-953. doi:10.1001/archinternmed .2010.107
  8. Madray V, Ginjupalli S, Hashmi O, et al. Access to dermatology services at free medical clinics: a nationwide cross-sectional survey. J Am Acad Dermatol. 2019;81:245-246. doi:10.1016/j.jaad.2018.12.011
  9. Pennsylvania free and income-based clinics. Accessed October 7, 2024. https://www.freeclinics.com/sta/pennsylvania
  10. United States Census Bureau. Decennial census. P1: race. Accessed October 7, 2024. https://data.census.gov/table/DECENNIALPL2020.P1?g=160XX00US4261000
  11. United States Census Bureau. American community survey. S1601: language spoken at home. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020S1601?g=160XX00US4261000
  12. United States Census Bureau. S2701: selected characteristics of health insurance coverage in the United States. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020.S2701?g=160XX00US4261000
  13. Lin CP, Loy S, Boothe WD, et al. Value of Dermatology Nights at a student-run free clinic. Proc (Bayl Univ Med Cent). 2020;34:260-261. doi:10.1080/08998280.2020.1834771
References
  1. Lim HW, Collins SAB, Resneck JS, et al. The burden of skin disease in the United States. J Am Acad Dermatol. 2017;76:958-972.e2. doi:10.1016/j.jaad.2016.12.043
  2. American Academy of Dermatology. Skin cancer. Accessed October 7, 2024. https://www.aad.org/media/stats-skin-cancer
  3. Suneja T, Smith ED, Chen GJ, et al. Waiting times to see a dermatologist are perceived as too long by dermatologists: implications for the dermatology workforce. Arch Dermatol. 2001;137:1303-1307. doi:10.1001/archderm.137.10.1303
  4. Grossberg AL, Carranza D, Lamp K, et al. Dermatologic care in the homeless and underserved populations: observations from the Venice Family Clinic. Cutis. 2012;89:25-32.
  5. Amini A, Rusthoven CG, Waxweiler TV, et al. Association of health insurance with outcomes in adults ages 18 to 64 years with melanoma in the United States. J Am Acad Dermatol. 2016;74:309-316. doi:10.1016/j.jaad.2015.09.054
  6. Su C, Nguyen KA, Bai HX, et al. Racial disparity in mycosis fungoides: an analysis of 4495 cases from the US National Cancer Database. J Am Acad Dermatol. 2017;77:497-502.e2. doi:10.1016/j.jaad .2017.04.1137
  7. Darnell JS. Free clinics in the United States: a nationwide survey. Arch Intern Med. 2010;170:946-953. doi:10.1001/archinternmed .2010.107
  8. Madray V, Ginjupalli S, Hashmi O, et al. Access to dermatology services at free medical clinics: a nationwide cross-sectional survey. J Am Acad Dermatol. 2019;81:245-246. doi:10.1016/j.jaad.2018.12.011
  9. Pennsylvania free and income-based clinics. Accessed October 7, 2024. https://www.freeclinics.com/sta/pennsylvania
  10. United States Census Bureau. Decennial census. P1: race. Accessed October 7, 2024. https://data.census.gov/table/DECENNIALPL2020.P1?g=160XX00US4261000
  11. United States Census Bureau. American community survey. S1601: language spoken at home. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020S1601?g=160XX00US4261000
  12. United States Census Bureau. S2701: selected characteristics of health insurance coverage in the United States. Accessed October 7, 2024. https://data.census.gov/table/ACSST5Y2020.S2701?g=160XX00US4261000
  13. Lin CP, Loy S, Boothe WD, et al. Value of Dermatology Nights at a student-run free clinic. Proc (Bayl Univ Med Cent). 2020;34:260-261. doi:10.1080/08998280.2020.1834771
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  • Both free clinics and insurance-based health care systems serve dermatology patients with diverse characteristics, necessitating inclusive health care models.
  • Dermatologic care can be improved at both free and insurance-based clinics by strengthening communication with individuals with limited English proficiency, providing skin care education, and offering social and scheduling services such as transportation, insurance assistance, and triage.
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Multidisciplinary Amputation Prevention at the DeBakey VA Hospital: Our First Decade

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Individuals with diabetes are at risk for developing foot ulcers or full-thickness defects in the epithelium of the foot. These defects can lead to bacterial invasion and foot infection, potentially resulting in leg amputation (Figure 1). Effective treatment to prevent leg amputation, known as limb salvage, requires management across multiple medical specialties including podiatry, vascular surgery, and infectious diseases. The multidisciplinary team approach to limb salvage was introduced in Boston in 1928 and has been the prevailing approach to this cross-specialty medical problem for at least a decade.1,2

Figure courtesy of Neal Barshes.

The Michael E. DeBakey Veterans Affairs Medical Center (MEDVAMC) has established an inpatient limb salvage program—a group of dedicated clinicians working collaboratively to provide evidence-guided management of patients hospitalized with foot ulcers, foot gangrene or any superimposed infection with the goal of avoiding leg amputations. We have seen a significant and durable reduction in the incidence of leg amputations among veterans at MEDVAMC.

This article describes the evolution and outcomes of the MEDVAMC limb salvage program over more than a decade. It includes changes to team structure and workflow, as well as past and present successes and challenges. The eAppendix provides a narrative summary with examples of how our clinical practice and research efforts have informed one another and how these findings are applied to clinical management. This process is part of the larger efforts of the Veterans Health Administration (VHA) to create a learning health system in which “internal data and experience are systematically integrated with external evidence, and that knowledge is put into practice.”3

Methods

Data from the VHA Support Service Center were used to obtain monthly major (leg) and minor (toe and partial foot) amputation records at MEDVAMC from October 2000 through May 2023. Yearly totals for the number of persons with diabetes and foot ulcers at MEDVAMC were also obtained from the support service center. Annual patient population sizes and number of persons with foot ulcers were converted to monthly estimates using cubic spline interpolation. Rates were calculated as 12-month rolling averages. Trend lines were created with locally weighted running line smoothing that used a span α of 0.1.

We characterized the patient population using data from cohorts of veterans treated for foot ulcers and foot infections at MEDVAMC. To compare the contemporary veteran population with nonveteran inpatients treated for foot ulcers and foot infections at other hospitals, we created a 2:1 nonveteran to veteran cohort matched by sex and zip code, using publicly available hospital admission data from the Texas Department of Health and State Health Services. Veterans used for this cohort comparison are consistent with the 100 consecutive patients who underwent angiography for limb salvage in 2022.

This research was approved by the Baylor College of Medicine Institutional Review Board (protocol H-34858) and the MEDVAMC Research Committee (IRBNet protocol 15A12. HB). All analyses used deidentified data in the R programming language version 4.2.2 using RStudio version 2022.06.0 Build 421.

Program Description

MEDVAMC is a 350-bed teaching hospital located in central Houston. Its hospital system includes 11 outpatient clinics, ranging from 28 to 126 miles (eAppendix, Supplemental Figure A) from MEDVAMC. MEDVAMC provides vascular, orthopedic, and podiatric surgery services, as well as many other highly specialized services such as liver and heart transplants. The hospital’s risk-adjusted rates of operative morbidity and mortality (observed-to-expected ratios) are significantly lower than expected.

Despite this, the incidence rate of leg amputations at MEDVAMC in early 2011 was nearly 3-times higher than the VHA average. The inpatient management of veterans with infected foot ulcers was fragmented, with the general, orthopedic, and vascular surgery teams separately providing siloed care. Delays in treatment were common. There was much service- and practitioner-level practice heterogeneity. No diagnostic or treatment protocols were used, and standard treatment components were sporadically provided.

Patient Population

Compared to the matched non-VHA patient cohort (Supplemental Table 1), veterans treated at MEDVAMC for limb salvage are older. Nearly half (46%) identify as Black, which is associated with a 2-fold higher riskadjusted rate of leg amputations.4 MEDVAMC patients also have significantly higher rates of diabetes, chronic kidney disease, and systolic heart failure. About 22% travel > 40 miles for treatment at MEDVAMC, double that of the matched cohort (10.7%). Additionally, 35% currently smoke and 37% have moderate to severe peripheral artery disease (PAD).5

Program Design

In late 2011, the MEDVAMC vascular surgery team led limb salvage efforts by implementing a single team model, which involved assuming the primary role of managing foot ulcers for all veterans, both infected and uninfected (eAppendix, Supplemental Figure B). Consultations were directed to a dedicated limb salvage pager. The vascular team provided interdisciplinary limb salvage management across the spectrum of disease, including the surgical treatment of infection, assessment for PAD, open surgical operations and endovascular interventions to treat PAD, and foot reconstruction (debridement, minor or partial foot amputations, and skin grafting). This care was complemented by frequent consultation with the infectious disease, vascular medicine, podiatry, and geriatric wound care teams. This approach streamlined the delivery of consistent multidisciplinary care.

This collaborative effort aimed to develop ideal multidisciplinary care plans through research spanning the spectrum of the diabetic foot infection disease process (eAppendix, Supplemental Table 1). Some of the most impactful practices were: (1) a proclivity towards surgical treatment of foot infections, especially osteomyelitis5; (2) improved identification of PAD6,7; (3) early surgical closure of foot wounds following revascularization8,9; and (4) palliative wound care as an alternative to leg amputation in veterans who are not candidates for revascularization and limb salvage.10 Initally, the vascular surgery team held monthly multidisciplinary limb salvage meetings to coordinate patient management, identify ways to streamline care and avoid waste, discuss research findings, and review the 12-month rolling average of the MEDVAMC leg amputation incidence rate.

During the study period, the MEDVAMC vascular surgery team consisted of 2 to 5 board certified vascular or general surgeons, 2 or 3 nurse practitioners, and 3 vascular ultrasound technologists. Associated specialists included 2 podiatrists, 3 geriatricians with wound care certification, as well as additional infectious diseases, vascular medicine, orthopedics, and general surgery specialists.

Program Assessment

We noted a significant and sustained decrease in the MEDVAMC leg amputation rate after implementing multidisciplinary meetings and a single- team model from early 2012 through 2017 (Figure 2). The amputation incidence rate decreased steadily over the period from a maximum of 160 per 100,000 per year in February 2012 to a nadir of 66 per 100,000 per year in April 2017, an overall 60% decrease. Increases were noted in early 2018 after ceasing the single- team model, and in the summer of 2022, following periods of bed shortages after the onset of the COVID-19 pandemic. Tracking this metric allowed clinicians to make course corrections.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center.

The decreased leg amputation rate at MEDVAMC does not seem to be mirroring national or regional trends. During this 10-year period, the VHA annualized amputation rate decreased minimally, from 58 to 54 per 100,000 (eAppendix Supplemental Figure C). Leg amputation incidence at non-VHA hospitals in Texas slightly increased over the same period.11

Value was also reflected in other metrics. MEDVAMC improved safety through a bundled strategy that reduced the risk-adjusted rate of surgical wound infections by 95%.12 MEDVAMC prioritized limb salvage when selecting patients for angiography and nearly eliminated using stent-grafts, cryopreserved allogeneic saphenous vein grafts, and expensive surgical and endovascular implants, which were identified as more expensive and less effective than other options (Figure 3).13-15 The MEDVAMC team achieved a > 90% patient trust rating on the Veterans Signals survey in fiscal years 2021 and 2022.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center

Challenges

A significant increase in the patient-physician ratio occurred 5 years into the program. In 2016, 2 vascular surgeons left MEDVAMC and a planned renovation of 1 of the 2 vascular surgery-assigned hybrid working facilities began even as the number of MEDVAMC patients with diabetes grew 120% (from 89,400 to 107,746 between 2010 and 2016), and the incidence rate of foot ulcers grew 300% (from 392 in 2010 to 1183 in 2016 per 100,000). The net result was a higher clinical workload among the remaining vascular surgeons with less operating room availability.

To stabilize surgeon retention, MEDVAMC reverted from the single team model back to inpatient care being distributed among general surgery, orthopedic surgery, and vascular surgery. After noting an increase in the leg amputation incidence rate, we adjusted the focus from multidisciplinary to interdisciplinary care (ie, majority of limb salvage clinical care can be provided by practitioners of any involved specialties). We worked to establish a local, written, interdisciplinary consensus on evaluating and managing veterans with nonhealing foot ulcers to mitigate the loss of a consolidated inpatient approach. Despite frequent staff turnover, ≥ 1 physician or surgeon from the core specialties of vascular surgery, podiatry, and infectious diseases remained throughout the study period.

The COVID-19 pandemic caused a shortage of hospital beds. This was followed by more bed shortages due to decreased nursing staff. Our health care system also had a period of restricted outpatient encounters early in the pandemic. During this time, we noted a delayed presentation of veterans with advanced infections and another increase in leg amputation incidence rate.

Like many health systems, MEDVAMC pivoted to telephone- and video-based outpatient encounters. Our team also used publicly available Texas hospitalization data to identify zip codes with particularly high leg amputation incidence rates, and > 3500 educational mailings to veterans categorized as moderate and high risk for leg amputation in these zip codes. These mailings provided information on recognizing foot ulcers and infections, emphasized timely evaluation, and named the MEDVAMC vascular surgery team as a point-of-contact. More recently, we have seen a further decrease in the MEDVAMC incidences of leg amputation to its lowest rate in > 20 years.

Discussion

A learning organization that directs its research based on clinical observations and informs its clinical care with research findings can produce palpable improvements in outcomes. Understanding the disease process and trying to better understand management across the entire range of this disease process has allowed our team to make consistent and systematic changes in care (Table). Consolidating inpatient care in a single team model seems to have been effective in reducing amputation rates among veterans with diabetes. The role the MEDVAMC vascular surgery team served for limb salvage patients may have been particularly beneficial because of the large impact untreated or unidentified PAD can have and because of the high prevalence of PAD among the limb salvage population seen at MEDVAMC. To be sustainable, though, a single-team model needs resources. A multiteam model can also be effective if the degree of multidisciplinary involvement for any given veteran is appropriate to the individual's clinical needs, teams are engaged and willing to contribute in a defined role within their specialty, and lines of communication remain open.

The primary challenge at MEDVAMC has been, and will continue to be, the retention of physicians and surgeons. MEDVAMC has excellent leadership and a collegial working environment, but better access to operating rooms for elective and time-sensitive operations, additional clinical staff support, and higher salary at non-VA positions have been the basis for many of physicians— especially surgeons—leaving MEDVAMC. Despite high staff turnover and a constant flow of resident and fellow trainees, MEDVAMC has been able to keep the clinical approach relatively consistent due to the use of written protocols and continuity of care as ≥ 1 physician or surgeon from each of the 4 main teams remained engaged with limb salvage throughout the entire period.

Going forward, we will work to ensure that all requirements of the 2022 Prevention of Amputation in Veterans Everywhere directive are incorporated into care.8 We plan to standardize MEDVAMC management algorithms further, both to streamline care and reduce the opportunity for disparities in treatment. More prophylactic podiatric procedures, surgical forms of offloading, and a shared multidisciplinary clinic space may also further help patients.

Conclusions

The introduction of multidisciplinary limb salvage at MEDVAMC has led to significant and sustained reductions in leg amputation incidence. These reductions do not seem dependent upon a specific team structure for inpatient care. To improve patient outcomes, efforts should focus on making improvements across the entire disease spectrum. For limb salvage, this includes primary prevention of foot ulcers, the treatment of foot infections, identification and management of PAD, surgical reconstruction/optimal wound healing, and care for patients who undergo leg amputation.

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References
  1. Sanders LJ, Robbins JM, Edmonds ME. History of the team approach to amputation prevention: pioneers and milestones. J Am Podiatr Med Assoc. 2010;100(5):317- 334. doi:10.7547/1000317
  2. Sumpio BE, Armstrong DG, Lavery LA, Andros G. The role of interdisciplinary team approach in the management of the diabetic foot: a joint statement from the society for vascular surgery and the American podiatric medical association. J Am Podiatr Med Assoc. 2010;100(4):309-311. doi:10.7547/1000309
  3. About learning health systems. Agency for Healthcare Research and Quality. Published March 2019. Updated May 2019. Accessed October 9, 2024. https://www.ahrq.gov/learning-health-systems/about.html
  4. Barshes NR, Minc SD. Healthcare disparities in vascular surgery: a critical review. J Vasc Surg. 2021;74(2S):6S-14S.
  5. Barshes NR, Mindru C, Ashong C, Rodriguez-Barradas M, Trautner BW. Treatment failure and leg amputation among patients with foot osteomyelitis. Int J Low Extrem Wounds. 2016;15(4):303-312. doi:10.1177/1534734616661058
  6. Barshes NR, Flores E, Belkin M, Kougias P, Armstrong DG, Mills JL Sr. The accuracy and cost-effectiveness of strategies used to identify peripheral artery disease among patients with diabetic foot ulcers. J Vasc Surg. 2016;64(6):1682-1690.e3. doi:10.1016/j.jvs.2016.04.056 e1. doi:10.1016/j.jvs.2021.03.055
  7. Choi JC, Miranda J, Greenleaf E, et al. Lower-extremity pressure, staging, and grading thresholds to identify chronic limb-threatening ischemia. Vasc Med. 2023;28(1):45-53. doi:10.1177/1358863X221147945
  8. Barshes NR, Chambers JD, Cohen J, Belkin M; Model To Optimize Healthcare Value in Ischemic Extremities 1 (MOVIE) Study Collaborators. Cost-effectiveness in the contemporary management of critical limb ischemia with tissue loss. J Vasc Surg. 2012;56(4):1015-24.e1. doi:10.1016/j.jvs.2012.02.069
  9. Barshes NR, Bechara CF, Pisimisis G, Kougias P. Preliminary experiences with early primary closure of foot wounds after lower extremity revascularization. Ann Vasc Surg. 2014;28(1):48-52. doi:10.1016/j.avsg.2013.06.012
  10. Barshes NR, Gold B, Garcia A, Bechara CF, Pisimisis G, Kougias P. Minor amputation and palliative wound care as a strategy to avoid major amputation in patients with foot infections and severe peripheral arterial disease. Int J Low Extrem Wounds. 2014;13(3):211-219. doi:10.1177/1534734614543663
  11. Garcia M, Hernandez B, Ellington TG, et al. A lack of decline in major nontraumatic amputations in Texas: contemporary trends, risk factor associations, and impact of revascularization. Diabetes Care. 2019;42(6):1061-1066. doi:10.2337/dc19-0078
  12. Zamani N, Sharath SE, Vo E, Awad SS, Kougias P, Barshes NR. A multi-component strategy to decrease wound complications after open infra-inguinal re-vascularization. Surg Infect (Larchmt). 2018;19(1):87-94. doi:10.1089/sur.2017.193
  13. Barshes NR, Ozaki CK, Kougias P, Belkin M. A costeffectiveness analysis of infrainguinal bypass in the absence of great saphenous vein conduit. J Vasc Surg. 2013;57(6):1466-1470. doi:10.1016/j.jvs.2012.11.115
  14. Zamani N, Sharath S, Browder R, et al. PC158 longterm outcomes after endovascular stent placement for symptomatic, long-segment superficial femoral artery lesions. J Vasc Surg. 2017;65(6):182S-183S. doi:10.1016/j.jvs.2017.03.344
  15. Zamani N, Sharath SE, Browder RC, et al. Outcomes after endovascular stent placement for long-segment superficial femoral artery lesions. Ann Vasc Surg. 2021;71:298-307. doi:10.1016/j.avsg.2020.08.124
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Author and Disclosure Information

Neal R. Barshes, MD, MPHa,b; Aimee D. Garcia, MDa,b; Cezarina Mindru, MDa,b; Maria Rodriguez-Barradas, MD, PhDa,b; Panos Kougias, MD, MSc; David M. Green, MD, MSa,b; Samir S. Awad, MD, MPHa,c

Author affiliations:
aMichael E. DeBakey Veterans Affairs Medical Center, Houston, Texas
bBaylor College of Medicine, Houston, Texas
cState University of New York (SUNY) Downstate, Brooklyn

Author disclosures: The authors report no actual or potential conflicts of interest with regard to this article.

Correspondence: Neal Barshes (neal.barshes@va.gov)

Fed Pract. 2024;41(suppl 5). Published online November 16. doi:10.12788/fp0519

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Neal R. Barshes, MD, MPHa,b; Aimee D. Garcia, MDa,b; Cezarina Mindru, MDa,b; Maria Rodriguez-Barradas, MD, PhDa,b; Panos Kougias, MD, MSc; David M. Green, MD, MSa,b; Samir S. Awad, MD, MPHa,c

Author affiliations:
aMichael E. DeBakey Veterans Affairs Medical Center, Houston, Texas
bBaylor College of Medicine, Houston, Texas
cState University of New York (SUNY) Downstate, Brooklyn

Author disclosures: The authors report no actual or potential conflicts of interest with regard to this article.

Correspondence: Neal Barshes (neal.barshes@va.gov)

Fed Pract. 2024;41(suppl 5). Published online November 16. doi:10.12788/fp0519

Author and Disclosure Information

Neal R. Barshes, MD, MPHa,b; Aimee D. Garcia, MDa,b; Cezarina Mindru, MDa,b; Maria Rodriguez-Barradas, MD, PhDa,b; Panos Kougias, MD, MSc; David M. Green, MD, MSa,b; Samir S. Awad, MD, MPHa,c

Author affiliations:
aMichael E. DeBakey Veterans Affairs Medical Center, Houston, Texas
bBaylor College of Medicine, Houston, Texas
cState University of New York (SUNY) Downstate, Brooklyn

Author disclosures: The authors report no actual or potential conflicts of interest with regard to this article.

Correspondence: Neal Barshes (neal.barshes@va.gov)

Fed Pract. 2024;41(suppl 5). Published online November 16. doi:10.12788/fp0519

Article PDF
Article PDF

Individuals with diabetes are at risk for developing foot ulcers or full-thickness defects in the epithelium of the foot. These defects can lead to bacterial invasion and foot infection, potentially resulting in leg amputation (Figure 1). Effective treatment to prevent leg amputation, known as limb salvage, requires management across multiple medical specialties including podiatry, vascular surgery, and infectious diseases. The multidisciplinary team approach to limb salvage was introduced in Boston in 1928 and has been the prevailing approach to this cross-specialty medical problem for at least a decade.1,2

Figure courtesy of Neal Barshes.

The Michael E. DeBakey Veterans Affairs Medical Center (MEDVAMC) has established an inpatient limb salvage program—a group of dedicated clinicians working collaboratively to provide evidence-guided management of patients hospitalized with foot ulcers, foot gangrene or any superimposed infection with the goal of avoiding leg amputations. We have seen a significant and durable reduction in the incidence of leg amputations among veterans at MEDVAMC.

This article describes the evolution and outcomes of the MEDVAMC limb salvage program over more than a decade. It includes changes to team structure and workflow, as well as past and present successes and challenges. The eAppendix provides a narrative summary with examples of how our clinical practice and research efforts have informed one another and how these findings are applied to clinical management. This process is part of the larger efforts of the Veterans Health Administration (VHA) to create a learning health system in which “internal data and experience are systematically integrated with external evidence, and that knowledge is put into practice.”3

Methods

Data from the VHA Support Service Center were used to obtain monthly major (leg) and minor (toe and partial foot) amputation records at MEDVAMC from October 2000 through May 2023. Yearly totals for the number of persons with diabetes and foot ulcers at MEDVAMC were also obtained from the support service center. Annual patient population sizes and number of persons with foot ulcers were converted to monthly estimates using cubic spline interpolation. Rates were calculated as 12-month rolling averages. Trend lines were created with locally weighted running line smoothing that used a span α of 0.1.

We characterized the patient population using data from cohorts of veterans treated for foot ulcers and foot infections at MEDVAMC. To compare the contemporary veteran population with nonveteran inpatients treated for foot ulcers and foot infections at other hospitals, we created a 2:1 nonveteran to veteran cohort matched by sex and zip code, using publicly available hospital admission data from the Texas Department of Health and State Health Services. Veterans used for this cohort comparison are consistent with the 100 consecutive patients who underwent angiography for limb salvage in 2022.

This research was approved by the Baylor College of Medicine Institutional Review Board (protocol H-34858) and the MEDVAMC Research Committee (IRBNet protocol 15A12. HB). All analyses used deidentified data in the R programming language version 4.2.2 using RStudio version 2022.06.0 Build 421.

Program Description

MEDVAMC is a 350-bed teaching hospital located in central Houston. Its hospital system includes 11 outpatient clinics, ranging from 28 to 126 miles (eAppendix, Supplemental Figure A) from MEDVAMC. MEDVAMC provides vascular, orthopedic, and podiatric surgery services, as well as many other highly specialized services such as liver and heart transplants. The hospital’s risk-adjusted rates of operative morbidity and mortality (observed-to-expected ratios) are significantly lower than expected.

Despite this, the incidence rate of leg amputations at MEDVAMC in early 2011 was nearly 3-times higher than the VHA average. The inpatient management of veterans with infected foot ulcers was fragmented, with the general, orthopedic, and vascular surgery teams separately providing siloed care. Delays in treatment were common. There was much service- and practitioner-level practice heterogeneity. No diagnostic or treatment protocols were used, and standard treatment components were sporadically provided.

Patient Population

Compared to the matched non-VHA patient cohort (Supplemental Table 1), veterans treated at MEDVAMC for limb salvage are older. Nearly half (46%) identify as Black, which is associated with a 2-fold higher riskadjusted rate of leg amputations.4 MEDVAMC patients also have significantly higher rates of diabetes, chronic kidney disease, and systolic heart failure. About 22% travel > 40 miles for treatment at MEDVAMC, double that of the matched cohort (10.7%). Additionally, 35% currently smoke and 37% have moderate to severe peripheral artery disease (PAD).5

Program Design

In late 2011, the MEDVAMC vascular surgery team led limb salvage efforts by implementing a single team model, which involved assuming the primary role of managing foot ulcers for all veterans, both infected and uninfected (eAppendix, Supplemental Figure B). Consultations were directed to a dedicated limb salvage pager. The vascular team provided interdisciplinary limb salvage management across the spectrum of disease, including the surgical treatment of infection, assessment for PAD, open surgical operations and endovascular interventions to treat PAD, and foot reconstruction (debridement, minor or partial foot amputations, and skin grafting). This care was complemented by frequent consultation with the infectious disease, vascular medicine, podiatry, and geriatric wound care teams. This approach streamlined the delivery of consistent multidisciplinary care.

This collaborative effort aimed to develop ideal multidisciplinary care plans through research spanning the spectrum of the diabetic foot infection disease process (eAppendix, Supplemental Table 1). Some of the most impactful practices were: (1) a proclivity towards surgical treatment of foot infections, especially osteomyelitis5; (2) improved identification of PAD6,7; (3) early surgical closure of foot wounds following revascularization8,9; and (4) palliative wound care as an alternative to leg amputation in veterans who are not candidates for revascularization and limb salvage.10 Initally, the vascular surgery team held monthly multidisciplinary limb salvage meetings to coordinate patient management, identify ways to streamline care and avoid waste, discuss research findings, and review the 12-month rolling average of the MEDVAMC leg amputation incidence rate.

During the study period, the MEDVAMC vascular surgery team consisted of 2 to 5 board certified vascular or general surgeons, 2 or 3 nurse practitioners, and 3 vascular ultrasound technologists. Associated specialists included 2 podiatrists, 3 geriatricians with wound care certification, as well as additional infectious diseases, vascular medicine, orthopedics, and general surgery specialists.

Program Assessment

We noted a significant and sustained decrease in the MEDVAMC leg amputation rate after implementing multidisciplinary meetings and a single- team model from early 2012 through 2017 (Figure 2). The amputation incidence rate decreased steadily over the period from a maximum of 160 per 100,000 per year in February 2012 to a nadir of 66 per 100,000 per year in April 2017, an overall 60% decrease. Increases were noted in early 2018 after ceasing the single- team model, and in the summer of 2022, following periods of bed shortages after the onset of the COVID-19 pandemic. Tracking this metric allowed clinicians to make course corrections.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center.

The decreased leg amputation rate at MEDVAMC does not seem to be mirroring national or regional trends. During this 10-year period, the VHA annualized amputation rate decreased minimally, from 58 to 54 per 100,000 (eAppendix Supplemental Figure C). Leg amputation incidence at non-VHA hospitals in Texas slightly increased over the same period.11

Value was also reflected in other metrics. MEDVAMC improved safety through a bundled strategy that reduced the risk-adjusted rate of surgical wound infections by 95%.12 MEDVAMC prioritized limb salvage when selecting patients for angiography and nearly eliminated using stent-grafts, cryopreserved allogeneic saphenous vein grafts, and expensive surgical and endovascular implants, which were identified as more expensive and less effective than other options (Figure 3).13-15 The MEDVAMC team achieved a > 90% patient trust rating on the Veterans Signals survey in fiscal years 2021 and 2022.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center

Challenges

A significant increase in the patient-physician ratio occurred 5 years into the program. In 2016, 2 vascular surgeons left MEDVAMC and a planned renovation of 1 of the 2 vascular surgery-assigned hybrid working facilities began even as the number of MEDVAMC patients with diabetes grew 120% (from 89,400 to 107,746 between 2010 and 2016), and the incidence rate of foot ulcers grew 300% (from 392 in 2010 to 1183 in 2016 per 100,000). The net result was a higher clinical workload among the remaining vascular surgeons with less operating room availability.

To stabilize surgeon retention, MEDVAMC reverted from the single team model back to inpatient care being distributed among general surgery, orthopedic surgery, and vascular surgery. After noting an increase in the leg amputation incidence rate, we adjusted the focus from multidisciplinary to interdisciplinary care (ie, majority of limb salvage clinical care can be provided by practitioners of any involved specialties). We worked to establish a local, written, interdisciplinary consensus on evaluating and managing veterans with nonhealing foot ulcers to mitigate the loss of a consolidated inpatient approach. Despite frequent staff turnover, ≥ 1 physician or surgeon from the core specialties of vascular surgery, podiatry, and infectious diseases remained throughout the study period.

The COVID-19 pandemic caused a shortage of hospital beds. This was followed by more bed shortages due to decreased nursing staff. Our health care system also had a period of restricted outpatient encounters early in the pandemic. During this time, we noted a delayed presentation of veterans with advanced infections and another increase in leg amputation incidence rate.

Like many health systems, MEDVAMC pivoted to telephone- and video-based outpatient encounters. Our team also used publicly available Texas hospitalization data to identify zip codes with particularly high leg amputation incidence rates, and > 3500 educational mailings to veterans categorized as moderate and high risk for leg amputation in these zip codes. These mailings provided information on recognizing foot ulcers and infections, emphasized timely evaluation, and named the MEDVAMC vascular surgery team as a point-of-contact. More recently, we have seen a further decrease in the MEDVAMC incidences of leg amputation to its lowest rate in > 20 years.

Discussion

A learning organization that directs its research based on clinical observations and informs its clinical care with research findings can produce palpable improvements in outcomes. Understanding the disease process and trying to better understand management across the entire range of this disease process has allowed our team to make consistent and systematic changes in care (Table). Consolidating inpatient care in a single team model seems to have been effective in reducing amputation rates among veterans with diabetes. The role the MEDVAMC vascular surgery team served for limb salvage patients may have been particularly beneficial because of the large impact untreated or unidentified PAD can have and because of the high prevalence of PAD among the limb salvage population seen at MEDVAMC. To be sustainable, though, a single-team model needs resources. A multiteam model can also be effective if the degree of multidisciplinary involvement for any given veteran is appropriate to the individual's clinical needs, teams are engaged and willing to contribute in a defined role within their specialty, and lines of communication remain open.

The primary challenge at MEDVAMC has been, and will continue to be, the retention of physicians and surgeons. MEDVAMC has excellent leadership and a collegial working environment, but better access to operating rooms for elective and time-sensitive operations, additional clinical staff support, and higher salary at non-VA positions have been the basis for many of physicians— especially surgeons—leaving MEDVAMC. Despite high staff turnover and a constant flow of resident and fellow trainees, MEDVAMC has been able to keep the clinical approach relatively consistent due to the use of written protocols and continuity of care as ≥ 1 physician or surgeon from each of the 4 main teams remained engaged with limb salvage throughout the entire period.

Going forward, we will work to ensure that all requirements of the 2022 Prevention of Amputation in Veterans Everywhere directive are incorporated into care.8 We plan to standardize MEDVAMC management algorithms further, both to streamline care and reduce the opportunity for disparities in treatment. More prophylactic podiatric procedures, surgical forms of offloading, and a shared multidisciplinary clinic space may also further help patients.

Conclusions

The introduction of multidisciplinary limb salvage at MEDVAMC has led to significant and sustained reductions in leg amputation incidence. These reductions do not seem dependent upon a specific team structure for inpatient care. To improve patient outcomes, efforts should focus on making improvements across the entire disease spectrum. For limb salvage, this includes primary prevention of foot ulcers, the treatment of foot infections, identification and management of PAD, surgical reconstruction/optimal wound healing, and care for patients who undergo leg amputation.

Individuals with diabetes are at risk for developing foot ulcers or full-thickness defects in the epithelium of the foot. These defects can lead to bacterial invasion and foot infection, potentially resulting in leg amputation (Figure 1). Effective treatment to prevent leg amputation, known as limb salvage, requires management across multiple medical specialties including podiatry, vascular surgery, and infectious diseases. The multidisciplinary team approach to limb salvage was introduced in Boston in 1928 and has been the prevailing approach to this cross-specialty medical problem for at least a decade.1,2

Figure courtesy of Neal Barshes.

The Michael E. DeBakey Veterans Affairs Medical Center (MEDVAMC) has established an inpatient limb salvage program—a group of dedicated clinicians working collaboratively to provide evidence-guided management of patients hospitalized with foot ulcers, foot gangrene or any superimposed infection with the goal of avoiding leg amputations. We have seen a significant and durable reduction in the incidence of leg amputations among veterans at MEDVAMC.

This article describes the evolution and outcomes of the MEDVAMC limb salvage program over more than a decade. It includes changes to team structure and workflow, as well as past and present successes and challenges. The eAppendix provides a narrative summary with examples of how our clinical practice and research efforts have informed one another and how these findings are applied to clinical management. This process is part of the larger efforts of the Veterans Health Administration (VHA) to create a learning health system in which “internal data and experience are systematically integrated with external evidence, and that knowledge is put into practice.”3

Methods

Data from the VHA Support Service Center were used to obtain monthly major (leg) and minor (toe and partial foot) amputation records at MEDVAMC from October 2000 through May 2023. Yearly totals for the number of persons with diabetes and foot ulcers at MEDVAMC were also obtained from the support service center. Annual patient population sizes and number of persons with foot ulcers were converted to monthly estimates using cubic spline interpolation. Rates were calculated as 12-month rolling averages. Trend lines were created with locally weighted running line smoothing that used a span α of 0.1.

We characterized the patient population using data from cohorts of veterans treated for foot ulcers and foot infections at MEDVAMC. To compare the contemporary veteran population with nonveteran inpatients treated for foot ulcers and foot infections at other hospitals, we created a 2:1 nonveteran to veteran cohort matched by sex and zip code, using publicly available hospital admission data from the Texas Department of Health and State Health Services. Veterans used for this cohort comparison are consistent with the 100 consecutive patients who underwent angiography for limb salvage in 2022.

This research was approved by the Baylor College of Medicine Institutional Review Board (protocol H-34858) and the MEDVAMC Research Committee (IRBNet protocol 15A12. HB). All analyses used deidentified data in the R programming language version 4.2.2 using RStudio version 2022.06.0 Build 421.

Program Description

MEDVAMC is a 350-bed teaching hospital located in central Houston. Its hospital system includes 11 outpatient clinics, ranging from 28 to 126 miles (eAppendix, Supplemental Figure A) from MEDVAMC. MEDVAMC provides vascular, orthopedic, and podiatric surgery services, as well as many other highly specialized services such as liver and heart transplants. The hospital’s risk-adjusted rates of operative morbidity and mortality (observed-to-expected ratios) are significantly lower than expected.

Despite this, the incidence rate of leg amputations at MEDVAMC in early 2011 was nearly 3-times higher than the VHA average. The inpatient management of veterans with infected foot ulcers was fragmented, with the general, orthopedic, and vascular surgery teams separately providing siloed care. Delays in treatment were common. There was much service- and practitioner-level practice heterogeneity. No diagnostic or treatment protocols were used, and standard treatment components were sporadically provided.

Patient Population

Compared to the matched non-VHA patient cohort (Supplemental Table 1), veterans treated at MEDVAMC for limb salvage are older. Nearly half (46%) identify as Black, which is associated with a 2-fold higher riskadjusted rate of leg amputations.4 MEDVAMC patients also have significantly higher rates of diabetes, chronic kidney disease, and systolic heart failure. About 22% travel > 40 miles for treatment at MEDVAMC, double that of the matched cohort (10.7%). Additionally, 35% currently smoke and 37% have moderate to severe peripheral artery disease (PAD).5

Program Design

In late 2011, the MEDVAMC vascular surgery team led limb salvage efforts by implementing a single team model, which involved assuming the primary role of managing foot ulcers for all veterans, both infected and uninfected (eAppendix, Supplemental Figure B). Consultations were directed to a dedicated limb salvage pager. The vascular team provided interdisciplinary limb salvage management across the spectrum of disease, including the surgical treatment of infection, assessment for PAD, open surgical operations and endovascular interventions to treat PAD, and foot reconstruction (debridement, minor or partial foot amputations, and skin grafting). This care was complemented by frequent consultation with the infectious disease, vascular medicine, podiatry, and geriatric wound care teams. This approach streamlined the delivery of consistent multidisciplinary care.

This collaborative effort aimed to develop ideal multidisciplinary care plans through research spanning the spectrum of the diabetic foot infection disease process (eAppendix, Supplemental Table 1). Some of the most impactful practices were: (1) a proclivity towards surgical treatment of foot infections, especially osteomyelitis5; (2) improved identification of PAD6,7; (3) early surgical closure of foot wounds following revascularization8,9; and (4) palliative wound care as an alternative to leg amputation in veterans who are not candidates for revascularization and limb salvage.10 Initally, the vascular surgery team held monthly multidisciplinary limb salvage meetings to coordinate patient management, identify ways to streamline care and avoid waste, discuss research findings, and review the 12-month rolling average of the MEDVAMC leg amputation incidence rate.

During the study period, the MEDVAMC vascular surgery team consisted of 2 to 5 board certified vascular or general surgeons, 2 or 3 nurse practitioners, and 3 vascular ultrasound technologists. Associated specialists included 2 podiatrists, 3 geriatricians with wound care certification, as well as additional infectious diseases, vascular medicine, orthopedics, and general surgery specialists.

Program Assessment

We noted a significant and sustained decrease in the MEDVAMC leg amputation rate after implementing multidisciplinary meetings and a single- team model from early 2012 through 2017 (Figure 2). The amputation incidence rate decreased steadily over the period from a maximum of 160 per 100,000 per year in February 2012 to a nadir of 66 per 100,000 per year in April 2017, an overall 60% decrease. Increases were noted in early 2018 after ceasing the single- team model, and in the summer of 2022, following periods of bed shortages after the onset of the COVID-19 pandemic. Tracking this metric allowed clinicians to make course corrections.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center.

The decreased leg amputation rate at MEDVAMC does not seem to be mirroring national or regional trends. During this 10-year period, the VHA annualized amputation rate decreased minimally, from 58 to 54 per 100,000 (eAppendix Supplemental Figure C). Leg amputation incidence at non-VHA hospitals in Texas slightly increased over the same period.11

Value was also reflected in other metrics. MEDVAMC improved safety through a bundled strategy that reduced the risk-adjusted rate of surgical wound infections by 95%.12 MEDVAMC prioritized limb salvage when selecting patients for angiography and nearly eliminated using stent-grafts, cryopreserved allogeneic saphenous vein grafts, and expensive surgical and endovascular implants, which were identified as more expensive and less effective than other options (Figure 3).13-15 The MEDVAMC team achieved a > 90% patient trust rating on the Veterans Signals survey in fiscal years 2021 and 2022.

Abbreviation: MEDVAMC, Michael E. DeBakey Veterans Affairs Medical Center

Challenges

A significant increase in the patient-physician ratio occurred 5 years into the program. In 2016, 2 vascular surgeons left MEDVAMC and a planned renovation of 1 of the 2 vascular surgery-assigned hybrid working facilities began even as the number of MEDVAMC patients with diabetes grew 120% (from 89,400 to 107,746 between 2010 and 2016), and the incidence rate of foot ulcers grew 300% (from 392 in 2010 to 1183 in 2016 per 100,000). The net result was a higher clinical workload among the remaining vascular surgeons with less operating room availability.

To stabilize surgeon retention, MEDVAMC reverted from the single team model back to inpatient care being distributed among general surgery, orthopedic surgery, and vascular surgery. After noting an increase in the leg amputation incidence rate, we adjusted the focus from multidisciplinary to interdisciplinary care (ie, majority of limb salvage clinical care can be provided by practitioners of any involved specialties). We worked to establish a local, written, interdisciplinary consensus on evaluating and managing veterans with nonhealing foot ulcers to mitigate the loss of a consolidated inpatient approach. Despite frequent staff turnover, ≥ 1 physician or surgeon from the core specialties of vascular surgery, podiatry, and infectious diseases remained throughout the study period.

The COVID-19 pandemic caused a shortage of hospital beds. This was followed by more bed shortages due to decreased nursing staff. Our health care system also had a period of restricted outpatient encounters early in the pandemic. During this time, we noted a delayed presentation of veterans with advanced infections and another increase in leg amputation incidence rate.

Like many health systems, MEDVAMC pivoted to telephone- and video-based outpatient encounters. Our team also used publicly available Texas hospitalization data to identify zip codes with particularly high leg amputation incidence rates, and > 3500 educational mailings to veterans categorized as moderate and high risk for leg amputation in these zip codes. These mailings provided information on recognizing foot ulcers and infections, emphasized timely evaluation, and named the MEDVAMC vascular surgery team as a point-of-contact. More recently, we have seen a further decrease in the MEDVAMC incidences of leg amputation to its lowest rate in > 20 years.

Discussion

A learning organization that directs its research based on clinical observations and informs its clinical care with research findings can produce palpable improvements in outcomes. Understanding the disease process and trying to better understand management across the entire range of this disease process has allowed our team to make consistent and systematic changes in care (Table). Consolidating inpatient care in a single team model seems to have been effective in reducing amputation rates among veterans with diabetes. The role the MEDVAMC vascular surgery team served for limb salvage patients may have been particularly beneficial because of the large impact untreated or unidentified PAD can have and because of the high prevalence of PAD among the limb salvage population seen at MEDVAMC. To be sustainable, though, a single-team model needs resources. A multiteam model can also be effective if the degree of multidisciplinary involvement for any given veteran is appropriate to the individual's clinical needs, teams are engaged and willing to contribute in a defined role within their specialty, and lines of communication remain open.

The primary challenge at MEDVAMC has been, and will continue to be, the retention of physicians and surgeons. MEDVAMC has excellent leadership and a collegial working environment, but better access to operating rooms for elective and time-sensitive operations, additional clinical staff support, and higher salary at non-VA positions have been the basis for many of physicians— especially surgeons—leaving MEDVAMC. Despite high staff turnover and a constant flow of resident and fellow trainees, MEDVAMC has been able to keep the clinical approach relatively consistent due to the use of written protocols and continuity of care as ≥ 1 physician or surgeon from each of the 4 main teams remained engaged with limb salvage throughout the entire period.

Going forward, we will work to ensure that all requirements of the 2022 Prevention of Amputation in Veterans Everywhere directive are incorporated into care.8 We plan to standardize MEDVAMC management algorithms further, both to streamline care and reduce the opportunity for disparities in treatment. More prophylactic podiatric procedures, surgical forms of offloading, and a shared multidisciplinary clinic space may also further help patients.

Conclusions

The introduction of multidisciplinary limb salvage at MEDVAMC has led to significant and sustained reductions in leg amputation incidence. These reductions do not seem dependent upon a specific team structure for inpatient care. To improve patient outcomes, efforts should focus on making improvements across the entire disease spectrum. For limb salvage, this includes primary prevention of foot ulcers, the treatment of foot infections, identification and management of PAD, surgical reconstruction/optimal wound healing, and care for patients who undergo leg amputation.

References
  1. Sanders LJ, Robbins JM, Edmonds ME. History of the team approach to amputation prevention: pioneers and milestones. J Am Podiatr Med Assoc. 2010;100(5):317- 334. doi:10.7547/1000317
  2. Sumpio BE, Armstrong DG, Lavery LA, Andros G. The role of interdisciplinary team approach in the management of the diabetic foot: a joint statement from the society for vascular surgery and the American podiatric medical association. J Am Podiatr Med Assoc. 2010;100(4):309-311. doi:10.7547/1000309
  3. About learning health systems. Agency for Healthcare Research and Quality. Published March 2019. Updated May 2019. Accessed October 9, 2024. https://www.ahrq.gov/learning-health-systems/about.html
  4. Barshes NR, Minc SD. Healthcare disparities in vascular surgery: a critical review. J Vasc Surg. 2021;74(2S):6S-14S.
  5. Barshes NR, Mindru C, Ashong C, Rodriguez-Barradas M, Trautner BW. Treatment failure and leg amputation among patients with foot osteomyelitis. Int J Low Extrem Wounds. 2016;15(4):303-312. doi:10.1177/1534734616661058
  6. Barshes NR, Flores E, Belkin M, Kougias P, Armstrong DG, Mills JL Sr. The accuracy and cost-effectiveness of strategies used to identify peripheral artery disease among patients with diabetic foot ulcers. J Vasc Surg. 2016;64(6):1682-1690.e3. doi:10.1016/j.jvs.2016.04.056 e1. doi:10.1016/j.jvs.2021.03.055
  7. Choi JC, Miranda J, Greenleaf E, et al. Lower-extremity pressure, staging, and grading thresholds to identify chronic limb-threatening ischemia. Vasc Med. 2023;28(1):45-53. doi:10.1177/1358863X221147945
  8. Barshes NR, Chambers JD, Cohen J, Belkin M; Model To Optimize Healthcare Value in Ischemic Extremities 1 (MOVIE) Study Collaborators. Cost-effectiveness in the contemporary management of critical limb ischemia with tissue loss. J Vasc Surg. 2012;56(4):1015-24.e1. doi:10.1016/j.jvs.2012.02.069
  9. Barshes NR, Bechara CF, Pisimisis G, Kougias P. Preliminary experiences with early primary closure of foot wounds after lower extremity revascularization. Ann Vasc Surg. 2014;28(1):48-52. doi:10.1016/j.avsg.2013.06.012
  10. Barshes NR, Gold B, Garcia A, Bechara CF, Pisimisis G, Kougias P. Minor amputation and palliative wound care as a strategy to avoid major amputation in patients with foot infections and severe peripheral arterial disease. Int J Low Extrem Wounds. 2014;13(3):211-219. doi:10.1177/1534734614543663
  11. Garcia M, Hernandez B, Ellington TG, et al. A lack of decline in major nontraumatic amputations in Texas: contemporary trends, risk factor associations, and impact of revascularization. Diabetes Care. 2019;42(6):1061-1066. doi:10.2337/dc19-0078
  12. Zamani N, Sharath SE, Vo E, Awad SS, Kougias P, Barshes NR. A multi-component strategy to decrease wound complications after open infra-inguinal re-vascularization. Surg Infect (Larchmt). 2018;19(1):87-94. doi:10.1089/sur.2017.193
  13. Barshes NR, Ozaki CK, Kougias P, Belkin M. A costeffectiveness analysis of infrainguinal bypass in the absence of great saphenous vein conduit. J Vasc Surg. 2013;57(6):1466-1470. doi:10.1016/j.jvs.2012.11.115
  14. Zamani N, Sharath S, Browder R, et al. PC158 longterm outcomes after endovascular stent placement for symptomatic, long-segment superficial femoral artery lesions. J Vasc Surg. 2017;65(6):182S-183S. doi:10.1016/j.jvs.2017.03.344
  15. Zamani N, Sharath SE, Browder RC, et al. Outcomes after endovascular stent placement for long-segment superficial femoral artery lesions. Ann Vasc Surg. 2021;71:298-307. doi:10.1016/j.avsg.2020.08.124
References
  1. Sanders LJ, Robbins JM, Edmonds ME. History of the team approach to amputation prevention: pioneers and milestones. J Am Podiatr Med Assoc. 2010;100(5):317- 334. doi:10.7547/1000317
  2. Sumpio BE, Armstrong DG, Lavery LA, Andros G. The role of interdisciplinary team approach in the management of the diabetic foot: a joint statement from the society for vascular surgery and the American podiatric medical association. J Am Podiatr Med Assoc. 2010;100(4):309-311. doi:10.7547/1000309
  3. About learning health systems. Agency for Healthcare Research and Quality. Published March 2019. Updated May 2019. Accessed October 9, 2024. https://www.ahrq.gov/learning-health-systems/about.html
  4. Barshes NR, Minc SD. Healthcare disparities in vascular surgery: a critical review. J Vasc Surg. 2021;74(2S):6S-14S.
  5. Barshes NR, Mindru C, Ashong C, Rodriguez-Barradas M, Trautner BW. Treatment failure and leg amputation among patients with foot osteomyelitis. Int J Low Extrem Wounds. 2016;15(4):303-312. doi:10.1177/1534734616661058
  6. Barshes NR, Flores E, Belkin M, Kougias P, Armstrong DG, Mills JL Sr. The accuracy and cost-effectiveness of strategies used to identify peripheral artery disease among patients with diabetic foot ulcers. J Vasc Surg. 2016;64(6):1682-1690.e3. doi:10.1016/j.jvs.2016.04.056 e1. doi:10.1016/j.jvs.2021.03.055
  7. Choi JC, Miranda J, Greenleaf E, et al. Lower-extremity pressure, staging, and grading thresholds to identify chronic limb-threatening ischemia. Vasc Med. 2023;28(1):45-53. doi:10.1177/1358863X221147945
  8. Barshes NR, Chambers JD, Cohen J, Belkin M; Model To Optimize Healthcare Value in Ischemic Extremities 1 (MOVIE) Study Collaborators. Cost-effectiveness in the contemporary management of critical limb ischemia with tissue loss. J Vasc Surg. 2012;56(4):1015-24.e1. doi:10.1016/j.jvs.2012.02.069
  9. Barshes NR, Bechara CF, Pisimisis G, Kougias P. Preliminary experiences with early primary closure of foot wounds after lower extremity revascularization. Ann Vasc Surg. 2014;28(1):48-52. doi:10.1016/j.avsg.2013.06.012
  10. Barshes NR, Gold B, Garcia A, Bechara CF, Pisimisis G, Kougias P. Minor amputation and palliative wound care as a strategy to avoid major amputation in patients with foot infections and severe peripheral arterial disease. Int J Low Extrem Wounds. 2014;13(3):211-219. doi:10.1177/1534734614543663
  11. Garcia M, Hernandez B, Ellington TG, et al. A lack of decline in major nontraumatic amputations in Texas: contemporary trends, risk factor associations, and impact of revascularization. Diabetes Care. 2019;42(6):1061-1066. doi:10.2337/dc19-0078
  12. Zamani N, Sharath SE, Vo E, Awad SS, Kougias P, Barshes NR. A multi-component strategy to decrease wound complications after open infra-inguinal re-vascularization. Surg Infect (Larchmt). 2018;19(1):87-94. doi:10.1089/sur.2017.193
  13. Barshes NR, Ozaki CK, Kougias P, Belkin M. A costeffectiveness analysis of infrainguinal bypass in the absence of great saphenous vein conduit. J Vasc Surg. 2013;57(6):1466-1470. doi:10.1016/j.jvs.2012.11.115
  14. Zamani N, Sharath S, Browder R, et al. PC158 longterm outcomes after endovascular stent placement for symptomatic, long-segment superficial femoral artery lesions. J Vasc Surg. 2017;65(6):182S-183S. doi:10.1016/j.jvs.2017.03.344
  15. Zamani N, Sharath SE, Browder RC, et al. Outcomes after endovascular stent placement for long-segment superficial femoral artery lesions. Ann Vasc Surg. 2021;71:298-307. doi:10.1016/j.avsg.2020.08.124
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THE DIAGNOSIS: White Fibrous Papulosis

Given the histopathology findings, location on a sun-exposed site, lack of any additional systemic signs or symptoms, and no family history of similar lesions to suggest an underlying genetic condition, a diagnosis of white fibrous papulosis (WFP) was made. White fibrous papulosis is a relatively rare cutaneous disorder that was first reported by Shimizu et al1 in 1985. It is characterized by numerous grouped, 2- to 3-mm, white to flesh-colored papules that in most cases are confined to the neck in middle-aged to elderly individuals; however, cases involving the upper trunk and axillae also have been reported.1-3 The etiology of this condition is unclear but is thought to be related to aging and chronic exposure to UV light. Although treatment is not required, various modalities including tretinoin, excision, and laser therapy have been trialed with varying success.2,4 Our patient elected not to proceed with treatment.

Histologically, WFP may manifest similarly to connective tissue nevi; the overall architecture is nonspecific with focally thickened collagen and often elastic fibers that may be normal to reduced and/or fragmented, as well as an overall decrease in superficial dermal elastic tissue.3,5 Therefore, the differential diagnosis may include connective tissue nevi and require clinical correlation to make a correct diagnosis.

Pseudoxanthoma elasticum (PXE) is an autosomalrecessive disorder most commonly related to mutations in the ATP binding cassette subfamily C member 6 (ABCC6) gene that tends to manifest clinically on the neck and flexural extremities.6 This disease affects elastic fibers, which may become calcified over time. Pseudoxanthoma elasticum is associated with ocular complications relating to the Bruch membrane of the retina and angioid streaks; choroidal neovascularization involving the damaged Bruch membrane and episodes of acute retinopathy may result in vision loss in later stages of the disease.7 Involvement of the elastic laminae of arteries can be associated with cardiovascular and cerebrovascular complications such as stroke, coronary artery disease, claudication, and aneurysms. Involvement of the gastrointestinal or genitourinary tracts also may occur and most commonly manifests with bleeding. Pathologic alterations in the elastic fibers of the lungs also have been reported in patients with PXE.8 Histologically, PXE exhibits increased abnormally clumped and fragmented elastic fibers in the superficial dermis, often with calcification (Figure 1). Pseudo-PXE related to D-penicillamine use often lacks calcification and has a bramble bush appearance.9

FIGURE 1. Pseudoxanthoma elasticum demonstrates increased abnormally clumped calcified and fragmented elastic fibers (H&E, original magnification ×100).

Fibrofolliculomas may manifest alone or in association with an underlying condition such as Birt-Hogg-Dubé syndrome, in which lesions are most frequently seen scattered on the scalp, face, ears, neck, or upper trunk.10 This condition is related to a folliculin (FLCN) gene germline mutation. Birt-Hogg-Dubé syndrome also may be associated with acrochordons, trichodiscomas, renal cancer, and lung cysts with or without spontaneous pneumothorax. Less frequently noted findings include oral papules, epidermal cysts, angiofibromas, lipomas/angiolipomas, parotid gland tumors, and thyroid neoplasms. Connective tissue nevi/collagenomas can appear clinically similar to fibrofolliculomas; true connective tissue nevi are reported less commonly in Birt-Hogg-Dubé syndrome.11 Histologically, a fibrofolliculoma manifests with epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (Figure 2).

FIGURE 2. Fibrofolliculoma demonstrates epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (H&E, original magnification ×20).

Elastofibroma dorsi is a benign tumor of connective tissue that most commonly manifests clinically as a solitary subcutaneous mass on the back near the inferior angle of the scapula; it typically develops below the rhomboid major and latissimus dorsi muscles.12 The pathogenesis is uncertain, but some patients have reported a family history of the condition or a history of repetitive shoulder movement/trauma prior to onset; the mass may be asymptomatic or associated with pain and/or swelling. Those affected tend to be older than 50 years.13 Histologically, thickened and rounded to beaded elastic fibers are seen admixed with collagen (Figure 3).

FIGURE 3. A and B, Elastofibroma demonstrates thickened and rounded to beaded elastic fibers (H&E, original magnification ×40), which stain deeply positive with Verhoff-Van Gieson (original magnification ×40).

Actinic (solar) elastosis frequently is encountered in many skin biopsies and is caused by chronic photodamage. More hypertrophic variants, such as papular or nodular solar elastosis, may clinically manifest similarly to WFP.14 Histologically, actinic elastosis manifests as a considerable increase in elastic tissue in the papillary and superficial reticular dermis (Figure 4).

FIGURE 4. Actinic elastosis manifests as basophilic degenerated elastic fibers in the dermis (H&E, original magnification ×100).

References
  1. Shimizu H, Nishikawa T, Kimura S. White fibrous papulosis of the neck: review of our 16 cases. Nihon Hifuka Gakkai Zasshi. 1985;95:1077-1084.
  2. Teo W, Pang S. White fibrous papulosis of the chest and back. J Am Acad Dermatol. 2012;66:AB33.
  3. Dokic Y, Tschen J. White fibrous papulosis of the axillae and neck. Cureus. 2020;12:E7635.
  4. Lueangarun S, Panchaprateep R. White fibrous papulosis of the neck treated with fractionated 1550-nm erbium glass laser: a case report. J Lasers Med Sci. 2016;7:256-258.
  5. Rios-Gomez M, Ramos-Garibay JA, Perez-Santana ME, et al. White fibrous papulosis of the neck: a case report. Cureus. 2022;14:E25661.
  6. Váradi A, Szabó Z, Pomozi V, et al. ABCC6 as a target in pseudoxanthoma elasticum. Curr Drug Targets. 2011;12:671-682.
  7. Gliem M, Birtel J, Müller PL, et al. Acute retinopathy in pseudoxanthoma elasticum. JAMA Ophthalmol. 2019;137:1165-1173.
  8. Germain DP. Pseudoxanthoma elasticum. Orphanet J Rare Dis. 2017;12:85. doi:10.1186/s13023-017-0639-8
  9. Chisti MA, Binamer Y, Alfadley A, et al. D-penicillamine-induced pseudo-pseudoxanthoma elasticum and extensive elastosis perforans serpiginosa with excellent response to acitretin. Ann Saudi Med. 2019;39:56-60.
  10. Criscito MC, Mu EW, Meehan SA, et al. Dermoscopic features of a solitary fibrofolliculoma on the left cheek. J Am Acad Dermatol. 2017;76(2 suppl 1):S8-S9.
  11. Sattler EC, Steinlein OK. Birt-Hogg-Dubé syndrome. In: Adam MP, Everman DB, Mirzaa GM, et al, eds. GeneReviews® [Internet]. Updated January 30, 2020. Accessed February 23, 2023. https://www.ncbi.nlm.nih.gov/books/NBK1522
  12. Patnayak R, Jena A, Settipalli S, et al. Elastofibroma: an uncommon tumor revisited. J Cutan Aesthet Surg. 2016;9:34-37. doi:10.4103/0974- 2077.178543
  13. Chandrasekar CR, Grimer RJ, Carter SR, et al. Elastofibroma dorsi: an uncommon benign pseudotumour. Sarcoma. 2008;2008:756565. doi:10.1155/2008/756565
  14. Kwittken J. Papular elastosis. Cutis. 2000;66:81-83.
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Drs. Wieser and Rohr are from the Department of Dermatology, University Hospitals, Cleveland, Ohio. Elise Keshock is from the University of Central Florida College of Medicine, Orlando. Dr. Chang is from Cleveland Skin Pathology, Beachwood, Ohio.

The authors have no relevant financial disclosures to report.

Correspondence: Jill Wieser, MD, 7840 Vinewood Ln N, Maple Grove, MN 55369 (jill.wieser.2@gmail.com).

Cutis. 2024 November;114(5):154,162-163. doi:10.12788/cutis.1119

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Drs. Wieser and Rohr are from the Department of Dermatology, University Hospitals, Cleveland, Ohio. Elise Keshock is from the University of Central Florida College of Medicine, Orlando. Dr. Chang is from Cleveland Skin Pathology, Beachwood, Ohio.

The authors have no relevant financial disclosures to report.

Correspondence: Jill Wieser, MD, 7840 Vinewood Ln N, Maple Grove, MN 55369 (jill.wieser.2@gmail.com).

Cutis. 2024 November;114(5):154,162-163. doi:10.12788/cutis.1119

Author and Disclosure Information

Drs. Wieser and Rohr are from the Department of Dermatology, University Hospitals, Cleveland, Ohio. Elise Keshock is from the University of Central Florida College of Medicine, Orlando. Dr. Chang is from Cleveland Skin Pathology, Beachwood, Ohio.

The authors have no relevant financial disclosures to report.

Correspondence: Jill Wieser, MD, 7840 Vinewood Ln N, Maple Grove, MN 55369 (jill.wieser.2@gmail.com).

Cutis. 2024 November;114(5):154,162-163. doi:10.12788/cutis.1119

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THE DIAGNOSIS: White Fibrous Papulosis

Given the histopathology findings, location on a sun-exposed site, lack of any additional systemic signs or symptoms, and no family history of similar lesions to suggest an underlying genetic condition, a diagnosis of white fibrous papulosis (WFP) was made. White fibrous papulosis is a relatively rare cutaneous disorder that was first reported by Shimizu et al1 in 1985. It is characterized by numerous grouped, 2- to 3-mm, white to flesh-colored papules that in most cases are confined to the neck in middle-aged to elderly individuals; however, cases involving the upper trunk and axillae also have been reported.1-3 The etiology of this condition is unclear but is thought to be related to aging and chronic exposure to UV light. Although treatment is not required, various modalities including tretinoin, excision, and laser therapy have been trialed with varying success.2,4 Our patient elected not to proceed with treatment.

Histologically, WFP may manifest similarly to connective tissue nevi; the overall architecture is nonspecific with focally thickened collagen and often elastic fibers that may be normal to reduced and/or fragmented, as well as an overall decrease in superficial dermal elastic tissue.3,5 Therefore, the differential diagnosis may include connective tissue nevi and require clinical correlation to make a correct diagnosis.

Pseudoxanthoma elasticum (PXE) is an autosomalrecessive disorder most commonly related to mutations in the ATP binding cassette subfamily C member 6 (ABCC6) gene that tends to manifest clinically on the neck and flexural extremities.6 This disease affects elastic fibers, which may become calcified over time. Pseudoxanthoma elasticum is associated with ocular complications relating to the Bruch membrane of the retina and angioid streaks; choroidal neovascularization involving the damaged Bruch membrane and episodes of acute retinopathy may result in vision loss in later stages of the disease.7 Involvement of the elastic laminae of arteries can be associated with cardiovascular and cerebrovascular complications such as stroke, coronary artery disease, claudication, and aneurysms. Involvement of the gastrointestinal or genitourinary tracts also may occur and most commonly manifests with bleeding. Pathologic alterations in the elastic fibers of the lungs also have been reported in patients with PXE.8 Histologically, PXE exhibits increased abnormally clumped and fragmented elastic fibers in the superficial dermis, often with calcification (Figure 1). Pseudo-PXE related to D-penicillamine use often lacks calcification and has a bramble bush appearance.9

FIGURE 1. Pseudoxanthoma elasticum demonstrates increased abnormally clumped calcified and fragmented elastic fibers (H&E, original magnification ×100).

Fibrofolliculomas may manifest alone or in association with an underlying condition such as Birt-Hogg-Dubé syndrome, in which lesions are most frequently seen scattered on the scalp, face, ears, neck, or upper trunk.10 This condition is related to a folliculin (FLCN) gene germline mutation. Birt-Hogg-Dubé syndrome also may be associated with acrochordons, trichodiscomas, renal cancer, and lung cysts with or without spontaneous pneumothorax. Less frequently noted findings include oral papules, epidermal cysts, angiofibromas, lipomas/angiolipomas, parotid gland tumors, and thyroid neoplasms. Connective tissue nevi/collagenomas can appear clinically similar to fibrofolliculomas; true connective tissue nevi are reported less commonly in Birt-Hogg-Dubé syndrome.11 Histologically, a fibrofolliculoma manifests with epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (Figure 2).

FIGURE 2. Fibrofolliculoma demonstrates epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (H&E, original magnification ×20).

Elastofibroma dorsi is a benign tumor of connective tissue that most commonly manifests clinically as a solitary subcutaneous mass on the back near the inferior angle of the scapula; it typically develops below the rhomboid major and latissimus dorsi muscles.12 The pathogenesis is uncertain, but some patients have reported a family history of the condition or a history of repetitive shoulder movement/trauma prior to onset; the mass may be asymptomatic or associated with pain and/or swelling. Those affected tend to be older than 50 years.13 Histologically, thickened and rounded to beaded elastic fibers are seen admixed with collagen (Figure 3).

FIGURE 3. A and B, Elastofibroma demonstrates thickened and rounded to beaded elastic fibers (H&E, original magnification ×40), which stain deeply positive with Verhoff-Van Gieson (original magnification ×40).

Actinic (solar) elastosis frequently is encountered in many skin biopsies and is caused by chronic photodamage. More hypertrophic variants, such as papular or nodular solar elastosis, may clinically manifest similarly to WFP.14 Histologically, actinic elastosis manifests as a considerable increase in elastic tissue in the papillary and superficial reticular dermis (Figure 4).

FIGURE 4. Actinic elastosis manifests as basophilic degenerated elastic fibers in the dermis (H&E, original magnification ×100).

THE DIAGNOSIS: White Fibrous Papulosis

Given the histopathology findings, location on a sun-exposed site, lack of any additional systemic signs or symptoms, and no family history of similar lesions to suggest an underlying genetic condition, a diagnosis of white fibrous papulosis (WFP) was made. White fibrous papulosis is a relatively rare cutaneous disorder that was first reported by Shimizu et al1 in 1985. It is characterized by numerous grouped, 2- to 3-mm, white to flesh-colored papules that in most cases are confined to the neck in middle-aged to elderly individuals; however, cases involving the upper trunk and axillae also have been reported.1-3 The etiology of this condition is unclear but is thought to be related to aging and chronic exposure to UV light. Although treatment is not required, various modalities including tretinoin, excision, and laser therapy have been trialed with varying success.2,4 Our patient elected not to proceed with treatment.

Histologically, WFP may manifest similarly to connective tissue nevi; the overall architecture is nonspecific with focally thickened collagen and often elastic fibers that may be normal to reduced and/or fragmented, as well as an overall decrease in superficial dermal elastic tissue.3,5 Therefore, the differential diagnosis may include connective tissue nevi and require clinical correlation to make a correct diagnosis.

Pseudoxanthoma elasticum (PXE) is an autosomalrecessive disorder most commonly related to mutations in the ATP binding cassette subfamily C member 6 (ABCC6) gene that tends to manifest clinically on the neck and flexural extremities.6 This disease affects elastic fibers, which may become calcified over time. Pseudoxanthoma elasticum is associated with ocular complications relating to the Bruch membrane of the retina and angioid streaks; choroidal neovascularization involving the damaged Bruch membrane and episodes of acute retinopathy may result in vision loss in later stages of the disease.7 Involvement of the elastic laminae of arteries can be associated with cardiovascular and cerebrovascular complications such as stroke, coronary artery disease, claudication, and aneurysms. Involvement of the gastrointestinal or genitourinary tracts also may occur and most commonly manifests with bleeding. Pathologic alterations in the elastic fibers of the lungs also have been reported in patients with PXE.8 Histologically, PXE exhibits increased abnormally clumped and fragmented elastic fibers in the superficial dermis, often with calcification (Figure 1). Pseudo-PXE related to D-penicillamine use often lacks calcification and has a bramble bush appearance.9

FIGURE 1. Pseudoxanthoma elasticum demonstrates increased abnormally clumped calcified and fragmented elastic fibers (H&E, original magnification ×100).

Fibrofolliculomas may manifest alone or in association with an underlying condition such as Birt-Hogg-Dubé syndrome, in which lesions are most frequently seen scattered on the scalp, face, ears, neck, or upper trunk.10 This condition is related to a folliculin (FLCN) gene germline mutation. Birt-Hogg-Dubé syndrome also may be associated with acrochordons, trichodiscomas, renal cancer, and lung cysts with or without spontaneous pneumothorax. Less frequently noted findings include oral papules, epidermal cysts, angiofibromas, lipomas/angiolipomas, parotid gland tumors, and thyroid neoplasms. Connective tissue nevi/collagenomas can appear clinically similar to fibrofolliculomas; true connective tissue nevi are reported less commonly in Birt-Hogg-Dubé syndrome.11 Histologically, a fibrofolliculoma manifests with epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (Figure 2).

FIGURE 2. Fibrofolliculoma demonstrates epidermal strands originating from a hair follicle associated with prominent surrounding connective tissue (H&E, original magnification ×20).

Elastofibroma dorsi is a benign tumor of connective tissue that most commonly manifests clinically as a solitary subcutaneous mass on the back near the inferior angle of the scapula; it typically develops below the rhomboid major and latissimus dorsi muscles.12 The pathogenesis is uncertain, but some patients have reported a family history of the condition or a history of repetitive shoulder movement/trauma prior to onset; the mass may be asymptomatic or associated with pain and/or swelling. Those affected tend to be older than 50 years.13 Histologically, thickened and rounded to beaded elastic fibers are seen admixed with collagen (Figure 3).

FIGURE 3. A and B, Elastofibroma demonstrates thickened and rounded to beaded elastic fibers (H&E, original magnification ×40), which stain deeply positive with Verhoff-Van Gieson (original magnification ×40).

Actinic (solar) elastosis frequently is encountered in many skin biopsies and is caused by chronic photodamage. More hypertrophic variants, such as papular or nodular solar elastosis, may clinically manifest similarly to WFP.14 Histologically, actinic elastosis manifests as a considerable increase in elastic tissue in the papillary and superficial reticular dermis (Figure 4).

FIGURE 4. Actinic elastosis manifests as basophilic degenerated elastic fibers in the dermis (H&E, original magnification ×100).

References
  1. Shimizu H, Nishikawa T, Kimura S. White fibrous papulosis of the neck: review of our 16 cases. Nihon Hifuka Gakkai Zasshi. 1985;95:1077-1084.
  2. Teo W, Pang S. White fibrous papulosis of the chest and back. J Am Acad Dermatol. 2012;66:AB33.
  3. Dokic Y, Tschen J. White fibrous papulosis of the axillae and neck. Cureus. 2020;12:E7635.
  4. Lueangarun S, Panchaprateep R. White fibrous papulosis of the neck treated with fractionated 1550-nm erbium glass laser: a case report. J Lasers Med Sci. 2016;7:256-258.
  5. Rios-Gomez M, Ramos-Garibay JA, Perez-Santana ME, et al. White fibrous papulosis of the neck: a case report. Cureus. 2022;14:E25661.
  6. Váradi A, Szabó Z, Pomozi V, et al. ABCC6 as a target in pseudoxanthoma elasticum. Curr Drug Targets. 2011;12:671-682.
  7. Gliem M, Birtel J, Müller PL, et al. Acute retinopathy in pseudoxanthoma elasticum. JAMA Ophthalmol. 2019;137:1165-1173.
  8. Germain DP. Pseudoxanthoma elasticum. Orphanet J Rare Dis. 2017;12:85. doi:10.1186/s13023-017-0639-8
  9. Chisti MA, Binamer Y, Alfadley A, et al. D-penicillamine-induced pseudo-pseudoxanthoma elasticum and extensive elastosis perforans serpiginosa with excellent response to acitretin. Ann Saudi Med. 2019;39:56-60.
  10. Criscito MC, Mu EW, Meehan SA, et al. Dermoscopic features of a solitary fibrofolliculoma on the left cheek. J Am Acad Dermatol. 2017;76(2 suppl 1):S8-S9.
  11. Sattler EC, Steinlein OK. Birt-Hogg-Dubé syndrome. In: Adam MP, Everman DB, Mirzaa GM, et al, eds. GeneReviews® [Internet]. Updated January 30, 2020. Accessed February 23, 2023. https://www.ncbi.nlm.nih.gov/books/NBK1522
  12. Patnayak R, Jena A, Settipalli S, et al. Elastofibroma: an uncommon tumor revisited. J Cutan Aesthet Surg. 2016;9:34-37. doi:10.4103/0974- 2077.178543
  13. Chandrasekar CR, Grimer RJ, Carter SR, et al. Elastofibroma dorsi: an uncommon benign pseudotumour. Sarcoma. 2008;2008:756565. doi:10.1155/2008/756565
  14. Kwittken J. Papular elastosis. Cutis. 2000;66:81-83.
References
  1. Shimizu H, Nishikawa T, Kimura S. White fibrous papulosis of the neck: review of our 16 cases. Nihon Hifuka Gakkai Zasshi. 1985;95:1077-1084.
  2. Teo W, Pang S. White fibrous papulosis of the chest and back. J Am Acad Dermatol. 2012;66:AB33.
  3. Dokic Y, Tschen J. White fibrous papulosis of the axillae and neck. Cureus. 2020;12:E7635.
  4. Lueangarun S, Panchaprateep R. White fibrous papulosis of the neck treated with fractionated 1550-nm erbium glass laser: a case report. J Lasers Med Sci. 2016;7:256-258.
  5. Rios-Gomez M, Ramos-Garibay JA, Perez-Santana ME, et al. White fibrous papulosis of the neck: a case report. Cureus. 2022;14:E25661.
  6. Váradi A, Szabó Z, Pomozi V, et al. ABCC6 as a target in pseudoxanthoma elasticum. Curr Drug Targets. 2011;12:671-682.
  7. Gliem M, Birtel J, Müller PL, et al. Acute retinopathy in pseudoxanthoma elasticum. JAMA Ophthalmol. 2019;137:1165-1173.
  8. Germain DP. Pseudoxanthoma elasticum. Orphanet J Rare Dis. 2017;12:85. doi:10.1186/s13023-017-0639-8
  9. Chisti MA, Binamer Y, Alfadley A, et al. D-penicillamine-induced pseudo-pseudoxanthoma elasticum and extensive elastosis perforans serpiginosa with excellent response to acitretin. Ann Saudi Med. 2019;39:56-60.
  10. Criscito MC, Mu EW, Meehan SA, et al. Dermoscopic features of a solitary fibrofolliculoma on the left cheek. J Am Acad Dermatol. 2017;76(2 suppl 1):S8-S9.
  11. Sattler EC, Steinlein OK. Birt-Hogg-Dubé syndrome. In: Adam MP, Everman DB, Mirzaa GM, et al, eds. GeneReviews® [Internet]. Updated January 30, 2020. Accessed February 23, 2023. https://www.ncbi.nlm.nih.gov/books/NBK1522
  12. Patnayak R, Jena A, Settipalli S, et al. Elastofibroma: an uncommon tumor revisited. J Cutan Aesthet Surg. 2016;9:34-37. doi:10.4103/0974- 2077.178543
  13. Chandrasekar CR, Grimer RJ, Carter SR, et al. Elastofibroma dorsi: an uncommon benign pseudotumour. Sarcoma. 2008;2008:756565. doi:10.1155/2008/756565
  14. Kwittken J. Papular elastosis. Cutis. 2000;66:81-83.
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A 70-year-old woman with a history of osteoporosis and breast cancer presented for evaluation of asymptomatic, 2- to 3-mm, white to flesh-colored papules concentrated on the inferior occipital scalp and posterior neck (inset) for at least several months. She had no additional systemic signs or symptoms, and there was no family history of similar skin findings. A punch biopsy was performed.

H&E, original magnification ×4 (inset, asymptomatic, 2- to 3-mm, white to flesh-colored papules concentrated on the posterior neck).

Verhoeff-Van Gieson, original magnification ×4.

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Eating Disorder Risk Factors and the Impact of Obesity in Patients With Psoriasis

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Eating Disorder Risk Factors and the Impact of Obesity in Patients With Psoriasis

Psoriasis is a chronic multisystemic inflammatory skin disease with a worldwide prevalence of 2% to 3%.1 Psoriasis can be accompanied by other conditions such as psoriatic arthritis, obesity, metabolic syndrome, diabetes mellitus, hypertension, dyslipidemia, atherosclerotic disease, inflammatory bowel disease, and anxiety/depression. It is important to manage comorbidities of psoriasis in addition to treating the cutaneous manifestations of the disease.1

Obesity is a major public health concern worldwide. Numerous observational and epidemiologic studies have reported a high prevalence of obesity among patients with psoriasis.2 Current evidence indicates that obesity may initiate or worsen psoriasis; furthermore, it is important to note that obesity may negatively impact the effectiveness of psoriasis-specific treatments or increase the incidence of adverse effects. Therefore, managing obesity is crucial in the treatment of psoriasis.3 Numerous studies have investigated the association between psoriasis and obesity, and they commonly conclude that both conditions share the same genetic metabolic pathways.2-4 However, it is important to consider environmental factors such as dietary habits, smoking, alcohol consumption, and a sedentary lifestyle—all of which are associated with psoriasis and also can contribute to the development of obesity.5 Because of the effects of obesity in psoriasis patients, factors that impact the development of obesity have become a popular research topic.

Eating disorders (EDs) are a crucial risk factor for both developing and maintaining obesity. In particular, two EDs that are associated with obesity include binge eating disorder and bulimia nervosa.6 According to the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition,7 binge eating disorder can be diagnosed when a patient has at least 1 episode of binge eating per week over a 3-month period. Bulimia nervosa can be diagnosed when a patient is excessively concerned with their body weight and shape and engages in behaviors to prevent weight gain (eg, forced vomiting, excessive use of laxatives).7 Psychiatrists who specialize in EDs make diagnoses based on these criteria. In daily practice, there are several quick and simple questionnaires available to screen for EDs that can be used by nonpsychiatrist physicians, including the commonly used 26-item Eating Attitudes Test (EAT-26).8 The EAT-26 has been used to screen for EDs in patients with inflammatory disorders.9

The aim of this study was to screen for EDs in patients with psoriasis to identify potential risk factors for development of obesity.

Materials and Methods

This study included patients with psoriasis who were screened for EDs at a tertiary dermatology clinic in Turkey between January 2021 and December 2023. This study was approved by the local ethics committee and was in accordance with the Declaration of Helsinki (decision number E-93471371-514.99-225000079).

Study Design and Patient Inclusion Criteria—This quantitative cross-sectional study utilized EAT-26, Dermatology Life Quality Index (DLQI), Attitude Scale for Healthy Nutrition (ASHN), and Depression Anxiety Stress Scale-21 (DASS-21) scores. All the questionnaire scales used in the study were adapted and validated in Turkey.8,10-12 The inclusion criteria consisted of being older than 18 years of age, being literate, having psoriasis for at least 1 year that was not treated topically or systemically, and having no psychiatric diseases outside an ED. The questionnaires were presented in written format following the clinical examination. Literacy was an inclusion criterion in this study due to the absence of auxiliary health personnel.

Study Variables—The study variables included age, sex, marital status (single/divorced or married), education status (primary/secondary school or high school/university), employment status (employed or unemployed/retired), body mass index (BMI), smoking status, alcohol-consumption status, Psoriasis Area Severity Index score, presence of nail psoriasis and psoriatic arthritis, duration of psoriasis, family history of psoriasis, EAT-26 score, ASHN score, DLQI score, and DASS-21 score. Body mass index was calculated by taking a participant’s weight in kilograms and dividing it by their height in meters squared. The BMI values were classified into 3 categories: normal (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), and obese (≥30 kg/m2).13

Questionnaires—The EAT-26 questionnaire includes 26 questions that are used to detect EDs. Responses to each question include Likert-type answer options (ie, “always,” “usually,” “often,” “sometimes,” “rarely,” and “never.”) Patients with scores of 20 points or higher (range, 0–78) are classified as high risk for EDs.8 In our study, EAT-26 scores were grouped into 2 categories: patients scoring less than 20 points and those scoring 20 points or higher.

The DLQI questionnaire includes 10 questions to measure dermatologic symptoms and qualiy of life. Responses to each question include Likert-type answer options (ie, “not at all,” “a little,” “a lot,” or “very much.”) On the DLQI scale, the higher the score, the lower the quality of life (score range, 0–30).10

The ASHN questionnaire includes 21 questions that measure attitudes toward healthy nutrition with 5 possible answer options (“strongly disagree,” “disagree,” “undecided,” “agree,” and “strongly agree”). On this scale, higher scores indicate the participant is more knowledgeable about healthy nutrition (score range, 0–78).11

The DASS-21 questionnaire includes 21 questions that measure the severity of a range of symptoms common to depression, anxiety, and stress. Responses include Likert-type answer options (eg, “never,” “sometimes,” “often,” and “almost always.”) On this scale, a higher score (range of 0–21 for each) indicates higher levels of depression, anxiety, and stress.12

Statistical Analysis—Descriptive statistics were analyzed using SPSS software version 22.0 (IBM). The Shapiro-Wilk test was applied to determine whether the data were normally distributed. For categorical variables, frequency differences among groups were compared using the Pearson χ2 test. A t test was used to compare the means of 2 independent groups with a normal distribution. One-way analysis of variance and Tukey Honest Significant Difference post hoc analysis were used to test whether there was a statistically significant difference among the normally distributed means of independent groups. Pearson correlation analysis was used to determine whether there was a linear relationship between 2 numeric measurements and, if so, to determine the direction and severity of this relationship. P<.05 indicated statistical significance in this study.

Results

Study Participant Demographics—This study included 82 participants with a mean age of 44.3 years; 52.4% (43/82) were female, and 85.4% (70/82) were married. The questionnaire took an average of 4.2 minutes for participants to complete. A total of 57.3% (47/82) of patients had completed primary/secondary education and 59.8% (49/82) were employed. The mean BMI was 28.1 kg/m2. According to the BMI classification, 26.8% (22/82) participants had a normal weight, 36.6% (30/82) were overweight, and 43.9% (36/82) were obese. A total of 48.8% (40/82) of participants smoked, and 4.9% (4/82) consumed alcohol. The mean Psoriasis Area and Severity Index score was 5.4. A total of 54.9% (45/82) of participants had nail psoriasis, and 24.4% (20/82) had psoriatic arthritis. The mean duration of psoriasis was 153 months. A total of 29.3% (24/82) of participants had a positive family history of psoriasis. The mean EAT-26 score was 11.1. A total of 12.2% (10/82) of participants had an EAT-26 score of 20 points or higher and were considered at high risk for an ED. The mean ASHN score was 72.9; the mean DLQI score was 5.5; and on the DASS-21 scale, mean scores for depression, anxiety, and stress were 6.3, 8.7, and 10.0, respectively (Table).

Comparative Evaluation of the BMI Groups—The only statistically significant differences among the 3 BMI groups were related to marital status, EAT-26 score, and anxiety and stress scores (P=.02, <.01, <.01, and <.01, respectively)(eTable 1). The number of single/divorced participants in the overweight group was significantly (P=.02) greater than in the normal weight group. The mean EAT-26 score for the normal weight group was significantly (P<.01) lower than for the overweight and obese groups; there was no significant difference in mean EAT-26 scores between the overweight and obese groups. The mean anxiety score was significantly (P<.01) lower in the normal weight group compared with the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean depression score. The mean stress and anxiety scores were significantly (P<.01) lower in the normal weight group than in the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean anxiety score.



Comparative Evaluation of the EAT-26 Scores—There were statistically significant differences among the EAT-26 scores related to sex; BMI; and depression, anxiety, and stress scores (P=.04, .02, <.01, <.01, and <.01, respectively). The number of females in the group with a score of 20 points or higher was significantly (P=.04) less than that in the group scoring less than 20 points. The mean BMI in the group with a score of 20 points or higher was significantly (P=.02) greater than in group scoring less than 20 points. The mean depression, anxiety, and stress scores of the group scoring 20 points or higher were significantly (P<.01 for all) greater than in the group scoring less than 20 points (eTable 2).



Correlation Analysis of the Study Variables—The EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress (P<.01 for all)(eTable 3).

Comment

Eating disorders are psychiatric conditions that require a multidisciplinary approach. Nonpsychiatric medical departments may be involved due to the severe consequences (eg, various skin changes14) of these disorders. Psoriasis is not known to be directly affected by the presence of an ED; however, it is possible that EDs could indirectly affect patients with psoriasis by influencing obesity. Therefore, this study aimed to examine the relationship between ED risk factors and obesity in this population.

The relationship between psoriasis and obesity has been a popular research topic in dermatology since the 1990s.15 Epidemiologic and observational studies have reported that patients with psoriasis are more likely to be overweight or have obesity, which is an independent risk factor for psoriasis.3,16 However, the causal relationship between psoriasis and obesity remains unclear. In a comprehensive review, Barros et al17 emphasized the causal relationship between obesity and psoriasis under several headings. Firstly, a higher BMI increases the risk for psoriasis by promoting cytokine release and immune system dysregulation. Secondly, a Western diet (eg, processed foods and fast food) triggers obesity and psoriasis by increasing adipose tissue. Thirdly, the alteration of the skin and gut microbiota triggers chronic inflammation as a result of bacterial translocation in patients with obesity. Fourthly, a high-fat diet and palmitic acid disrupt the intestinal integrity of the gut and increase the risk for psoriasis and obesity by triggering chronic inflammation of bacterial fragments that pass into the blood. Finally, the decrease in the amount of adiponectin and the increase in the amount of leptin in patients with obesity may cause psoriasis by increasing proinflammatory cytokines, which are similar to those involved in the pathogenesis of psoriasis.17 Additionally, psoriatic inflammation can cause insulin resistance and metabolic dysfunction, leading to obesity.18 The relationship between psoriasis and obesity cannot be solely explained by metabolic pathways. Smoking, alcohol consumption, and a sedentary lifestyle all are associated with psoriasis and also can contribute to obesity.5 Our study revealed no significant difference in smoking or alcohol consumption between the normal weight and overweight/obesity groups. Based on our data, we determined that smoking and alcohol consumption did not affect obesity in our patients with psoriasis.

Observational and epidemiologic studies have shown that patients with psoriasis experience increased rates of depression, anxiety, and stress.19 In studies of pathogenesis, a connection between depression and psoriatic inflammation has been established.20 It is known that inflammatory cytokines similar to those in psoriasis are involved in the development of obesity.18 In addition, depression and anxiety can lead to binge eating, unhealthy food choices, and a more sedentary lifestyle.5 All of these variables may contribute to the associations between depression and anxiety with psoriasis and obesity. Zafiriou et al21 conducted a study to investigate the relationship between psoriasis, obesity, and depression through inflammatory pathways with a focus on the importance of IL-17. Data showing that IL-17–producing Th17-cell subgroups play a considerable role in the development of obesity and depression prompted the authors to suggest that psoriasis, obesity, and ­anxiety/depression may be interconnected manifestations of immune dysregulation, potentially linked to IL-17 and its associated cells.21 Mrowietz et al22 also suggested that metabolic inflammation may contribute to obesity and depression in patients with psoriasis and highlighted the importance of several cytokines, including tumor necrosis factor α, IL-6, IL-8, IL-17, and IL-23. Our study revealed no significant differences in depression scores between BMI groups. Another meta-analysis reported conflicting findings on the incidence of depression in obese patients with psoriasis.23 Some of the studies had a small number of participants. Compared to depression, anxiety has received less attention in studies of patients with obesity with psoriasis. However, these studies have shown a positive correlation between anxiety scores and BMI in patients with psoriasis.24,25 In our study, similar to the findings of previous studies, overweight patients and those with obesitywho have psoriasis had significantly (P<.01) greater anxiety and stress scores than did normal weight patients with psoriasis.

Obesity should be assessed in patients with psoriasis via a biopsychosocial approach that takes into account genetic, behavioral, and environmental factors.26 Eating disorders are considered to be one of the factors contributing to obesity. Numerous studies in the literature have demonstrated a greater incidence of EDs in patients with obesity vs those without obesity.5,6,27 Obesity and EDs have a bidirectional relationship: individuals with obesity are at risk for EDs due to body dissatisfaction, dieting habits, and depressive states. Conversely, poor eating behaviors in individuals with a normal weight can lead to obesity.28

There are few studies in the literature exploring the relationship between psoriasis and EDs. Crosta et al29 demonstrated that patients with psoriasis had impaired results on ED screening tests and that these scores deteriorated further as BMI increased. Moreover, Altunay et al30 demonstrated that patients with psoriasis and metabolic syndrome had higher scores on the ED screening test. In this study, patients with higher scores also exhibited high levels of anxiety.30 In our study, similar to the findings of previous studies, patients with psoriasis who were overweight or had obesity had significantly (P<.01) greater EAT-26 scores than those in the normal weight group. Patients with high EAT-26 scores also exhibited elevated levels of depression, anxiety, and stress. Additionally, EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress scores. Our study as well as other studies in the literature indicate that additional research is needed to determine the associations between EDs and obesity in psoriasis.

Conclusion

Managing obesity is crucial for patients with psoriasis. This study showed that EAT-26 scores were higher in patients with psoriasis who were overweight or had obesity than in those who were normal weight. Participants with high EAT-26 scores (≥20 points) were more likely to be female and have higher anxiety and stress scores. In addition, EAT-26 scores were positively correlated with BMI as well as depression, anxiety, and stress scores. Eating disorders may contribute to the development of obesity in patients with psoriasis. Although our study was limited by a small sample size, the results suggest that there is a need for large-scale multicenter studies to investigate the relationship between psoriasis and EDs.

References
  1. Kalkan G. Comorbidities in psoriasis: the recognition of psoriasis as a systemic disease and current management. Turkderm-Turk Arch Dermatol Venereol. 2017;51:71-77.
  2. Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutr Diabetes. 2012;2:E54.
  3. Jensen P, Skov L. Psoriasis and obesity. Dermatology. 2016;232:633-639.
  4. Mirghani H, Altemani AT, Altemani ST, et al. The cross talk between psoriasis, obesity, and dyslipidemia: a meta-analysis. Cureus. 2023;15:e49253.
  5. Roehring M, Mashep MR, White MA, et al. The metabolic syndrome and behavioral correlates in obese patients with binge disorders. Obesity. 2009;17:481-486.
  6. da Luz FQ, Hay P, Touyz S, et al. Obesity with comorbid eating disorders: associated health risks and treatment approaches. Nutrients. 2018;10:829.
  7. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition. American Psychiatric Association; 2013.
  8. Ergüney Okumus¸ FE, Sertel Berk HÖ. The psychometric properties of the Eating Attitudes Test short form (EAT-26) in a college sample. Stud Psychol. 2020;40:57-78.
  9. Stoleru G, Leopold A, Auerbach A, et al. Female gender, dissatisfaction with weight, and number of IBD related surgeries as independent risk factors for eating disorders among patients with inflammatory bowel diseases. BMC Gastroenterol. 2022;22:438.
  10. Öztürkcan S, Ermertcan AT, Eser E, et al. Cross validation of the Turkish version of dermatology life quality index. Int J Dermatol. 2006;45:1300-1307.
  11. Demir GT, Ciciog˘lu HI˙. Attitude scale for healthy nutrition (ASHN): validity and reliability study. Gaziantep Univ J Sport Sci. 2019;4:256-274.
  12. Yılmaz O, Boz H, Arslan A. The validity and reliability of depression stress and anxiety scale (DASS 21) Turkish short form. Res Financial Econ Soc Stud. 2017;2:78-91.
  13. Nuttall FQ. Body mass index: obesity, BMI, and health: a critical review. Nutr Today. 2015;50:117-128.
  14. Strumia R, Manzata E, Gualandi M. Is there a role for dermatologists in eating disorders? Expert Rev Dermatol. 2017; 2:109-112.
  15. Henseler T, Christophers E. Disease concomitance in psoriasis. J Am Acad Dermatol. 1995;32:982-986.
  16. Naldi L, Addis A, Chimenti S, et al. Impact of body mass index and obesity on clinical response to systemic treatment for psoriasis. evidence from the Psocare project. Dermatology. 2008;217:365-373.
  17. Barros G, Duran P, Vera I, et al. Exploring the links between obesity and psoriasis: a comprehensive review. Int J Mol Sci. 2022;23:7499.
  18. Hao Y, Zhu YJ, Zou S, et al. Metabolic syndrome and psoriasis: mechanisms and future directions. Front Immunol. 2021;12:711060.
  19. Jing D, Xiao H, Shen M, et al. Association of psoriasis with anxiety and depression: a case–control study in Chinese patients. Front Med (Lausanne). 2021;8:771645.
  20. Sahi FM, Masood A, Danawar NA, et al. Association between psoriasis and depression: a traditional review. Cureus. 2020;12:E9708.
  21. Zafiriou E, Daponte AI, Siokas V, et al. Depression and obesity in patients with psoriasis and psoriatic arthritis: is IL-17–mediated immune dysregulation the connecting link? Front Immunol. 2021;12:699848.
  22. Mrowietz U, Sümbül M, Gerdes S. Depression, a major comorbidity of psoriatic disease, is caused by metabolic inflammation. J Eur Acad Dermatol Venereol. 2023;37:1731-1738.
  23. Pavlova NT, Kioskli K, Smith C, et al. Psychosocial aspects of obesity in adults with psoriasis: a systematic review. Skin Health Dis. 2021;1:E33.
  24. Innamorati M, Quinto RM, Imperatori C, et al. Health-related quality of life and its association with alexithymia and difficulties in emotion regulation in patients with psoriasis. Compr Psychiatry. 2016;70:200-208.
  25. Tabolli S, Naldi L, Pagliarello C, et al. Evaluation of the impact of writing exercises interventions on quality of life in patients with psoriasis undergoing systemic treatments. Br J Dermatol. 2012;167:1254‐1264.
  26. Albuquerque D, Nóbrega C, Manco L, et al. The contribution of genetics and environment to obesity. Br Med Bull. 2017;123:159‐173.
  27. Balantekin KN, Grammer AC, Fitzsimmons-Craft EE, et al. Overweight and obesity are associated with increased eating disorder correlates and general psychopathology in university women with eating disorders. Eat Behav. 2021;41:101482.
  28. Jebeile H, Lister NB, Baur LA, et al. Eating disorder risk in adolescents with obesity. Obes Rev. 2021;22:E13173.
  29. Crosta ML, Caldarola G, Fraietta S, et al. Psychopathology and eating disorders in patients with psoriasis. G Ital Dermatol Venereol. 2014;149:355-361.
  30. Altunay I, Demirci GT, Ates B, et al. Do eating disorders accompany metabolic syndrome in psoriasis patients? results of a preliminary study. Clin Cosmet Investig Dermatol. 2011;4:139-143.
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From the Department of Dermatology, Ministry of Health, Ankara Training and Research Hospital, Turkey.

The authors have no relevant financial disclosures to report.

The eTables are available in the Appendix online at www.mdedge.com/dermatology.

Correspondence: Berkay Temel, MD, Department of Dermatology, Ankara Training and Research Hospital, Ulucanlar St No: 89, Ankara, Turkey (berkaytemel42@gmail.com).

Cutis. 2024 November;114(5):164-168, E1-E5. doi:10.12788/cutis.1130

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The eTables are available in the Appendix online at www.mdedge.com/dermatology.

Correspondence: Berkay Temel, MD, Department of Dermatology, Ankara Training and Research Hospital, Ulucanlar St No: 89, Ankara, Turkey (berkaytemel42@gmail.com).

Cutis. 2024 November;114(5):164-168, E1-E5. doi:10.12788/cutis.1130

Author and Disclosure Information

From the Department of Dermatology, Ministry of Health, Ankara Training and Research Hospital, Turkey.

The authors have no relevant financial disclosures to report.

The eTables are available in the Appendix online at www.mdedge.com/dermatology.

Correspondence: Berkay Temel, MD, Department of Dermatology, Ankara Training and Research Hospital, Ulucanlar St No: 89, Ankara, Turkey (berkaytemel42@gmail.com).

Cutis. 2024 November;114(5):164-168, E1-E5. doi:10.12788/cutis.1130

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Psoriasis is a chronic multisystemic inflammatory skin disease with a worldwide prevalence of 2% to 3%.1 Psoriasis can be accompanied by other conditions such as psoriatic arthritis, obesity, metabolic syndrome, diabetes mellitus, hypertension, dyslipidemia, atherosclerotic disease, inflammatory bowel disease, and anxiety/depression. It is important to manage comorbidities of psoriasis in addition to treating the cutaneous manifestations of the disease.1

Obesity is a major public health concern worldwide. Numerous observational and epidemiologic studies have reported a high prevalence of obesity among patients with psoriasis.2 Current evidence indicates that obesity may initiate or worsen psoriasis; furthermore, it is important to note that obesity may negatively impact the effectiveness of psoriasis-specific treatments or increase the incidence of adverse effects. Therefore, managing obesity is crucial in the treatment of psoriasis.3 Numerous studies have investigated the association between psoriasis and obesity, and they commonly conclude that both conditions share the same genetic metabolic pathways.2-4 However, it is important to consider environmental factors such as dietary habits, smoking, alcohol consumption, and a sedentary lifestyle—all of which are associated with psoriasis and also can contribute to the development of obesity.5 Because of the effects of obesity in psoriasis patients, factors that impact the development of obesity have become a popular research topic.

Eating disorders (EDs) are a crucial risk factor for both developing and maintaining obesity. In particular, two EDs that are associated with obesity include binge eating disorder and bulimia nervosa.6 According to the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition,7 binge eating disorder can be diagnosed when a patient has at least 1 episode of binge eating per week over a 3-month period. Bulimia nervosa can be diagnosed when a patient is excessively concerned with their body weight and shape and engages in behaviors to prevent weight gain (eg, forced vomiting, excessive use of laxatives).7 Psychiatrists who specialize in EDs make diagnoses based on these criteria. In daily practice, there are several quick and simple questionnaires available to screen for EDs that can be used by nonpsychiatrist physicians, including the commonly used 26-item Eating Attitudes Test (EAT-26).8 The EAT-26 has been used to screen for EDs in patients with inflammatory disorders.9

The aim of this study was to screen for EDs in patients with psoriasis to identify potential risk factors for development of obesity.

Materials and Methods

This study included patients with psoriasis who were screened for EDs at a tertiary dermatology clinic in Turkey between January 2021 and December 2023. This study was approved by the local ethics committee and was in accordance with the Declaration of Helsinki (decision number E-93471371-514.99-225000079).

Study Design and Patient Inclusion Criteria—This quantitative cross-sectional study utilized EAT-26, Dermatology Life Quality Index (DLQI), Attitude Scale for Healthy Nutrition (ASHN), and Depression Anxiety Stress Scale-21 (DASS-21) scores. All the questionnaire scales used in the study were adapted and validated in Turkey.8,10-12 The inclusion criteria consisted of being older than 18 years of age, being literate, having psoriasis for at least 1 year that was not treated topically or systemically, and having no psychiatric diseases outside an ED. The questionnaires were presented in written format following the clinical examination. Literacy was an inclusion criterion in this study due to the absence of auxiliary health personnel.

Study Variables—The study variables included age, sex, marital status (single/divorced or married), education status (primary/secondary school or high school/university), employment status (employed or unemployed/retired), body mass index (BMI), smoking status, alcohol-consumption status, Psoriasis Area Severity Index score, presence of nail psoriasis and psoriatic arthritis, duration of psoriasis, family history of psoriasis, EAT-26 score, ASHN score, DLQI score, and DASS-21 score. Body mass index was calculated by taking a participant’s weight in kilograms and dividing it by their height in meters squared. The BMI values were classified into 3 categories: normal (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), and obese (≥30 kg/m2).13

Questionnaires—The EAT-26 questionnaire includes 26 questions that are used to detect EDs. Responses to each question include Likert-type answer options (ie, “always,” “usually,” “often,” “sometimes,” “rarely,” and “never.”) Patients with scores of 20 points or higher (range, 0–78) are classified as high risk for EDs.8 In our study, EAT-26 scores were grouped into 2 categories: patients scoring less than 20 points and those scoring 20 points or higher.

The DLQI questionnaire includes 10 questions to measure dermatologic symptoms and qualiy of life. Responses to each question include Likert-type answer options (ie, “not at all,” “a little,” “a lot,” or “very much.”) On the DLQI scale, the higher the score, the lower the quality of life (score range, 0–30).10

The ASHN questionnaire includes 21 questions that measure attitudes toward healthy nutrition with 5 possible answer options (“strongly disagree,” “disagree,” “undecided,” “agree,” and “strongly agree”). On this scale, higher scores indicate the participant is more knowledgeable about healthy nutrition (score range, 0–78).11

The DASS-21 questionnaire includes 21 questions that measure the severity of a range of symptoms common to depression, anxiety, and stress. Responses include Likert-type answer options (eg, “never,” “sometimes,” “often,” and “almost always.”) On this scale, a higher score (range of 0–21 for each) indicates higher levels of depression, anxiety, and stress.12

Statistical Analysis—Descriptive statistics were analyzed using SPSS software version 22.0 (IBM). The Shapiro-Wilk test was applied to determine whether the data were normally distributed. For categorical variables, frequency differences among groups were compared using the Pearson χ2 test. A t test was used to compare the means of 2 independent groups with a normal distribution. One-way analysis of variance and Tukey Honest Significant Difference post hoc analysis were used to test whether there was a statistically significant difference among the normally distributed means of independent groups. Pearson correlation analysis was used to determine whether there was a linear relationship between 2 numeric measurements and, if so, to determine the direction and severity of this relationship. P<.05 indicated statistical significance in this study.

Results

Study Participant Demographics—This study included 82 participants with a mean age of 44.3 years; 52.4% (43/82) were female, and 85.4% (70/82) were married. The questionnaire took an average of 4.2 minutes for participants to complete. A total of 57.3% (47/82) of patients had completed primary/secondary education and 59.8% (49/82) were employed. The mean BMI was 28.1 kg/m2. According to the BMI classification, 26.8% (22/82) participants had a normal weight, 36.6% (30/82) were overweight, and 43.9% (36/82) were obese. A total of 48.8% (40/82) of participants smoked, and 4.9% (4/82) consumed alcohol. The mean Psoriasis Area and Severity Index score was 5.4. A total of 54.9% (45/82) of participants had nail psoriasis, and 24.4% (20/82) had psoriatic arthritis. The mean duration of psoriasis was 153 months. A total of 29.3% (24/82) of participants had a positive family history of psoriasis. The mean EAT-26 score was 11.1. A total of 12.2% (10/82) of participants had an EAT-26 score of 20 points or higher and were considered at high risk for an ED. The mean ASHN score was 72.9; the mean DLQI score was 5.5; and on the DASS-21 scale, mean scores for depression, anxiety, and stress were 6.3, 8.7, and 10.0, respectively (Table).

Comparative Evaluation of the BMI Groups—The only statistically significant differences among the 3 BMI groups were related to marital status, EAT-26 score, and anxiety and stress scores (P=.02, <.01, <.01, and <.01, respectively)(eTable 1). The number of single/divorced participants in the overweight group was significantly (P=.02) greater than in the normal weight group. The mean EAT-26 score for the normal weight group was significantly (P<.01) lower than for the overweight and obese groups; there was no significant difference in mean EAT-26 scores between the overweight and obese groups. The mean anxiety score was significantly (P<.01) lower in the normal weight group compared with the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean depression score. The mean stress and anxiety scores were significantly (P<.01) lower in the normal weight group than in the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean anxiety score.



Comparative Evaluation of the EAT-26 Scores—There were statistically significant differences among the EAT-26 scores related to sex; BMI; and depression, anxiety, and stress scores (P=.04, .02, <.01, <.01, and <.01, respectively). The number of females in the group with a score of 20 points or higher was significantly (P=.04) less than that in the group scoring less than 20 points. The mean BMI in the group with a score of 20 points or higher was significantly (P=.02) greater than in group scoring less than 20 points. The mean depression, anxiety, and stress scores of the group scoring 20 points or higher were significantly (P<.01 for all) greater than in the group scoring less than 20 points (eTable 2).



Correlation Analysis of the Study Variables—The EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress (P<.01 for all)(eTable 3).

Comment

Eating disorders are psychiatric conditions that require a multidisciplinary approach. Nonpsychiatric medical departments may be involved due to the severe consequences (eg, various skin changes14) of these disorders. Psoriasis is not known to be directly affected by the presence of an ED; however, it is possible that EDs could indirectly affect patients with psoriasis by influencing obesity. Therefore, this study aimed to examine the relationship between ED risk factors and obesity in this population.

The relationship between psoriasis and obesity has been a popular research topic in dermatology since the 1990s.15 Epidemiologic and observational studies have reported that patients with psoriasis are more likely to be overweight or have obesity, which is an independent risk factor for psoriasis.3,16 However, the causal relationship between psoriasis and obesity remains unclear. In a comprehensive review, Barros et al17 emphasized the causal relationship between obesity and psoriasis under several headings. Firstly, a higher BMI increases the risk for psoriasis by promoting cytokine release and immune system dysregulation. Secondly, a Western diet (eg, processed foods and fast food) triggers obesity and psoriasis by increasing adipose tissue. Thirdly, the alteration of the skin and gut microbiota triggers chronic inflammation as a result of bacterial translocation in patients with obesity. Fourthly, a high-fat diet and palmitic acid disrupt the intestinal integrity of the gut and increase the risk for psoriasis and obesity by triggering chronic inflammation of bacterial fragments that pass into the blood. Finally, the decrease in the amount of adiponectin and the increase in the amount of leptin in patients with obesity may cause psoriasis by increasing proinflammatory cytokines, which are similar to those involved in the pathogenesis of psoriasis.17 Additionally, psoriatic inflammation can cause insulin resistance and metabolic dysfunction, leading to obesity.18 The relationship between psoriasis and obesity cannot be solely explained by metabolic pathways. Smoking, alcohol consumption, and a sedentary lifestyle all are associated with psoriasis and also can contribute to obesity.5 Our study revealed no significant difference in smoking or alcohol consumption between the normal weight and overweight/obesity groups. Based on our data, we determined that smoking and alcohol consumption did not affect obesity in our patients with psoriasis.

Observational and epidemiologic studies have shown that patients with psoriasis experience increased rates of depression, anxiety, and stress.19 In studies of pathogenesis, a connection between depression and psoriatic inflammation has been established.20 It is known that inflammatory cytokines similar to those in psoriasis are involved in the development of obesity.18 In addition, depression and anxiety can lead to binge eating, unhealthy food choices, and a more sedentary lifestyle.5 All of these variables may contribute to the associations between depression and anxiety with psoriasis and obesity. Zafiriou et al21 conducted a study to investigate the relationship between psoriasis, obesity, and depression through inflammatory pathways with a focus on the importance of IL-17. Data showing that IL-17–producing Th17-cell subgroups play a considerable role in the development of obesity and depression prompted the authors to suggest that psoriasis, obesity, and ­anxiety/depression may be interconnected manifestations of immune dysregulation, potentially linked to IL-17 and its associated cells.21 Mrowietz et al22 also suggested that metabolic inflammation may contribute to obesity and depression in patients with psoriasis and highlighted the importance of several cytokines, including tumor necrosis factor α, IL-6, IL-8, IL-17, and IL-23. Our study revealed no significant differences in depression scores between BMI groups. Another meta-analysis reported conflicting findings on the incidence of depression in obese patients with psoriasis.23 Some of the studies had a small number of participants. Compared to depression, anxiety has received less attention in studies of patients with obesity with psoriasis. However, these studies have shown a positive correlation between anxiety scores and BMI in patients with psoriasis.24,25 In our study, similar to the findings of previous studies, overweight patients and those with obesitywho have psoriasis had significantly (P<.01) greater anxiety and stress scores than did normal weight patients with psoriasis.

Obesity should be assessed in patients with psoriasis via a biopsychosocial approach that takes into account genetic, behavioral, and environmental factors.26 Eating disorders are considered to be one of the factors contributing to obesity. Numerous studies in the literature have demonstrated a greater incidence of EDs in patients with obesity vs those without obesity.5,6,27 Obesity and EDs have a bidirectional relationship: individuals with obesity are at risk for EDs due to body dissatisfaction, dieting habits, and depressive states. Conversely, poor eating behaviors in individuals with a normal weight can lead to obesity.28

There are few studies in the literature exploring the relationship between psoriasis and EDs. Crosta et al29 demonstrated that patients with psoriasis had impaired results on ED screening tests and that these scores deteriorated further as BMI increased. Moreover, Altunay et al30 demonstrated that patients with psoriasis and metabolic syndrome had higher scores on the ED screening test. In this study, patients with higher scores also exhibited high levels of anxiety.30 In our study, similar to the findings of previous studies, patients with psoriasis who were overweight or had obesity had significantly (P<.01) greater EAT-26 scores than those in the normal weight group. Patients with high EAT-26 scores also exhibited elevated levels of depression, anxiety, and stress. Additionally, EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress scores. Our study as well as other studies in the literature indicate that additional research is needed to determine the associations between EDs and obesity in psoriasis.

Conclusion

Managing obesity is crucial for patients with psoriasis. This study showed that EAT-26 scores were higher in patients with psoriasis who were overweight or had obesity than in those who were normal weight. Participants with high EAT-26 scores (≥20 points) were more likely to be female and have higher anxiety and stress scores. In addition, EAT-26 scores were positively correlated with BMI as well as depression, anxiety, and stress scores. Eating disorders may contribute to the development of obesity in patients with psoriasis. Although our study was limited by a small sample size, the results suggest that there is a need for large-scale multicenter studies to investigate the relationship between psoriasis and EDs.

Psoriasis is a chronic multisystemic inflammatory skin disease with a worldwide prevalence of 2% to 3%.1 Psoriasis can be accompanied by other conditions such as psoriatic arthritis, obesity, metabolic syndrome, diabetes mellitus, hypertension, dyslipidemia, atherosclerotic disease, inflammatory bowel disease, and anxiety/depression. It is important to manage comorbidities of psoriasis in addition to treating the cutaneous manifestations of the disease.1

Obesity is a major public health concern worldwide. Numerous observational and epidemiologic studies have reported a high prevalence of obesity among patients with psoriasis.2 Current evidence indicates that obesity may initiate or worsen psoriasis; furthermore, it is important to note that obesity may negatively impact the effectiveness of psoriasis-specific treatments or increase the incidence of adverse effects. Therefore, managing obesity is crucial in the treatment of psoriasis.3 Numerous studies have investigated the association between psoriasis and obesity, and they commonly conclude that both conditions share the same genetic metabolic pathways.2-4 However, it is important to consider environmental factors such as dietary habits, smoking, alcohol consumption, and a sedentary lifestyle—all of which are associated with psoriasis and also can contribute to the development of obesity.5 Because of the effects of obesity in psoriasis patients, factors that impact the development of obesity have become a popular research topic.

Eating disorders (EDs) are a crucial risk factor for both developing and maintaining obesity. In particular, two EDs that are associated with obesity include binge eating disorder and bulimia nervosa.6 According to the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition,7 binge eating disorder can be diagnosed when a patient has at least 1 episode of binge eating per week over a 3-month period. Bulimia nervosa can be diagnosed when a patient is excessively concerned with their body weight and shape and engages in behaviors to prevent weight gain (eg, forced vomiting, excessive use of laxatives).7 Psychiatrists who specialize in EDs make diagnoses based on these criteria. In daily practice, there are several quick and simple questionnaires available to screen for EDs that can be used by nonpsychiatrist physicians, including the commonly used 26-item Eating Attitudes Test (EAT-26).8 The EAT-26 has been used to screen for EDs in patients with inflammatory disorders.9

The aim of this study was to screen for EDs in patients with psoriasis to identify potential risk factors for development of obesity.

Materials and Methods

This study included patients with psoriasis who were screened for EDs at a tertiary dermatology clinic in Turkey between January 2021 and December 2023. This study was approved by the local ethics committee and was in accordance with the Declaration of Helsinki (decision number E-93471371-514.99-225000079).

Study Design and Patient Inclusion Criteria—This quantitative cross-sectional study utilized EAT-26, Dermatology Life Quality Index (DLQI), Attitude Scale for Healthy Nutrition (ASHN), and Depression Anxiety Stress Scale-21 (DASS-21) scores. All the questionnaire scales used in the study were adapted and validated in Turkey.8,10-12 The inclusion criteria consisted of being older than 18 years of age, being literate, having psoriasis for at least 1 year that was not treated topically or systemically, and having no psychiatric diseases outside an ED. The questionnaires were presented in written format following the clinical examination. Literacy was an inclusion criterion in this study due to the absence of auxiliary health personnel.

Study Variables—The study variables included age, sex, marital status (single/divorced or married), education status (primary/secondary school or high school/university), employment status (employed or unemployed/retired), body mass index (BMI), smoking status, alcohol-consumption status, Psoriasis Area Severity Index score, presence of nail psoriasis and psoriatic arthritis, duration of psoriasis, family history of psoriasis, EAT-26 score, ASHN score, DLQI score, and DASS-21 score. Body mass index was calculated by taking a participant’s weight in kilograms and dividing it by their height in meters squared. The BMI values were classified into 3 categories: normal (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), and obese (≥30 kg/m2).13

Questionnaires—The EAT-26 questionnaire includes 26 questions that are used to detect EDs. Responses to each question include Likert-type answer options (ie, “always,” “usually,” “often,” “sometimes,” “rarely,” and “never.”) Patients with scores of 20 points or higher (range, 0–78) are classified as high risk for EDs.8 In our study, EAT-26 scores were grouped into 2 categories: patients scoring less than 20 points and those scoring 20 points or higher.

The DLQI questionnaire includes 10 questions to measure dermatologic symptoms and qualiy of life. Responses to each question include Likert-type answer options (ie, “not at all,” “a little,” “a lot,” or “very much.”) On the DLQI scale, the higher the score, the lower the quality of life (score range, 0–30).10

The ASHN questionnaire includes 21 questions that measure attitudes toward healthy nutrition with 5 possible answer options (“strongly disagree,” “disagree,” “undecided,” “agree,” and “strongly agree”). On this scale, higher scores indicate the participant is more knowledgeable about healthy nutrition (score range, 0–78).11

The DASS-21 questionnaire includes 21 questions that measure the severity of a range of symptoms common to depression, anxiety, and stress. Responses include Likert-type answer options (eg, “never,” “sometimes,” “often,” and “almost always.”) On this scale, a higher score (range of 0–21 for each) indicates higher levels of depression, anxiety, and stress.12

Statistical Analysis—Descriptive statistics were analyzed using SPSS software version 22.0 (IBM). The Shapiro-Wilk test was applied to determine whether the data were normally distributed. For categorical variables, frequency differences among groups were compared using the Pearson χ2 test. A t test was used to compare the means of 2 independent groups with a normal distribution. One-way analysis of variance and Tukey Honest Significant Difference post hoc analysis were used to test whether there was a statistically significant difference among the normally distributed means of independent groups. Pearson correlation analysis was used to determine whether there was a linear relationship between 2 numeric measurements and, if so, to determine the direction and severity of this relationship. P<.05 indicated statistical significance in this study.

Results

Study Participant Demographics—This study included 82 participants with a mean age of 44.3 years; 52.4% (43/82) were female, and 85.4% (70/82) were married. The questionnaire took an average of 4.2 minutes for participants to complete. A total of 57.3% (47/82) of patients had completed primary/secondary education and 59.8% (49/82) were employed. The mean BMI was 28.1 kg/m2. According to the BMI classification, 26.8% (22/82) participants had a normal weight, 36.6% (30/82) were overweight, and 43.9% (36/82) were obese. A total of 48.8% (40/82) of participants smoked, and 4.9% (4/82) consumed alcohol. The mean Psoriasis Area and Severity Index score was 5.4. A total of 54.9% (45/82) of participants had nail psoriasis, and 24.4% (20/82) had psoriatic arthritis. The mean duration of psoriasis was 153 months. A total of 29.3% (24/82) of participants had a positive family history of psoriasis. The mean EAT-26 score was 11.1. A total of 12.2% (10/82) of participants had an EAT-26 score of 20 points or higher and were considered at high risk for an ED. The mean ASHN score was 72.9; the mean DLQI score was 5.5; and on the DASS-21 scale, mean scores for depression, anxiety, and stress were 6.3, 8.7, and 10.0, respectively (Table).

Comparative Evaluation of the BMI Groups—The only statistically significant differences among the 3 BMI groups were related to marital status, EAT-26 score, and anxiety and stress scores (P=.02, <.01, <.01, and <.01, respectively)(eTable 1). The number of single/divorced participants in the overweight group was significantly (P=.02) greater than in the normal weight group. The mean EAT-26 score for the normal weight group was significantly (P<.01) lower than for the overweight and obese groups; there was no significant difference in mean EAT-26 scores between the overweight and obese groups. The mean anxiety score was significantly (P<.01) lower in the normal weight group compared with the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean depression score. The mean stress and anxiety scores were significantly (P<.01) lower in the normal weight group than in the overweight and obese groups. There was no significant difference between the overweight and obese groups according to the mean anxiety score.



Comparative Evaluation of the EAT-26 Scores—There were statistically significant differences among the EAT-26 scores related to sex; BMI; and depression, anxiety, and stress scores (P=.04, .02, <.01, <.01, and <.01, respectively). The number of females in the group with a score of 20 points or higher was significantly (P=.04) less than that in the group scoring less than 20 points. The mean BMI in the group with a score of 20 points or higher was significantly (P=.02) greater than in group scoring less than 20 points. The mean depression, anxiety, and stress scores of the group scoring 20 points or higher were significantly (P<.01 for all) greater than in the group scoring less than 20 points (eTable 2).



Correlation Analysis of the Study Variables—The EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress (P<.01 for all)(eTable 3).

Comment

Eating disorders are psychiatric conditions that require a multidisciplinary approach. Nonpsychiatric medical departments may be involved due to the severe consequences (eg, various skin changes14) of these disorders. Psoriasis is not known to be directly affected by the presence of an ED; however, it is possible that EDs could indirectly affect patients with psoriasis by influencing obesity. Therefore, this study aimed to examine the relationship between ED risk factors and obesity in this population.

The relationship between psoriasis and obesity has been a popular research topic in dermatology since the 1990s.15 Epidemiologic and observational studies have reported that patients with psoriasis are more likely to be overweight or have obesity, which is an independent risk factor for psoriasis.3,16 However, the causal relationship between psoriasis and obesity remains unclear. In a comprehensive review, Barros et al17 emphasized the causal relationship between obesity and psoriasis under several headings. Firstly, a higher BMI increases the risk for psoriasis by promoting cytokine release and immune system dysregulation. Secondly, a Western diet (eg, processed foods and fast food) triggers obesity and psoriasis by increasing adipose tissue. Thirdly, the alteration of the skin and gut microbiota triggers chronic inflammation as a result of bacterial translocation in patients with obesity. Fourthly, a high-fat diet and palmitic acid disrupt the intestinal integrity of the gut and increase the risk for psoriasis and obesity by triggering chronic inflammation of bacterial fragments that pass into the blood. Finally, the decrease in the amount of adiponectin and the increase in the amount of leptin in patients with obesity may cause psoriasis by increasing proinflammatory cytokines, which are similar to those involved in the pathogenesis of psoriasis.17 Additionally, psoriatic inflammation can cause insulin resistance and metabolic dysfunction, leading to obesity.18 The relationship between psoriasis and obesity cannot be solely explained by metabolic pathways. Smoking, alcohol consumption, and a sedentary lifestyle all are associated with psoriasis and also can contribute to obesity.5 Our study revealed no significant difference in smoking or alcohol consumption between the normal weight and overweight/obesity groups. Based on our data, we determined that smoking and alcohol consumption did not affect obesity in our patients with psoriasis.

Observational and epidemiologic studies have shown that patients with psoriasis experience increased rates of depression, anxiety, and stress.19 In studies of pathogenesis, a connection between depression and psoriatic inflammation has been established.20 It is known that inflammatory cytokines similar to those in psoriasis are involved in the development of obesity.18 In addition, depression and anxiety can lead to binge eating, unhealthy food choices, and a more sedentary lifestyle.5 All of these variables may contribute to the associations between depression and anxiety with psoriasis and obesity. Zafiriou et al21 conducted a study to investigate the relationship between psoriasis, obesity, and depression through inflammatory pathways with a focus on the importance of IL-17. Data showing that IL-17–producing Th17-cell subgroups play a considerable role in the development of obesity and depression prompted the authors to suggest that psoriasis, obesity, and ­anxiety/depression may be interconnected manifestations of immune dysregulation, potentially linked to IL-17 and its associated cells.21 Mrowietz et al22 also suggested that metabolic inflammation may contribute to obesity and depression in patients with psoriasis and highlighted the importance of several cytokines, including tumor necrosis factor α, IL-6, IL-8, IL-17, and IL-23. Our study revealed no significant differences in depression scores between BMI groups. Another meta-analysis reported conflicting findings on the incidence of depression in obese patients with psoriasis.23 Some of the studies had a small number of participants. Compared to depression, anxiety has received less attention in studies of patients with obesity with psoriasis. However, these studies have shown a positive correlation between anxiety scores and BMI in patients with psoriasis.24,25 In our study, similar to the findings of previous studies, overweight patients and those with obesitywho have psoriasis had significantly (P<.01) greater anxiety and stress scores than did normal weight patients with psoriasis.

Obesity should be assessed in patients with psoriasis via a biopsychosocial approach that takes into account genetic, behavioral, and environmental factors.26 Eating disorders are considered to be one of the factors contributing to obesity. Numerous studies in the literature have demonstrated a greater incidence of EDs in patients with obesity vs those without obesity.5,6,27 Obesity and EDs have a bidirectional relationship: individuals with obesity are at risk for EDs due to body dissatisfaction, dieting habits, and depressive states. Conversely, poor eating behaviors in individuals with a normal weight can lead to obesity.28

There are few studies in the literature exploring the relationship between psoriasis and EDs. Crosta et al29 demonstrated that patients with psoriasis had impaired results on ED screening tests and that these scores deteriorated further as BMI increased. Moreover, Altunay et al30 demonstrated that patients with psoriasis and metabolic syndrome had higher scores on the ED screening test. In this study, patients with higher scores also exhibited high levels of anxiety.30 In our study, similar to the findings of previous studies, patients with psoriasis who were overweight or had obesity had significantly (P<.01) greater EAT-26 scores than those in the normal weight group. Patients with high EAT-26 scores also exhibited elevated levels of depression, anxiety, and stress. Additionally, EAT-26 scores were positively correlated with BMI, anxiety, depression, and stress scores. Our study as well as other studies in the literature indicate that additional research is needed to determine the associations between EDs and obesity in psoriasis.

Conclusion

Managing obesity is crucial for patients with psoriasis. This study showed that EAT-26 scores were higher in patients with psoriasis who were overweight or had obesity than in those who were normal weight. Participants with high EAT-26 scores (≥20 points) were more likely to be female and have higher anxiety and stress scores. In addition, EAT-26 scores were positively correlated with BMI as well as depression, anxiety, and stress scores. Eating disorders may contribute to the development of obesity in patients with psoriasis. Although our study was limited by a small sample size, the results suggest that there is a need for large-scale multicenter studies to investigate the relationship between psoriasis and EDs.

References
  1. Kalkan G. Comorbidities in psoriasis: the recognition of psoriasis as a systemic disease and current management. Turkderm-Turk Arch Dermatol Venereol. 2017;51:71-77.
  2. Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutr Diabetes. 2012;2:E54.
  3. Jensen P, Skov L. Psoriasis and obesity. Dermatology. 2016;232:633-639.
  4. Mirghani H, Altemani AT, Altemani ST, et al. The cross talk between psoriasis, obesity, and dyslipidemia: a meta-analysis. Cureus. 2023;15:e49253.
  5. Roehring M, Mashep MR, White MA, et al. The metabolic syndrome and behavioral correlates in obese patients with binge disorders. Obesity. 2009;17:481-486.
  6. da Luz FQ, Hay P, Touyz S, et al. Obesity with comorbid eating disorders: associated health risks and treatment approaches. Nutrients. 2018;10:829.
  7. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition. American Psychiatric Association; 2013.
  8. Ergüney Okumus¸ FE, Sertel Berk HÖ. The psychometric properties of the Eating Attitudes Test short form (EAT-26) in a college sample. Stud Psychol. 2020;40:57-78.
  9. Stoleru G, Leopold A, Auerbach A, et al. Female gender, dissatisfaction with weight, and number of IBD related surgeries as independent risk factors for eating disorders among patients with inflammatory bowel diseases. BMC Gastroenterol. 2022;22:438.
  10. Öztürkcan S, Ermertcan AT, Eser E, et al. Cross validation of the Turkish version of dermatology life quality index. Int J Dermatol. 2006;45:1300-1307.
  11. Demir GT, Ciciog˘lu HI˙. Attitude scale for healthy nutrition (ASHN): validity and reliability study. Gaziantep Univ J Sport Sci. 2019;4:256-274.
  12. Yılmaz O, Boz H, Arslan A. The validity and reliability of depression stress and anxiety scale (DASS 21) Turkish short form. Res Financial Econ Soc Stud. 2017;2:78-91.
  13. Nuttall FQ. Body mass index: obesity, BMI, and health: a critical review. Nutr Today. 2015;50:117-128.
  14. Strumia R, Manzata E, Gualandi M. Is there a role for dermatologists in eating disorders? Expert Rev Dermatol. 2017; 2:109-112.
  15. Henseler T, Christophers E. Disease concomitance in psoriasis. J Am Acad Dermatol. 1995;32:982-986.
  16. Naldi L, Addis A, Chimenti S, et al. Impact of body mass index and obesity on clinical response to systemic treatment for psoriasis. evidence from the Psocare project. Dermatology. 2008;217:365-373.
  17. Barros G, Duran P, Vera I, et al. Exploring the links between obesity and psoriasis: a comprehensive review. Int J Mol Sci. 2022;23:7499.
  18. Hao Y, Zhu YJ, Zou S, et al. Metabolic syndrome and psoriasis: mechanisms and future directions. Front Immunol. 2021;12:711060.
  19. Jing D, Xiao H, Shen M, et al. Association of psoriasis with anxiety and depression: a case–control study in Chinese patients. Front Med (Lausanne). 2021;8:771645.
  20. Sahi FM, Masood A, Danawar NA, et al. Association between psoriasis and depression: a traditional review. Cureus. 2020;12:E9708.
  21. Zafiriou E, Daponte AI, Siokas V, et al. Depression and obesity in patients with psoriasis and psoriatic arthritis: is IL-17–mediated immune dysregulation the connecting link? Front Immunol. 2021;12:699848.
  22. Mrowietz U, Sümbül M, Gerdes S. Depression, a major comorbidity of psoriatic disease, is caused by metabolic inflammation. J Eur Acad Dermatol Venereol. 2023;37:1731-1738.
  23. Pavlova NT, Kioskli K, Smith C, et al. Psychosocial aspects of obesity in adults with psoriasis: a systematic review. Skin Health Dis. 2021;1:E33.
  24. Innamorati M, Quinto RM, Imperatori C, et al. Health-related quality of life and its association with alexithymia and difficulties in emotion regulation in patients with psoriasis. Compr Psychiatry. 2016;70:200-208.
  25. Tabolli S, Naldi L, Pagliarello C, et al. Evaluation of the impact of writing exercises interventions on quality of life in patients with psoriasis undergoing systemic treatments. Br J Dermatol. 2012;167:1254‐1264.
  26. Albuquerque D, Nóbrega C, Manco L, et al. The contribution of genetics and environment to obesity. Br Med Bull. 2017;123:159‐173.
  27. Balantekin KN, Grammer AC, Fitzsimmons-Craft EE, et al. Overweight and obesity are associated with increased eating disorder correlates and general psychopathology in university women with eating disorders. Eat Behav. 2021;41:101482.
  28. Jebeile H, Lister NB, Baur LA, et al. Eating disorder risk in adolescents with obesity. Obes Rev. 2021;22:E13173.
  29. Crosta ML, Caldarola G, Fraietta S, et al. Psychopathology and eating disorders in patients with psoriasis. G Ital Dermatol Venereol. 2014;149:355-361.
  30. Altunay I, Demirci GT, Ates B, et al. Do eating disorders accompany metabolic syndrome in psoriasis patients? results of a preliminary study. Clin Cosmet Investig Dermatol. 2011;4:139-143.
References
  1. Kalkan G. Comorbidities in psoriasis: the recognition of psoriasis as a systemic disease and current management. Turkderm-Turk Arch Dermatol Venereol. 2017;51:71-77.
  2. Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutr Diabetes. 2012;2:E54.
  3. Jensen P, Skov L. Psoriasis and obesity. Dermatology. 2016;232:633-639.
  4. Mirghani H, Altemani AT, Altemani ST, et al. The cross talk between psoriasis, obesity, and dyslipidemia: a meta-analysis. Cureus. 2023;15:e49253.
  5. Roehring M, Mashep MR, White MA, et al. The metabolic syndrome and behavioral correlates in obese patients with binge disorders. Obesity. 2009;17:481-486.
  6. da Luz FQ, Hay P, Touyz S, et al. Obesity with comorbid eating disorders: associated health risks and treatment approaches. Nutrients. 2018;10:829.
  7. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition. American Psychiatric Association; 2013.
  8. Ergüney Okumus¸ FE, Sertel Berk HÖ. The psychometric properties of the Eating Attitudes Test short form (EAT-26) in a college sample. Stud Psychol. 2020;40:57-78.
  9. Stoleru G, Leopold A, Auerbach A, et al. Female gender, dissatisfaction with weight, and number of IBD related surgeries as independent risk factors for eating disorders among patients with inflammatory bowel diseases. BMC Gastroenterol. 2022;22:438.
  10. Öztürkcan S, Ermertcan AT, Eser E, et al. Cross validation of the Turkish version of dermatology life quality index. Int J Dermatol. 2006;45:1300-1307.
  11. Demir GT, Ciciog˘lu HI˙. Attitude scale for healthy nutrition (ASHN): validity and reliability study. Gaziantep Univ J Sport Sci. 2019;4:256-274.
  12. Yılmaz O, Boz H, Arslan A. The validity and reliability of depression stress and anxiety scale (DASS 21) Turkish short form. Res Financial Econ Soc Stud. 2017;2:78-91.
  13. Nuttall FQ. Body mass index: obesity, BMI, and health: a critical review. Nutr Today. 2015;50:117-128.
  14. Strumia R, Manzata E, Gualandi M. Is there a role for dermatologists in eating disorders? Expert Rev Dermatol. 2017; 2:109-112.
  15. Henseler T, Christophers E. Disease concomitance in psoriasis. J Am Acad Dermatol. 1995;32:982-986.
  16. Naldi L, Addis A, Chimenti S, et al. Impact of body mass index and obesity on clinical response to systemic treatment for psoriasis. evidence from the Psocare project. Dermatology. 2008;217:365-373.
  17. Barros G, Duran P, Vera I, et al. Exploring the links between obesity and psoriasis: a comprehensive review. Int J Mol Sci. 2022;23:7499.
  18. Hao Y, Zhu YJ, Zou S, et al. Metabolic syndrome and psoriasis: mechanisms and future directions. Front Immunol. 2021;12:711060.
  19. Jing D, Xiao H, Shen M, et al. Association of psoriasis with anxiety and depression: a case–control study in Chinese patients. Front Med (Lausanne). 2021;8:771645.
  20. Sahi FM, Masood A, Danawar NA, et al. Association between psoriasis and depression: a traditional review. Cureus. 2020;12:E9708.
  21. Zafiriou E, Daponte AI, Siokas V, et al. Depression and obesity in patients with psoriasis and psoriatic arthritis: is IL-17–mediated immune dysregulation the connecting link? Front Immunol. 2021;12:699848.
  22. Mrowietz U, Sümbül M, Gerdes S. Depression, a major comorbidity of psoriatic disease, is caused by metabolic inflammation. J Eur Acad Dermatol Venereol. 2023;37:1731-1738.
  23. Pavlova NT, Kioskli K, Smith C, et al. Psychosocial aspects of obesity in adults with psoriasis: a systematic review. Skin Health Dis. 2021;1:E33.
  24. Innamorati M, Quinto RM, Imperatori C, et al. Health-related quality of life and its association with alexithymia and difficulties in emotion regulation in patients with psoriasis. Compr Psychiatry. 2016;70:200-208.
  25. Tabolli S, Naldi L, Pagliarello C, et al. Evaluation of the impact of writing exercises interventions on quality of life in patients with psoriasis undergoing systemic treatments. Br J Dermatol. 2012;167:1254‐1264.
  26. Albuquerque D, Nóbrega C, Manco L, et al. The contribution of genetics and environment to obesity. Br Med Bull. 2017;123:159‐173.
  27. Balantekin KN, Grammer AC, Fitzsimmons-Craft EE, et al. Overweight and obesity are associated with increased eating disorder correlates and general psychopathology in university women with eating disorders. Eat Behav. 2021;41:101482.
  28. Jebeile H, Lister NB, Baur LA, et al. Eating disorder risk in adolescents with obesity. Obes Rev. 2021;22:E13173.
  29. Crosta ML, Caldarola G, Fraietta S, et al. Psychopathology and eating disorders in patients with psoriasis. G Ital Dermatol Venereol. 2014;149:355-361.
  30. Altunay I, Demirci GT, Ates B, et al. Do eating disorders accompany metabolic syndrome in psoriasis patients? results of a preliminary study. Clin Cosmet Investig Dermatol. 2011;4:139-143.
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  • Eating disorders are considered a contributing factor in obesity.
  • Obesity is prevalent in patients with psoriasis, and current evidence indicates that obesity may initiate psoriasis or worsen existing disease.
  • Obesity should be considered as contributory to the development of psoriasis via a biopsychosocial approach that accounts for genetic, behavioral, and environmental factors.
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Disparities in Skin Cancer Outcomes in the Latine/Hispanic Population

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Disparities in Skin Cancer Outcomes in the Latine/Hispanic Population

The Latine/Hispanic population in the United States comprises one of the largest and youngest skin of color communities.1,2 In 2020, this group accounted for 19% of all Americans—a percentage expected to increase to more than 25% by 2060.3

It must be emphasized that the Latine/Hispanic community in the United States is incredibly diverse.4 Approximately one-third of individuals in this group are foreign-born, and this community is made up of people from all racialized groups, religions, languages, and cultural identities.2 The heterogeneity of the Latine/Hispanic population translates into a wide representation of skin tones, reflecting a rich range of ancestries, ethnicities, and cultures. The percentage of individuals from each origin group may differ according to where they live in the United States; for instance, individuals who identify as Mexican comprise more than 80% of the Latine/Hispanic population in both Texas and California but only 17% in Florida, where more than half of Latine/Hispanic people identify as Cuban or Puerto Rican.4,5 As a result, when it comes to skin cancer epidemiology, variations in incidence and mortality may exist within each of these subgroups who identify as part of the Latine/Hispanic community, as reported for other cancers.6,7 Further research is needed to investigate these potential differences.Unfortunately, considerable health disparities persist among this rapidly growing population, including increased morbidity and mortality from melanoma and keratinocyte carcinomas (KCs) despite overall low lifetime incidence.8,9 In this review, the epidemiology, clinical manifestation, and ethnic disparities for skin cancer among the US Latine/Hispanic population are summarized; other factors impacting overall health and health care, including sociocultural factors, also are briefly discussed.

Terminology

Before a meaningful dialogue can be had about skin cancer in the Latine/Hispanic population, it is important to contextualize the terms used to identify this patient population, including Latino/Latine and Hispanic. In the early 1970s, the United States adopted the term Hispanic as a way of conglomerating Spanish-speaking individuals from Spain, the Caribbean, and Central and South America. The goal was to implement a common identifier that enabled the US government to study the economic and social development of these groups.10 Nevertheless, considerable differences (eg, variations in skin pigmentation, sun sensitivity) exist among Hispanic communities, with some having stronger European, African, or Amerindian influences due to colonization of their ­distinct countries.11

In contrast, Latino is a geographic term and refers to people with roots in Latin America and the Caribbean (Table 1).12,13 For example, a person from Brazil may be considered Latino but not Hispanic as Brazilians speak Portuguese; alternatively, Spaniards (who are considered Hispanic) are not Latino because Spain is not a Latin American country. A person from Mexico would be considered both Latino and Hispanic.13



More recently, the term Latine has been introduced as an alternative to the gender binary inherent in the Spanish language.12 For the purposes of this article, the terms Latine and Hispanic will be used interchangeably (unless otherwise specified) depending on how they are cited in the existing literature. Furthermore, the term non-Hispanic White (NHW) will be used to refer to individuals who have been socially ascribed or who self-identify as White in terms of race or ethnicity.

Melanoma

Melanoma, the deadliest form of skin cancer, is more likely to metastasize compared to other forms of skin cancer, including basal cell carcinoma (BCC) and squamous cell carcinoma (SCC). For Latine/Hispanic individuals living in the United States, the lifetime risk for melanoma is 1 in 200 compared to 1 in 33 for NHW individuals.14 While the lifetime risk for melanoma is low for the Latine/Hispanic population, Hispanic individuals are diagnosed with melanoma at an earlier age (mean, 56 years), and the rate of new cases is marginally higher for women (4.9 per 100,000) compared to men (4.8 per 100,000).15,16

Typical sites of melanoma manifestation in Latine/Hispanic individuals include the torso (most common site in Hispanic men), lower extremities (most common site in Hispanic women), and acral sites (palms, soles, and nails).9,16,17 Anatomic location also can vary according to age for both men and women. For men, the incidence of melanoma on the trunk appears to decrease with age, while the incidence on the head and neck may increase. For women, the incidence of melanoma on the lower extremities and hip increases with age. Cutaneous melanoma may manifest as a lesion with asymmetry, irregular borders, variation in pigmentation, large diameter (>6 mm), and evolution over time. In patients with skin of color, melanoma easily can be missed, as it also typically mimics more benign skin conditions and may develop from an existing black- or dark brown–­pigmented macule.18 The most common histologic subtype reported among Latine/Hispanic individuals in the United States is superficial spreading melanoma (20%–23%) followed by nodular melanoma and acral lentiginous melanoma.16,19 Until additional risk factors associated with melanoma susceptibility in Hispanic/Latine people are better elucidated, it may be appropriate to use an alternative acronym, such as CUBED (Table 2), in addition to the standard ABCDE system to help recognize potential melanoma on acral sites.18



Although the lifetime risk for melanoma among Hispanic individuals in the United States is lower than that for NHW individuals, Hispanic patients who are diagnosed with melanoma are more likely to present with increased tumor thickness and later-stage diagnosis compared to NHW individuals.8,16,20 In a recent study by Qian et al,8 advanced stage melanoma—defined as regional or distant stage disease—was present in 12.6% of NHW individuals. In contrast, the percentage of Hispanics with advanced disease was higher at 21%.8 Even after controlling for insurance and poverty status, Hispanic individuals were at greater risk than NHW individuals for late-stage diagnosis.16,20

Morbidity and mortality also have been shown to be higher in Hispanic patients with cutaneous melanoma.9,17 Reasons for this are multifactorial, with studies specific to melanoma citing challenges associated with early detection in individuals with deeply pigmented skin, a lack of awareness and knowledge about skin cancer among Latine/Hispanic patients, and treatment disparities.21-23 Moreover, very few studies have reported comprehensive data on patients from Africa and Latin America. Studies examining the role of genetic ancestry, epigenetic variants, and skin pigmentation and the risk for melanoma among the Latine/Hispanic population therefore are much needed.24

Keratinocyte Carcinomas

Keratinocyte carcinomas, also known as nonmelanoma skin cancers, include BCC and SCC. In comparison to the high-quality data available for melanoma from cancer registries, there are less reliable incidence data for KCs, especially among individuals with skin of color.25 As a result, KC epidemiology in the United States is drawn largely from case series (especially for individuals with skin of color) or claims data from small data sets often from geographically restricted regions within the United States.25,26

Basal Cell Carcinoma—Basal cell carcinoma is the most common malignant skin cancer in Latine/Hispanic individuals. Among those with lighter skin tones, the lifetime risk for BCC is about 30%.27,28 Men typically are affected at a higher rate than women, and the median age for diagnosis is 68 years.29 The development of BCC primarily is linked to lifetime accumulated UV radiation exposure. Even though BCC has a low mortality rate, it can lead to substantial morbidity due to factors such as tumor location, size, and rate of invasion, resulting in cosmetic and functional issues. Given its low metastatic potential, treatment of BCC typically is aimed at local control.30 Options for treatment include Mohs micrographic surgery (MMS), curettage and electrodessication, cryosurgery, photodynamic therapy, radiation therapy, and topical therapies. Systemic therapies are reserved for patients with locally advanced or metastatic disease.30

Latine/Hispanic patients characteristically present with BCCs on sun-exposed areas of the skin such as the head and neck region. In most patients, BCC manifests as a translucent pearly nodule with superficial telangiectasias and/or a nonhealing ulcer with a central depression and rolled nontender borders. However, in patients with skin of color, 66% of BCCs manifest with pigmentation; in fact, pigmented BCC (a subtype of BCC) has been shown to have a higher prevalence among Hispanic individuals, with an incidence twice as frequent as in NHW individuals.31 In addition, there are reports of increased tendency among Latine/Hispanic individuals to develop multiple BCCs.32,33

The relationship between UV exposure and KCs could explain the relatively higher incidence in populations with skin of color living in warmer climates, including Hispanic individuals.34 Even so, the development of BCCs appears to correlate directly with the degree of pigmentation in the skin, as it is most common in individuals with lighter skin tones within the Hispanic population.25,34,35 Other risk factors associated with BCC development include albinism, arsenic ingestion, chronic infections, immunosuppression, history of radiation treatment, and history of scars or ulcers due to physical/thermal trauma.35-37

Squamous Cell Carcinoma—Squamous cell carcinoma is the second most common skin cancer among Latine/Hispanic patients. In contrast with NHW patients, evidence supporting the role of UV exposure as a primary risk factor for SCC in patients with skin of color remains limited.25,38 Reports linking UV exposure and KCs in Hispanic and Black individuals predominantly include case series or population-based studies that do not consider levels of UV exposure.25

More recently, genetic ancestry analyses of a large multiethnic cohort found an increased risk for cutaneous SCC among Latine/Hispanic individuals with European ancestry compared to those with Native American or African ancestry; however, these genetic ancestry associations were attenuated (although not eliminated) after considering skin pigmentation (using loci associated with skin pigmentation), history of sun exposure (using actinic keratoses as a covariate for chronic sun exposure), and sun-protected vs sun-exposed anatomic sites, supporting the role of other environmental or sociocultural factors in the development of SCC.39 Similar to BCCs, immunosuppression, chronic scarring, skin irritation, and inflammatory disease also are documented risk factors.9,32

Among NHW individuals with lighter skin tones, SCC characteristically manifests on sun-exposed areas of the skin such as the head and neck region. Typically, a lesion may appear as a scaly erythematous papule or plaque that may be verrucous in nature or a nonhealing bleeding ulcer. In patients with more deeply pigmented skin, SCC tends to develop in the perianal region and on the penis and lower legs; pigmented lesions also may be present (as commonly reported in BCCs).9,32,36

Unfortunately, the lower incidence of KCs and lack of surveillance in populations with skin of color result in a low index of clinical suspicion, leading to delayed diagnoses and increased morbidity.40 Keratinocyte carcinomas are more costly to treat and require more health care resources for Latine/Hispanic and Black patients compared to their NHW counterparts; for example, KCs are associated with more ambulatory visits, more prescription medications, and greater cost on a per-person, per-year basis in Latine/Hispanic and Black patients compared with NHW patients.41 Moreover, a recent multicenter retrospective study found Hispanic patients had 17% larger MMS defects following treatment for KCs compared to NHW patients after adjustment for age, sex, and insurance type.42

Hispanic patients tend to present initially with SCCs in areas associated with advanced disease, such as the anogenital region, penis, and the lower extremities. Latine and Black men have the highest incidence of penile SCC, which is rare with high morbidity and mortality.32,43,44 The higher incidence of penile SCC among Hispanic individuals living in southern states could correspond to circumcision or HPV infection rates,44 ultimately impacting incidence.45

Dermatofibrosarcoma Protuberans

Dermatofibrosarcoma protuberans (DFSP) is a rare locally aggressive cutaneous sarcoma. According to population studies, overall incidence of DFSP is around 4.1 to 4.2 per million in the United States. Population-based studies on DFSP are limited, but available data suggest that Black patients as well as women have the highest incidence.46

Dermatofibrosarcoma protuberans is characterized by its capacity to invade surrounding tissues in a tentaclelike pattern.47 This characteristic often leads to inadequate initial resection of the lesion as well as a high recurrence rate despite its low metastatic potential.48 In early stages, DFSP typically manifests as an asymptomatic plaque with a slow growth rate. The color of the lesion ranges from reddish brown to flesh colored. The pigmented form of DFSP, known as Bednar tumor, is the most common among Black patients.47 As the tumor grows, it tends to become firm and nodular. The most common location for DFSP is on the trunk or the upper and lower extremities.47

Although current guidelines designate MMS as the first-line treatment for DFSP, the procedure may be inaccessible for certain populations.49 Patients with skin of color are more likely to undergo wide local excision (WLE) than MMS; however, WLE is less effective, with a recurrence rate of 30% compared with 3% in those treated with MMS.50 A retrospective cohort study of more than 2000 patients revealed that Hispanic and Black patients were less likely to undergo MMS. In addition, the authors noted that WLE recipients more commonly were deceased at the end of the study.51

Despite undergoing treatment for a primary DFSP, Hispanic patients also appear to be at increased risk for a second surgery.52 Additional studies are needed to elucidate the reasons behind higher recurrence rates in Latine/Hispanic patients compared to NHW individuals.

Factors Influencing Skin Cancer Outcomes

In recent years, racial and ethnic disparities in health care use, medical treatment, and quality of care among minoritized populations (including Latine/Hispanic groups) have been documented in the medical literature.53,54 These systemic inequities, which are rooted in structural racism,55 have contributed to poorer health outcomes, worse health status, and lower-quality care for minoritized patients living in the United States, including those impacted by dermatologic conditions.8,43,55-57 Becoming familiar with the sociocultural factors influencing skin cancer outcomes in the Latine/Hispanic community (including the lack of or inadequate health insurance, medical mistrust, language, and other cultural elements) and the paucity of research in this domain could help eliminate existing health inequities in this population.

Health Insurance Coverage—Although the uninsured rates in the Latine population have decreased since the passage of the Affordable Care Act (from 30% in 2013 to a low of 19% in 2017),58 inadequate health insurance coverage remains one of the largest barriers to health care access and a contributor to health disparities among the Latine community. Nearly 1 in 5 Latine individuals in the United States are uninsured compared to 8% of NHW individuals.58 Even though Latine individuals are more likely than non-Latine individuals to be part of the workforce, Latine employees are less likely to receive employer-sponsored coverage (27% vs 53% for NHW individuals).59

Not surprisingly, noncitizens are far less likely to be insured; this includes lawfully present immigrants (ie, permanent residents or green card holders, refugees, asylees, and others who are authorized to live in the United States temporarily or permanently) and undocumented immigrants (including individuals who entered the country without authorization and individuals who entered the country lawfully and stayed after their visa or status expired). The higher uninsured rate among noncitizens reflects not only limited access to employer-sponsored coverage but includes immigrant eligibility restrictions for federal programs such as Medicaid, the Children’s Health Insurance Program, and the Affordable Care Act Marketplace coverage.60

With approximately 9 million Americans living in mixed-status families (and nearly 10% of babies born each year with at least one undocumented parent), restrictive federal or state health care policies may extend beyond their stated target and impact both Latine citizens and noncitizens.61-65 For instance, Vargas et al64 found that both Latine citizens and noncitizens who lived in states with a high number of immigration-related laws had decreased odds of reporting optimal health as compared to Latine respondents in states with fewer immigration-related laws.Other barriers to enrollment include fears and confusion about program qualification, even if eligible.58

Medical Mistrust and Unfamiliarity—Mistrust of medical professionals has been shown to reduce patient adherence to treatment as prescribed by their medical provider and can negatively influence health outcomes.53 For racial/ethnic minoritized groups (including Latine/Hispanic patients), medical mistrust may be rooted in patients’ experience of discrimination in the health care setting. In a recent cross-sectional study, results from a survey of California adults (including 704 non-Hispanic Black, 711 Hispanic, and 913 NHW adults) found links between levels of medical mistrust and perceived discrimination based on race/ethnicity and language as well as perceived discrimination due to income level and type or lack of insurance.53 Interestingly, discrimination attributed to income level and insurance status remained after controlling for race/ethnicity and language. As expected, patients reliant on public insurance programs such as Medicare have been reported to have greater medical mistrust and suspicion compared with private insurance holders.65 Together, these findings support the notion that individuals who have low socioeconomic status and lack insurance coverage—disproportionately historically marginalized populations—are more likely to perceive discrimination in health care settings, have greater medical mistrust, and experience poorer health outcomes.53

It also is important for health care providers to consider that the US health care system is unfamiliar to many Latine/Hispanic individuals. Costs of medical services tend to be substantially higher in the United States, which can contribute to mistrust in the system.66 In addition, unethical medical experimentations have negatively affected both Latine and especially non-Hispanic Black populations, with long-lasting perceptions of deception and exploitation.67 These beliefs have undermined the trust that these populations have in clinicians and the health care system.54,67

Language and Other Cultural Elements—The inability to effectively communicate with health care providers could contribute to disparities in access to and use of health care services among Latine/Hispanic individuals. In a Medical Expenditure Panel Survey analysis, half of Hispanic patients with limited comfort speaking English did not have a usual source of care, and almost 90% of those with a usual source of care had a provider who spoke Spanish or used interpreters—indicating that few Hispanic individuals with limited comfort speaking English selected a usual source of care without language assistance.68,69 In other examples, language barriers ­contributed to disparities in cancer screening, and individuals with limited English proficiency were more likely to have difficulty understanding their physician due to language barriers.68,70

Improving cultural misconceptions regarding skin conditions, especially skin cancer, is another important consideration in the Latine/Hispanic community. Many Latine/Hispanic individuals wrongly believe they cannot develop skin cancer due to their darker skin tones and lack of family history.26 Moreover, multiple studies assessing melanoma knowledge and perception among participants with skin of color (including one with an equal number of Latine/Hispanic, Black/African American, and Asian individuals for a total of 120 participants) revealed that many were unaware of the risk for melanoma on acral sites.71 Participants expressed a need for more culturally relevant content from both clinicians and public materials (eg, images of acral melanoma in a person with skin of color).71-73

Paucity of Research—There is limited research regarding skin cancer risks and methods of prevention for patients with skin of color, including the Latine/Hispanic population. Efforts to engage and include patients from these communities, as well as clinicians or investigators from similar backgrounds, in clinical studies are desperately needed. It also is important that clinical studies collect data beyond population descriptors to account for both clinical and genetic variations observed in the Latine/Hispanic population. 

Latine/Hispanic individuals are quite diverse with many variable factors that may influence skin cancer outcomes. Often, cancer surveillance data are available in aggregate only, which could mask this heterogeneity.74 Rigorous studies that collect more granular data, including objective measures of skin pigmentation beyond self-reported Fitzpatrick skin type, culture/beliefs, lifestyle/behavior, geographic location, socioeconomic status, genetics, or epigenetics could help fully elucidate skin cancer risks and mitigate health disparities among individuals who identify as part of this population.

Final Thoughts

The Latine/Hispanic community—the largest ethnic minoritized group in the United States—is disproportionately affected by dermatologic health disparities. We hope this review helps to increase recognition of the clinical manifestations of skin cancer in Latine/Hispanic patients. Other factors that may impact skin cancer outcomes in this population include (but are not limited to) lack of or inadequate health insurance, medical mistrust, linguistic barriers and/or individual/cultural perspectives, along with limited research. Recognizing and addressing these (albeit complex) barriers that contribute to the inequitable access to health care in this population remains a critical step toward improving skin cancer outcomes.

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  58. Office of the Assistant Secretary for Planning and Evaluation. Health insurance coverage and access to care among Latinos: recent rrends and key challenges (HP-2021-22). October 8, 2021. Accessed September 3, 2024. https://aspe.hhs.gov/reports/health-insurance-coverage-access-care-among-latinos
  59. Keisler-Starkey K, Bunch LN. Health insurance coverage in the United States: 2020 (Current Population Reports No. P60-274). US Census Bureau; 2021. https://www.census.gov/content/dam/Census/library/publications/2021/demo/p60-274.pdf
  60. Kaiser Family Foundation. Key facts on health coverage of immigrants. Updated June 26, 2024. Accessed September 3, 2024. https://www.kff.org/racial-equity-and-health-policy/fact-sheet/key-facts-on-health-coverage-of-immigrants/
  61. Pew Research Center. Unauthorized immigrants: length of residency, patterns of parenthood. Published December 1, 2011. Accessed October 28, 2024. https://www.pewresearch.org/race-and-ethnicity/2011/12/01/unauthorized-immigrants-length-of-residency-patterns-of-parenthood/
  62. Schneider J, Schmitt M. Understanding the relationship between racial discrimination and mental health among African American adults: a review. SAGE Open. 2015;5:1-10.
  63. Philbin MM, Flake M, Hatzenbuehler ML, et al. State-level immigration and immigrant-focused policies as drivers of Latino health disparities in the United States. Soc Sci Med. 2018;199:29-38.
  64. Vargas ED, Sanchez GR, Juarez M. The impact of punitive immigrant laws on the health of Latina/o Populations. Polit Policy. 2017;45:312-337.
  65. Sutton AL, He J, Edmonds MC, et al. Medical mistrust in Black breast cancer patients: acknowledging the roles of the trustor and the trustee. J Cancer Educ. 2019;34:600-607.
  66. Jacobs J. An overview of Latin American healthcare systems. Pacific Prime Latin America. July 31, 2023. Accessed September 3, 2024. https://www.pacificprime.lat/blog/an-overview-of-latin-american-healthcare-systems/
  67. CDC. Unfair and unjust practices and conditions harm Hispanic and Latino people and drive health disparities. May 15, 2024. Accessed September 3, 2024. https://www.cdc.gov/tobacco-health-equity/collection/hispanic-latino-unfair-and-unjust.html
  68. Hall IJ, Rim SH, Dasari S. Preventive care use among Hispanic adults with limited comfort speaking English: an analysis of the Medical Expenditure Panel Survey data. Prev Med. 2022;159:107042.
  69. Brach C, Chevarley FM. Demographics and health care access and utilization of limited-English-proficient and English-proficient Hispanics. Agency for Healthcare Research and Quality. February 2008. http://meps.ahrq.gov/mepsweb/data_files/publications//rf28/rf28.pdf
  70. Berdahl TA, Kirby JB. Patient-provider communication disparities by limited English proficiency (LEP): trends from the US Medical Expenditure Panel Survey, 2006-2015. J General Intern Med. 2019;34:1434-1440.
  71. Robinson JK, Joshi KM, Ortiz S, et al. Melanoma knowledge, perception, and awareness in ethnic minorities in Chicago: recommendations regarding education. Psychooncology. 2011;20:313-320.
  72. Robinson JK, Nodal M, Chavez L, et al. Enhancing the relevance of skin self-examination for Latinos. JAMA Dermatol. 2017;153:717-718.
  73. Buchanan Lunsford N, Berktold J, Holman DM, et al. Skin cancer knowledge, awareness, beliefs and preventive behaviors among black and hispanic men and women. Prev Med Rep. 2018;12:203-209.
  74. Madrigal JM, Correa-Mendez M, Arias JD, et al. Hispanic, Latino/a, Latinx, Latine: disentangling the identities of Hispanic/Latino Americans. National Cancer Institute Division of Cancer Epidemiology & Genetics. October 20, 2022. Accessed September 3, 2024. https://dceg.cancer.gov/about/diversity-inclusion/inclusivity-minute/2022/disentangling-identities-hispanic-latino-americans
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Dr. Valencia is from the Department of Internal Medicine, John Hopkins Bayview Medical Center, Baltimore, Maryland. Fabiola Ramirez is from the Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center, El Paso. Claudia Dubocq-Ortiz is from the University of Puerto Rico School of Medicine, Medical School Campus, San Juan. Dr. Vasquez is from the Department of Dermatology, UT Southwestern Medical Center, Dallas.

The authors have no relevant financial disclosures to report.

Correspondence: Rebecca Vasquez, MD, Department of Dermatology, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Box 9190, Dallas, TX 75390 (rebecca.vasquez@utsouthwestern.edu).

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Author and Disclosure Information

Dr. Valencia is from the Department of Internal Medicine, John Hopkins Bayview Medical Center, Baltimore, Maryland. Fabiola Ramirez is from the Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center, El Paso. Claudia Dubocq-Ortiz is from the University of Puerto Rico School of Medicine, Medical School Campus, San Juan. Dr. Vasquez is from the Department of Dermatology, UT Southwestern Medical Center, Dallas.

The authors have no relevant financial disclosures to report.

Correspondence: Rebecca Vasquez, MD, Department of Dermatology, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Box 9190, Dallas, TX 75390 (rebecca.vasquez@utsouthwestern.edu).

Cutis. 2024 November;114(5):146-152. doi:10.12788/cutis.1129

Author and Disclosure Information

Dr. Valencia is from the Department of Internal Medicine, John Hopkins Bayview Medical Center, Baltimore, Maryland. Fabiola Ramirez is from the Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center, El Paso. Claudia Dubocq-Ortiz is from the University of Puerto Rico School of Medicine, Medical School Campus, San Juan. Dr. Vasquez is from the Department of Dermatology, UT Southwestern Medical Center, Dallas.

The authors have no relevant financial disclosures to report.

Correspondence: Rebecca Vasquez, MD, Department of Dermatology, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Box 9190, Dallas, TX 75390 (rebecca.vasquez@utsouthwestern.edu).

Cutis. 2024 November;114(5):146-152. doi:10.12788/cutis.1129

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The Latine/Hispanic population in the United States comprises one of the largest and youngest skin of color communities.1,2 In 2020, this group accounted for 19% of all Americans—a percentage expected to increase to more than 25% by 2060.3

It must be emphasized that the Latine/Hispanic community in the United States is incredibly diverse.4 Approximately one-third of individuals in this group are foreign-born, and this community is made up of people from all racialized groups, religions, languages, and cultural identities.2 The heterogeneity of the Latine/Hispanic population translates into a wide representation of skin tones, reflecting a rich range of ancestries, ethnicities, and cultures. The percentage of individuals from each origin group may differ according to where they live in the United States; for instance, individuals who identify as Mexican comprise more than 80% of the Latine/Hispanic population in both Texas and California but only 17% in Florida, where more than half of Latine/Hispanic people identify as Cuban or Puerto Rican.4,5 As a result, when it comes to skin cancer epidemiology, variations in incidence and mortality may exist within each of these subgroups who identify as part of the Latine/Hispanic community, as reported for other cancers.6,7 Further research is needed to investigate these potential differences.Unfortunately, considerable health disparities persist among this rapidly growing population, including increased morbidity and mortality from melanoma and keratinocyte carcinomas (KCs) despite overall low lifetime incidence.8,9 In this review, the epidemiology, clinical manifestation, and ethnic disparities for skin cancer among the US Latine/Hispanic population are summarized; other factors impacting overall health and health care, including sociocultural factors, also are briefly discussed.

Terminology

Before a meaningful dialogue can be had about skin cancer in the Latine/Hispanic population, it is important to contextualize the terms used to identify this patient population, including Latino/Latine and Hispanic. In the early 1970s, the United States adopted the term Hispanic as a way of conglomerating Spanish-speaking individuals from Spain, the Caribbean, and Central and South America. The goal was to implement a common identifier that enabled the US government to study the economic and social development of these groups.10 Nevertheless, considerable differences (eg, variations in skin pigmentation, sun sensitivity) exist among Hispanic communities, with some having stronger European, African, or Amerindian influences due to colonization of their ­distinct countries.11

In contrast, Latino is a geographic term and refers to people with roots in Latin America and the Caribbean (Table 1).12,13 For example, a person from Brazil may be considered Latino but not Hispanic as Brazilians speak Portuguese; alternatively, Spaniards (who are considered Hispanic) are not Latino because Spain is not a Latin American country. A person from Mexico would be considered both Latino and Hispanic.13



More recently, the term Latine has been introduced as an alternative to the gender binary inherent in the Spanish language.12 For the purposes of this article, the terms Latine and Hispanic will be used interchangeably (unless otherwise specified) depending on how they are cited in the existing literature. Furthermore, the term non-Hispanic White (NHW) will be used to refer to individuals who have been socially ascribed or who self-identify as White in terms of race or ethnicity.

Melanoma

Melanoma, the deadliest form of skin cancer, is more likely to metastasize compared to other forms of skin cancer, including basal cell carcinoma (BCC) and squamous cell carcinoma (SCC). For Latine/Hispanic individuals living in the United States, the lifetime risk for melanoma is 1 in 200 compared to 1 in 33 for NHW individuals.14 While the lifetime risk for melanoma is low for the Latine/Hispanic population, Hispanic individuals are diagnosed with melanoma at an earlier age (mean, 56 years), and the rate of new cases is marginally higher for women (4.9 per 100,000) compared to men (4.8 per 100,000).15,16

Typical sites of melanoma manifestation in Latine/Hispanic individuals include the torso (most common site in Hispanic men), lower extremities (most common site in Hispanic women), and acral sites (palms, soles, and nails).9,16,17 Anatomic location also can vary according to age for both men and women. For men, the incidence of melanoma on the trunk appears to decrease with age, while the incidence on the head and neck may increase. For women, the incidence of melanoma on the lower extremities and hip increases with age. Cutaneous melanoma may manifest as a lesion with asymmetry, irregular borders, variation in pigmentation, large diameter (>6 mm), and evolution over time. In patients with skin of color, melanoma easily can be missed, as it also typically mimics more benign skin conditions and may develop from an existing black- or dark brown–­pigmented macule.18 The most common histologic subtype reported among Latine/Hispanic individuals in the United States is superficial spreading melanoma (20%–23%) followed by nodular melanoma and acral lentiginous melanoma.16,19 Until additional risk factors associated with melanoma susceptibility in Hispanic/Latine people are better elucidated, it may be appropriate to use an alternative acronym, such as CUBED (Table 2), in addition to the standard ABCDE system to help recognize potential melanoma on acral sites.18



Although the lifetime risk for melanoma among Hispanic individuals in the United States is lower than that for NHW individuals, Hispanic patients who are diagnosed with melanoma are more likely to present with increased tumor thickness and later-stage diagnosis compared to NHW individuals.8,16,20 In a recent study by Qian et al,8 advanced stage melanoma—defined as regional or distant stage disease—was present in 12.6% of NHW individuals. In contrast, the percentage of Hispanics with advanced disease was higher at 21%.8 Even after controlling for insurance and poverty status, Hispanic individuals were at greater risk than NHW individuals for late-stage diagnosis.16,20

Morbidity and mortality also have been shown to be higher in Hispanic patients with cutaneous melanoma.9,17 Reasons for this are multifactorial, with studies specific to melanoma citing challenges associated with early detection in individuals with deeply pigmented skin, a lack of awareness and knowledge about skin cancer among Latine/Hispanic patients, and treatment disparities.21-23 Moreover, very few studies have reported comprehensive data on patients from Africa and Latin America. Studies examining the role of genetic ancestry, epigenetic variants, and skin pigmentation and the risk for melanoma among the Latine/Hispanic population therefore are much needed.24

Keratinocyte Carcinomas

Keratinocyte carcinomas, also known as nonmelanoma skin cancers, include BCC and SCC. In comparison to the high-quality data available for melanoma from cancer registries, there are less reliable incidence data for KCs, especially among individuals with skin of color.25 As a result, KC epidemiology in the United States is drawn largely from case series (especially for individuals with skin of color) or claims data from small data sets often from geographically restricted regions within the United States.25,26

Basal Cell Carcinoma—Basal cell carcinoma is the most common malignant skin cancer in Latine/Hispanic individuals. Among those with lighter skin tones, the lifetime risk for BCC is about 30%.27,28 Men typically are affected at a higher rate than women, and the median age for diagnosis is 68 years.29 The development of BCC primarily is linked to lifetime accumulated UV radiation exposure. Even though BCC has a low mortality rate, it can lead to substantial morbidity due to factors such as tumor location, size, and rate of invasion, resulting in cosmetic and functional issues. Given its low metastatic potential, treatment of BCC typically is aimed at local control.30 Options for treatment include Mohs micrographic surgery (MMS), curettage and electrodessication, cryosurgery, photodynamic therapy, radiation therapy, and topical therapies. Systemic therapies are reserved for patients with locally advanced or metastatic disease.30

Latine/Hispanic patients characteristically present with BCCs on sun-exposed areas of the skin such as the head and neck region. In most patients, BCC manifests as a translucent pearly nodule with superficial telangiectasias and/or a nonhealing ulcer with a central depression and rolled nontender borders. However, in patients with skin of color, 66% of BCCs manifest with pigmentation; in fact, pigmented BCC (a subtype of BCC) has been shown to have a higher prevalence among Hispanic individuals, with an incidence twice as frequent as in NHW individuals.31 In addition, there are reports of increased tendency among Latine/Hispanic individuals to develop multiple BCCs.32,33

The relationship between UV exposure and KCs could explain the relatively higher incidence in populations with skin of color living in warmer climates, including Hispanic individuals.34 Even so, the development of BCCs appears to correlate directly with the degree of pigmentation in the skin, as it is most common in individuals with lighter skin tones within the Hispanic population.25,34,35 Other risk factors associated with BCC development include albinism, arsenic ingestion, chronic infections, immunosuppression, history of radiation treatment, and history of scars or ulcers due to physical/thermal trauma.35-37

Squamous Cell Carcinoma—Squamous cell carcinoma is the second most common skin cancer among Latine/Hispanic patients. In contrast with NHW patients, evidence supporting the role of UV exposure as a primary risk factor for SCC in patients with skin of color remains limited.25,38 Reports linking UV exposure and KCs in Hispanic and Black individuals predominantly include case series or population-based studies that do not consider levels of UV exposure.25

More recently, genetic ancestry analyses of a large multiethnic cohort found an increased risk for cutaneous SCC among Latine/Hispanic individuals with European ancestry compared to those with Native American or African ancestry; however, these genetic ancestry associations were attenuated (although not eliminated) after considering skin pigmentation (using loci associated with skin pigmentation), history of sun exposure (using actinic keratoses as a covariate for chronic sun exposure), and sun-protected vs sun-exposed anatomic sites, supporting the role of other environmental or sociocultural factors in the development of SCC.39 Similar to BCCs, immunosuppression, chronic scarring, skin irritation, and inflammatory disease also are documented risk factors.9,32

Among NHW individuals with lighter skin tones, SCC characteristically manifests on sun-exposed areas of the skin such as the head and neck region. Typically, a lesion may appear as a scaly erythematous papule or plaque that may be verrucous in nature or a nonhealing bleeding ulcer. In patients with more deeply pigmented skin, SCC tends to develop in the perianal region and on the penis and lower legs; pigmented lesions also may be present (as commonly reported in BCCs).9,32,36

Unfortunately, the lower incidence of KCs and lack of surveillance in populations with skin of color result in a low index of clinical suspicion, leading to delayed diagnoses and increased morbidity.40 Keratinocyte carcinomas are more costly to treat and require more health care resources for Latine/Hispanic and Black patients compared to their NHW counterparts; for example, KCs are associated with more ambulatory visits, more prescription medications, and greater cost on a per-person, per-year basis in Latine/Hispanic and Black patients compared with NHW patients.41 Moreover, a recent multicenter retrospective study found Hispanic patients had 17% larger MMS defects following treatment for KCs compared to NHW patients after adjustment for age, sex, and insurance type.42

Hispanic patients tend to present initially with SCCs in areas associated with advanced disease, such as the anogenital region, penis, and the lower extremities. Latine and Black men have the highest incidence of penile SCC, which is rare with high morbidity and mortality.32,43,44 The higher incidence of penile SCC among Hispanic individuals living in southern states could correspond to circumcision or HPV infection rates,44 ultimately impacting incidence.45

Dermatofibrosarcoma Protuberans

Dermatofibrosarcoma protuberans (DFSP) is a rare locally aggressive cutaneous sarcoma. According to population studies, overall incidence of DFSP is around 4.1 to 4.2 per million in the United States. Population-based studies on DFSP are limited, but available data suggest that Black patients as well as women have the highest incidence.46

Dermatofibrosarcoma protuberans is characterized by its capacity to invade surrounding tissues in a tentaclelike pattern.47 This characteristic often leads to inadequate initial resection of the lesion as well as a high recurrence rate despite its low metastatic potential.48 In early stages, DFSP typically manifests as an asymptomatic plaque with a slow growth rate. The color of the lesion ranges from reddish brown to flesh colored. The pigmented form of DFSP, known as Bednar tumor, is the most common among Black patients.47 As the tumor grows, it tends to become firm and nodular. The most common location for DFSP is on the trunk or the upper and lower extremities.47

Although current guidelines designate MMS as the first-line treatment for DFSP, the procedure may be inaccessible for certain populations.49 Patients with skin of color are more likely to undergo wide local excision (WLE) than MMS; however, WLE is less effective, with a recurrence rate of 30% compared with 3% in those treated with MMS.50 A retrospective cohort study of more than 2000 patients revealed that Hispanic and Black patients were less likely to undergo MMS. In addition, the authors noted that WLE recipients more commonly were deceased at the end of the study.51

Despite undergoing treatment for a primary DFSP, Hispanic patients also appear to be at increased risk for a second surgery.52 Additional studies are needed to elucidate the reasons behind higher recurrence rates in Latine/Hispanic patients compared to NHW individuals.

Factors Influencing Skin Cancer Outcomes

In recent years, racial and ethnic disparities in health care use, medical treatment, and quality of care among minoritized populations (including Latine/Hispanic groups) have been documented in the medical literature.53,54 These systemic inequities, which are rooted in structural racism,55 have contributed to poorer health outcomes, worse health status, and lower-quality care for minoritized patients living in the United States, including those impacted by dermatologic conditions.8,43,55-57 Becoming familiar with the sociocultural factors influencing skin cancer outcomes in the Latine/Hispanic community (including the lack of or inadequate health insurance, medical mistrust, language, and other cultural elements) and the paucity of research in this domain could help eliminate existing health inequities in this population.

Health Insurance Coverage—Although the uninsured rates in the Latine population have decreased since the passage of the Affordable Care Act (from 30% in 2013 to a low of 19% in 2017),58 inadequate health insurance coverage remains one of the largest barriers to health care access and a contributor to health disparities among the Latine community. Nearly 1 in 5 Latine individuals in the United States are uninsured compared to 8% of NHW individuals.58 Even though Latine individuals are more likely than non-Latine individuals to be part of the workforce, Latine employees are less likely to receive employer-sponsored coverage (27% vs 53% for NHW individuals).59

Not surprisingly, noncitizens are far less likely to be insured; this includes lawfully present immigrants (ie, permanent residents or green card holders, refugees, asylees, and others who are authorized to live in the United States temporarily or permanently) and undocumented immigrants (including individuals who entered the country without authorization and individuals who entered the country lawfully and stayed after their visa or status expired). The higher uninsured rate among noncitizens reflects not only limited access to employer-sponsored coverage but includes immigrant eligibility restrictions for federal programs such as Medicaid, the Children’s Health Insurance Program, and the Affordable Care Act Marketplace coverage.60

With approximately 9 million Americans living in mixed-status families (and nearly 10% of babies born each year with at least one undocumented parent), restrictive federal or state health care policies may extend beyond their stated target and impact both Latine citizens and noncitizens.61-65 For instance, Vargas et al64 found that both Latine citizens and noncitizens who lived in states with a high number of immigration-related laws had decreased odds of reporting optimal health as compared to Latine respondents in states with fewer immigration-related laws.Other barriers to enrollment include fears and confusion about program qualification, even if eligible.58

Medical Mistrust and Unfamiliarity—Mistrust of medical professionals has been shown to reduce patient adherence to treatment as prescribed by their medical provider and can negatively influence health outcomes.53 For racial/ethnic minoritized groups (including Latine/Hispanic patients), medical mistrust may be rooted in patients’ experience of discrimination in the health care setting. In a recent cross-sectional study, results from a survey of California adults (including 704 non-Hispanic Black, 711 Hispanic, and 913 NHW adults) found links between levels of medical mistrust and perceived discrimination based on race/ethnicity and language as well as perceived discrimination due to income level and type or lack of insurance.53 Interestingly, discrimination attributed to income level and insurance status remained after controlling for race/ethnicity and language. As expected, patients reliant on public insurance programs such as Medicare have been reported to have greater medical mistrust and suspicion compared with private insurance holders.65 Together, these findings support the notion that individuals who have low socioeconomic status and lack insurance coverage—disproportionately historically marginalized populations—are more likely to perceive discrimination in health care settings, have greater medical mistrust, and experience poorer health outcomes.53

It also is important for health care providers to consider that the US health care system is unfamiliar to many Latine/Hispanic individuals. Costs of medical services tend to be substantially higher in the United States, which can contribute to mistrust in the system.66 In addition, unethical medical experimentations have negatively affected both Latine and especially non-Hispanic Black populations, with long-lasting perceptions of deception and exploitation.67 These beliefs have undermined the trust that these populations have in clinicians and the health care system.54,67

Language and Other Cultural Elements—The inability to effectively communicate with health care providers could contribute to disparities in access to and use of health care services among Latine/Hispanic individuals. In a Medical Expenditure Panel Survey analysis, half of Hispanic patients with limited comfort speaking English did not have a usual source of care, and almost 90% of those with a usual source of care had a provider who spoke Spanish or used interpreters—indicating that few Hispanic individuals with limited comfort speaking English selected a usual source of care without language assistance.68,69 In other examples, language barriers ­contributed to disparities in cancer screening, and individuals with limited English proficiency were more likely to have difficulty understanding their physician due to language barriers.68,70

Improving cultural misconceptions regarding skin conditions, especially skin cancer, is another important consideration in the Latine/Hispanic community. Many Latine/Hispanic individuals wrongly believe they cannot develop skin cancer due to their darker skin tones and lack of family history.26 Moreover, multiple studies assessing melanoma knowledge and perception among participants with skin of color (including one with an equal number of Latine/Hispanic, Black/African American, and Asian individuals for a total of 120 participants) revealed that many were unaware of the risk for melanoma on acral sites.71 Participants expressed a need for more culturally relevant content from both clinicians and public materials (eg, images of acral melanoma in a person with skin of color).71-73

Paucity of Research—There is limited research regarding skin cancer risks and methods of prevention for patients with skin of color, including the Latine/Hispanic population. Efforts to engage and include patients from these communities, as well as clinicians or investigators from similar backgrounds, in clinical studies are desperately needed. It also is important that clinical studies collect data beyond population descriptors to account for both clinical and genetic variations observed in the Latine/Hispanic population. 

Latine/Hispanic individuals are quite diverse with many variable factors that may influence skin cancer outcomes. Often, cancer surveillance data are available in aggregate only, which could mask this heterogeneity.74 Rigorous studies that collect more granular data, including objective measures of skin pigmentation beyond self-reported Fitzpatrick skin type, culture/beliefs, lifestyle/behavior, geographic location, socioeconomic status, genetics, or epigenetics could help fully elucidate skin cancer risks and mitigate health disparities among individuals who identify as part of this population.

Final Thoughts

The Latine/Hispanic community—the largest ethnic minoritized group in the United States—is disproportionately affected by dermatologic health disparities. We hope this review helps to increase recognition of the clinical manifestations of skin cancer in Latine/Hispanic patients. Other factors that may impact skin cancer outcomes in this population include (but are not limited to) lack of or inadequate health insurance, medical mistrust, linguistic barriers and/or individual/cultural perspectives, along with limited research. Recognizing and addressing these (albeit complex) barriers that contribute to the inequitable access to health care in this population remains a critical step toward improving skin cancer outcomes.

The Latine/Hispanic population in the United States comprises one of the largest and youngest skin of color communities.1,2 In 2020, this group accounted for 19% of all Americans—a percentage expected to increase to more than 25% by 2060.3

It must be emphasized that the Latine/Hispanic community in the United States is incredibly diverse.4 Approximately one-third of individuals in this group are foreign-born, and this community is made up of people from all racialized groups, religions, languages, and cultural identities.2 The heterogeneity of the Latine/Hispanic population translates into a wide representation of skin tones, reflecting a rich range of ancestries, ethnicities, and cultures. The percentage of individuals from each origin group may differ according to where they live in the United States; for instance, individuals who identify as Mexican comprise more than 80% of the Latine/Hispanic population in both Texas and California but only 17% in Florida, where more than half of Latine/Hispanic people identify as Cuban or Puerto Rican.4,5 As a result, when it comes to skin cancer epidemiology, variations in incidence and mortality may exist within each of these subgroups who identify as part of the Latine/Hispanic community, as reported for other cancers.6,7 Further research is needed to investigate these potential differences.Unfortunately, considerable health disparities persist among this rapidly growing population, including increased morbidity and mortality from melanoma and keratinocyte carcinomas (KCs) despite overall low lifetime incidence.8,9 In this review, the epidemiology, clinical manifestation, and ethnic disparities for skin cancer among the US Latine/Hispanic population are summarized; other factors impacting overall health and health care, including sociocultural factors, also are briefly discussed.

Terminology

Before a meaningful dialogue can be had about skin cancer in the Latine/Hispanic population, it is important to contextualize the terms used to identify this patient population, including Latino/Latine and Hispanic. In the early 1970s, the United States adopted the term Hispanic as a way of conglomerating Spanish-speaking individuals from Spain, the Caribbean, and Central and South America. The goal was to implement a common identifier that enabled the US government to study the economic and social development of these groups.10 Nevertheless, considerable differences (eg, variations in skin pigmentation, sun sensitivity) exist among Hispanic communities, with some having stronger European, African, or Amerindian influences due to colonization of their ­distinct countries.11

In contrast, Latino is a geographic term and refers to people with roots in Latin America and the Caribbean (Table 1).12,13 For example, a person from Brazil may be considered Latino but not Hispanic as Brazilians speak Portuguese; alternatively, Spaniards (who are considered Hispanic) are not Latino because Spain is not a Latin American country. A person from Mexico would be considered both Latino and Hispanic.13



More recently, the term Latine has been introduced as an alternative to the gender binary inherent in the Spanish language.12 For the purposes of this article, the terms Latine and Hispanic will be used interchangeably (unless otherwise specified) depending on how they are cited in the existing literature. Furthermore, the term non-Hispanic White (NHW) will be used to refer to individuals who have been socially ascribed or who self-identify as White in terms of race or ethnicity.

Melanoma

Melanoma, the deadliest form of skin cancer, is more likely to metastasize compared to other forms of skin cancer, including basal cell carcinoma (BCC) and squamous cell carcinoma (SCC). For Latine/Hispanic individuals living in the United States, the lifetime risk for melanoma is 1 in 200 compared to 1 in 33 for NHW individuals.14 While the lifetime risk for melanoma is low for the Latine/Hispanic population, Hispanic individuals are diagnosed with melanoma at an earlier age (mean, 56 years), and the rate of new cases is marginally higher for women (4.9 per 100,000) compared to men (4.8 per 100,000).15,16

Typical sites of melanoma manifestation in Latine/Hispanic individuals include the torso (most common site in Hispanic men), lower extremities (most common site in Hispanic women), and acral sites (palms, soles, and nails).9,16,17 Anatomic location also can vary according to age for both men and women. For men, the incidence of melanoma on the trunk appears to decrease with age, while the incidence on the head and neck may increase. For women, the incidence of melanoma on the lower extremities and hip increases with age. Cutaneous melanoma may manifest as a lesion with asymmetry, irregular borders, variation in pigmentation, large diameter (>6 mm), and evolution over time. In patients with skin of color, melanoma easily can be missed, as it also typically mimics more benign skin conditions and may develop from an existing black- or dark brown–­pigmented macule.18 The most common histologic subtype reported among Latine/Hispanic individuals in the United States is superficial spreading melanoma (20%–23%) followed by nodular melanoma and acral lentiginous melanoma.16,19 Until additional risk factors associated with melanoma susceptibility in Hispanic/Latine people are better elucidated, it may be appropriate to use an alternative acronym, such as CUBED (Table 2), in addition to the standard ABCDE system to help recognize potential melanoma on acral sites.18



Although the lifetime risk for melanoma among Hispanic individuals in the United States is lower than that for NHW individuals, Hispanic patients who are diagnosed with melanoma are more likely to present with increased tumor thickness and later-stage diagnosis compared to NHW individuals.8,16,20 In a recent study by Qian et al,8 advanced stage melanoma—defined as regional or distant stage disease—was present in 12.6% of NHW individuals. In contrast, the percentage of Hispanics with advanced disease was higher at 21%.8 Even after controlling for insurance and poverty status, Hispanic individuals were at greater risk than NHW individuals for late-stage diagnosis.16,20

Morbidity and mortality also have been shown to be higher in Hispanic patients with cutaneous melanoma.9,17 Reasons for this are multifactorial, with studies specific to melanoma citing challenges associated with early detection in individuals with deeply pigmented skin, a lack of awareness and knowledge about skin cancer among Latine/Hispanic patients, and treatment disparities.21-23 Moreover, very few studies have reported comprehensive data on patients from Africa and Latin America. Studies examining the role of genetic ancestry, epigenetic variants, and skin pigmentation and the risk for melanoma among the Latine/Hispanic population therefore are much needed.24

Keratinocyte Carcinomas

Keratinocyte carcinomas, also known as nonmelanoma skin cancers, include BCC and SCC. In comparison to the high-quality data available for melanoma from cancer registries, there are less reliable incidence data for KCs, especially among individuals with skin of color.25 As a result, KC epidemiology in the United States is drawn largely from case series (especially for individuals with skin of color) or claims data from small data sets often from geographically restricted regions within the United States.25,26

Basal Cell Carcinoma—Basal cell carcinoma is the most common malignant skin cancer in Latine/Hispanic individuals. Among those with lighter skin tones, the lifetime risk for BCC is about 30%.27,28 Men typically are affected at a higher rate than women, and the median age for diagnosis is 68 years.29 The development of BCC primarily is linked to lifetime accumulated UV radiation exposure. Even though BCC has a low mortality rate, it can lead to substantial morbidity due to factors such as tumor location, size, and rate of invasion, resulting in cosmetic and functional issues. Given its low metastatic potential, treatment of BCC typically is aimed at local control.30 Options for treatment include Mohs micrographic surgery (MMS), curettage and electrodessication, cryosurgery, photodynamic therapy, radiation therapy, and topical therapies. Systemic therapies are reserved for patients with locally advanced or metastatic disease.30

Latine/Hispanic patients characteristically present with BCCs on sun-exposed areas of the skin such as the head and neck region. In most patients, BCC manifests as a translucent pearly nodule with superficial telangiectasias and/or a nonhealing ulcer with a central depression and rolled nontender borders. However, in patients with skin of color, 66% of BCCs manifest with pigmentation; in fact, pigmented BCC (a subtype of BCC) has been shown to have a higher prevalence among Hispanic individuals, with an incidence twice as frequent as in NHW individuals.31 In addition, there are reports of increased tendency among Latine/Hispanic individuals to develop multiple BCCs.32,33

The relationship between UV exposure and KCs could explain the relatively higher incidence in populations with skin of color living in warmer climates, including Hispanic individuals.34 Even so, the development of BCCs appears to correlate directly with the degree of pigmentation in the skin, as it is most common in individuals with lighter skin tones within the Hispanic population.25,34,35 Other risk factors associated with BCC development include albinism, arsenic ingestion, chronic infections, immunosuppression, history of radiation treatment, and history of scars or ulcers due to physical/thermal trauma.35-37

Squamous Cell Carcinoma—Squamous cell carcinoma is the second most common skin cancer among Latine/Hispanic patients. In contrast with NHW patients, evidence supporting the role of UV exposure as a primary risk factor for SCC in patients with skin of color remains limited.25,38 Reports linking UV exposure and KCs in Hispanic and Black individuals predominantly include case series or population-based studies that do not consider levels of UV exposure.25

More recently, genetic ancestry analyses of a large multiethnic cohort found an increased risk for cutaneous SCC among Latine/Hispanic individuals with European ancestry compared to those with Native American or African ancestry; however, these genetic ancestry associations were attenuated (although not eliminated) after considering skin pigmentation (using loci associated with skin pigmentation), history of sun exposure (using actinic keratoses as a covariate for chronic sun exposure), and sun-protected vs sun-exposed anatomic sites, supporting the role of other environmental or sociocultural factors in the development of SCC.39 Similar to BCCs, immunosuppression, chronic scarring, skin irritation, and inflammatory disease also are documented risk factors.9,32

Among NHW individuals with lighter skin tones, SCC characteristically manifests on sun-exposed areas of the skin such as the head and neck region. Typically, a lesion may appear as a scaly erythematous papule or plaque that may be verrucous in nature or a nonhealing bleeding ulcer. In patients with more deeply pigmented skin, SCC tends to develop in the perianal region and on the penis and lower legs; pigmented lesions also may be present (as commonly reported in BCCs).9,32,36

Unfortunately, the lower incidence of KCs and lack of surveillance in populations with skin of color result in a low index of clinical suspicion, leading to delayed diagnoses and increased morbidity.40 Keratinocyte carcinomas are more costly to treat and require more health care resources for Latine/Hispanic and Black patients compared to their NHW counterparts; for example, KCs are associated with more ambulatory visits, more prescription medications, and greater cost on a per-person, per-year basis in Latine/Hispanic and Black patients compared with NHW patients.41 Moreover, a recent multicenter retrospective study found Hispanic patients had 17% larger MMS defects following treatment for KCs compared to NHW patients after adjustment for age, sex, and insurance type.42

Hispanic patients tend to present initially with SCCs in areas associated with advanced disease, such as the anogenital region, penis, and the lower extremities. Latine and Black men have the highest incidence of penile SCC, which is rare with high morbidity and mortality.32,43,44 The higher incidence of penile SCC among Hispanic individuals living in southern states could correspond to circumcision or HPV infection rates,44 ultimately impacting incidence.45

Dermatofibrosarcoma Protuberans

Dermatofibrosarcoma protuberans (DFSP) is a rare locally aggressive cutaneous sarcoma. According to population studies, overall incidence of DFSP is around 4.1 to 4.2 per million in the United States. Population-based studies on DFSP are limited, but available data suggest that Black patients as well as women have the highest incidence.46

Dermatofibrosarcoma protuberans is characterized by its capacity to invade surrounding tissues in a tentaclelike pattern.47 This characteristic often leads to inadequate initial resection of the lesion as well as a high recurrence rate despite its low metastatic potential.48 In early stages, DFSP typically manifests as an asymptomatic plaque with a slow growth rate. The color of the lesion ranges from reddish brown to flesh colored. The pigmented form of DFSP, known as Bednar tumor, is the most common among Black patients.47 As the tumor grows, it tends to become firm and nodular. The most common location for DFSP is on the trunk or the upper and lower extremities.47

Although current guidelines designate MMS as the first-line treatment for DFSP, the procedure may be inaccessible for certain populations.49 Patients with skin of color are more likely to undergo wide local excision (WLE) than MMS; however, WLE is less effective, with a recurrence rate of 30% compared with 3% in those treated with MMS.50 A retrospective cohort study of more than 2000 patients revealed that Hispanic and Black patients were less likely to undergo MMS. In addition, the authors noted that WLE recipients more commonly were deceased at the end of the study.51

Despite undergoing treatment for a primary DFSP, Hispanic patients also appear to be at increased risk for a second surgery.52 Additional studies are needed to elucidate the reasons behind higher recurrence rates in Latine/Hispanic patients compared to NHW individuals.

Factors Influencing Skin Cancer Outcomes

In recent years, racial and ethnic disparities in health care use, medical treatment, and quality of care among minoritized populations (including Latine/Hispanic groups) have been documented in the medical literature.53,54 These systemic inequities, which are rooted in structural racism,55 have contributed to poorer health outcomes, worse health status, and lower-quality care for minoritized patients living in the United States, including those impacted by dermatologic conditions.8,43,55-57 Becoming familiar with the sociocultural factors influencing skin cancer outcomes in the Latine/Hispanic community (including the lack of or inadequate health insurance, medical mistrust, language, and other cultural elements) and the paucity of research in this domain could help eliminate existing health inequities in this population.

Health Insurance Coverage—Although the uninsured rates in the Latine population have decreased since the passage of the Affordable Care Act (from 30% in 2013 to a low of 19% in 2017),58 inadequate health insurance coverage remains one of the largest barriers to health care access and a contributor to health disparities among the Latine community. Nearly 1 in 5 Latine individuals in the United States are uninsured compared to 8% of NHW individuals.58 Even though Latine individuals are more likely than non-Latine individuals to be part of the workforce, Latine employees are less likely to receive employer-sponsored coverage (27% vs 53% for NHW individuals).59

Not surprisingly, noncitizens are far less likely to be insured; this includes lawfully present immigrants (ie, permanent residents or green card holders, refugees, asylees, and others who are authorized to live in the United States temporarily or permanently) and undocumented immigrants (including individuals who entered the country without authorization and individuals who entered the country lawfully and stayed after their visa or status expired). The higher uninsured rate among noncitizens reflects not only limited access to employer-sponsored coverage but includes immigrant eligibility restrictions for federal programs such as Medicaid, the Children’s Health Insurance Program, and the Affordable Care Act Marketplace coverage.60

With approximately 9 million Americans living in mixed-status families (and nearly 10% of babies born each year with at least one undocumented parent), restrictive federal or state health care policies may extend beyond their stated target and impact both Latine citizens and noncitizens.61-65 For instance, Vargas et al64 found that both Latine citizens and noncitizens who lived in states with a high number of immigration-related laws had decreased odds of reporting optimal health as compared to Latine respondents in states with fewer immigration-related laws.Other barriers to enrollment include fears and confusion about program qualification, even if eligible.58

Medical Mistrust and Unfamiliarity—Mistrust of medical professionals has been shown to reduce patient adherence to treatment as prescribed by their medical provider and can negatively influence health outcomes.53 For racial/ethnic minoritized groups (including Latine/Hispanic patients), medical mistrust may be rooted in patients’ experience of discrimination in the health care setting. In a recent cross-sectional study, results from a survey of California adults (including 704 non-Hispanic Black, 711 Hispanic, and 913 NHW adults) found links between levels of medical mistrust and perceived discrimination based on race/ethnicity and language as well as perceived discrimination due to income level and type or lack of insurance.53 Interestingly, discrimination attributed to income level and insurance status remained after controlling for race/ethnicity and language. As expected, patients reliant on public insurance programs such as Medicare have been reported to have greater medical mistrust and suspicion compared with private insurance holders.65 Together, these findings support the notion that individuals who have low socioeconomic status and lack insurance coverage—disproportionately historically marginalized populations—are more likely to perceive discrimination in health care settings, have greater medical mistrust, and experience poorer health outcomes.53

It also is important for health care providers to consider that the US health care system is unfamiliar to many Latine/Hispanic individuals. Costs of medical services tend to be substantially higher in the United States, which can contribute to mistrust in the system.66 In addition, unethical medical experimentations have negatively affected both Latine and especially non-Hispanic Black populations, with long-lasting perceptions of deception and exploitation.67 These beliefs have undermined the trust that these populations have in clinicians and the health care system.54,67

Language and Other Cultural Elements—The inability to effectively communicate with health care providers could contribute to disparities in access to and use of health care services among Latine/Hispanic individuals. In a Medical Expenditure Panel Survey analysis, half of Hispanic patients with limited comfort speaking English did not have a usual source of care, and almost 90% of those with a usual source of care had a provider who spoke Spanish or used interpreters—indicating that few Hispanic individuals with limited comfort speaking English selected a usual source of care without language assistance.68,69 In other examples, language barriers ­contributed to disparities in cancer screening, and individuals with limited English proficiency were more likely to have difficulty understanding their physician due to language barriers.68,70

Improving cultural misconceptions regarding skin conditions, especially skin cancer, is another important consideration in the Latine/Hispanic community. Many Latine/Hispanic individuals wrongly believe they cannot develop skin cancer due to their darker skin tones and lack of family history.26 Moreover, multiple studies assessing melanoma knowledge and perception among participants with skin of color (including one with an equal number of Latine/Hispanic, Black/African American, and Asian individuals for a total of 120 participants) revealed that many were unaware of the risk for melanoma on acral sites.71 Participants expressed a need for more culturally relevant content from both clinicians and public materials (eg, images of acral melanoma in a person with skin of color).71-73

Paucity of Research—There is limited research regarding skin cancer risks and methods of prevention for patients with skin of color, including the Latine/Hispanic population. Efforts to engage and include patients from these communities, as well as clinicians or investigators from similar backgrounds, in clinical studies are desperately needed. It also is important that clinical studies collect data beyond population descriptors to account for both clinical and genetic variations observed in the Latine/Hispanic population. 

Latine/Hispanic individuals are quite diverse with many variable factors that may influence skin cancer outcomes. Often, cancer surveillance data are available in aggregate only, which could mask this heterogeneity.74 Rigorous studies that collect more granular data, including objective measures of skin pigmentation beyond self-reported Fitzpatrick skin type, culture/beliefs, lifestyle/behavior, geographic location, socioeconomic status, genetics, or epigenetics could help fully elucidate skin cancer risks and mitigate health disparities among individuals who identify as part of this population.

Final Thoughts

The Latine/Hispanic community—the largest ethnic minoritized group in the United States—is disproportionately affected by dermatologic health disparities. We hope this review helps to increase recognition of the clinical manifestations of skin cancer in Latine/Hispanic patients. Other factors that may impact skin cancer outcomes in this population include (but are not limited to) lack of or inadequate health insurance, medical mistrust, linguistic barriers and/or individual/cultural perspectives, along with limited research. Recognizing and addressing these (albeit complex) barriers that contribute to the inequitable access to health care in this population remains a critical step toward improving skin cancer outcomes.

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References
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  8. Qian Y, Johannet P, Sawyers A, et al. The ongoing racial disparities in melanoma: an analysis of the Surveillance, Epidemiology, and End Results database (1975-2016). J Am Acad Dermatol. 2021;84:1585-1593.
  9. Hogue L, Harvey VM. Basal cell carcinoma, squamous cell carcinoma, and cutaneous melanoma in skin of color patients. Dermatol Clin. 2019;37:519-526.
  10. Cruzval-O’Reilly E, Lugo-Somolinos A. Melanoma in Hispanics: we may have it all wrong. Cutis. 2020;106:28-30.
  11. Borrell LN, Elhawary JR, Fuentes-Afflick E, et al. Race and genetic ancestry in medicine—a time for reckoning with racism. N Engl J Med. 2021;384:474-480.
  12. Lopez MH, Krogstad JM, Passel JS. Who is Hispanic? September 5, 2023. Accessed September 3, 2024. https://www.pewresearch.org/short-reads/2023/09/05/who-is-hispanic/
  13. Carrasquillo OY, Lambert J, Merritt BG. Comment on “Disparities in nonmelanoma skin cancer in Hispanic/Latino patients based on Mohs micrographic surgery defect size: a multicenter retrospective study.”J Am Acad Dermatol. 2022;87:E129-E130.
  14. American Cancer Society. Key statistics for melanoma skin cancer. Updated January 17, 2024. Accessed September 3, 2024. https://www.cancer.org/cancer/types/melanoma-skin-cancer/about/key-statistics.html
  15. National Cancer Institute. Melanoma of the skin: recent trends in SEER age-adjusted incidence rates, 2000-2021. Updated June 27, 2024. Accessed September 3, 2024. https://seer.cancer.gov/statistics-network/explorer/application.htmlsite=53&data_type=1&graph_type=2&compareBy=sex&chk_sex_3=3&chk_sex_2=2&rate_type=2&race=6&age_range=1&stage=101&advopt_precision=1&advopt_show_ci=on&hdn_view=0&advopt_display=2
  16. Garnett E, Townsend J, Steele B, et al. Characteristics, rates, and trends of melanoma incidence among Hispanics in the USA. Cancer Causes Control. 2016;27:647-659.
  17. Higgins S, Nazemi A, Feinstein S, et al. Clinical presentations of melanoma in African Americans, Hispanics, and Asians. Dermatol Surg. 2019;45:791-801.
  18. Bristow IR, de Berker DA, Acland KM, et al. Clinical guidelines for the recognition of melanoma of the foot and nail unit. J Foot Ankle Res. 2010;3:25.
  19. Fernandez JM, Mata EM, Behbahani S, et al. Survival of Hispanic patients with cutaneous melanoma: a retrospective cohort analysis of 6016 cases from the National Cancer Database. J Am Acad Dermatol. 2023;88:1135-1138.
  20. Hu S, Sherman R, Arheart K, et al. Predictors of neighborhood risk for late-stage melanoma: addressing disparities through spatial analysis and area-based measures. J Investigative Dermatol. 2014;134:937-945.
  21. Buster KJ, You Z, Fouad M, et al. Skin cancer risk perceptions: a comparison across ethnicity, age, education, gender, and income. J Am Acad Dermatol. 2012;66:771-779.
  22. Halpern MT, Ward EM, Pavluck AL, et al. Association of insurance status and ethnicity with cancer stage at diagnosis for 12 cancer sites: a retrospective analysis. Lancet Oncology. 2008;9:222-231.
  23. Weiss J, Kirsner RS, Hu S. Trends in primary skin cancer prevention among US Hispanics: a systematic review. J Drugs Dermatol. 2012;11:580-586.
  24. Carvalho LAD, Aguiar FC, Smalley KSM, et al. Acral melanoma: new insights into the immune and genomic landscape. Neoplasia. 2023;46:100947.
  25. Kolitz E, Lopes F, Arffa M, et al. UV Exposure and the risk of keratinocyte carcinoma in skin of color: a systematic review. JAMA Dermatol. 2022;158:542-546.
  26. Lukowiak TM, Aizman L, Perz A, et al. Association of age, sex, race, and geographic region with variation of the ratio of basal cell to cutaneous squamous cell carcinomas in the United States. JAMA Dermatol. 2020;156:1192-1198.
  27. Basset-Seguin N, Herms F. Update in the management of basal cell carcinoma. Acta Derm Venereol. 2020;100:adv00140.
  28. McDaniel B, Badri T, Steele RB. Basal cell carcinoma. StatPearls [Internet]. Updated March 13, 2024. Accessed September 3, 2024. https://www.ncbi.nlm.nih.gov/books/NBK482439/
  29. Dessinioti C, Antoniou C, Katsambas A, et al. Basal cell carcinoma: what’s new under the sun. Photochem Photobiol. 2010;86:481-491.
  30. Kim DP, Kus KJB, Ruiz E. Basal cell carcinoma review. Hematol Oncol Clin North Am. 2019;33:13-24.
  31. Bigler C, Feldman J, Hall E, et al. Pigmented basal cell carcinoma in Hispanics. J Am Acad Dermatol. 1996;34(5 pt 1):751-752.
  32. Higgins S, Nazemi A, Chow M, et al. Review of nonmelanoma skin cancer in African Americans, Hispanics, and Asians. Dermatol Surg. 2018;44:903-910.
  33. Byrd-Miles K, Toombs EL, Peck GL. Skin cancer in individuals of African, Asian, Latin-American, and American-Indian descent: differences in incidence, clinical presentation, and survival compared to Caucasians. J Drugs Dermatol. 2007;6:10-16.
  34. Rivas M, Rojas E, Calaf GM, et al. Association between non-melanoma and melanoma skin cancer rates, vitamin D and latitude. Oncol Lett. 2017;13:3787-3792.
  35. Bradford PT. Skin cancer in skin of color. Dermatol Nurs. 2009;21:170-177, 206.
  36. Davis DS, Robinson C, Callender VD. Skin cancer in women of color: epidemiology, pathogenesis and clinical manifestations. Int J Womens Dermatol. 2021;7:127-134.
  37. Maafs E, De la Barreda F, Delgado R, et al. Basal cell carcinoma of trunk and extremities. Int J Dermatol. 1997;36:622-628.
  38. Munjal A, Ferguson N. Skin cancer in skin of color. Dermatol Clin. 2023;41:481-489.
  39. Jorgenson E, Choquet H, Yin J, et al. Genetic ancestry, skin pigmentation, and the risk of cutaneous squamous cell carcinoma in Hispanic/Latino and non-Hispanic white populations. Commun Biol. 2020;3:765.
  40. Soliman YS, Mieczkowska K, Zhu TR, et al. Characterizing basal cell carcinoma in Hispanic individuals undergoing Mohs micrographic surgery: a 7-year retrospective review at an academic institution in the Bronx. Brit J Dermatol. 2022;187:597-599.
  41. Sierro TJ, Blumenthal LY, Hekmatjah J, et al. Differences in health care resource utilization and costs for keratinocyte carcinoma among racioethnic groups: a population-based study. J Am Acad Dermatol. 2022;86:373-378.
  42. Blumenthal LY, Arzeno J, Syder N, et al. Disparities in nonmelanoma skin cancer in Hispanic/Latino patients based on Mohs micrographic surgery defect size: a multicenter retrospective study. J Am Acad Dermatol. 2022;86:353-358.
  43. Slopnick EA, Kim SP, Kiechle JE, et al. Racial disparities differ for African Americans and Hispanics in the diagnosis and treatment of penile cancer. Urology. 2016;96:22-28.
  44. Goodman MT, Hernandez BY, Shvetsov YB. Demographic and pathologic differences in the incidence of invasive penile cancer in the United States, 1995-2003. Cancer Epidemiol Biomarkers Prev. 2007;16:1833-1839.
  45. Thompson EL, Rosen BL, Maness SB. Social determinants of health and human papillomavirus vaccination among young adults, National Health Interview Survey 2016. J Community Health. 2019;44:149-158.
  46. Hao X, Billings SD, Wu F, et al. Dermatofibrosarcoma protuberans: update on the diagnosis and treatment. J Clin Med. 2020;9:1752.
  47. Mosallaei D, Lee EB, Lobl M, et al. Rare cutaneous malignancies in skin of color. Dermatol Surg. 2022;48:606-612.
  48. Criscito MC, Martires KJ, Stein JA. Prognostic factors, treatment, and survival in dermatofibrosarcoma protuberans. JAMA Dermatol. 2016;152:1365-1371.
  49. Orenstein LAV, Nelson MM, Wolner Z, et al. Differences in outpatient dermatology encounter work relative value units and net payments by patient race, sex, and age. JAMA Dermatol. 2021;157:406-412.
  50. Lowe GC, Onajin O, Baum CL, et al. A comparison of Mohs micrographic surgery and wide local excision for treatment of dermatofibrosarcoma protuberans with long-term follow-up: the Mayo Clinic experience. Dermatol Surg. 2017;43:98-106.
  51. Moore KJ, Chang MS, Weiss J, et al. Racial and ethnic differences in the surgical treatment of dermatofibrosarcoma protuberans: a retrospective cohort analysis. J Am Acad Dermatol. 2022;87:245-247.
  52. Trofymenko O, Bordeaux JS, Zeitouni NC. Survival in patients with primary dermatofibrosarcoma protuberans: National Cancer Database analysis. J Am Acad Dermatol. 2018;78:1125-1134.
  53. Bazargan M, Cobb S, Assari S. Discrimination and medical mistrust in a racially and ethnically diverse sample of California adults. Ann Fam Med. 2021;19:4-15.
  54. Smedley BD, Stith AY, Nelson AR, eds. Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care. Washington, DC; 2003.
  55. Bailey ZD, Krieger N, Agenor M, et al. Structural racism and health inequities in the USA: evidence and interventions. Lancet. 2017;389:1453-1463.
  56. Tackett KJ, Jenkins F, Morrell DS, et al. Structural racism and its influence on the severity of atopic dermatitis in African American children. Pediatric Dermatol. 2020;37:142-146.
  57. Greif C, Srivastava D, Nijhawan RI. A retrospective cohort study of dermatofibrosarcoma protuberans at a large metropolitan academic center. JAAD Int. 2022;6:104-106.
  58. Office of the Assistant Secretary for Planning and Evaluation. Health insurance coverage and access to care among Latinos: recent rrends and key challenges (HP-2021-22). October 8, 2021. Accessed September 3, 2024. https://aspe.hhs.gov/reports/health-insurance-coverage-access-care-among-latinos
  59. Keisler-Starkey K, Bunch LN. Health insurance coverage in the United States: 2020 (Current Population Reports No. P60-274). US Census Bureau; 2021. https://www.census.gov/content/dam/Census/library/publications/2021/demo/p60-274.pdf
  60. Kaiser Family Foundation. Key facts on health coverage of immigrants. Updated June 26, 2024. Accessed September 3, 2024. https://www.kff.org/racial-equity-and-health-policy/fact-sheet/key-facts-on-health-coverage-of-immigrants/
  61. Pew Research Center. Unauthorized immigrants: length of residency, patterns of parenthood. Published December 1, 2011. Accessed October 28, 2024. https://www.pewresearch.org/race-and-ethnicity/2011/12/01/unauthorized-immigrants-length-of-residency-patterns-of-parenthood/
  62. Schneider J, Schmitt M. Understanding the relationship between racial discrimination and mental health among African American adults: a review. SAGE Open. 2015;5:1-10.
  63. Philbin MM, Flake M, Hatzenbuehler ML, et al. State-level immigration and immigrant-focused policies as drivers of Latino health disparities in the United States. Soc Sci Med. 2018;199:29-38.
  64. Vargas ED, Sanchez GR, Juarez M. The impact of punitive immigrant laws on the health of Latina/o Populations. Polit Policy. 2017;45:312-337.
  65. Sutton AL, He J, Edmonds MC, et al. Medical mistrust in Black breast cancer patients: acknowledging the roles of the trustor and the trustee. J Cancer Educ. 2019;34:600-607.
  66. Jacobs J. An overview of Latin American healthcare systems. Pacific Prime Latin America. July 31, 2023. Accessed September 3, 2024. https://www.pacificprime.lat/blog/an-overview-of-latin-american-healthcare-systems/
  67. CDC. Unfair and unjust practices and conditions harm Hispanic and Latino people and drive health disparities. May 15, 2024. Accessed September 3, 2024. https://www.cdc.gov/tobacco-health-equity/collection/hispanic-latino-unfair-and-unjust.html
  68. Hall IJ, Rim SH, Dasari S. Preventive care use among Hispanic adults with limited comfort speaking English: an analysis of the Medical Expenditure Panel Survey data. Prev Med. 2022;159:107042.
  69. Brach C, Chevarley FM. Demographics and health care access and utilization of limited-English-proficient and English-proficient Hispanics. Agency for Healthcare Research and Quality. February 2008. http://meps.ahrq.gov/mepsweb/data_files/publications//rf28/rf28.pdf
  70. Berdahl TA, Kirby JB. Patient-provider communication disparities by limited English proficiency (LEP): trends from the US Medical Expenditure Panel Survey, 2006-2015. J General Intern Med. 2019;34:1434-1440.
  71. Robinson JK, Joshi KM, Ortiz S, et al. Melanoma knowledge, perception, and awareness in ethnic minorities in Chicago: recommendations regarding education. Psychooncology. 2011;20:313-320.
  72. Robinson JK, Nodal M, Chavez L, et al. Enhancing the relevance of skin self-examination for Latinos. JAMA Dermatol. 2017;153:717-718.
  73. Buchanan Lunsford N, Berktold J, Holman DM, et al. Skin cancer knowledge, awareness, beliefs and preventive behaviors among black and hispanic men and women. Prev Med Rep. 2018;12:203-209.
  74. Madrigal JM, Correa-Mendez M, Arias JD, et al. Hispanic, Latino/a, Latinx, Latine: disentangling the identities of Hispanic/Latino Americans. National Cancer Institute Division of Cancer Epidemiology & Genetics. October 20, 2022. Accessed September 3, 2024. https://dceg.cancer.gov/about/diversity-inclusion/inclusivity-minute/2022/disentangling-identities-hispanic-latino-americans
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  • The Latine/Hispanic community—the largest ethnic minoritized group in the United States—is disproportionately affected by disparities in skin cancer outcomes.
  • Factors influencing skin cancer outcomes in Latine/Hispanic patients in the United States are complex and multidimensional, including lack of familiarity among dermatologists with skin cancer manifestation in this population compared to non-Hispanic White individuals as well as limited data elucidating risk factors for skin cancer in patients with skin of color and sociocultural factors.
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Pinto Bean Pressure Wraps: A Novel Approach to Treating Digital Warts

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Pinto Bean Pressure Wraps: A Novel Approach to Treating Digital Warts

Practice Gap

Verruca vulgaris is a common dermatologic challenge due to its high prevalence and tendency to recur following routinely employed destructive modalities (eg, cryotherapy, electrosurgery), which can incur a considerable amount of pain and some risk for scarring.1,2 Other treatment methods for warts such as topical salicylic acid preparations, topical immunotherapy, or intralesional allergen injections often require multiple treatment sessions.3,4 Furthermore, the financial burden of traditional wart treatment can be substantial.4 Better techniques are needed to improve the clinician’s approach to treating warts. We describe a home-based technique to treat common digital warts using pinto bean pressure wraps to induce ischemic changes in wart tissue with similar response rates to commonly used modalities.

Technique

Our technique utilizes a small, hard, convex object that is applied directly over the digital wart. A simple self-adhesive wrap is used to cover the object and maintain constant pressure on the wart overnight. We typically use a dried pinto bean (a variety of the common bean Phaseolus vulgaris) acquired from a local grocery store due to its ideal size, hard surface, and convex shape (Figure 1). The bean is taped in place directly overlying the wart and covered with a self-adhesive wrap overnight. The wrap is removed in the morning, and often no further treatment is needed. The ischemic wart tissue is allowed to slough spontaneously over 1 to 2 weeks. No wound care or dressing is necessary (Figure 2). Larger warts may require application of the pressure wraps for 2 to 3 additional nights. While most warts resolve with this technique, we have observed a recurrence rate similar to that for cryotherapy. Patients are advised that any recurrent warts can be re-treated monthly, if needed, until resolution.

FIGURE 1. A, The home pressure wrap kit includes pinto beans, stretch tape, and a self-adherent wrap. B, A pinto bean is taped in place directly over the wart. C, The selfadherent wrap is applied to augment the pressure of the secured bean.

FIGURE 2. A–C, The digital wart before treatment, 2 days after a single overnight pressure wrap application showing necrosis of the wart, and 6 days posttreatment showing evidence of sloughing.

What to Use and How to Prepare—Any small, hard, convex object can be used for the pressure wrap; we also have used appropriately sized and shaped plastic shirt buttons with similar results. Home kits can be assembled in advance and provided to patients at their initial visit along with appropriate instructions (Figure 1A).

Effects on the Skin and Distal Digit—Application of pressure wraps does not harm normal skin; however, care should be taken when the self-adherent wrap is applied so as not to induce ischemia of the distal digit. The wrap should be applied using gentle pressure with patients experiencing minimal discomfort from the overnight application.

Indications—This pressure wrap technique can be employed on most digital warts, including periungual warts, which can be difficult to treat by other means. However, in our experience this technique is not effective for nondigital warts, likely due to the inability to maintain adequate pressure with the overlying dressing. Patients at risk for compromised digital perfusion, such as those with Raynaud phenomenon or systemic sclerosis, should not be treated with pressure wraps due to possible digital ischemia.

Precautions—Patients should be advised that the pinto bean should only be used if dry and should not be ingested. The bean can be a choking hazard for small children, therefore appropriate precautions should be used. Allergic contact dermatitis to the materials used in this technique is possible, but we have never observed this. The pinto bean can be reused for future application as long as it remains dry and provides a hard convex surface.

Practice Implications

The probable mechanism of the ischemic changes to the wart tissue likely is the occlusion of tortuous blood vessels in the dermal papillae, which are intrinsic to wart tissue and absent in normal skin.1 This pressure-induced ischemic injury allows for selective destruction of the wart tissue with sparing of the normal skin. Our technique is fairly novel, although at least one report in the literature has described the use of a mechanical device to induce ischemic changes in skin tags.5

The use of pinto bean pressure wraps to induce ischemic change in digital warts provides a low-risk and nearly pain-free alternative to more expensive and invasive treatment methods. Moreover, this technique allows for a low-cost home-based therapy that can be repeated easily for other digital sites or if recurrence is noted.

References
  1. Cardoso J, Calonje E. Cutaneous manifestations of human papillomaviruses: a review. Acta Dermatovenerol Alp Pannonica Adriat. 2011;20:145-154. 
  2. Lipke M. An armamentarium of wart treatments. Clin Med Res. 2006;4:273-293. doi:10.3121/cmr.4.4.273 
  3. Muse M, Stiff K, Glines K, et al. A review of intralesional wart therapy. Dermatol Online J. 2020;26:2. doi:10.5070/D3263048027
  4. Berna R, Margolis D, Barbieri J. Annual health care utilization and costs for treatment of cutaneous and anogenital warts among a commercially insured population in the US, 2017-2019. JAMA Dermatol. 2022;158:695-697. doi:10.1001/jamadermatol.2022.0964
  5. Fredriksson C, Ilias M, Anderson C. New mechanical device for effective removal of skin tags in routine health care. Dermatol Online J. 2009;15:9. doi:10.5070/D37tj2800k
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Cutis. 2024 November;114(5):169-170. doi:10.12788/cutis.1121

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Cutis. 2024 November;114(5):169-170. doi:10.12788/cutis.1121

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Cutis. 2024 November;114(5):169-170. doi:10.12788/cutis.1121

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Practice Gap

Verruca vulgaris is a common dermatologic challenge due to its high prevalence and tendency to recur following routinely employed destructive modalities (eg, cryotherapy, electrosurgery), which can incur a considerable amount of pain and some risk for scarring.1,2 Other treatment methods for warts such as topical salicylic acid preparations, topical immunotherapy, or intralesional allergen injections often require multiple treatment sessions.3,4 Furthermore, the financial burden of traditional wart treatment can be substantial.4 Better techniques are needed to improve the clinician’s approach to treating warts. We describe a home-based technique to treat common digital warts using pinto bean pressure wraps to induce ischemic changes in wart tissue with similar response rates to commonly used modalities.

Technique

Our technique utilizes a small, hard, convex object that is applied directly over the digital wart. A simple self-adhesive wrap is used to cover the object and maintain constant pressure on the wart overnight. We typically use a dried pinto bean (a variety of the common bean Phaseolus vulgaris) acquired from a local grocery store due to its ideal size, hard surface, and convex shape (Figure 1). The bean is taped in place directly overlying the wart and covered with a self-adhesive wrap overnight. The wrap is removed in the morning, and often no further treatment is needed. The ischemic wart tissue is allowed to slough spontaneously over 1 to 2 weeks. No wound care or dressing is necessary (Figure 2). Larger warts may require application of the pressure wraps for 2 to 3 additional nights. While most warts resolve with this technique, we have observed a recurrence rate similar to that for cryotherapy. Patients are advised that any recurrent warts can be re-treated monthly, if needed, until resolution.

FIGURE 1. A, The home pressure wrap kit includes pinto beans, stretch tape, and a self-adherent wrap. B, A pinto bean is taped in place directly over the wart. C, The selfadherent wrap is applied to augment the pressure of the secured bean.

FIGURE 2. A–C, The digital wart before treatment, 2 days after a single overnight pressure wrap application showing necrosis of the wart, and 6 days posttreatment showing evidence of sloughing.

What to Use and How to Prepare—Any small, hard, convex object can be used for the pressure wrap; we also have used appropriately sized and shaped plastic shirt buttons with similar results. Home kits can be assembled in advance and provided to patients at their initial visit along with appropriate instructions (Figure 1A).

Effects on the Skin and Distal Digit—Application of pressure wraps does not harm normal skin; however, care should be taken when the self-adherent wrap is applied so as not to induce ischemia of the distal digit. The wrap should be applied using gentle pressure with patients experiencing minimal discomfort from the overnight application.

Indications—This pressure wrap technique can be employed on most digital warts, including periungual warts, which can be difficult to treat by other means. However, in our experience this technique is not effective for nondigital warts, likely due to the inability to maintain adequate pressure with the overlying dressing. Patients at risk for compromised digital perfusion, such as those with Raynaud phenomenon or systemic sclerosis, should not be treated with pressure wraps due to possible digital ischemia.

Precautions—Patients should be advised that the pinto bean should only be used if dry and should not be ingested. The bean can be a choking hazard for small children, therefore appropriate precautions should be used. Allergic contact dermatitis to the materials used in this technique is possible, but we have never observed this. The pinto bean can be reused for future application as long as it remains dry and provides a hard convex surface.

Practice Implications

The probable mechanism of the ischemic changes to the wart tissue likely is the occlusion of tortuous blood vessels in the dermal papillae, which are intrinsic to wart tissue and absent in normal skin.1 This pressure-induced ischemic injury allows for selective destruction of the wart tissue with sparing of the normal skin. Our technique is fairly novel, although at least one report in the literature has described the use of a mechanical device to induce ischemic changes in skin tags.5

The use of pinto bean pressure wraps to induce ischemic change in digital warts provides a low-risk and nearly pain-free alternative to more expensive and invasive treatment methods. Moreover, this technique allows for a low-cost home-based therapy that can be repeated easily for other digital sites or if recurrence is noted.

Practice Gap

Verruca vulgaris is a common dermatologic challenge due to its high prevalence and tendency to recur following routinely employed destructive modalities (eg, cryotherapy, electrosurgery), which can incur a considerable amount of pain and some risk for scarring.1,2 Other treatment methods for warts such as topical salicylic acid preparations, topical immunotherapy, or intralesional allergen injections often require multiple treatment sessions.3,4 Furthermore, the financial burden of traditional wart treatment can be substantial.4 Better techniques are needed to improve the clinician’s approach to treating warts. We describe a home-based technique to treat common digital warts using pinto bean pressure wraps to induce ischemic changes in wart tissue with similar response rates to commonly used modalities.

Technique

Our technique utilizes a small, hard, convex object that is applied directly over the digital wart. A simple self-adhesive wrap is used to cover the object and maintain constant pressure on the wart overnight. We typically use a dried pinto bean (a variety of the common bean Phaseolus vulgaris) acquired from a local grocery store due to its ideal size, hard surface, and convex shape (Figure 1). The bean is taped in place directly overlying the wart and covered with a self-adhesive wrap overnight. The wrap is removed in the morning, and often no further treatment is needed. The ischemic wart tissue is allowed to slough spontaneously over 1 to 2 weeks. No wound care or dressing is necessary (Figure 2). Larger warts may require application of the pressure wraps for 2 to 3 additional nights. While most warts resolve with this technique, we have observed a recurrence rate similar to that for cryotherapy. Patients are advised that any recurrent warts can be re-treated monthly, if needed, until resolution.

FIGURE 1. A, The home pressure wrap kit includes pinto beans, stretch tape, and a self-adherent wrap. B, A pinto bean is taped in place directly over the wart. C, The selfadherent wrap is applied to augment the pressure of the secured bean.

FIGURE 2. A–C, The digital wart before treatment, 2 days after a single overnight pressure wrap application showing necrosis of the wart, and 6 days posttreatment showing evidence of sloughing.

What to Use and How to Prepare—Any small, hard, convex object can be used for the pressure wrap; we also have used appropriately sized and shaped plastic shirt buttons with similar results. Home kits can be assembled in advance and provided to patients at their initial visit along with appropriate instructions (Figure 1A).

Effects on the Skin and Distal Digit—Application of pressure wraps does not harm normal skin; however, care should be taken when the self-adherent wrap is applied so as not to induce ischemia of the distal digit. The wrap should be applied using gentle pressure with patients experiencing minimal discomfort from the overnight application.

Indications—This pressure wrap technique can be employed on most digital warts, including periungual warts, which can be difficult to treat by other means. However, in our experience this technique is not effective for nondigital warts, likely due to the inability to maintain adequate pressure with the overlying dressing. Patients at risk for compromised digital perfusion, such as those with Raynaud phenomenon or systemic sclerosis, should not be treated with pressure wraps due to possible digital ischemia.

Precautions—Patients should be advised that the pinto bean should only be used if dry and should not be ingested. The bean can be a choking hazard for small children, therefore appropriate precautions should be used. Allergic contact dermatitis to the materials used in this technique is possible, but we have never observed this. The pinto bean can be reused for future application as long as it remains dry and provides a hard convex surface.

Practice Implications

The probable mechanism of the ischemic changes to the wart tissue likely is the occlusion of tortuous blood vessels in the dermal papillae, which are intrinsic to wart tissue and absent in normal skin.1 This pressure-induced ischemic injury allows for selective destruction of the wart tissue with sparing of the normal skin. Our technique is fairly novel, although at least one report in the literature has described the use of a mechanical device to induce ischemic changes in skin tags.5

The use of pinto bean pressure wraps to induce ischemic change in digital warts provides a low-risk and nearly pain-free alternative to more expensive and invasive treatment methods. Moreover, this technique allows for a low-cost home-based therapy that can be repeated easily for other digital sites or if recurrence is noted.

References
  1. Cardoso J, Calonje E. Cutaneous manifestations of human papillomaviruses: a review. Acta Dermatovenerol Alp Pannonica Adriat. 2011;20:145-154. 
  2. Lipke M. An armamentarium of wart treatments. Clin Med Res. 2006;4:273-293. doi:10.3121/cmr.4.4.273 
  3. Muse M, Stiff K, Glines K, et al. A review of intralesional wart therapy. Dermatol Online J. 2020;26:2. doi:10.5070/D3263048027
  4. Berna R, Margolis D, Barbieri J. Annual health care utilization and costs for treatment of cutaneous and anogenital warts among a commercially insured population in the US, 2017-2019. JAMA Dermatol. 2022;158:695-697. doi:10.1001/jamadermatol.2022.0964
  5. Fredriksson C, Ilias M, Anderson C. New mechanical device for effective removal of skin tags in routine health care. Dermatol Online J. 2009;15:9. doi:10.5070/D37tj2800k
References
  1. Cardoso J, Calonje E. Cutaneous manifestations of human papillomaviruses: a review. Acta Dermatovenerol Alp Pannonica Adriat. 2011;20:145-154. 
  2. Lipke M. An armamentarium of wart treatments. Clin Med Res. 2006;4:273-293. doi:10.3121/cmr.4.4.273 
  3. Muse M, Stiff K, Glines K, et al. A review of intralesional wart therapy. Dermatol Online J. 2020;26:2. doi:10.5070/D3263048027
  4. Berna R, Margolis D, Barbieri J. Annual health care utilization and costs for treatment of cutaneous and anogenital warts among a commercially insured population in the US, 2017-2019. JAMA Dermatol. 2022;158:695-697. doi:10.1001/jamadermatol.2022.0964
  5. Fredriksson C, Ilias M, Anderson C. New mechanical device for effective removal of skin tags in routine health care. Dermatol Online J. 2009;15:9. doi:10.5070/D37tj2800k
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Alopecia Induced by Poly-L-Lactic Acid Injection

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Alopecia Induced by Poly-L-Lactic Acid Injection

Cosmetic procedures carry inherent risks of adverse events. Transient and permanent alopecia are rare complications of these procedures. Although they have not been fully elucidated, several pathologic mechanisms for hair loss following cosmetic procedures have been proposed, including extravascular compression (a phenomenon that has been well documented in bed­ridden patients) as well as intravascular occlusion leading to inflammation and necrosis, which has been associated with hyaluronic acid (HA) fillers.¹ Cases of alopecia also have been reported following mesotherapy and calcium hydroxyapatite, deoxycholic acid, and botulinum toxin injections.² We report a case of alopecia resulting from poly-L-lactic acid (PLLA) injection in a 35-year-old woman with the intent to raise awareness of this rare adverse event.

Case Report

A healthy 35-year-old woman received aesthetic PLLA injections on the face and frontal hairline performed by an outside dermatologist using the vector technique. During the procedure, the patient experienced intense itchiness at the right temporal artery vascular territory and reported a substantial headache the next day. She also presented with erythema and edema of the frontal and right parietal scalp with a well-delimited livedoid vascular area along the temporal artery territory on the right side of the head 1 day after the procedure (Figure 1). These signs were reported to the outside dermatologist who performed the procedure, but they were not assumed to be adverse events at that time.

FIGURE 1. A, The patient presented with an ischemic event delimiting vascular territory in the frontal and temporal regions on the right hemiface 1 day following injection with poly-L-lactic acid. B, A single patch of alopecia (upper) started 27 days after the cosmetic procedure, and an additional patch of alopecia (lower) was noted on day 41.

The condition persisted for 4 days followed by the development of an irregular 3×2-cm patch of alopecia on the right parietal scalp. A 3-day course of self-administered oral prednisolone 0.2 mg/kg/d was prescribed.

Twenty-seven days after the procedure, the patient presented to our trichology clinic for evaluation of a single patch of nonscarring alopecia on the right parietal scalp. Trichoscopy showed multiple yellow and black dots, broken hairs, pigment deposits, and an erythematous background mainly composed of linear telangiectatic vessels (Figure 2). Histopathologic analysis revealed a lymphocytic inflammatory infiltrate surrounding the follicular units that was compatible with an alopecia areata–like pattern as well as PLLA deposits in the subcutaneous tissue forming foreign body granulomas (Figure 3). The diagnosis of PLLA-induced alopecia was made based on the detection of PLLA at the biopsy site within the patchy alopecia.

FIGURE 2. A, Trichoscopy performed 27 days after the initial procedure showed multiple yellow and black dots and broken hairs in addition to an irregular vascular proliferation composed of ectatic vessels, erythema of the fundus, and pigment deposits. B, Partial hair regrowth was noted after 6 weeks of intralesional triamcinolone administered at the alopecic patch. Trichoscopy showed broken hairs as a possible sign of late inflammatory activity 3.5 months after poly-L-lactic acid injection.

FIGURE 3. A, Histology showed a lymphocytic inflammatory infiltrate around the follicular units with increased catagen/telogen counts and miniaturization (H&E, original magnification ×200). B, Birefringence showed poly-L-lactic acid deposits in deeper sections of the subcutaneous tissue forming foreign body granulomas, confirming the diagnosis of alopecia induced by poly-L-lactic acid injection (original magnification ×400).


Intralesional triamcinolone acetonide 5 mg/mL was administered at 1-cm intervals in the subdermal space (0.1 mL/puncture site). After 14 days, the patient developed an additional patch of alopecia in the same vascular territory as the right temporal artery, positioned just beneath the initial patch, with similar trichoscopy findings. The patches were treated with intralesional triamcinolone acetonide for 3 additional sessions, administered every 4 weeks. Long-term monitoring of the patient revealed regrowth with comparable hair count to the unaffected contralateral scalp, indicative of a nonscarring alopecia.

Comment

Poly-L-lactic acid is a biostimulator synthesized from the α-hydroxy acid family in 1954 that has been safely used in suture materials, resorbable plates, and orthopedic screws.4 Alopecia has been reported as a systemic allergic reaction to biodegradable screws following an orthopedic procedure.5 Prior reports of embolization and retinal ischemia with PLLA have raised concerns regarding its occlusive potential.6-9

Approved by the US Food and Drug Administration in 2004 for soft tissue restoration in HIV-related lipoatrophy, PLLA was expanded to cosmetic applications in 2009. As previously reported with HA fillers, we hypothesize that extravascular compression resulting from the placement of the filler material (due to the volume injected in the scalp area) contributes to the development of alopecia plus PLLA embolism–induced ischemic alopecia in the affected areas.10 In our case, the diagnosis of PLLA-induced alopecia was confirmed based on the finding of the filler material in the subcutaneous tissue on histopathology, probably due to embolization. Moreover, trichoscopic findings were all similar to those described after HA embolization.11 The features found in our patient due to the PLLA local reaction were similar to those seen in other conditions such as alopecia areata, pressure alopecia, and chemotherapy-induced alopecia; therefore, histopathology confirmation is mandatory in cases of hair loss associated with PLLA.

The emergence of a secondary patch of alopecia prompts consideration of an intrinsic late inflammatory propensity of PLLA. Immune cells recognize PLLA as a foreign body, and subclinical inflammatory foreign body reactions can cause PLLA-induced collagen synthesis.12 This phenomenon underscores the need for further investigation into the immunologic implications of PLLA in alopecia pathogenesis.

The angiogenic properties of the anagen phase require an adequate blood supply for effective hair growth; therefore, the lack of blood and nutrient supply to the hair bulb triggers miniaturization, a possible explanation for the hair thinning found in the alopecic patch.13

Conclusion

Alopecia as an adverse effect of cosmetic procedures can be distressing for patients, even when reversible. A detailed understanding of scalp anatomy is critical for satisfactory outcomes with aesthetic procedures. Physicians must pay attention to the amount and area of material injected in order to avoid possible mechanisms of ischemia—embolization and/or extravascular compression—especially in highly vascularized areas.

We present a rare report of alopecia as an adverse event of PLLA injection. Dermatologists must be aware of this rare condition, and trichoscopy combined with histopathologic analysis are encouraged for early recognition and proper management.

References
  1. Issa NT, Kaiser M, Martinez-Velasco A, et al. Alopecia after cosmetic injection procedures: a review. Dermatol Surg. 2022;48:855-861.
  2. Alopecia with foreign body granulomas induced by Radiesse injection: a case report. J Cosmet Laser Ther. 2018;20:462-464.
  3. Munia C, Parada M, de Alvarenga Morais MH. Changes in facial morphology using poly-L-lactic acid application according to vector technique: a case series. J Clin Aesthet Dermatol. 2022;15:38-42.
  4. Attenello NH, Maas CS. Injectable fillers: review of material and properties. Facial Plast Surg. 2015;31:29-34.
  5. Mastrokalos DS, Paessler HH. Allergic reaction to biodegradable interference poly-L-lactic acid screws after anterior cruciate ligament reconstruction with bone-patellar tendon-bone graft. Arthroscopy. 2008;24:732-733.
  6. Wu CW, Wu HJ. Retinal artery occlusion following cosmetic injection of poly-L-lactic acid. Taiwan J Ophthalmol. 2021;11:317-320.
  7. Yuan JT, Chang TW, Yu SS, et al. Mental artery occlusion from poly-L-lactic acid injection at the lateral chin. Dermatol Surg. 2017;43:1402-1405.
  8. Ragam A, Agemy SA, Dave SB, et al. Ipsilateral ophthalmic and cerebral infarctions after cosmetic polylactic acid injection into the forehead. J Neuroophthalmol. 2017;37:77-80.
  9. Witmanowski H, Błochowiak K. Another face of dermal fillers. Postepy Dermatol Alergol. 2020;37:651-659.
  10. Yang Q, Qiu L, Yi C, et al. Reversible alopecia with localized scalp necrosis after accidental embolization of the parietal artery with hyaluronic acid. Aesthetic Plast Surg. 2017;41:695-699.
  11. Asz-Sigall D, Iñigo-Gomez K, Ortega-Springall MF, et al. Alopecia secondary to hyaluronic acid embolization: trichoscopic findings. Skin Appendage Disord. 2019;5:396-400.
  12. Oh S, Lee JH, Kim HM, et al. Poly-L-lactic acid fillers improved dermal collagen synthesis by modulating M2 macrophage polarization in aged animal skin. Cells. 2023;12:1320. doi:10.3390/cells12091320
  13. Natarelli N, Gahoonia N, Sivamani RK. Integrative and mechanistic approach to the hair growth cycle and hair loss. J Clin Med. 2023;12:893.2. Liu RF, Kuo TT, Chao YY, et al.
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Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Bagatin, and Nascimento are from the Federal University of São Paulo, Brazil. Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Bagatin, and Nascimento are from the Department of Dermatology, and Dr. Michalany is from the Department of Dermatopathology. Drs. Cortez de Almeida and Melo are from Department of Dermatology, Rio de Janeiro State University, Brazil.

Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Cortez de Almeida, Melo, and Nascimento have no relevant financial disclosures to report. Dr. Bagatin is a speaker for L’Oréal and has received a research grant from Pierre Fabre Dermo-Cosmetique.

Correspondence: Gabriel Lazzeri Cortez, MD, Department of Dermatology, Federal University of São Paulo, Rua Botucatu, 740, Vila Clementino, São Paulo, 04023-062, Brazil (gabriel.cortez@unifesp.br).

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Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Bagatin, and Nascimento are from the Federal University of São Paulo, Brazil. Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Bagatin, and Nascimento are from the Department of Dermatology, and Dr. Michalany is from the Department of Dermatopathology. Drs. Cortez de Almeida and Melo are from Department of Dermatology, Rio de Janeiro State University, Brazil.

Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Cortez de Almeida, Melo, and Nascimento have no relevant financial disclosures to report. Dr. Bagatin is a speaker for L’Oréal and has received a research grant from Pierre Fabre Dermo-Cosmetique.

Correspondence: Gabriel Lazzeri Cortez, MD, Department of Dermatology, Federal University of São Paulo, Rua Botucatu, 740, Vila Clementino, São Paulo, 04023-062, Brazil (gabriel.cortez@unifesp.br).

Cutis. 2024 November;114(5):159-161. doi:10.12788/cutis.115

Author and Disclosure Information

Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Bagatin, and Nascimento are from the Federal University of São Paulo, Brazil. Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Bagatin, and Nascimento are from the Department of Dermatology, and Dr. Michalany is from the Department of Dermatopathology. Drs. Cortez de Almeida and Melo are from Department of Dermatology, Rio de Janeiro State University, Brazil.

Drs. Cortez, Hassun, Linhares, Pinheiro, Florenço, Michalany, Cortez de Almeida, Melo, and Nascimento have no relevant financial disclosures to report. Dr. Bagatin is a speaker for L’Oréal and has received a research grant from Pierre Fabre Dermo-Cosmetique.

Correspondence: Gabriel Lazzeri Cortez, MD, Department of Dermatology, Federal University of São Paulo, Rua Botucatu, 740, Vila Clementino, São Paulo, 04023-062, Brazil (gabriel.cortez@unifesp.br).

Cutis. 2024 November;114(5):159-161. doi:10.12788/cutis.115

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Article PDF

Cosmetic procedures carry inherent risks of adverse events. Transient and permanent alopecia are rare complications of these procedures. Although they have not been fully elucidated, several pathologic mechanisms for hair loss following cosmetic procedures have been proposed, including extravascular compression (a phenomenon that has been well documented in bed­ridden patients) as well as intravascular occlusion leading to inflammation and necrosis, which has been associated with hyaluronic acid (HA) fillers.¹ Cases of alopecia also have been reported following mesotherapy and calcium hydroxyapatite, deoxycholic acid, and botulinum toxin injections.² We report a case of alopecia resulting from poly-L-lactic acid (PLLA) injection in a 35-year-old woman with the intent to raise awareness of this rare adverse event.

Case Report

A healthy 35-year-old woman received aesthetic PLLA injections on the face and frontal hairline performed by an outside dermatologist using the vector technique. During the procedure, the patient experienced intense itchiness at the right temporal artery vascular territory and reported a substantial headache the next day. She also presented with erythema and edema of the frontal and right parietal scalp with a well-delimited livedoid vascular area along the temporal artery territory on the right side of the head 1 day after the procedure (Figure 1). These signs were reported to the outside dermatologist who performed the procedure, but they were not assumed to be adverse events at that time.

FIGURE 1. A, The patient presented with an ischemic event delimiting vascular territory in the frontal and temporal regions on the right hemiface 1 day following injection with poly-L-lactic acid. B, A single patch of alopecia (upper) started 27 days after the cosmetic procedure, and an additional patch of alopecia (lower) was noted on day 41.

The condition persisted for 4 days followed by the development of an irregular 3×2-cm patch of alopecia on the right parietal scalp. A 3-day course of self-administered oral prednisolone 0.2 mg/kg/d was prescribed.

Twenty-seven days after the procedure, the patient presented to our trichology clinic for evaluation of a single patch of nonscarring alopecia on the right parietal scalp. Trichoscopy showed multiple yellow and black dots, broken hairs, pigment deposits, and an erythematous background mainly composed of linear telangiectatic vessels (Figure 2). Histopathologic analysis revealed a lymphocytic inflammatory infiltrate surrounding the follicular units that was compatible with an alopecia areata–like pattern as well as PLLA deposits in the subcutaneous tissue forming foreign body granulomas (Figure 3). The diagnosis of PLLA-induced alopecia was made based on the detection of PLLA at the biopsy site within the patchy alopecia.

FIGURE 2. A, Trichoscopy performed 27 days after the initial procedure showed multiple yellow and black dots and broken hairs in addition to an irregular vascular proliferation composed of ectatic vessels, erythema of the fundus, and pigment deposits. B, Partial hair regrowth was noted after 6 weeks of intralesional triamcinolone administered at the alopecic patch. Trichoscopy showed broken hairs as a possible sign of late inflammatory activity 3.5 months after poly-L-lactic acid injection.

FIGURE 3. A, Histology showed a lymphocytic inflammatory infiltrate around the follicular units with increased catagen/telogen counts and miniaturization (H&E, original magnification ×200). B, Birefringence showed poly-L-lactic acid deposits in deeper sections of the subcutaneous tissue forming foreign body granulomas, confirming the diagnosis of alopecia induced by poly-L-lactic acid injection (original magnification ×400).


Intralesional triamcinolone acetonide 5 mg/mL was administered at 1-cm intervals in the subdermal space (0.1 mL/puncture site). After 14 days, the patient developed an additional patch of alopecia in the same vascular territory as the right temporal artery, positioned just beneath the initial patch, with similar trichoscopy findings. The patches were treated with intralesional triamcinolone acetonide for 3 additional sessions, administered every 4 weeks. Long-term monitoring of the patient revealed regrowth with comparable hair count to the unaffected contralateral scalp, indicative of a nonscarring alopecia.

Comment

Poly-L-lactic acid is a biostimulator synthesized from the α-hydroxy acid family in 1954 that has been safely used in suture materials, resorbable plates, and orthopedic screws.4 Alopecia has been reported as a systemic allergic reaction to biodegradable screws following an orthopedic procedure.5 Prior reports of embolization and retinal ischemia with PLLA have raised concerns regarding its occlusive potential.6-9

Approved by the US Food and Drug Administration in 2004 for soft tissue restoration in HIV-related lipoatrophy, PLLA was expanded to cosmetic applications in 2009. As previously reported with HA fillers, we hypothesize that extravascular compression resulting from the placement of the filler material (due to the volume injected in the scalp area) contributes to the development of alopecia plus PLLA embolism–induced ischemic alopecia in the affected areas.10 In our case, the diagnosis of PLLA-induced alopecia was confirmed based on the finding of the filler material in the subcutaneous tissue on histopathology, probably due to embolization. Moreover, trichoscopic findings were all similar to those described after HA embolization.11 The features found in our patient due to the PLLA local reaction were similar to those seen in other conditions such as alopecia areata, pressure alopecia, and chemotherapy-induced alopecia; therefore, histopathology confirmation is mandatory in cases of hair loss associated with PLLA.

The emergence of a secondary patch of alopecia prompts consideration of an intrinsic late inflammatory propensity of PLLA. Immune cells recognize PLLA as a foreign body, and subclinical inflammatory foreign body reactions can cause PLLA-induced collagen synthesis.12 This phenomenon underscores the need for further investigation into the immunologic implications of PLLA in alopecia pathogenesis.

The angiogenic properties of the anagen phase require an adequate blood supply for effective hair growth; therefore, the lack of blood and nutrient supply to the hair bulb triggers miniaturization, a possible explanation for the hair thinning found in the alopecic patch.13

Conclusion

Alopecia as an adverse effect of cosmetic procedures can be distressing for patients, even when reversible. A detailed understanding of scalp anatomy is critical for satisfactory outcomes with aesthetic procedures. Physicians must pay attention to the amount and area of material injected in order to avoid possible mechanisms of ischemia—embolization and/or extravascular compression—especially in highly vascularized areas.

We present a rare report of alopecia as an adverse event of PLLA injection. Dermatologists must be aware of this rare condition, and trichoscopy combined with histopathologic analysis are encouraged for early recognition and proper management.

Cosmetic procedures carry inherent risks of adverse events. Transient and permanent alopecia are rare complications of these procedures. Although they have not been fully elucidated, several pathologic mechanisms for hair loss following cosmetic procedures have been proposed, including extravascular compression (a phenomenon that has been well documented in bed­ridden patients) as well as intravascular occlusion leading to inflammation and necrosis, which has been associated with hyaluronic acid (HA) fillers.¹ Cases of alopecia also have been reported following mesotherapy and calcium hydroxyapatite, deoxycholic acid, and botulinum toxin injections.² We report a case of alopecia resulting from poly-L-lactic acid (PLLA) injection in a 35-year-old woman with the intent to raise awareness of this rare adverse event.

Case Report

A healthy 35-year-old woman received aesthetic PLLA injections on the face and frontal hairline performed by an outside dermatologist using the vector technique. During the procedure, the patient experienced intense itchiness at the right temporal artery vascular territory and reported a substantial headache the next day. She also presented with erythema and edema of the frontal and right parietal scalp with a well-delimited livedoid vascular area along the temporal artery territory on the right side of the head 1 day after the procedure (Figure 1). These signs were reported to the outside dermatologist who performed the procedure, but they were not assumed to be adverse events at that time.

FIGURE 1. A, The patient presented with an ischemic event delimiting vascular territory in the frontal and temporal regions on the right hemiface 1 day following injection with poly-L-lactic acid. B, A single patch of alopecia (upper) started 27 days after the cosmetic procedure, and an additional patch of alopecia (lower) was noted on day 41.

The condition persisted for 4 days followed by the development of an irregular 3×2-cm patch of alopecia on the right parietal scalp. A 3-day course of self-administered oral prednisolone 0.2 mg/kg/d was prescribed.

Twenty-seven days after the procedure, the patient presented to our trichology clinic for evaluation of a single patch of nonscarring alopecia on the right parietal scalp. Trichoscopy showed multiple yellow and black dots, broken hairs, pigment deposits, and an erythematous background mainly composed of linear telangiectatic vessels (Figure 2). Histopathologic analysis revealed a lymphocytic inflammatory infiltrate surrounding the follicular units that was compatible with an alopecia areata–like pattern as well as PLLA deposits in the subcutaneous tissue forming foreign body granulomas (Figure 3). The diagnosis of PLLA-induced alopecia was made based on the detection of PLLA at the biopsy site within the patchy alopecia.

FIGURE 2. A, Trichoscopy performed 27 days after the initial procedure showed multiple yellow and black dots and broken hairs in addition to an irregular vascular proliferation composed of ectatic vessels, erythema of the fundus, and pigment deposits. B, Partial hair regrowth was noted after 6 weeks of intralesional triamcinolone administered at the alopecic patch. Trichoscopy showed broken hairs as a possible sign of late inflammatory activity 3.5 months after poly-L-lactic acid injection.

FIGURE 3. A, Histology showed a lymphocytic inflammatory infiltrate around the follicular units with increased catagen/telogen counts and miniaturization (H&E, original magnification ×200). B, Birefringence showed poly-L-lactic acid deposits in deeper sections of the subcutaneous tissue forming foreign body granulomas, confirming the diagnosis of alopecia induced by poly-L-lactic acid injection (original magnification ×400).


Intralesional triamcinolone acetonide 5 mg/mL was administered at 1-cm intervals in the subdermal space (0.1 mL/puncture site). After 14 days, the patient developed an additional patch of alopecia in the same vascular territory as the right temporal artery, positioned just beneath the initial patch, with similar trichoscopy findings. The patches were treated with intralesional triamcinolone acetonide for 3 additional sessions, administered every 4 weeks. Long-term monitoring of the patient revealed regrowth with comparable hair count to the unaffected contralateral scalp, indicative of a nonscarring alopecia.

Comment

Poly-L-lactic acid is a biostimulator synthesized from the α-hydroxy acid family in 1954 that has been safely used in suture materials, resorbable plates, and orthopedic screws.4 Alopecia has been reported as a systemic allergic reaction to biodegradable screws following an orthopedic procedure.5 Prior reports of embolization and retinal ischemia with PLLA have raised concerns regarding its occlusive potential.6-9

Approved by the US Food and Drug Administration in 2004 for soft tissue restoration in HIV-related lipoatrophy, PLLA was expanded to cosmetic applications in 2009. As previously reported with HA fillers, we hypothesize that extravascular compression resulting from the placement of the filler material (due to the volume injected in the scalp area) contributes to the development of alopecia plus PLLA embolism–induced ischemic alopecia in the affected areas.10 In our case, the diagnosis of PLLA-induced alopecia was confirmed based on the finding of the filler material in the subcutaneous tissue on histopathology, probably due to embolization. Moreover, trichoscopic findings were all similar to those described after HA embolization.11 The features found in our patient due to the PLLA local reaction were similar to those seen in other conditions such as alopecia areata, pressure alopecia, and chemotherapy-induced alopecia; therefore, histopathology confirmation is mandatory in cases of hair loss associated with PLLA.

The emergence of a secondary patch of alopecia prompts consideration of an intrinsic late inflammatory propensity of PLLA. Immune cells recognize PLLA as a foreign body, and subclinical inflammatory foreign body reactions can cause PLLA-induced collagen synthesis.12 This phenomenon underscores the need for further investigation into the immunologic implications of PLLA in alopecia pathogenesis.

The angiogenic properties of the anagen phase require an adequate blood supply for effective hair growth; therefore, the lack of blood and nutrient supply to the hair bulb triggers miniaturization, a possible explanation for the hair thinning found in the alopecic patch.13

Conclusion

Alopecia as an adverse effect of cosmetic procedures can be distressing for patients, even when reversible. A detailed understanding of scalp anatomy is critical for satisfactory outcomes with aesthetic procedures. Physicians must pay attention to the amount and area of material injected in order to avoid possible mechanisms of ischemia—embolization and/or extravascular compression—especially in highly vascularized areas.

We present a rare report of alopecia as an adverse event of PLLA injection. Dermatologists must be aware of this rare condition, and trichoscopy combined with histopathologic analysis are encouraged for early recognition and proper management.

References
  1. Issa NT, Kaiser M, Martinez-Velasco A, et al. Alopecia after cosmetic injection procedures: a review. Dermatol Surg. 2022;48:855-861.
  2. Alopecia with foreign body granulomas induced by Radiesse injection: a case report. J Cosmet Laser Ther. 2018;20:462-464.
  3. Munia C, Parada M, de Alvarenga Morais MH. Changes in facial morphology using poly-L-lactic acid application according to vector technique: a case series. J Clin Aesthet Dermatol. 2022;15:38-42.
  4. Attenello NH, Maas CS. Injectable fillers: review of material and properties. Facial Plast Surg. 2015;31:29-34.
  5. Mastrokalos DS, Paessler HH. Allergic reaction to biodegradable interference poly-L-lactic acid screws after anterior cruciate ligament reconstruction with bone-patellar tendon-bone graft. Arthroscopy. 2008;24:732-733.
  6. Wu CW, Wu HJ. Retinal artery occlusion following cosmetic injection of poly-L-lactic acid. Taiwan J Ophthalmol. 2021;11:317-320.
  7. Yuan JT, Chang TW, Yu SS, et al. Mental artery occlusion from poly-L-lactic acid injection at the lateral chin. Dermatol Surg. 2017;43:1402-1405.
  8. Ragam A, Agemy SA, Dave SB, et al. Ipsilateral ophthalmic and cerebral infarctions after cosmetic polylactic acid injection into the forehead. J Neuroophthalmol. 2017;37:77-80.
  9. Witmanowski H, Błochowiak K. Another face of dermal fillers. Postepy Dermatol Alergol. 2020;37:651-659.
  10. Yang Q, Qiu L, Yi C, et al. Reversible alopecia with localized scalp necrosis after accidental embolization of the parietal artery with hyaluronic acid. Aesthetic Plast Surg. 2017;41:695-699.
  11. Asz-Sigall D, Iñigo-Gomez K, Ortega-Springall MF, et al. Alopecia secondary to hyaluronic acid embolization: trichoscopic findings. Skin Appendage Disord. 2019;5:396-400.
  12. Oh S, Lee JH, Kim HM, et al. Poly-L-lactic acid fillers improved dermal collagen synthesis by modulating M2 macrophage polarization in aged animal skin. Cells. 2023;12:1320. doi:10.3390/cells12091320
  13. Natarelli N, Gahoonia N, Sivamani RK. Integrative and mechanistic approach to the hair growth cycle and hair loss. J Clin Med. 2023;12:893.2. Liu RF, Kuo TT, Chao YY, et al.
References
  1. Issa NT, Kaiser M, Martinez-Velasco A, et al. Alopecia after cosmetic injection procedures: a review. Dermatol Surg. 2022;48:855-861.
  2. Alopecia with foreign body granulomas induced by Radiesse injection: a case report. J Cosmet Laser Ther. 2018;20:462-464.
  3. Munia C, Parada M, de Alvarenga Morais MH. Changes in facial morphology using poly-L-lactic acid application according to vector technique: a case series. J Clin Aesthet Dermatol. 2022;15:38-42.
  4. Attenello NH, Maas CS. Injectable fillers: review of material and properties. Facial Plast Surg. 2015;31:29-34.
  5. Mastrokalos DS, Paessler HH. Allergic reaction to biodegradable interference poly-L-lactic acid screws after anterior cruciate ligament reconstruction with bone-patellar tendon-bone graft. Arthroscopy. 2008;24:732-733.
  6. Wu CW, Wu HJ. Retinal artery occlusion following cosmetic injection of poly-L-lactic acid. Taiwan J Ophthalmol. 2021;11:317-320.
  7. Yuan JT, Chang TW, Yu SS, et al. Mental artery occlusion from poly-L-lactic acid injection at the lateral chin. Dermatol Surg. 2017;43:1402-1405.
  8. Ragam A, Agemy SA, Dave SB, et al. Ipsilateral ophthalmic and cerebral infarctions after cosmetic polylactic acid injection into the forehead. J Neuroophthalmol. 2017;37:77-80.
  9. Witmanowski H, Błochowiak K. Another face of dermal fillers. Postepy Dermatol Alergol. 2020;37:651-659.
  10. Yang Q, Qiu L, Yi C, et al. Reversible alopecia with localized scalp necrosis after accidental embolization of the parietal artery with hyaluronic acid. Aesthetic Plast Surg. 2017;41:695-699.
  11. Asz-Sigall D, Iñigo-Gomez K, Ortega-Springall MF, et al. Alopecia secondary to hyaluronic acid embolization: trichoscopic findings. Skin Appendage Disord. 2019;5:396-400.
  12. Oh S, Lee JH, Kim HM, et al. Poly-L-lactic acid fillers improved dermal collagen synthesis by modulating M2 macrophage polarization in aged animal skin. Cells. 2023;12:1320. doi:10.3390/cells12091320
  13. Natarelli N, Gahoonia N, Sivamani RK. Integrative and mechanistic approach to the hair growth cycle and hair loss. J Clin Med. 2023;12:893.2. Liu RF, Kuo TT, Chao YY, et al.
Issue
Cutis - 114(5)
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Cutis - 114(5)
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159-161
Page Number
159-161
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Alopecia Induced by Poly-L-Lactic Acid Injection
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Alopecia Induced by Poly-L-Lactic Acid Injection
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  • Alopecia is a potential adverse event of ­poly-L-lactic acid (PLLA) injection, and prior reports of embolization and retinal ischemia with PLLA use raise the concern of its occlusive potential.
  • The combination of extravascular compression due to the presence of the filler material in the subcutaneous tissue as well as intravascular PLLA embolism may contribute to tissue ischemia–induced alopecia in the affected areas.
  • Poly-L-lactic acid also may cause a local inflammatory reaction that is alopecia areata–like, which would explain its similar trichoscopy findings.
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