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The Effect of Arthroscopic Rotator Interval Closure on Glenohumeral Volume
Since Neer described the rotator interval in 1970, its closure, often used in conjunction with capsulorrhaphy, has become an important surgical technique in managing shoulder instability.1-11 Numerous studies have sought to define the function of the rotator interval.1-3,6-20 The etiology of lesions of the rotator interval has been debated, and there is evidence that such lesions may be in part congenital.21 Increased rotator interval depth and width, along with increased size of the distended inferior and posteroinferior joint capsule on magnetic resonance arthrography, have been reported in cases of multidirectional shoulder instability.22 However, confusion remains about the role of the rotator interval in shoulder instability and about the effect its closure has on shoulder function. No one knows the degree of volume reduction that results from closure of the rotator interval and whether medial and lateral sutures differ in the volume reduction achieved.
Cadaveric studies have shown that the rotator interval has an important role in shoulder motion.6,13-16,19,20,23 Harryman and colleagues13 found that sectioning the coracohumeral ligament (CHL) increased shoulder range of motion (ROM), and medial-to-lateral closure of the rotator interval restricted motion in all planes. Most notably, interval closure limited inferior translation in the adducted shoulder, posterior translation in the flexed adducted shoulder, and external rotation in the neutral position. Subsequent studies,17,18 using rotator interval closure combined with thermal capsulorrhaphy, confirmed the results reported by Harryman and colleagues.13
More recent cadaveric studies using superior-to-inferior rotator interval closures have shown a decrease in anterior translation but not posterior translation.14-16,19-21 A superior-to-inferior interval closure technique limited external rotation less than a medial-to-lateral closure did.13-16,19-21 The majority of arthroscopically described rotator interval closures involve a superior-to-inferior technique and use 2 or 3 sutures.1,3,9-11
Plausinis and colleagues15 examined the effects of an isolated medial, an isolated lateral, and a medial combined with a lateral closure of the rotator interval. They noted that all 3 methods limited anterior translation and motion by means of 6° flexion and 10° external rotation; however, there was no statistical difference between methods. They also found that occasionally the medial interval closure resulted in massive loss of external rotation. Earlier, Jost and colleagues14 noted that a medial rotator interval could cause this massive loss by tethering the CHL, resulting in a medial-to-lateral imbrication of the CHL.
Arthroscopic rotator interval closure has clinically demonstrated an additive effect on shoulder stability. The recurrence rate was lower for arthroscopic Bankart repair combined with arthroscopic rotator interval closure (8%) than for arthroscopic Bankart repair alone (13%).24 In addition, time to recurrent dislocation was longer (42 vs 13 months) for the group that underwent the combination of Bankart repair and rotator interval closure. Regarding the concern about loss of motion after arthroscopic rotator interval closure, Chiang and colleagues25 recently noted no significant loss of motion 5 years after arthroscopic Bankart repair with rotator interval closure.
What effect rotator interval closure has on intra-articular glenohumeral volume (GHV) remains unknown. Using a cadaveric model, Yamamoto and colleagues20 showed that decreasing GHV can increase the responsiveness of the glenohumeral joint to the intra-articular pressure. Thus, reducing the volume can improve stability in vitro by increasing the magnitude of negative pressure stabilizing the glenohumeral joint.
We conducted a study to quantify the effects of arthroscopic rotator interval closure on capsular volume and to determine whether medial and lateral interval closures resulted in different degrees of volume reduction. Our hypothesis was that shoulder volume would be significantly reduced by closing the rotator interval.
Materials and Methods
Previous studies have not specifically evaluated GHV after rotator interval closure. Our power analysis was performed with data from a study by Karas and colleagues,26 who evaluated GHV after capsular plication. To detect a capsular volume reduction of 20% per stitch, with a 2-sided 5% significance level and a power of 80%, we needed a sample size of 5 specimens per group.
After receiving institutional review board approval for this study, we obtained 10 cadaveric shoulders (5 matched pairs). Exclusion criteria included arthroscopic evaluation revealing a full-thickness rotator cuff tear or significant osteoarthritis. Two shoulders had full-thickness cuff tears, leaving 8 shoulders to be tested; 6 of these were matched pairs. The shoulders were from 1 man (matched pair) and 4 women (2 matched pairs). Age ranged from 38 to 70 years (mean, 59.6 years). Differences in material properties between the specimens were accounted for by using primarily matched pairs.
The 2 study groups consisted of 4 shoulders each. After specimens were thawed, the skin, subcutaneous tissues, and periscapular muscles were removed from the shoulder. Only the capsule, biceps, and rotator cuff remained. For measurement purposes, the shoulders were mounted in a vice clamp in a beach-chair orientation. We placed a total of 2 portals with fully threaded 8.25-mm cannulas (Arthrex, Naples, Florida). A standard posterior portal was placed in the soft spot. A low anterior portal was then placed just superior to the subscapularis tendon. For arthroscopic examination and instrumentation in a saline environment, the shoulders were rotated into the lateral decubitus position, with suspension in 30° abduction and 20° forward flexion, by a rope attached to a pin in the distal shaft of the humerus.
In both groups, medial and lateral stitches with No. 2 FiberWire (Arthrex) were used to close the interval. The medial interval closure stitch was placed more than 10 mm away from the glenoid to prevent unpredictable CHL tethering; the lateral closure stitch was placed 10 mm lateral to the medial stitch (Figure 1).14 All sutures were placed intra-articularly under direct arthroscopic visualization, similar to the methods described in the literature.1,3,9-11 Sutures were passed through the superior glenohumeral ligament (SGHL) and through the upper subscapularis using a suture shuttle (SutureLasso; Arthrex) and Penetrator II Suture Retriever (Arthrex). The upper subscapularis was incorporated because of the unpredictable nature of the middle glenohumeral ligament (MGHL). Both rotator interval sutures were placed before tying either. In the medial group, the medial stitch was tied first, using alternating half-hitches, followed by the lateral stitch. In the lateral group, the lateral stitch was tied first, followed by the medial stitch. GHV was measured at baseline and after tying each stitch. Dr. Ponce instrumented all shoulders.
Modifying a beach-chair technique described by Miller and colleagues,27 we used a viscous fatty-acid sulfate solution, liquid soap, to measure GHV.27-29 A small slit in line with the fibers was made in the supraspinatus tendon just lateral to the musculotendinous junction. A 3-way stop-cock was placed into the joint though this defect. A 20-mL syringe with a 16-gauge needle was used to inject the soap. The needle was inserted into the rotator cuff interval, and the viscous solution was injected in 5-mL increments until there was active extravasation through the supraspinatus cannula (Figure 2). This technique, the “volcano method,” marked the maximum capacity of the joint. The joint was then copiously irrigated with normal saline and suctioned until all normal saline was evacuated. Dr. Rosenzweig took 2 measurements on each shoulder, and their mean was used for analysis.
The baseline measurement was taken with the 2 working cannulas in the shoulder joint. Measurements were obtained with cannulas to simulate normal clinical conditions. Subsequent measurements were done with the cannulas in place and inserted up to the same thread each time so as not to change the volume. The capsule and the rotator cuff were then dissected from the humerus so the size of the capsulolabral plication could be directly evaluated. Methylene blue was used to mark the capsular suture holes before removing the sutures. With use of a caliper, the size of the plication bite was measured (in millimeters).
Statistical Analysis
The primary outcome was percent reduction in GHV as a function of number of plications and size of plication. When only the first plication was tightened, the effect of position (medial or lateral) was also of interest. Percent volume reduction was calculated as (original – new) / original × 100. SAS 8.02 (SAS Institute, Cary, North Carolina) was used to fit a repeated random-intercept regression model for each outcome. This technique properly accounts for the paired nature of the specimens and the repeated measures (baseline plus 2 plications). Model fit was assessed by the method of difference in log likelihood.
Results
In the medial group, GHV was reduced by a mean of 24.2% with a single medial stitch; in the lateral group, GHV was reduced by a mean of 35.1% (Figure 3). The difference was significant (P < .02). In the medial group, when a second lateral stitch was used, GHV was reduced by another 18.7%; in the lateral group, when a medial stitch was added, GHV was reduced by another 11.4%. Final GHV for the medial and lateral groups was 42.9% and 46.5%, respectively. There was no statistical difference in final GHV, regardless of which stitch was placed first. When the 2 groups were combined, GHV was reduced by 44.9% with use of medial and lateral rotator interval closure stitches.
Mean amount of tissue purchased, or “bite size,” was 18 mm with a lateral suture and 15 mm with a medial suture (P < .05). In addition, an increase in bite size to GHV reduction was essentially linear, where an increase in bite size of 1 mm reduced GHV by about 1% (Figure 4).
Discussion
Although there have been numerous clinical series and biomechanical studies focused on isolated rotator interval closure (or its use as an adjunct) in shoulder stabilization, the precise function of the rotator interval remains poorly understood.1-3,6-11,19 Consequently, the in vivo effects of interval closure are unknown.
Initial studies proposed that rotator interval closure limited inferior and posterior translation.30 More recent studies have demonstrated that rotator interval closure confers little effect on posterior instability but increases anterior stability in cadaveric models.15,16 Clinical series have provided evidence that rotator interval closure can increase anterior stability.1,3,7,9,12 In a series of isolated rotator interval closures for multidirectional instability, Field and colleagues12 found that preoperative anterior and inferior symptoms predominated over posterior symptoms. Isolated closure of the rotator interval resulted in 100% excellent results with no cases of recurrent instability. Moon and colleagues31 reported that arthroscopic rotator interval closure with or without inferior capsular plication in multidirectional instability and predominant symptomatic inferior instability has shown benefit by improving function and stability. Other clinical reports of rotator interval closure in conjunction with arthroscopic Bankart repair have suggested it has an additive effect on anterior shoulder stability without limiting motion.24,25
In our study, arthroscopic closure of the rotator interval with 2 superior-to-inferior stitches reduced intracapsular volume by 45%. Even though open capsular shifts use different surgical techniques, similar technique volume reduction studies have reported reductions between 34% and 54% with open shifts.27,30 It is unknown if the stability resulting from decreased GHV is primarily from increasing intra-articular pressures or from restricting ROM, or from a combination of both. In shoulders with multidirectional instability, the joint volume may be increased, the joint capsule may be enlarged, or the glenohumeral ligaments may be lax and thin.4,6,32,33 Yamamoto and colleagues19 stated that intra-articular pressure is determined by 3 factors: load, joint volume, and material properties of the capsule. Load is a constant; joint volume and material properties can be changed.19 In our study, material properties were controlled by using a majority of matched specimens. Regardless of the stabilizing mechanism, our study results demonstrated that arthroscopic rotator interval closure may be a powerful tool in reducing shoulder volume, a consistent principle of surgical techniques used in reestablishing shoulder stability.19,20
When a single rotator interval closure stitch was used, volume reduction with a lateral stitch was superior to that with a medial stitch. This finding is logical, as anatomically the dimensions of the rotator interval are larger laterally as the CHL fans out to insert on the greater and lesser tuberosities.14 This finding has also been reported in open capsular shifts for multidirectional instability, with a lateral humeral shift having a larger volume reduction than a medial glenoid shift.27 Miller and colleagues27 used the image of a cone, with its larger opening facing the humerus and narrower side facing the glenoid, to illustrate this difference in open capsular shifts.
Our study also showed a larger volume reduction with 2 rotator interval closure stitches than with a single interval stitch. As ROM testing has not shown a difference between results with 1 and 2 sutures, we recommend a minimum of 2 sutures for arthroscopic rotator interval closure.15 If a single plication stitch is preferred, a lateral stitch (vs a medial stitch) can be used for a significantly larger reduction in shoulder volume. We think this is because of a larger amount of capsule being purchased with lateral closure (Figure 5). However, if a medial stitch is used, it is important to not place it too near the glenoid to avoid CHL tethering and subsequent excessive loss of external rotation.15
This study had several weaknesses. First, it was a cadaveric study, and use of specimens not known to have instability or specific rotator interval injury may make generalization to a clinical situation difficult. Second, although our power analysis called for 5 shoulders in each group, full-thickness rotator cuff tears rendered 2 shoulders unusable. This reduced our sample sizes and potentially decreased the power of the study, though the data demonstrated statistically significant differences. Third, we did not compare the effects of an open medial-to-lateral imbrication of the rotator interval on intracapsular volume with the effects of our arthroscopic method. We also did not assess our specimens’ ROM, effects of interval closure stitches on shoulder stability, or glenohumeral contact surface pressures, as these factors have already been studied.13-19 Instead, we focused on the effects of rotator interval closure on intracapsular volume, which had not been quantified until now. The clinical significance of such a volume reduction is unknown, especially with respect to influence on ROM, but the degree of volume reduction was larger than with previously reported arthroscopic instability repairs and smaller than with open capsular shifts, demonstrating that it may be a powerful tool in restoring stability in an unstable shoulder.26-30,34 Fourth, the role of isolated rotator interval closure is poorly defined, as only 1 clinical series of isolated rotator interval closure has been reported thus far.12 It has been far more common for rotator interval closure to be used with Bankart repair or capsulorrhaphy.1-3,7-9
In a cadaveric study by Provencher and colleagues,16 open rotator interval closure with medial-to-lateral imbrication of the interval altered shoulder kinematics differently from what occurred with arthroscopic closure of the MGHL to the SGHL, resulting in superior-to-inferior shift. Comparing the 2 methods may therefore be inappropriate. Currently we reserve rotator interval closure for infrequent cases of revision instability and cases in which glenoid bone loss is marginal (5%-15%) and there is a willingness to potentially sacrifice ROM to restore stability and avoid an open stabilization procedure. Continued investigation into the clinical role of rotator interval closure in shoulder stability is needed. We should identify the pathology in a patient with instability and use this technique as an adjuvant to other stabilization procedures.
Conclusion
Arthroscopic rotator interval closure with 2 plication stitches is a powerful tool in reducing the intracapsular volume of the shoulder. If a single plication stitch is preferred, a lateral rotator interval closure stitch (vs a medial stitch) can be used for a larger reduction in shoulder volume.
1. Creighton RA, Romeo AA, Brown FM, Hayden JK, Verma NN. Revision arthroscopic shoulder instability repair. Arthroscopy. 2007;23(7):703-709.
2. Gartsman GM, Roddey TS, Hammerman SM. Arthroscopic treatment of anterior-inferior glenohumeral instability. Two to five-year follow-up. J Bone Joint Surg Am. 2000;82(7):991-1003.
3. Gartsman GM, Taverna E, Hammerman SM. Arthroscopic rotator interval repair in glenohumeral instability: description of an operative technique. Arthroscopy. 1999;15(3):330-332.
4. Neer CS 2nd, Foster CR. Inferior capsular shift for involuntary inferior and multidirectional instability of the shoulder: a preliminary report. J Bone Joint Surg Am. 1980;62(6):897-908.
5. Neer CS 2nd. Displaced proximal humerus fractures: I. Classification and evaluation. J Bone Joint Surg Am. 1970;52(6):1077-1089.
6. Nobuhara K, Ikeda H. Rotator interval lesion. Clin Orthop. 1987;(223):44-50.
7. Rowe CR, Zarins B, Ciullo JV. Recurrent anterior dislocation of the shoulder after surgical repair. J Bone Joint Surg Am. 1984;66(2):159-168.
8. Rowe CR, Zarins B. Recurrent transient subluxation of the shoulder. J Bone Joint Surg Am. 1981;63(6):863-872.
9. Stokes DA, Savoie FH, Field LD. Arthroscopic repair of anterior glenohumeral instability and rotator interval lesions. Orthop Clin North Am. 2003;34(4):529-539.
10. Taverna E, Sansone V, Battistella F. Arthroscopic rotator interval repair: the three-step all-inside technique. Arthroscopy. 2004;20 Suppl 2:105-109.
11. Treacy SH, Field LD, Savoie FH. Rotator interval capsule closure: an arthroscopic technique. Arthroscopy. 1997;13(1):103-106.
12. Field LD, Warren RF, O’Brien SJ, Altcheck DW, Wickiewicz TL. Isolated closure of rotator interval defects for shoulder instability. Am J Sports Med. 1995;23(5):557-563.
13. Harryman DT 2nd, Sidles JA, Harris SL, Matsen FA 3rd. The role of the rotator interval capsule in passive motion and stability of the shoulder. J Bone Joint Surg Am. 1992;74(1):53-66.
14. Jost B, Koch PP, Gerber C. Anatomy and functional aspects of the rotator interval. J Shoulder Elbow Surg. 2000;9(4):336-341.
15. Plausinis D, Bravman JT, Heywood C, Kummer FJ, Kwon YM, Jazrawi LM. Arthroscopic rotator interval closure: effect of sutures on glenohumeral motion and anterior-posterior translation. Am J Sports Med. 2006;34(10):1656-1661.
16. Provencher MT, Mologne TS, Hongo M, Zhao K, Tasto JP, An KN. Arthroscopic versus open rotator interval closure: biomechanical evaluation of stability and motion. Arthroscopy. 2007;23(6):583-592.
17. Selecky MT, Tibone JE, Yang BY, et al. Glenohumeral joint translation after thermal capsuloplasty of the rotator interval. J Shoulder Elbow Surg. 2003;12(2):139-143.
18. Wolf R, Zheng N, Iero J, Weichel D. The effects of thermal capsulorrhaphy and rotator interval closure on multidirectional laxity in the glenohumeral joint: a cadaveric biomechanical study. Arthroscopy. 2004;20(10):1044-1049.
19. Yamamoto N, Itoi E, Tuoheti Y, et al. Effect of rotator interval closure on glenohumeral stability and motion: a cadaveric study. J Shoulder Elbow Surg. 2006;15(6):750-758.
20. Yamamoto N, Itoi E, Tuoheti Y, et al. The effect of the inferior capsular shift on shoulder intra-articular pressure: a cadaveric study. Am J Sports Med. 2006;34(6):939-944.
21. Cole BJ, Rodeo SA, O’Brien SJ, et al. The anatomy and histology of the rotator interval capsule of the shoulder. Clin Orthop. 2001;(390):129-137.
22. Lee HJ, Kim NR, Moon SG, Ko SM, Park JY. Multidirectional instability of the shoulder: rotator interval dimension and capsular laxity evaluation using MR arthrography. Skeletal Radiol. 2013;42(2):231-238.
23. Warner JP, Deng X, Warren RF, Torzilli PA, O’Brien SJ. Superoinferior translation in intact and vented glenohumeral joint. J Shoulder Elbow Surg. 1993;2(2):99-105.
24. Chechik O, Maman E, Dolkart O, Khashan M, Shabtai L, Mozes G. Arthroscopic rotator interval closure in shoulder instability repair: a retrospective study. J Shoulder Elbow Surg. 2010;19(7):1056-1062.
25. Chiang, E, Wang J, Wang S, et al. Arthroscopic posteroinferior capsular plication and rotator interval closure after Bankart repair in patients with traumatic anterior glenohumeral instability—a minimum follow-up of 5 years. Injury. 2010;41(10):1075-1078.
26. Karas SG, Creighton RA, DeMorat GJ. Glenohumeral volume reduction in arthroscopic shoulder reconstruction: a cadaveric analysis of suture plication and thermal capsulorrhaphy. Arthroscopy. 2004;20(2):179-184.
27. Miller MD, Larsen KM, Luke T, Leis HT, Plancher KD. Anterior capsular shift volume reduction: an in vitro comparison of 3 techniques. J Shoulder Elbow Surg. 2003;12(4):350-354.
28. Luke TA, Rovner AD, Karas SG, Hawkins RJ, Plancher KD. Volumetric change in the shoulder capsule after open inferior capsular shift versus arthroscopic thermal capsular shrinkage: a cadaveric model. J Shoulder Elbow Surg. 2004;13(2):146-149.
29. Ponce BA, Rosenzweig SD, Thompson KJ, Tokish J. Sequential volume reduction with capsular plications: relationship between cumulative size of plications and volumetric reduction for multidirectional instability of the shoulder. Am J Sports Med. 2011;39(3):526-531.
30. Lubowitz J, Bartolozzi A, Rubenstein D, et al. How much does inferior capsular shift reduce shoulder volume? Clin Orthop. 1996;(328):86-90.
31. Moon YL, Singh H, Yang H, Chul LK. Arthroscopic rotator interval closure by purse string suture for symptomatic inferior shoulder instability. Orthopedics. 2011;34(4).
32. Jerosch J, Castro WH. Shoulder instability in Ehlers-Danlos syndrome: an indication for surgical treatment? Acta Orthop Belg. 1990;56(2):451-453.
33. Schenk TJ, Brems JJ. Multidirectional instability of the shoulder: pathophysiology, diagnosis, and management. J Am Acad Orthop Surg. 1998;6(1):65-72.
34. Cohen SB, Wiley W, Goradia VK, Pearson S, Miller MD. Anterior capsulorrhaphy: an in vitro comparison of volume reduction. Arthroscopic plication versus open capsular shift. Arthroscopy. 2005;21(6):659-664.
Since Neer described the rotator interval in 1970, its closure, often used in conjunction with capsulorrhaphy, has become an important surgical technique in managing shoulder instability.1-11 Numerous studies have sought to define the function of the rotator interval.1-3,6-20 The etiology of lesions of the rotator interval has been debated, and there is evidence that such lesions may be in part congenital.21 Increased rotator interval depth and width, along with increased size of the distended inferior and posteroinferior joint capsule on magnetic resonance arthrography, have been reported in cases of multidirectional shoulder instability.22 However, confusion remains about the role of the rotator interval in shoulder instability and about the effect its closure has on shoulder function. No one knows the degree of volume reduction that results from closure of the rotator interval and whether medial and lateral sutures differ in the volume reduction achieved.
Cadaveric studies have shown that the rotator interval has an important role in shoulder motion.6,13-16,19,20,23 Harryman and colleagues13 found that sectioning the coracohumeral ligament (CHL) increased shoulder range of motion (ROM), and medial-to-lateral closure of the rotator interval restricted motion in all planes. Most notably, interval closure limited inferior translation in the adducted shoulder, posterior translation in the flexed adducted shoulder, and external rotation in the neutral position. Subsequent studies,17,18 using rotator interval closure combined with thermal capsulorrhaphy, confirmed the results reported by Harryman and colleagues.13
More recent cadaveric studies using superior-to-inferior rotator interval closures have shown a decrease in anterior translation but not posterior translation.14-16,19-21 A superior-to-inferior interval closure technique limited external rotation less than a medial-to-lateral closure did.13-16,19-21 The majority of arthroscopically described rotator interval closures involve a superior-to-inferior technique and use 2 or 3 sutures.1,3,9-11
Plausinis and colleagues15 examined the effects of an isolated medial, an isolated lateral, and a medial combined with a lateral closure of the rotator interval. They noted that all 3 methods limited anterior translation and motion by means of 6° flexion and 10° external rotation; however, there was no statistical difference between methods. They also found that occasionally the medial interval closure resulted in massive loss of external rotation. Earlier, Jost and colleagues14 noted that a medial rotator interval could cause this massive loss by tethering the CHL, resulting in a medial-to-lateral imbrication of the CHL.
Arthroscopic rotator interval closure has clinically demonstrated an additive effect on shoulder stability. The recurrence rate was lower for arthroscopic Bankart repair combined with arthroscopic rotator interval closure (8%) than for arthroscopic Bankart repair alone (13%).24 In addition, time to recurrent dislocation was longer (42 vs 13 months) for the group that underwent the combination of Bankart repair and rotator interval closure. Regarding the concern about loss of motion after arthroscopic rotator interval closure, Chiang and colleagues25 recently noted no significant loss of motion 5 years after arthroscopic Bankart repair with rotator interval closure.
What effect rotator interval closure has on intra-articular glenohumeral volume (GHV) remains unknown. Using a cadaveric model, Yamamoto and colleagues20 showed that decreasing GHV can increase the responsiveness of the glenohumeral joint to the intra-articular pressure. Thus, reducing the volume can improve stability in vitro by increasing the magnitude of negative pressure stabilizing the glenohumeral joint.
We conducted a study to quantify the effects of arthroscopic rotator interval closure on capsular volume and to determine whether medial and lateral interval closures resulted in different degrees of volume reduction. Our hypothesis was that shoulder volume would be significantly reduced by closing the rotator interval.
Materials and Methods
Previous studies have not specifically evaluated GHV after rotator interval closure. Our power analysis was performed with data from a study by Karas and colleagues,26 who evaluated GHV after capsular plication. To detect a capsular volume reduction of 20% per stitch, with a 2-sided 5% significance level and a power of 80%, we needed a sample size of 5 specimens per group.
After receiving institutional review board approval for this study, we obtained 10 cadaveric shoulders (5 matched pairs). Exclusion criteria included arthroscopic evaluation revealing a full-thickness rotator cuff tear or significant osteoarthritis. Two shoulders had full-thickness cuff tears, leaving 8 shoulders to be tested; 6 of these were matched pairs. The shoulders were from 1 man (matched pair) and 4 women (2 matched pairs). Age ranged from 38 to 70 years (mean, 59.6 years). Differences in material properties between the specimens were accounted for by using primarily matched pairs.
The 2 study groups consisted of 4 shoulders each. After specimens were thawed, the skin, subcutaneous tissues, and periscapular muscles were removed from the shoulder. Only the capsule, biceps, and rotator cuff remained. For measurement purposes, the shoulders were mounted in a vice clamp in a beach-chair orientation. We placed a total of 2 portals with fully threaded 8.25-mm cannulas (Arthrex, Naples, Florida). A standard posterior portal was placed in the soft spot. A low anterior portal was then placed just superior to the subscapularis tendon. For arthroscopic examination and instrumentation in a saline environment, the shoulders were rotated into the lateral decubitus position, with suspension in 30° abduction and 20° forward flexion, by a rope attached to a pin in the distal shaft of the humerus.
In both groups, medial and lateral stitches with No. 2 FiberWire (Arthrex) were used to close the interval. The medial interval closure stitch was placed more than 10 mm away from the glenoid to prevent unpredictable CHL tethering; the lateral closure stitch was placed 10 mm lateral to the medial stitch (Figure 1).14 All sutures were placed intra-articularly under direct arthroscopic visualization, similar to the methods described in the literature.1,3,9-11 Sutures were passed through the superior glenohumeral ligament (SGHL) and through the upper subscapularis using a suture shuttle (SutureLasso; Arthrex) and Penetrator II Suture Retriever (Arthrex). The upper subscapularis was incorporated because of the unpredictable nature of the middle glenohumeral ligament (MGHL). Both rotator interval sutures were placed before tying either. In the medial group, the medial stitch was tied first, using alternating half-hitches, followed by the lateral stitch. In the lateral group, the lateral stitch was tied first, followed by the medial stitch. GHV was measured at baseline and after tying each stitch. Dr. Ponce instrumented all shoulders.
Modifying a beach-chair technique described by Miller and colleagues,27 we used a viscous fatty-acid sulfate solution, liquid soap, to measure GHV.27-29 A small slit in line with the fibers was made in the supraspinatus tendon just lateral to the musculotendinous junction. A 3-way stop-cock was placed into the joint though this defect. A 20-mL syringe with a 16-gauge needle was used to inject the soap. The needle was inserted into the rotator cuff interval, and the viscous solution was injected in 5-mL increments until there was active extravasation through the supraspinatus cannula (Figure 2). This technique, the “volcano method,” marked the maximum capacity of the joint. The joint was then copiously irrigated with normal saline and suctioned until all normal saline was evacuated. Dr. Rosenzweig took 2 measurements on each shoulder, and their mean was used for analysis.
The baseline measurement was taken with the 2 working cannulas in the shoulder joint. Measurements were obtained with cannulas to simulate normal clinical conditions. Subsequent measurements were done with the cannulas in place and inserted up to the same thread each time so as not to change the volume. The capsule and the rotator cuff were then dissected from the humerus so the size of the capsulolabral plication could be directly evaluated. Methylene blue was used to mark the capsular suture holes before removing the sutures. With use of a caliper, the size of the plication bite was measured (in millimeters).
Statistical Analysis
The primary outcome was percent reduction in GHV as a function of number of plications and size of plication. When only the first plication was tightened, the effect of position (medial or lateral) was also of interest. Percent volume reduction was calculated as (original – new) / original × 100. SAS 8.02 (SAS Institute, Cary, North Carolina) was used to fit a repeated random-intercept regression model for each outcome. This technique properly accounts for the paired nature of the specimens and the repeated measures (baseline plus 2 plications). Model fit was assessed by the method of difference in log likelihood.
Results
In the medial group, GHV was reduced by a mean of 24.2% with a single medial stitch; in the lateral group, GHV was reduced by a mean of 35.1% (Figure 3). The difference was significant (P < .02). In the medial group, when a second lateral stitch was used, GHV was reduced by another 18.7%; in the lateral group, when a medial stitch was added, GHV was reduced by another 11.4%. Final GHV for the medial and lateral groups was 42.9% and 46.5%, respectively. There was no statistical difference in final GHV, regardless of which stitch was placed first. When the 2 groups were combined, GHV was reduced by 44.9% with use of medial and lateral rotator interval closure stitches.
Mean amount of tissue purchased, or “bite size,” was 18 mm with a lateral suture and 15 mm with a medial suture (P < .05). In addition, an increase in bite size to GHV reduction was essentially linear, where an increase in bite size of 1 mm reduced GHV by about 1% (Figure 4).
Discussion
Although there have been numerous clinical series and biomechanical studies focused on isolated rotator interval closure (or its use as an adjunct) in shoulder stabilization, the precise function of the rotator interval remains poorly understood.1-3,6-11,19 Consequently, the in vivo effects of interval closure are unknown.
Initial studies proposed that rotator interval closure limited inferior and posterior translation.30 More recent studies have demonstrated that rotator interval closure confers little effect on posterior instability but increases anterior stability in cadaveric models.15,16 Clinical series have provided evidence that rotator interval closure can increase anterior stability.1,3,7,9,12 In a series of isolated rotator interval closures for multidirectional instability, Field and colleagues12 found that preoperative anterior and inferior symptoms predominated over posterior symptoms. Isolated closure of the rotator interval resulted in 100% excellent results with no cases of recurrent instability. Moon and colleagues31 reported that arthroscopic rotator interval closure with or without inferior capsular plication in multidirectional instability and predominant symptomatic inferior instability has shown benefit by improving function and stability. Other clinical reports of rotator interval closure in conjunction with arthroscopic Bankart repair have suggested it has an additive effect on anterior shoulder stability without limiting motion.24,25
In our study, arthroscopic closure of the rotator interval with 2 superior-to-inferior stitches reduced intracapsular volume by 45%. Even though open capsular shifts use different surgical techniques, similar technique volume reduction studies have reported reductions between 34% and 54% with open shifts.27,30 It is unknown if the stability resulting from decreased GHV is primarily from increasing intra-articular pressures or from restricting ROM, or from a combination of both. In shoulders with multidirectional instability, the joint volume may be increased, the joint capsule may be enlarged, or the glenohumeral ligaments may be lax and thin.4,6,32,33 Yamamoto and colleagues19 stated that intra-articular pressure is determined by 3 factors: load, joint volume, and material properties of the capsule. Load is a constant; joint volume and material properties can be changed.19 In our study, material properties were controlled by using a majority of matched specimens. Regardless of the stabilizing mechanism, our study results demonstrated that arthroscopic rotator interval closure may be a powerful tool in reducing shoulder volume, a consistent principle of surgical techniques used in reestablishing shoulder stability.19,20
When a single rotator interval closure stitch was used, volume reduction with a lateral stitch was superior to that with a medial stitch. This finding is logical, as anatomically the dimensions of the rotator interval are larger laterally as the CHL fans out to insert on the greater and lesser tuberosities.14 This finding has also been reported in open capsular shifts for multidirectional instability, with a lateral humeral shift having a larger volume reduction than a medial glenoid shift.27 Miller and colleagues27 used the image of a cone, with its larger opening facing the humerus and narrower side facing the glenoid, to illustrate this difference in open capsular shifts.
Our study also showed a larger volume reduction with 2 rotator interval closure stitches than with a single interval stitch. As ROM testing has not shown a difference between results with 1 and 2 sutures, we recommend a minimum of 2 sutures for arthroscopic rotator interval closure.15 If a single plication stitch is preferred, a lateral stitch (vs a medial stitch) can be used for a significantly larger reduction in shoulder volume. We think this is because of a larger amount of capsule being purchased with lateral closure (Figure 5). However, if a medial stitch is used, it is important to not place it too near the glenoid to avoid CHL tethering and subsequent excessive loss of external rotation.15
This study had several weaknesses. First, it was a cadaveric study, and use of specimens not known to have instability or specific rotator interval injury may make generalization to a clinical situation difficult. Second, although our power analysis called for 5 shoulders in each group, full-thickness rotator cuff tears rendered 2 shoulders unusable. This reduced our sample sizes and potentially decreased the power of the study, though the data demonstrated statistically significant differences. Third, we did not compare the effects of an open medial-to-lateral imbrication of the rotator interval on intracapsular volume with the effects of our arthroscopic method. We also did not assess our specimens’ ROM, effects of interval closure stitches on shoulder stability, or glenohumeral contact surface pressures, as these factors have already been studied.13-19 Instead, we focused on the effects of rotator interval closure on intracapsular volume, which had not been quantified until now. The clinical significance of such a volume reduction is unknown, especially with respect to influence on ROM, but the degree of volume reduction was larger than with previously reported arthroscopic instability repairs and smaller than with open capsular shifts, demonstrating that it may be a powerful tool in restoring stability in an unstable shoulder.26-30,34 Fourth, the role of isolated rotator interval closure is poorly defined, as only 1 clinical series of isolated rotator interval closure has been reported thus far.12 It has been far more common for rotator interval closure to be used with Bankart repair or capsulorrhaphy.1-3,7-9
In a cadaveric study by Provencher and colleagues,16 open rotator interval closure with medial-to-lateral imbrication of the interval altered shoulder kinematics differently from what occurred with arthroscopic closure of the MGHL to the SGHL, resulting in superior-to-inferior shift. Comparing the 2 methods may therefore be inappropriate. Currently we reserve rotator interval closure for infrequent cases of revision instability and cases in which glenoid bone loss is marginal (5%-15%) and there is a willingness to potentially sacrifice ROM to restore stability and avoid an open stabilization procedure. Continued investigation into the clinical role of rotator interval closure in shoulder stability is needed. We should identify the pathology in a patient with instability and use this technique as an adjuvant to other stabilization procedures.
Conclusion
Arthroscopic rotator interval closure with 2 plication stitches is a powerful tool in reducing the intracapsular volume of the shoulder. If a single plication stitch is preferred, a lateral rotator interval closure stitch (vs a medial stitch) can be used for a larger reduction in shoulder volume.
Since Neer described the rotator interval in 1970, its closure, often used in conjunction with capsulorrhaphy, has become an important surgical technique in managing shoulder instability.1-11 Numerous studies have sought to define the function of the rotator interval.1-3,6-20 The etiology of lesions of the rotator interval has been debated, and there is evidence that such lesions may be in part congenital.21 Increased rotator interval depth and width, along with increased size of the distended inferior and posteroinferior joint capsule on magnetic resonance arthrography, have been reported in cases of multidirectional shoulder instability.22 However, confusion remains about the role of the rotator interval in shoulder instability and about the effect its closure has on shoulder function. No one knows the degree of volume reduction that results from closure of the rotator interval and whether medial and lateral sutures differ in the volume reduction achieved.
Cadaveric studies have shown that the rotator interval has an important role in shoulder motion.6,13-16,19,20,23 Harryman and colleagues13 found that sectioning the coracohumeral ligament (CHL) increased shoulder range of motion (ROM), and medial-to-lateral closure of the rotator interval restricted motion in all planes. Most notably, interval closure limited inferior translation in the adducted shoulder, posterior translation in the flexed adducted shoulder, and external rotation in the neutral position. Subsequent studies,17,18 using rotator interval closure combined with thermal capsulorrhaphy, confirmed the results reported by Harryman and colleagues.13
More recent cadaveric studies using superior-to-inferior rotator interval closures have shown a decrease in anterior translation but not posterior translation.14-16,19-21 A superior-to-inferior interval closure technique limited external rotation less than a medial-to-lateral closure did.13-16,19-21 The majority of arthroscopically described rotator interval closures involve a superior-to-inferior technique and use 2 or 3 sutures.1,3,9-11
Plausinis and colleagues15 examined the effects of an isolated medial, an isolated lateral, and a medial combined with a lateral closure of the rotator interval. They noted that all 3 methods limited anterior translation and motion by means of 6° flexion and 10° external rotation; however, there was no statistical difference between methods. They also found that occasionally the medial interval closure resulted in massive loss of external rotation. Earlier, Jost and colleagues14 noted that a medial rotator interval could cause this massive loss by tethering the CHL, resulting in a medial-to-lateral imbrication of the CHL.
Arthroscopic rotator interval closure has clinically demonstrated an additive effect on shoulder stability. The recurrence rate was lower for arthroscopic Bankart repair combined with arthroscopic rotator interval closure (8%) than for arthroscopic Bankart repair alone (13%).24 In addition, time to recurrent dislocation was longer (42 vs 13 months) for the group that underwent the combination of Bankart repair and rotator interval closure. Regarding the concern about loss of motion after arthroscopic rotator interval closure, Chiang and colleagues25 recently noted no significant loss of motion 5 years after arthroscopic Bankart repair with rotator interval closure.
What effect rotator interval closure has on intra-articular glenohumeral volume (GHV) remains unknown. Using a cadaveric model, Yamamoto and colleagues20 showed that decreasing GHV can increase the responsiveness of the glenohumeral joint to the intra-articular pressure. Thus, reducing the volume can improve stability in vitro by increasing the magnitude of negative pressure stabilizing the glenohumeral joint.
We conducted a study to quantify the effects of arthroscopic rotator interval closure on capsular volume and to determine whether medial and lateral interval closures resulted in different degrees of volume reduction. Our hypothesis was that shoulder volume would be significantly reduced by closing the rotator interval.
Materials and Methods
Previous studies have not specifically evaluated GHV after rotator interval closure. Our power analysis was performed with data from a study by Karas and colleagues,26 who evaluated GHV after capsular plication. To detect a capsular volume reduction of 20% per stitch, with a 2-sided 5% significance level and a power of 80%, we needed a sample size of 5 specimens per group.
After receiving institutional review board approval for this study, we obtained 10 cadaveric shoulders (5 matched pairs). Exclusion criteria included arthroscopic evaluation revealing a full-thickness rotator cuff tear or significant osteoarthritis. Two shoulders had full-thickness cuff tears, leaving 8 shoulders to be tested; 6 of these were matched pairs. The shoulders were from 1 man (matched pair) and 4 women (2 matched pairs). Age ranged from 38 to 70 years (mean, 59.6 years). Differences in material properties between the specimens were accounted for by using primarily matched pairs.
The 2 study groups consisted of 4 shoulders each. After specimens were thawed, the skin, subcutaneous tissues, and periscapular muscles were removed from the shoulder. Only the capsule, biceps, and rotator cuff remained. For measurement purposes, the shoulders were mounted in a vice clamp in a beach-chair orientation. We placed a total of 2 portals with fully threaded 8.25-mm cannulas (Arthrex, Naples, Florida). A standard posterior portal was placed in the soft spot. A low anterior portal was then placed just superior to the subscapularis tendon. For arthroscopic examination and instrumentation in a saline environment, the shoulders were rotated into the lateral decubitus position, with suspension in 30° abduction and 20° forward flexion, by a rope attached to a pin in the distal shaft of the humerus.
In both groups, medial and lateral stitches with No. 2 FiberWire (Arthrex) were used to close the interval. The medial interval closure stitch was placed more than 10 mm away from the glenoid to prevent unpredictable CHL tethering; the lateral closure stitch was placed 10 mm lateral to the medial stitch (Figure 1).14 All sutures were placed intra-articularly under direct arthroscopic visualization, similar to the methods described in the literature.1,3,9-11 Sutures were passed through the superior glenohumeral ligament (SGHL) and through the upper subscapularis using a suture shuttle (SutureLasso; Arthrex) and Penetrator II Suture Retriever (Arthrex). The upper subscapularis was incorporated because of the unpredictable nature of the middle glenohumeral ligament (MGHL). Both rotator interval sutures were placed before tying either. In the medial group, the medial stitch was tied first, using alternating half-hitches, followed by the lateral stitch. In the lateral group, the lateral stitch was tied first, followed by the medial stitch. GHV was measured at baseline and after tying each stitch. Dr. Ponce instrumented all shoulders.
Modifying a beach-chair technique described by Miller and colleagues,27 we used a viscous fatty-acid sulfate solution, liquid soap, to measure GHV.27-29 A small slit in line with the fibers was made in the supraspinatus tendon just lateral to the musculotendinous junction. A 3-way stop-cock was placed into the joint though this defect. A 20-mL syringe with a 16-gauge needle was used to inject the soap. The needle was inserted into the rotator cuff interval, and the viscous solution was injected in 5-mL increments until there was active extravasation through the supraspinatus cannula (Figure 2). This technique, the “volcano method,” marked the maximum capacity of the joint. The joint was then copiously irrigated with normal saline and suctioned until all normal saline was evacuated. Dr. Rosenzweig took 2 measurements on each shoulder, and their mean was used for analysis.
The baseline measurement was taken with the 2 working cannulas in the shoulder joint. Measurements were obtained with cannulas to simulate normal clinical conditions. Subsequent measurements were done with the cannulas in place and inserted up to the same thread each time so as not to change the volume. The capsule and the rotator cuff were then dissected from the humerus so the size of the capsulolabral plication could be directly evaluated. Methylene blue was used to mark the capsular suture holes before removing the sutures. With use of a caliper, the size of the plication bite was measured (in millimeters).
Statistical Analysis
The primary outcome was percent reduction in GHV as a function of number of plications and size of plication. When only the first plication was tightened, the effect of position (medial or lateral) was also of interest. Percent volume reduction was calculated as (original – new) / original × 100. SAS 8.02 (SAS Institute, Cary, North Carolina) was used to fit a repeated random-intercept regression model for each outcome. This technique properly accounts for the paired nature of the specimens and the repeated measures (baseline plus 2 plications). Model fit was assessed by the method of difference in log likelihood.
Results
In the medial group, GHV was reduced by a mean of 24.2% with a single medial stitch; in the lateral group, GHV was reduced by a mean of 35.1% (Figure 3). The difference was significant (P < .02). In the medial group, when a second lateral stitch was used, GHV was reduced by another 18.7%; in the lateral group, when a medial stitch was added, GHV was reduced by another 11.4%. Final GHV for the medial and lateral groups was 42.9% and 46.5%, respectively. There was no statistical difference in final GHV, regardless of which stitch was placed first. When the 2 groups were combined, GHV was reduced by 44.9% with use of medial and lateral rotator interval closure stitches.
Mean amount of tissue purchased, or “bite size,” was 18 mm with a lateral suture and 15 mm with a medial suture (P < .05). In addition, an increase in bite size to GHV reduction was essentially linear, where an increase in bite size of 1 mm reduced GHV by about 1% (Figure 4).
Discussion
Although there have been numerous clinical series and biomechanical studies focused on isolated rotator interval closure (or its use as an adjunct) in shoulder stabilization, the precise function of the rotator interval remains poorly understood.1-3,6-11,19 Consequently, the in vivo effects of interval closure are unknown.
Initial studies proposed that rotator interval closure limited inferior and posterior translation.30 More recent studies have demonstrated that rotator interval closure confers little effect on posterior instability but increases anterior stability in cadaveric models.15,16 Clinical series have provided evidence that rotator interval closure can increase anterior stability.1,3,7,9,12 In a series of isolated rotator interval closures for multidirectional instability, Field and colleagues12 found that preoperative anterior and inferior symptoms predominated over posterior symptoms. Isolated closure of the rotator interval resulted in 100% excellent results with no cases of recurrent instability. Moon and colleagues31 reported that arthroscopic rotator interval closure with or without inferior capsular plication in multidirectional instability and predominant symptomatic inferior instability has shown benefit by improving function and stability. Other clinical reports of rotator interval closure in conjunction with arthroscopic Bankart repair have suggested it has an additive effect on anterior shoulder stability without limiting motion.24,25
In our study, arthroscopic closure of the rotator interval with 2 superior-to-inferior stitches reduced intracapsular volume by 45%. Even though open capsular shifts use different surgical techniques, similar technique volume reduction studies have reported reductions between 34% and 54% with open shifts.27,30 It is unknown if the stability resulting from decreased GHV is primarily from increasing intra-articular pressures or from restricting ROM, or from a combination of both. In shoulders with multidirectional instability, the joint volume may be increased, the joint capsule may be enlarged, or the glenohumeral ligaments may be lax and thin.4,6,32,33 Yamamoto and colleagues19 stated that intra-articular pressure is determined by 3 factors: load, joint volume, and material properties of the capsule. Load is a constant; joint volume and material properties can be changed.19 In our study, material properties were controlled by using a majority of matched specimens. Regardless of the stabilizing mechanism, our study results demonstrated that arthroscopic rotator interval closure may be a powerful tool in reducing shoulder volume, a consistent principle of surgical techniques used in reestablishing shoulder stability.19,20
When a single rotator interval closure stitch was used, volume reduction with a lateral stitch was superior to that with a medial stitch. This finding is logical, as anatomically the dimensions of the rotator interval are larger laterally as the CHL fans out to insert on the greater and lesser tuberosities.14 This finding has also been reported in open capsular shifts for multidirectional instability, with a lateral humeral shift having a larger volume reduction than a medial glenoid shift.27 Miller and colleagues27 used the image of a cone, with its larger opening facing the humerus and narrower side facing the glenoid, to illustrate this difference in open capsular shifts.
Our study also showed a larger volume reduction with 2 rotator interval closure stitches than with a single interval stitch. As ROM testing has not shown a difference between results with 1 and 2 sutures, we recommend a minimum of 2 sutures for arthroscopic rotator interval closure.15 If a single plication stitch is preferred, a lateral stitch (vs a medial stitch) can be used for a significantly larger reduction in shoulder volume. We think this is because of a larger amount of capsule being purchased with lateral closure (Figure 5). However, if a medial stitch is used, it is important to not place it too near the glenoid to avoid CHL tethering and subsequent excessive loss of external rotation.15
This study had several weaknesses. First, it was a cadaveric study, and use of specimens not known to have instability or specific rotator interval injury may make generalization to a clinical situation difficult. Second, although our power analysis called for 5 shoulders in each group, full-thickness rotator cuff tears rendered 2 shoulders unusable. This reduced our sample sizes and potentially decreased the power of the study, though the data demonstrated statistically significant differences. Third, we did not compare the effects of an open medial-to-lateral imbrication of the rotator interval on intracapsular volume with the effects of our arthroscopic method. We also did not assess our specimens’ ROM, effects of interval closure stitches on shoulder stability, or glenohumeral contact surface pressures, as these factors have already been studied.13-19 Instead, we focused on the effects of rotator interval closure on intracapsular volume, which had not been quantified until now. The clinical significance of such a volume reduction is unknown, especially with respect to influence on ROM, but the degree of volume reduction was larger than with previously reported arthroscopic instability repairs and smaller than with open capsular shifts, demonstrating that it may be a powerful tool in restoring stability in an unstable shoulder.26-30,34 Fourth, the role of isolated rotator interval closure is poorly defined, as only 1 clinical series of isolated rotator interval closure has been reported thus far.12 It has been far more common for rotator interval closure to be used with Bankart repair or capsulorrhaphy.1-3,7-9
In a cadaveric study by Provencher and colleagues,16 open rotator interval closure with medial-to-lateral imbrication of the interval altered shoulder kinematics differently from what occurred with arthroscopic closure of the MGHL to the SGHL, resulting in superior-to-inferior shift. Comparing the 2 methods may therefore be inappropriate. Currently we reserve rotator interval closure for infrequent cases of revision instability and cases in which glenoid bone loss is marginal (5%-15%) and there is a willingness to potentially sacrifice ROM to restore stability and avoid an open stabilization procedure. Continued investigation into the clinical role of rotator interval closure in shoulder stability is needed. We should identify the pathology in a patient with instability and use this technique as an adjuvant to other stabilization procedures.
Conclusion
Arthroscopic rotator interval closure with 2 plication stitches is a powerful tool in reducing the intracapsular volume of the shoulder. If a single plication stitch is preferred, a lateral rotator interval closure stitch (vs a medial stitch) can be used for a larger reduction in shoulder volume.
1. Creighton RA, Romeo AA, Brown FM, Hayden JK, Verma NN. Revision arthroscopic shoulder instability repair. Arthroscopy. 2007;23(7):703-709.
2. Gartsman GM, Roddey TS, Hammerman SM. Arthroscopic treatment of anterior-inferior glenohumeral instability. Two to five-year follow-up. J Bone Joint Surg Am. 2000;82(7):991-1003.
3. Gartsman GM, Taverna E, Hammerman SM. Arthroscopic rotator interval repair in glenohumeral instability: description of an operative technique. Arthroscopy. 1999;15(3):330-332.
4. Neer CS 2nd, Foster CR. Inferior capsular shift for involuntary inferior and multidirectional instability of the shoulder: a preliminary report. J Bone Joint Surg Am. 1980;62(6):897-908.
5. Neer CS 2nd. Displaced proximal humerus fractures: I. Classification and evaluation. J Bone Joint Surg Am. 1970;52(6):1077-1089.
6. Nobuhara K, Ikeda H. Rotator interval lesion. Clin Orthop. 1987;(223):44-50.
7. Rowe CR, Zarins B, Ciullo JV. Recurrent anterior dislocation of the shoulder after surgical repair. J Bone Joint Surg Am. 1984;66(2):159-168.
8. Rowe CR, Zarins B. Recurrent transient subluxation of the shoulder. J Bone Joint Surg Am. 1981;63(6):863-872.
9. Stokes DA, Savoie FH, Field LD. Arthroscopic repair of anterior glenohumeral instability and rotator interval lesions. Orthop Clin North Am. 2003;34(4):529-539.
10. Taverna E, Sansone V, Battistella F. Arthroscopic rotator interval repair: the three-step all-inside technique. Arthroscopy. 2004;20 Suppl 2:105-109.
11. Treacy SH, Field LD, Savoie FH. Rotator interval capsule closure: an arthroscopic technique. Arthroscopy. 1997;13(1):103-106.
12. Field LD, Warren RF, O’Brien SJ, Altcheck DW, Wickiewicz TL. Isolated closure of rotator interval defects for shoulder instability. Am J Sports Med. 1995;23(5):557-563.
13. Harryman DT 2nd, Sidles JA, Harris SL, Matsen FA 3rd. The role of the rotator interval capsule in passive motion and stability of the shoulder. J Bone Joint Surg Am. 1992;74(1):53-66.
14. Jost B, Koch PP, Gerber C. Anatomy and functional aspects of the rotator interval. J Shoulder Elbow Surg. 2000;9(4):336-341.
15. Plausinis D, Bravman JT, Heywood C, Kummer FJ, Kwon YM, Jazrawi LM. Arthroscopic rotator interval closure: effect of sutures on glenohumeral motion and anterior-posterior translation. Am J Sports Med. 2006;34(10):1656-1661.
16. Provencher MT, Mologne TS, Hongo M, Zhao K, Tasto JP, An KN. Arthroscopic versus open rotator interval closure: biomechanical evaluation of stability and motion. Arthroscopy. 2007;23(6):583-592.
17. Selecky MT, Tibone JE, Yang BY, et al. Glenohumeral joint translation after thermal capsuloplasty of the rotator interval. J Shoulder Elbow Surg. 2003;12(2):139-143.
18. Wolf R, Zheng N, Iero J, Weichel D. The effects of thermal capsulorrhaphy and rotator interval closure on multidirectional laxity in the glenohumeral joint: a cadaveric biomechanical study. Arthroscopy. 2004;20(10):1044-1049.
19. Yamamoto N, Itoi E, Tuoheti Y, et al. Effect of rotator interval closure on glenohumeral stability and motion: a cadaveric study. J Shoulder Elbow Surg. 2006;15(6):750-758.
20. Yamamoto N, Itoi E, Tuoheti Y, et al. The effect of the inferior capsular shift on shoulder intra-articular pressure: a cadaveric study. Am J Sports Med. 2006;34(6):939-944.
21. Cole BJ, Rodeo SA, O’Brien SJ, et al. The anatomy and histology of the rotator interval capsule of the shoulder. Clin Orthop. 2001;(390):129-137.
22. Lee HJ, Kim NR, Moon SG, Ko SM, Park JY. Multidirectional instability of the shoulder: rotator interval dimension and capsular laxity evaluation using MR arthrography. Skeletal Radiol. 2013;42(2):231-238.
23. Warner JP, Deng X, Warren RF, Torzilli PA, O’Brien SJ. Superoinferior translation in intact and vented glenohumeral joint. J Shoulder Elbow Surg. 1993;2(2):99-105.
24. Chechik O, Maman E, Dolkart O, Khashan M, Shabtai L, Mozes G. Arthroscopic rotator interval closure in shoulder instability repair: a retrospective study. J Shoulder Elbow Surg. 2010;19(7):1056-1062.
25. Chiang, E, Wang J, Wang S, et al. Arthroscopic posteroinferior capsular plication and rotator interval closure after Bankart repair in patients with traumatic anterior glenohumeral instability—a minimum follow-up of 5 years. Injury. 2010;41(10):1075-1078.
26. Karas SG, Creighton RA, DeMorat GJ. Glenohumeral volume reduction in arthroscopic shoulder reconstruction: a cadaveric analysis of suture plication and thermal capsulorrhaphy. Arthroscopy. 2004;20(2):179-184.
27. Miller MD, Larsen KM, Luke T, Leis HT, Plancher KD. Anterior capsular shift volume reduction: an in vitro comparison of 3 techniques. J Shoulder Elbow Surg. 2003;12(4):350-354.
28. Luke TA, Rovner AD, Karas SG, Hawkins RJ, Plancher KD. Volumetric change in the shoulder capsule after open inferior capsular shift versus arthroscopic thermal capsular shrinkage: a cadaveric model. J Shoulder Elbow Surg. 2004;13(2):146-149.
29. Ponce BA, Rosenzweig SD, Thompson KJ, Tokish J. Sequential volume reduction with capsular plications: relationship between cumulative size of plications and volumetric reduction for multidirectional instability of the shoulder. Am J Sports Med. 2011;39(3):526-531.
30. Lubowitz J, Bartolozzi A, Rubenstein D, et al. How much does inferior capsular shift reduce shoulder volume? Clin Orthop. 1996;(328):86-90.
31. Moon YL, Singh H, Yang H, Chul LK. Arthroscopic rotator interval closure by purse string suture for symptomatic inferior shoulder instability. Orthopedics. 2011;34(4).
32. Jerosch J, Castro WH. Shoulder instability in Ehlers-Danlos syndrome: an indication for surgical treatment? Acta Orthop Belg. 1990;56(2):451-453.
33. Schenk TJ, Brems JJ. Multidirectional instability of the shoulder: pathophysiology, diagnosis, and management. J Am Acad Orthop Surg. 1998;6(1):65-72.
34. Cohen SB, Wiley W, Goradia VK, Pearson S, Miller MD. Anterior capsulorrhaphy: an in vitro comparison of volume reduction. Arthroscopic plication versus open capsular shift. Arthroscopy. 2005;21(6):659-664.
1. Creighton RA, Romeo AA, Brown FM, Hayden JK, Verma NN. Revision arthroscopic shoulder instability repair. Arthroscopy. 2007;23(7):703-709.
2. Gartsman GM, Roddey TS, Hammerman SM. Arthroscopic treatment of anterior-inferior glenohumeral instability. Two to five-year follow-up. J Bone Joint Surg Am. 2000;82(7):991-1003.
3. Gartsman GM, Taverna E, Hammerman SM. Arthroscopic rotator interval repair in glenohumeral instability: description of an operative technique. Arthroscopy. 1999;15(3):330-332.
4. Neer CS 2nd, Foster CR. Inferior capsular shift for involuntary inferior and multidirectional instability of the shoulder: a preliminary report. J Bone Joint Surg Am. 1980;62(6):897-908.
5. Neer CS 2nd. Displaced proximal humerus fractures: I. Classification and evaluation. J Bone Joint Surg Am. 1970;52(6):1077-1089.
6. Nobuhara K, Ikeda H. Rotator interval lesion. Clin Orthop. 1987;(223):44-50.
7. Rowe CR, Zarins B, Ciullo JV. Recurrent anterior dislocation of the shoulder after surgical repair. J Bone Joint Surg Am. 1984;66(2):159-168.
8. Rowe CR, Zarins B. Recurrent transient subluxation of the shoulder. J Bone Joint Surg Am. 1981;63(6):863-872.
9. Stokes DA, Savoie FH, Field LD. Arthroscopic repair of anterior glenohumeral instability and rotator interval lesions. Orthop Clin North Am. 2003;34(4):529-539.
10. Taverna E, Sansone V, Battistella F. Arthroscopic rotator interval repair: the three-step all-inside technique. Arthroscopy. 2004;20 Suppl 2:105-109.
11. Treacy SH, Field LD, Savoie FH. Rotator interval capsule closure: an arthroscopic technique. Arthroscopy. 1997;13(1):103-106.
12. Field LD, Warren RF, O’Brien SJ, Altcheck DW, Wickiewicz TL. Isolated closure of rotator interval defects for shoulder instability. Am J Sports Med. 1995;23(5):557-563.
13. Harryman DT 2nd, Sidles JA, Harris SL, Matsen FA 3rd. The role of the rotator interval capsule in passive motion and stability of the shoulder. J Bone Joint Surg Am. 1992;74(1):53-66.
14. Jost B, Koch PP, Gerber C. Anatomy and functional aspects of the rotator interval. J Shoulder Elbow Surg. 2000;9(4):336-341.
15. Plausinis D, Bravman JT, Heywood C, Kummer FJ, Kwon YM, Jazrawi LM. Arthroscopic rotator interval closure: effect of sutures on glenohumeral motion and anterior-posterior translation. Am J Sports Med. 2006;34(10):1656-1661.
16. Provencher MT, Mologne TS, Hongo M, Zhao K, Tasto JP, An KN. Arthroscopic versus open rotator interval closure: biomechanical evaluation of stability and motion. Arthroscopy. 2007;23(6):583-592.
17. Selecky MT, Tibone JE, Yang BY, et al. Glenohumeral joint translation after thermal capsuloplasty of the rotator interval. J Shoulder Elbow Surg. 2003;12(2):139-143.
18. Wolf R, Zheng N, Iero J, Weichel D. The effects of thermal capsulorrhaphy and rotator interval closure on multidirectional laxity in the glenohumeral joint: a cadaveric biomechanical study. Arthroscopy. 2004;20(10):1044-1049.
19. Yamamoto N, Itoi E, Tuoheti Y, et al. Effect of rotator interval closure on glenohumeral stability and motion: a cadaveric study. J Shoulder Elbow Surg. 2006;15(6):750-758.
20. Yamamoto N, Itoi E, Tuoheti Y, et al. The effect of the inferior capsular shift on shoulder intra-articular pressure: a cadaveric study. Am J Sports Med. 2006;34(6):939-944.
21. Cole BJ, Rodeo SA, O’Brien SJ, et al. The anatomy and histology of the rotator interval capsule of the shoulder. Clin Orthop. 2001;(390):129-137.
22. Lee HJ, Kim NR, Moon SG, Ko SM, Park JY. Multidirectional instability of the shoulder: rotator interval dimension and capsular laxity evaluation using MR arthrography. Skeletal Radiol. 2013;42(2):231-238.
23. Warner JP, Deng X, Warren RF, Torzilli PA, O’Brien SJ. Superoinferior translation in intact and vented glenohumeral joint. J Shoulder Elbow Surg. 1993;2(2):99-105.
24. Chechik O, Maman E, Dolkart O, Khashan M, Shabtai L, Mozes G. Arthroscopic rotator interval closure in shoulder instability repair: a retrospective study. J Shoulder Elbow Surg. 2010;19(7):1056-1062.
25. Chiang, E, Wang J, Wang S, et al. Arthroscopic posteroinferior capsular plication and rotator interval closure after Bankart repair in patients with traumatic anterior glenohumeral instability—a minimum follow-up of 5 years. Injury. 2010;41(10):1075-1078.
26. Karas SG, Creighton RA, DeMorat GJ. Glenohumeral volume reduction in arthroscopic shoulder reconstruction: a cadaveric analysis of suture plication and thermal capsulorrhaphy. Arthroscopy. 2004;20(2):179-184.
27. Miller MD, Larsen KM, Luke T, Leis HT, Plancher KD. Anterior capsular shift volume reduction: an in vitro comparison of 3 techniques. J Shoulder Elbow Surg. 2003;12(4):350-354.
28. Luke TA, Rovner AD, Karas SG, Hawkins RJ, Plancher KD. Volumetric change in the shoulder capsule after open inferior capsular shift versus arthroscopic thermal capsular shrinkage: a cadaveric model. J Shoulder Elbow Surg. 2004;13(2):146-149.
29. Ponce BA, Rosenzweig SD, Thompson KJ, Tokish J. Sequential volume reduction with capsular plications: relationship between cumulative size of plications and volumetric reduction for multidirectional instability of the shoulder. Am J Sports Med. 2011;39(3):526-531.
30. Lubowitz J, Bartolozzi A, Rubenstein D, et al. How much does inferior capsular shift reduce shoulder volume? Clin Orthop. 1996;(328):86-90.
31. Moon YL, Singh H, Yang H, Chul LK. Arthroscopic rotator interval closure by purse string suture for symptomatic inferior shoulder instability. Orthopedics. 2011;34(4).
32. Jerosch J, Castro WH. Shoulder instability in Ehlers-Danlos syndrome: an indication for surgical treatment? Acta Orthop Belg. 1990;56(2):451-453.
33. Schenk TJ, Brems JJ. Multidirectional instability of the shoulder: pathophysiology, diagnosis, and management. J Am Acad Orthop Surg. 1998;6(1):65-72.
34. Cohen SB, Wiley W, Goradia VK, Pearson S, Miller MD. Anterior capsulorrhaphy: an in vitro comparison of volume reduction. Arthroscopic plication versus open capsular shift. Arthroscopy. 2005;21(6):659-664.
Assessing the Reading Level of Online Sarcoma Patient Education Materials
The diagnosis of cancer is a life-changing event for the patient as well as the patient’s family, friends, and relatives. Once diagnosed, most cancer patients want more information about their prognosis, future procedures, and/or treatment options.1 Receiving such information has been shown to reduce patient anxiety, increase patient satisfaction with care, and improve self-care.2-6 With the evolution of the Internet, patients in general7-9 and, specifically, cancer patients10-17 have turned to websites and online patient education materials (PEMs) to gather more health information.
For online PEMs to convey health information, their reading level must match the health literacy of the individuals who access them. Health literacy is the ability of an individual to gather and comprehend information about their condition to make the best decisions for their health.18 According to a report by the Institute of Medicine, 90 million American adults cannot properly use the US health care system because they do not possess adequate health literacy.18 Additionally, 36% of adults in the United States have basic or less-than-basic health literacy.19 This is starkly contrasted with the 12% of US adults who have proficient health literacy. A 2012 survey showed that about 31% of individuals who look for health information on the Internet have a high school education or less.8 In order to address the low health literacy of adults, the National Institutes of Health (NIH) has recommended that online PEMs be written at a sixth- to seventh-grade reading level.20
Unfortunately, many online PEMs related to certain cancer21-25 and orthopedic conditions26-31 do not meet NIH recommendations. Only 1 study has specifically looked at PEMs related to an orthopedic cancer condition.32 Lam and colleagues32 evaluated the readability of osteosarcoma PEMs from 56 websites using only 2 readability instruments and identified 86% of the websites as having a greater than eighth-grade reading level. No study has thoroughly assessed the readability of PEMs about bone and soft-tissue sarcomas and related conditions nor has any used 10 different readability instruments. Since each readability instrument has different variables (eg, sentence length, number of paragraphs, or number of complex words), averaging the scores of 10 of these instruments may result in less bias.
The purpose of this study was to evaluate the readability of online PEMs concerning bone and soft-tissue sarcomas and related conditions. The online PEMs came from websites that sarcoma patients may visit to obtain information about their condition. Our hypothesis was that the majority of these online PEMs will have a higher reading level than the NIH recommendations.
Materials and Methods
In May 2013, we identified online PEMs that included background, diagnosis, tests, or treatments for bone and soft-tissue sarcomas and conditions that mimic bone sarcoma. We included articles from the Tumors section of the American Academy of Orthopaedic Surgeons (AAOS) website.33 A second source of online PEMs came from a list of academic training centers created through the American Medical Association’s Fellowship and Residency Electronic Internet Database (FREIDA) with search criteria narrowed to orthopedic surgery. If we did not find PEMs of bone and soft-tissue cancers in the orthopedic department of a given academic training center’s website, we searched its cancer center website. We chose 4 programs with PEMs relevant to bone and soft-tissue sarcomas from each region in FREIDA for a balanced representation, except for the Territory region because it had only 1 academic training center and no relevant PEMs. Specialized websites, including Bonetumor.org, Sarcoma Alliance (Sarcomaalliance.org), and Sarcoma Foundation of America (Curesarcoma.org), were also evaluated. Within the Sarcoma Specialists section of the Sarcoma Alliance website,34 sarcoma specialists who were not identified from the FREIDA search for academic training centers were selected for review.
Because 8 of 10 individuals looking for health information on the Internet start their investigation at search engines, we also looked for PEMs through a Google search (Google.com) of bone cancer, and evaluated the first 10 hits for PEMs.8 Of these 10 hits, 8 had relevant PEMs, which we searched for additional PEMs about bone and soft-tissue cancers and related conditions. We also conducted a Google search of the most common bone sarcoma and soft-tissue sarcoma, osteosarcoma and malignant fibrous histiocytoma, respectively, and found 2 additional websites with relevant PEMs. LaCoursiere and colleagues35 surveyed cancer patients who used the Internet and found that they preferred WebMD (Webmd.com) and Medscape (Medscape.com) as sources for content about their medical condition.35 WebMD had been identified in the Google search, and we gathered the PEMs from Medscape also. It is worth noting that some of these websites are written for patients as well as clinicians.
Text from these PEMs were copied and pasted into separate Microsoft Word documents (Microsoft, Redmond, Washington). Advertisements, pictures, picture text, hyperlinks, copyright notices, page navigation links, paragraphs with no text, and any text that was not related to the given condition were deleted from the document to format the text for the readability software. Then, each Microsoft Word document was uploaded into the software package Readability Studio Professional (RSP) Edition Version 2012.1 for Windows (Oleander Software, Vandalia, Ohio). The 10 distinct readability instruments that were used to gauge the readability of each document were the Flesch Reading Ease score (FRE), the New Fog Count, the New Automated Readability Index, the Coleman-Liau Index (CLI), the Fry readability graph, the New Dale-Chall formula (NDC), the Gunning Frequency of Gobbledygook (Gunning FOG), the Powers-Sumner-Kearl formula, the Simple Measure of Gobbledygook (SMOG), and the Raygor Estimate Graph.
The FRE’s formula takes the average number of words per sentence and average number of syllables per word to compute a score ranging from 0 to 100 with 0 being the hardest to read.36 The New Fog Count tallies the number of sentences, easy words, and hard words (polysyllables) to calculate the grade level of the document.37 The New Automated Readability Index takes the average characters per word and average words per sentence to calculate a grade level for the document.37 The CLI randomly samples a few hundred words from the document, averages the number of letters and sentences per sample, and calculates an estimated grade level.38 The Fry readability graph selects samples of 100 words from the document, averages the number of syllables and sentences per 100 words, plots these data points on a graph, with the intersection determining the reading level.39 The NDC uses a list of 3000 familiar words that most fourth-grade students know.40 The percentage of difficult words, which are not on the list of familiar words, and the average sentence length in words are used to calculate the reading grade level of the document. The Gunning FOG uses the average sentence length in words and the percentage of hard words from a sample of at least 100 words to determine the reading grade level of the document.41 The Powers-Sumner-Kearl formula uses the average sentence length and percentage of monosyllables from a 100-word sample passage to calculate the reading grade level.42 The SMOG formula counts the number of polysyllabic words from 30 sentences and calculates the reading grade level of the document.43 In contrast to other formulas that test for 50% to 75% comprehension, the SMOG formula tests for 100% comprehension. As a result, the SMOG formula generally assigns a reading level 2 grades higher than the Dale-Chall level. The Raygor Estimate Graph selects a 100-word passage, counts the number of sentences and number of words with 6 or more letters, and plots the 2 variables on a graph to determine the reading grade level.44 The software package calculated the results from each reading instrument and reported the mean grade level score
for each document.
Results
We identified a total of 72 websites with relevant PEMs and included them in this study. Of these 72 websites, 36 websites were academic training centers, 10 were Google search hits, and 21 were from the Sarcoma Alliance list of sarcoma specialists. The remaining 5 websites were AAOS, Bonetumor.org, Sarcoma Alliance, Sarcoma Foundation of America, and Medscape. A list of conditions and treatments that were considered relevant PEMs is found in Appendix 1. A total of 774 articles were obtained from the 72 websites.
None of the websites had a mean readability score of 7 (seventh grade) or lower (Figures 1A, 1B). Mid-America Sarcoma Institute’s PEMs had the lowest mean readability score, 8.9. The lowest readability score was 5.3, which the New Fog Count readability instrument calculated for Vanderbilt University Medical Center’s (VUMC’s) PEMs (Appendix 2). The mean readability score of all websites was 11.4 (range, 8.9-15.5) (Appendix 2).
Seventy of 72 websites (97%) had PEMs that were fairly difficult or difficult, according to the FRE analysis (Figure 2). The American Cancer Society and Mid-America Sarcoma Institute had PEMs that were written in plain English. Sixty-nine of 72 websites (96%) had PEMs with a readability score of 10 or higher, according to the Raygor readability estimate (Figure 3). Using this instrument, the scores of the American Cancer Society and the University of Pennsylvania–Joan Karnell Cancer Center were 9; Mid-America Sarcoma Institute’s score was 8.
Discussion
Many cancer patients have turned to websites and online PEMs to gather health information about their condition.10-17 Basch and colleagues10 reported almost a decade ago that 44% of cancer patients, as well as 60% of their companions, used the Internet to find cancer-related information.10 When LaCoursiere and colleagues35 surveyed cancer patients, they found that patients handled their condition better and had less anxiety and uncertainty after using the Internet to find health information and support.35 In addition, many orthopedic patients, specifically 46% of orthopedic community outpatients,45 consult the Internet for information about their condition and future surgical procedures.46,47
This study comprehensively evaluated the readability of online PEMs of bone and soft-tissue sarcomas and related conditions by using 10 different readability instruments. After identifying 72 websites and 774 articles, we found that all 72 websites’ PEMs had a mean readability score that did not meet the NIH recommendation of writing PEMs at a sixth- to seventh-grade reading level. These results are consistent with studies evaluating the readability of online PEMs related to other cancer conditions21-25 and other orthopedic conditions.26-31
The combination of low health literacy of many US adults and high reading grade levels of the majority of online PEMs is not conducive to patients’ better understanding their condition(s). Even individuals with high reading skills prefer information that is simpler to read.48 In many areas of medicine, there is evidence that patients’ understanding of their condition has a positive impact on health outcomes, well-being, and the patient–physician relationship.49-61 Regarding cancer patients, Davis and colleagues54 and Peterson and colleagues57 showed that lower health literacy contributes to less knowledge and lower rates of breast54 and colorectal cancer57 screening tests. Even low health literacy of family caregivers of cancer patients can result in increased stress and lack of communication of important medical information between caregiver and physician.52 Among cancer patients, poor health literacy has been associated with mental distress60 as well as decreased compliance with treatment and lower involvement in clinical trials.55
The disparity between patients’ health literacy and the readability of online PEMs needs to be addressed by finding methods to improve patients’ understanding of their condition and to lower the readability scores of online PEMs. Better communication between patient and physician may improve patients’ comprehension of their condition and different aspects of their care.59,62-66 Doak and colleagues63 recommend giving cancer patients the most important information first; presenting information to patients in smaller doses; intermittently asking patients questions; and incorporating graphs, tables, and drawings into communication with patients.63 Additionally, allowing patients to repeat information they have just received/heard to the physician is another useful tool to improve patient education.62,64-66
Another way to address the disparity between patients’ health literacy and the readability of online PEMs is to reduce the reading grade level of existing PEMs. According to results from this study and others, the majority of online PEMs are above the reading grade level of a significant number of US adults. Many available and inexpensive readability instruments allow authors to assess their articles’ readability. Many writing guidelines also exist to help authors improve the readability of their PEMs.20,64,67-71 Living Word Vocabulary70 and Plain Language71 help authors replace complex words or medical terms with simpler words.29 Visual aids, audio, and video help patients with low health literacy remember the information.64
Efforts to improve PEM readability are effective. Of all the websites reviewed, VUMC was identified as having PEMs with the lowest readability score (5.3). This score was reported by the New Fog Count readability instrument, which accounts for the number of sentences, easy words, and hard words. In 2011, VUMC formed the Department of Patient Education to review and update its online and printed PEMs to make sure patients could read them.72 Additionally, the mean readability scores of the websites of the National Cancer Institute and MedlinePlus are in the top 50% of the websites included in this study. The NIH sponsors both sites, which follow the NIH guidelines for writing online PEMs at a reading level suitable for individuals with lower health literacy.20 These materials serve as potential models to improve the readability of PEMs, and, thus, help patients to better understand their condition, medical procedures, and/or treatment options.
To illustrate ways to improve the reading grade level of PEMs, we used the article “Ewing’s Sarcoma” from the AAOS website73 and followed the NIH guidelines to improve the reading grade level of the article.20 We identified complex words and defined them at an eighth-grade reading level. If that word was mentioned later in the article, simpler terminology was used instead of the initial complex word. For example, Ewing’s sarcoma was defined early and then referred to as bone tumor later in the article. We also identified every word that was 3 syllables or longer and used Microsoft Word’s thesaurus to replace those words with ones that were less than 3 syllables. Lastly, all sentences longer than 15 words were rewritten to be less than 15 words. After making these 3 changes to the article, the mean reading grade level dropped from 11.2 to 7.3.
This study has limitations. First, some readability instruments evaluate the number of syllables per word or polysyllabic words as part of their formula and, thus, can underestimate or overestimate the reading grade level of a document. Some readability formulas consider medical terms such as ulna, femur, or carpal as “easy” words because they have 2 syllables, but many laypersons may not comprehend these words. On the other hand, some readability formulas consider medical terms such as medications, diagnosis, or radiation as “hard” words because they contain 3 or more syllables, but the majority of laypersons likely comprehend these words. Second, the reading level of the patient population accessing those online sites was not assessed. Third, the readability instruments in this study did not evaluate the accuracy of the content, pictures, or tables of the PEMs. However, using 10 readability instruments allowed evaluation of many different readability aspects of the text. Fourth, because some websites identified in this study, such as Bonetumor.org, were written for patients as well as clinicians, the reading grade level of these sites may be higher than that of those sites written just for patients.
Conclusion
Because many orthopedic cancer patients rely on the Internet as a source of information, the need for online PEMs to match the reading skills of the patient population who accesses them is vital. However, this study shows that many organizations, academic training centers, and other entities need to update their online PEMs because all PEMs in this study had a mean readability grade level higher than the NIH recommendation. Further research needs to evaluate the effectiveness of other media, such as video, illustrations, and audio, to provide health information to patients. With many guidelines available that provide plans and advice to improve the readability of PEMs, research also must assess the most effective plans and advice in order to allow authors to focus their attention on 1 set of guidelines to improve the readability of their PEMs.
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23. Hoppe IC. Readability of patient information regarding breast cancer prevention from the Web site of the National Cancer Institute. J Cancer Educ. 2010;25(4):490-492.
24. Misra P, Kasabwala K, Agarwal N, Eloy JA, Liu JK. Readability analysis of internet-based patient information regarding skull base tumors. J Neurooncol. 2012;109(3):573-580.
25. Stinson JN, White M, Breakey V, et al. Perspectives on quality and content of information on the internet for adolescents with cancer. Pediatr Blood Cancer. 2011;57(1):97-104.
26. Badarudeen S, Sabharwal S. Readability of patient education materials from the American Academy of Orthopaedic Surgeons and Pediatric Orthopaedic Society of North America web sites. J Bone Joint Surg Am. 2008;90(1):199-204.
27. Bluman EM, Foley RP, Chiodo CP. Readability of the Patient Education Section of the AOFAS Website. Foot Ankle Int. 2009;30(4):287-291.
28. Polishchuk DL, Hashem J, Sabharwal S. Readability of online patient education materials on adult reconstruction Web sites. J Arthroplasty. 2012;27(5):716-719.
29. Sabharwal S, Badarudeen S, Unes Kunju S. Readability of online patient education materials from the AAOS web site. Clin Orthop. 2008;466(5):1245-1250.
30. Vives M, Young L, Sabharwal S. Readability of spine-related patient education materials from subspecialty organization and spine practitioner websites. Spine. 2009;34(25):2826-2831.
31. Wang SW, Capo JT, Orillaza N. Readability and comprehensibility of patient education material in hand-related web sites. J Hand Surg Am. 2009;34(7):1308-1315.
32. Lam CG, Roter DL, Cohen KJ. Survey of quality, readability, and social reach of websites on osteosarcoma in adolescents. Patient Educ Couns. 2013;90(1):82-87.
33. Tumors. Quinn RH, ed. OrthoInfo. American Academy of Orthopaedic Surgeons website. http://orthoinfo.aaos.org/menus/tumors.cfm. Accessed November 18, 2014.
34. Sarcoma specialists. Sarcoma Alliance website. sarcomaalliance.org/sarcoma-centers. Accessed November 18, 2014.
35. LaCoursiere SP, Knobf MT, McCorkle R. Cancer patients’ self-reported attitudes about the Internet. J Med Internet Res. 2005;7(3):e22.
36. Test your document’s readability. Microsoft Office website. office.microsoft.com/en-us/word-help/test-your-document-s-readability-HP010148506.aspx. Accessed November 18, 2014.
37. Kincaid JP, Fishburne RP, Rogers RL, Chissom BS. Derivation of new readability formulas (Automated Readability Index, Fog Count and Flesch Reading Ease Formula) for Navy enlisted personnel. Naval Technical Training Command. Research Branch Report 8-75. www.dtic.mil/dtic/tr/fulltext/u2/a006655.pdf. Published February 1975. Accessed November 18, 2014.
38. Coleman M, Liau TL. A computer readability formula designed for machine scoring. J Appl Psychol. 1975;60(2):283-284.
39. Fry E. Fry’s readability graph: clarifications, validity, and extension to Level 17. J Reading. 1977;21(3):242-252.
40. Chall JS, Dale E. Manual for the New Dale-Chall Readability Formula. Cambridge, MA: Brookline Books; 1995.
41. Gunning R. The Technique of Clear Writing. Rev. ed. New York, NY: McGraw-Hill; 1968.
42. Powers RD, Sumner WA, Kearl BE. A recalculation of four adult readability formulas. J Educ Psychol. 1958;49(2):99-105.
43. McLaughlin GH. SMOG grading—a new readability formula. J Reading. 1969;22,639-646.
44. Raygor L. The Raygor readability estimate: a quick and easy way to determine difficulty. In: Pearson PD, Hansen J, eds. Reading Theory, Research and Practice. Twenty-Sixth Yearbook of the National Reading Conference. Clemson, SC: National Reading Conference Inc; 1977:259-263.
45. Krempec J, Hall J, Biermann JS. Internet use by patients in orthopaedic surgery. Iowa Orthop J. 2003;23:80-82.
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47. Beall MS, Beall MS, Greenfield ML, Biermann JS. Patient Internet use in a community outpatient orthopaedic practice. Iowa Orthop J. 2002;22:103-107.
48. Davis TC, Bocchini JA, Fredrickson D, et al. Parent comprehension of polio vaccine information pamphlets. Pediatrics. 1996;97(6 Pt 1):804-810.
49. Apter AJ, Wan F, Reisine S, et al. The association of health literacy with adherence and outcomes in moderate-severe asthma. J Allergy Clin Immunol. 2013;132(2):321-327.
50. Baker DW, Parker RM, Williams MV, Clark WS. Health literacy and the risk of hospital admission. J Gen Intern Med. 1998;13(12):791-798.
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52. Bevan JL, Pecchioni LL. Understanding the impact of family caregiver cancer literacy on patient health outcomes. Patient Educ Couns. 2008;71(3):356-364.
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58. Peterson PN, Shetterly SM, Clarke CL, et al. Health literacy and outcomes among patients with heart failure. JAMA. 2011;305(16):1695-1701.
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61. Williams MV, Davis T, Parker RM, Weiss BD. The role of health literacy in patient-physician communication. Fam Med. 2002;34(5):383-389.
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The diagnosis of cancer is a life-changing event for the patient as well as the patient’s family, friends, and relatives. Once diagnosed, most cancer patients want more information about their prognosis, future procedures, and/or treatment options.1 Receiving such information has been shown to reduce patient anxiety, increase patient satisfaction with care, and improve self-care.2-6 With the evolution of the Internet, patients in general7-9 and, specifically, cancer patients10-17 have turned to websites and online patient education materials (PEMs) to gather more health information.
For online PEMs to convey health information, their reading level must match the health literacy of the individuals who access them. Health literacy is the ability of an individual to gather and comprehend information about their condition to make the best decisions for their health.18 According to a report by the Institute of Medicine, 90 million American adults cannot properly use the US health care system because they do not possess adequate health literacy.18 Additionally, 36% of adults in the United States have basic or less-than-basic health literacy.19 This is starkly contrasted with the 12% of US adults who have proficient health literacy. A 2012 survey showed that about 31% of individuals who look for health information on the Internet have a high school education or less.8 In order to address the low health literacy of adults, the National Institutes of Health (NIH) has recommended that online PEMs be written at a sixth- to seventh-grade reading level.20
Unfortunately, many online PEMs related to certain cancer21-25 and orthopedic conditions26-31 do not meet NIH recommendations. Only 1 study has specifically looked at PEMs related to an orthopedic cancer condition.32 Lam and colleagues32 evaluated the readability of osteosarcoma PEMs from 56 websites using only 2 readability instruments and identified 86% of the websites as having a greater than eighth-grade reading level. No study has thoroughly assessed the readability of PEMs about bone and soft-tissue sarcomas and related conditions nor has any used 10 different readability instruments. Since each readability instrument has different variables (eg, sentence length, number of paragraphs, or number of complex words), averaging the scores of 10 of these instruments may result in less bias.
The purpose of this study was to evaluate the readability of online PEMs concerning bone and soft-tissue sarcomas and related conditions. The online PEMs came from websites that sarcoma patients may visit to obtain information about their condition. Our hypothesis was that the majority of these online PEMs will have a higher reading level than the NIH recommendations.
Materials and Methods
In May 2013, we identified online PEMs that included background, diagnosis, tests, or treatments for bone and soft-tissue sarcomas and conditions that mimic bone sarcoma. We included articles from the Tumors section of the American Academy of Orthopaedic Surgeons (AAOS) website.33 A second source of online PEMs came from a list of academic training centers created through the American Medical Association’s Fellowship and Residency Electronic Internet Database (FREIDA) with search criteria narrowed to orthopedic surgery. If we did not find PEMs of bone and soft-tissue cancers in the orthopedic department of a given academic training center’s website, we searched its cancer center website. We chose 4 programs with PEMs relevant to bone and soft-tissue sarcomas from each region in FREIDA for a balanced representation, except for the Territory region because it had only 1 academic training center and no relevant PEMs. Specialized websites, including Bonetumor.org, Sarcoma Alliance (Sarcomaalliance.org), and Sarcoma Foundation of America (Curesarcoma.org), were also evaluated. Within the Sarcoma Specialists section of the Sarcoma Alliance website,34 sarcoma specialists who were not identified from the FREIDA search for academic training centers were selected for review.
Because 8 of 10 individuals looking for health information on the Internet start their investigation at search engines, we also looked for PEMs through a Google search (Google.com) of bone cancer, and evaluated the first 10 hits for PEMs.8 Of these 10 hits, 8 had relevant PEMs, which we searched for additional PEMs about bone and soft-tissue cancers and related conditions. We also conducted a Google search of the most common bone sarcoma and soft-tissue sarcoma, osteosarcoma and malignant fibrous histiocytoma, respectively, and found 2 additional websites with relevant PEMs. LaCoursiere and colleagues35 surveyed cancer patients who used the Internet and found that they preferred WebMD (Webmd.com) and Medscape (Medscape.com) as sources for content about their medical condition.35 WebMD had been identified in the Google search, and we gathered the PEMs from Medscape also. It is worth noting that some of these websites are written for patients as well as clinicians.
Text from these PEMs were copied and pasted into separate Microsoft Word documents (Microsoft, Redmond, Washington). Advertisements, pictures, picture text, hyperlinks, copyright notices, page navigation links, paragraphs with no text, and any text that was not related to the given condition were deleted from the document to format the text for the readability software. Then, each Microsoft Word document was uploaded into the software package Readability Studio Professional (RSP) Edition Version 2012.1 for Windows (Oleander Software, Vandalia, Ohio). The 10 distinct readability instruments that were used to gauge the readability of each document were the Flesch Reading Ease score (FRE), the New Fog Count, the New Automated Readability Index, the Coleman-Liau Index (CLI), the Fry readability graph, the New Dale-Chall formula (NDC), the Gunning Frequency of Gobbledygook (Gunning FOG), the Powers-Sumner-Kearl formula, the Simple Measure of Gobbledygook (SMOG), and the Raygor Estimate Graph.
The FRE’s formula takes the average number of words per sentence and average number of syllables per word to compute a score ranging from 0 to 100 with 0 being the hardest to read.36 The New Fog Count tallies the number of sentences, easy words, and hard words (polysyllables) to calculate the grade level of the document.37 The New Automated Readability Index takes the average characters per word and average words per sentence to calculate a grade level for the document.37 The CLI randomly samples a few hundred words from the document, averages the number of letters and sentences per sample, and calculates an estimated grade level.38 The Fry readability graph selects samples of 100 words from the document, averages the number of syllables and sentences per 100 words, plots these data points on a graph, with the intersection determining the reading level.39 The NDC uses a list of 3000 familiar words that most fourth-grade students know.40 The percentage of difficult words, which are not on the list of familiar words, and the average sentence length in words are used to calculate the reading grade level of the document. The Gunning FOG uses the average sentence length in words and the percentage of hard words from a sample of at least 100 words to determine the reading grade level of the document.41 The Powers-Sumner-Kearl formula uses the average sentence length and percentage of monosyllables from a 100-word sample passage to calculate the reading grade level.42 The SMOG formula counts the number of polysyllabic words from 30 sentences and calculates the reading grade level of the document.43 In contrast to other formulas that test for 50% to 75% comprehension, the SMOG formula tests for 100% comprehension. As a result, the SMOG formula generally assigns a reading level 2 grades higher than the Dale-Chall level. The Raygor Estimate Graph selects a 100-word passage, counts the number of sentences and number of words with 6 or more letters, and plots the 2 variables on a graph to determine the reading grade level.44 The software package calculated the results from each reading instrument and reported the mean grade level score
for each document.
Results
We identified a total of 72 websites with relevant PEMs and included them in this study. Of these 72 websites, 36 websites were academic training centers, 10 were Google search hits, and 21 were from the Sarcoma Alliance list of sarcoma specialists. The remaining 5 websites were AAOS, Bonetumor.org, Sarcoma Alliance, Sarcoma Foundation of America, and Medscape. A list of conditions and treatments that were considered relevant PEMs is found in Appendix 1. A total of 774 articles were obtained from the 72 websites.
None of the websites had a mean readability score of 7 (seventh grade) or lower (Figures 1A, 1B). Mid-America Sarcoma Institute’s PEMs had the lowest mean readability score, 8.9. The lowest readability score was 5.3, which the New Fog Count readability instrument calculated for Vanderbilt University Medical Center’s (VUMC’s) PEMs (Appendix 2). The mean readability score of all websites was 11.4 (range, 8.9-15.5) (Appendix 2).
Seventy of 72 websites (97%) had PEMs that were fairly difficult or difficult, according to the FRE analysis (Figure 2). The American Cancer Society and Mid-America Sarcoma Institute had PEMs that were written in plain English. Sixty-nine of 72 websites (96%) had PEMs with a readability score of 10 or higher, according to the Raygor readability estimate (Figure 3). Using this instrument, the scores of the American Cancer Society and the University of Pennsylvania–Joan Karnell Cancer Center were 9; Mid-America Sarcoma Institute’s score was 8.
Discussion
Many cancer patients have turned to websites and online PEMs to gather health information about their condition.10-17 Basch and colleagues10 reported almost a decade ago that 44% of cancer patients, as well as 60% of their companions, used the Internet to find cancer-related information.10 When LaCoursiere and colleagues35 surveyed cancer patients, they found that patients handled their condition better and had less anxiety and uncertainty after using the Internet to find health information and support.35 In addition, many orthopedic patients, specifically 46% of orthopedic community outpatients,45 consult the Internet for information about their condition and future surgical procedures.46,47
This study comprehensively evaluated the readability of online PEMs of bone and soft-tissue sarcomas and related conditions by using 10 different readability instruments. After identifying 72 websites and 774 articles, we found that all 72 websites’ PEMs had a mean readability score that did not meet the NIH recommendation of writing PEMs at a sixth- to seventh-grade reading level. These results are consistent with studies evaluating the readability of online PEMs related to other cancer conditions21-25 and other orthopedic conditions.26-31
The combination of low health literacy of many US adults and high reading grade levels of the majority of online PEMs is not conducive to patients’ better understanding their condition(s). Even individuals with high reading skills prefer information that is simpler to read.48 In many areas of medicine, there is evidence that patients’ understanding of their condition has a positive impact on health outcomes, well-being, and the patient–physician relationship.49-61 Regarding cancer patients, Davis and colleagues54 and Peterson and colleagues57 showed that lower health literacy contributes to less knowledge and lower rates of breast54 and colorectal cancer57 screening tests. Even low health literacy of family caregivers of cancer patients can result in increased stress and lack of communication of important medical information between caregiver and physician.52 Among cancer patients, poor health literacy has been associated with mental distress60 as well as decreased compliance with treatment and lower involvement in clinical trials.55
The disparity between patients’ health literacy and the readability of online PEMs needs to be addressed by finding methods to improve patients’ understanding of their condition and to lower the readability scores of online PEMs. Better communication between patient and physician may improve patients’ comprehension of their condition and different aspects of their care.59,62-66 Doak and colleagues63 recommend giving cancer patients the most important information first; presenting information to patients in smaller doses; intermittently asking patients questions; and incorporating graphs, tables, and drawings into communication with patients.63 Additionally, allowing patients to repeat information they have just received/heard to the physician is another useful tool to improve patient education.62,64-66
Another way to address the disparity between patients’ health literacy and the readability of online PEMs is to reduce the reading grade level of existing PEMs. According to results from this study and others, the majority of online PEMs are above the reading grade level of a significant number of US adults. Many available and inexpensive readability instruments allow authors to assess their articles’ readability. Many writing guidelines also exist to help authors improve the readability of their PEMs.20,64,67-71 Living Word Vocabulary70 and Plain Language71 help authors replace complex words or medical terms with simpler words.29 Visual aids, audio, and video help patients with low health literacy remember the information.64
Efforts to improve PEM readability are effective. Of all the websites reviewed, VUMC was identified as having PEMs with the lowest readability score (5.3). This score was reported by the New Fog Count readability instrument, which accounts for the number of sentences, easy words, and hard words. In 2011, VUMC formed the Department of Patient Education to review and update its online and printed PEMs to make sure patients could read them.72 Additionally, the mean readability scores of the websites of the National Cancer Institute and MedlinePlus are in the top 50% of the websites included in this study. The NIH sponsors both sites, which follow the NIH guidelines for writing online PEMs at a reading level suitable for individuals with lower health literacy.20 These materials serve as potential models to improve the readability of PEMs, and, thus, help patients to better understand their condition, medical procedures, and/or treatment options.
To illustrate ways to improve the reading grade level of PEMs, we used the article “Ewing’s Sarcoma” from the AAOS website73 and followed the NIH guidelines to improve the reading grade level of the article.20 We identified complex words and defined them at an eighth-grade reading level. If that word was mentioned later in the article, simpler terminology was used instead of the initial complex word. For example, Ewing’s sarcoma was defined early and then referred to as bone tumor later in the article. We also identified every word that was 3 syllables or longer and used Microsoft Word’s thesaurus to replace those words with ones that were less than 3 syllables. Lastly, all sentences longer than 15 words were rewritten to be less than 15 words. After making these 3 changes to the article, the mean reading grade level dropped from 11.2 to 7.3.
This study has limitations. First, some readability instruments evaluate the number of syllables per word or polysyllabic words as part of their formula and, thus, can underestimate or overestimate the reading grade level of a document. Some readability formulas consider medical terms such as ulna, femur, or carpal as “easy” words because they have 2 syllables, but many laypersons may not comprehend these words. On the other hand, some readability formulas consider medical terms such as medications, diagnosis, or radiation as “hard” words because they contain 3 or more syllables, but the majority of laypersons likely comprehend these words. Second, the reading level of the patient population accessing those online sites was not assessed. Third, the readability instruments in this study did not evaluate the accuracy of the content, pictures, or tables of the PEMs. However, using 10 readability instruments allowed evaluation of many different readability aspects of the text. Fourth, because some websites identified in this study, such as Bonetumor.org, were written for patients as well as clinicians, the reading grade level of these sites may be higher than that of those sites written just for patients.
Conclusion
Because many orthopedic cancer patients rely on the Internet as a source of information, the need for online PEMs to match the reading skills of the patient population who accesses them is vital. However, this study shows that many organizations, academic training centers, and other entities need to update their online PEMs because all PEMs in this study had a mean readability grade level higher than the NIH recommendation. Further research needs to evaluate the effectiveness of other media, such as video, illustrations, and audio, to provide health information to patients. With many guidelines available that provide plans and advice to improve the readability of PEMs, research also must assess the most effective plans and advice in order to allow authors to focus their attention on 1 set of guidelines to improve the readability of their PEMs.
The diagnosis of cancer is a life-changing event for the patient as well as the patient’s family, friends, and relatives. Once diagnosed, most cancer patients want more information about their prognosis, future procedures, and/or treatment options.1 Receiving such information has been shown to reduce patient anxiety, increase patient satisfaction with care, and improve self-care.2-6 With the evolution of the Internet, patients in general7-9 and, specifically, cancer patients10-17 have turned to websites and online patient education materials (PEMs) to gather more health information.
For online PEMs to convey health information, their reading level must match the health literacy of the individuals who access them. Health literacy is the ability of an individual to gather and comprehend information about their condition to make the best decisions for their health.18 According to a report by the Institute of Medicine, 90 million American adults cannot properly use the US health care system because they do not possess adequate health literacy.18 Additionally, 36% of adults in the United States have basic or less-than-basic health literacy.19 This is starkly contrasted with the 12% of US adults who have proficient health literacy. A 2012 survey showed that about 31% of individuals who look for health information on the Internet have a high school education or less.8 In order to address the low health literacy of adults, the National Institutes of Health (NIH) has recommended that online PEMs be written at a sixth- to seventh-grade reading level.20
Unfortunately, many online PEMs related to certain cancer21-25 and orthopedic conditions26-31 do not meet NIH recommendations. Only 1 study has specifically looked at PEMs related to an orthopedic cancer condition.32 Lam and colleagues32 evaluated the readability of osteosarcoma PEMs from 56 websites using only 2 readability instruments and identified 86% of the websites as having a greater than eighth-grade reading level. No study has thoroughly assessed the readability of PEMs about bone and soft-tissue sarcomas and related conditions nor has any used 10 different readability instruments. Since each readability instrument has different variables (eg, sentence length, number of paragraphs, or number of complex words), averaging the scores of 10 of these instruments may result in less bias.
The purpose of this study was to evaluate the readability of online PEMs concerning bone and soft-tissue sarcomas and related conditions. The online PEMs came from websites that sarcoma patients may visit to obtain information about their condition. Our hypothesis was that the majority of these online PEMs will have a higher reading level than the NIH recommendations.
Materials and Methods
In May 2013, we identified online PEMs that included background, diagnosis, tests, or treatments for bone and soft-tissue sarcomas and conditions that mimic bone sarcoma. We included articles from the Tumors section of the American Academy of Orthopaedic Surgeons (AAOS) website.33 A second source of online PEMs came from a list of academic training centers created through the American Medical Association’s Fellowship and Residency Electronic Internet Database (FREIDA) with search criteria narrowed to orthopedic surgery. If we did not find PEMs of bone and soft-tissue cancers in the orthopedic department of a given academic training center’s website, we searched its cancer center website. We chose 4 programs with PEMs relevant to bone and soft-tissue sarcomas from each region in FREIDA for a balanced representation, except for the Territory region because it had only 1 academic training center and no relevant PEMs. Specialized websites, including Bonetumor.org, Sarcoma Alliance (Sarcomaalliance.org), and Sarcoma Foundation of America (Curesarcoma.org), were also evaluated. Within the Sarcoma Specialists section of the Sarcoma Alliance website,34 sarcoma specialists who were not identified from the FREIDA search for academic training centers were selected for review.
Because 8 of 10 individuals looking for health information on the Internet start their investigation at search engines, we also looked for PEMs through a Google search (Google.com) of bone cancer, and evaluated the first 10 hits for PEMs.8 Of these 10 hits, 8 had relevant PEMs, which we searched for additional PEMs about bone and soft-tissue cancers and related conditions. We also conducted a Google search of the most common bone sarcoma and soft-tissue sarcoma, osteosarcoma and malignant fibrous histiocytoma, respectively, and found 2 additional websites with relevant PEMs. LaCoursiere and colleagues35 surveyed cancer patients who used the Internet and found that they preferred WebMD (Webmd.com) and Medscape (Medscape.com) as sources for content about their medical condition.35 WebMD had been identified in the Google search, and we gathered the PEMs from Medscape also. It is worth noting that some of these websites are written for patients as well as clinicians.
Text from these PEMs were copied and pasted into separate Microsoft Word documents (Microsoft, Redmond, Washington). Advertisements, pictures, picture text, hyperlinks, copyright notices, page navigation links, paragraphs with no text, and any text that was not related to the given condition were deleted from the document to format the text for the readability software. Then, each Microsoft Word document was uploaded into the software package Readability Studio Professional (RSP) Edition Version 2012.1 for Windows (Oleander Software, Vandalia, Ohio). The 10 distinct readability instruments that were used to gauge the readability of each document were the Flesch Reading Ease score (FRE), the New Fog Count, the New Automated Readability Index, the Coleman-Liau Index (CLI), the Fry readability graph, the New Dale-Chall formula (NDC), the Gunning Frequency of Gobbledygook (Gunning FOG), the Powers-Sumner-Kearl formula, the Simple Measure of Gobbledygook (SMOG), and the Raygor Estimate Graph.
The FRE’s formula takes the average number of words per sentence and average number of syllables per word to compute a score ranging from 0 to 100 with 0 being the hardest to read.36 The New Fog Count tallies the number of sentences, easy words, and hard words (polysyllables) to calculate the grade level of the document.37 The New Automated Readability Index takes the average characters per word and average words per sentence to calculate a grade level for the document.37 The CLI randomly samples a few hundred words from the document, averages the number of letters and sentences per sample, and calculates an estimated grade level.38 The Fry readability graph selects samples of 100 words from the document, averages the number of syllables and sentences per 100 words, plots these data points on a graph, with the intersection determining the reading level.39 The NDC uses a list of 3000 familiar words that most fourth-grade students know.40 The percentage of difficult words, which are not on the list of familiar words, and the average sentence length in words are used to calculate the reading grade level of the document. The Gunning FOG uses the average sentence length in words and the percentage of hard words from a sample of at least 100 words to determine the reading grade level of the document.41 The Powers-Sumner-Kearl formula uses the average sentence length and percentage of monosyllables from a 100-word sample passage to calculate the reading grade level.42 The SMOG formula counts the number of polysyllabic words from 30 sentences and calculates the reading grade level of the document.43 In contrast to other formulas that test for 50% to 75% comprehension, the SMOG formula tests for 100% comprehension. As a result, the SMOG formula generally assigns a reading level 2 grades higher than the Dale-Chall level. The Raygor Estimate Graph selects a 100-word passage, counts the number of sentences and number of words with 6 or more letters, and plots the 2 variables on a graph to determine the reading grade level.44 The software package calculated the results from each reading instrument and reported the mean grade level score
for each document.
Results
We identified a total of 72 websites with relevant PEMs and included them in this study. Of these 72 websites, 36 websites were academic training centers, 10 were Google search hits, and 21 were from the Sarcoma Alliance list of sarcoma specialists. The remaining 5 websites were AAOS, Bonetumor.org, Sarcoma Alliance, Sarcoma Foundation of America, and Medscape. A list of conditions and treatments that were considered relevant PEMs is found in Appendix 1. A total of 774 articles were obtained from the 72 websites.
None of the websites had a mean readability score of 7 (seventh grade) or lower (Figures 1A, 1B). Mid-America Sarcoma Institute’s PEMs had the lowest mean readability score, 8.9. The lowest readability score was 5.3, which the New Fog Count readability instrument calculated for Vanderbilt University Medical Center’s (VUMC’s) PEMs (Appendix 2). The mean readability score of all websites was 11.4 (range, 8.9-15.5) (Appendix 2).
Seventy of 72 websites (97%) had PEMs that were fairly difficult or difficult, according to the FRE analysis (Figure 2). The American Cancer Society and Mid-America Sarcoma Institute had PEMs that were written in plain English. Sixty-nine of 72 websites (96%) had PEMs with a readability score of 10 or higher, according to the Raygor readability estimate (Figure 3). Using this instrument, the scores of the American Cancer Society and the University of Pennsylvania–Joan Karnell Cancer Center were 9; Mid-America Sarcoma Institute’s score was 8.
Discussion
Many cancer patients have turned to websites and online PEMs to gather health information about their condition.10-17 Basch and colleagues10 reported almost a decade ago that 44% of cancer patients, as well as 60% of their companions, used the Internet to find cancer-related information.10 When LaCoursiere and colleagues35 surveyed cancer patients, they found that patients handled their condition better and had less anxiety and uncertainty after using the Internet to find health information and support.35 In addition, many orthopedic patients, specifically 46% of orthopedic community outpatients,45 consult the Internet for information about their condition and future surgical procedures.46,47
This study comprehensively evaluated the readability of online PEMs of bone and soft-tissue sarcomas and related conditions by using 10 different readability instruments. After identifying 72 websites and 774 articles, we found that all 72 websites’ PEMs had a mean readability score that did not meet the NIH recommendation of writing PEMs at a sixth- to seventh-grade reading level. These results are consistent with studies evaluating the readability of online PEMs related to other cancer conditions21-25 and other orthopedic conditions.26-31
The combination of low health literacy of many US adults and high reading grade levels of the majority of online PEMs is not conducive to patients’ better understanding their condition(s). Even individuals with high reading skills prefer information that is simpler to read.48 In many areas of medicine, there is evidence that patients’ understanding of their condition has a positive impact on health outcomes, well-being, and the patient–physician relationship.49-61 Regarding cancer patients, Davis and colleagues54 and Peterson and colleagues57 showed that lower health literacy contributes to less knowledge and lower rates of breast54 and colorectal cancer57 screening tests. Even low health literacy of family caregivers of cancer patients can result in increased stress and lack of communication of important medical information between caregiver and physician.52 Among cancer patients, poor health literacy has been associated with mental distress60 as well as decreased compliance with treatment and lower involvement in clinical trials.55
The disparity between patients’ health literacy and the readability of online PEMs needs to be addressed by finding methods to improve patients’ understanding of their condition and to lower the readability scores of online PEMs. Better communication between patient and physician may improve patients’ comprehension of their condition and different aspects of their care.59,62-66 Doak and colleagues63 recommend giving cancer patients the most important information first; presenting information to patients in smaller doses; intermittently asking patients questions; and incorporating graphs, tables, and drawings into communication with patients.63 Additionally, allowing patients to repeat information they have just received/heard to the physician is another useful tool to improve patient education.62,64-66
Another way to address the disparity between patients’ health literacy and the readability of online PEMs is to reduce the reading grade level of existing PEMs. According to results from this study and others, the majority of online PEMs are above the reading grade level of a significant number of US adults. Many available and inexpensive readability instruments allow authors to assess their articles’ readability. Many writing guidelines also exist to help authors improve the readability of their PEMs.20,64,67-71 Living Word Vocabulary70 and Plain Language71 help authors replace complex words or medical terms with simpler words.29 Visual aids, audio, and video help patients with low health literacy remember the information.64
Efforts to improve PEM readability are effective. Of all the websites reviewed, VUMC was identified as having PEMs with the lowest readability score (5.3). This score was reported by the New Fog Count readability instrument, which accounts for the number of sentences, easy words, and hard words. In 2011, VUMC formed the Department of Patient Education to review and update its online and printed PEMs to make sure patients could read them.72 Additionally, the mean readability scores of the websites of the National Cancer Institute and MedlinePlus are in the top 50% of the websites included in this study. The NIH sponsors both sites, which follow the NIH guidelines for writing online PEMs at a reading level suitable for individuals with lower health literacy.20 These materials serve as potential models to improve the readability of PEMs, and, thus, help patients to better understand their condition, medical procedures, and/or treatment options.
To illustrate ways to improve the reading grade level of PEMs, we used the article “Ewing’s Sarcoma” from the AAOS website73 and followed the NIH guidelines to improve the reading grade level of the article.20 We identified complex words and defined them at an eighth-grade reading level. If that word was mentioned later in the article, simpler terminology was used instead of the initial complex word. For example, Ewing’s sarcoma was defined early and then referred to as bone tumor later in the article. We also identified every word that was 3 syllables or longer and used Microsoft Word’s thesaurus to replace those words with ones that were less than 3 syllables. Lastly, all sentences longer than 15 words were rewritten to be less than 15 words. After making these 3 changes to the article, the mean reading grade level dropped from 11.2 to 7.3.
This study has limitations. First, some readability instruments evaluate the number of syllables per word or polysyllabic words as part of their formula and, thus, can underestimate or overestimate the reading grade level of a document. Some readability formulas consider medical terms such as ulna, femur, or carpal as “easy” words because they have 2 syllables, but many laypersons may not comprehend these words. On the other hand, some readability formulas consider medical terms such as medications, diagnosis, or radiation as “hard” words because they contain 3 or more syllables, but the majority of laypersons likely comprehend these words. Second, the reading level of the patient population accessing those online sites was not assessed. Third, the readability instruments in this study did not evaluate the accuracy of the content, pictures, or tables of the PEMs. However, using 10 readability instruments allowed evaluation of many different readability aspects of the text. Fourth, because some websites identified in this study, such as Bonetumor.org, were written for patients as well as clinicians, the reading grade level of these sites may be higher than that of those sites written just for patients.
Conclusion
Because many orthopedic cancer patients rely on the Internet as a source of information, the need for online PEMs to match the reading skills of the patient population who accesses them is vital. However, this study shows that many organizations, academic training centers, and other entities need to update their online PEMs because all PEMs in this study had a mean readability grade level higher than the NIH recommendation. Further research needs to evaluate the effectiveness of other media, such as video, illustrations, and audio, to provide health information to patients. With many guidelines available that provide plans and advice to improve the readability of PEMs, research also must assess the most effective plans and advice in order to allow authors to focus their attention on 1 set of guidelines to improve the readability of their PEMs.
1. Piredda M, Rocci L, Gualandi R, Petitti T, Vincenzi B, De Marinis MG. Survey on learning needs and preferred sources of information to meet these needs in Italian oncology patients receiving chemotherapy. Eur J Oncol Nurs. 2008;12(2):120-126.
2. Fernsler JI, Cannon CA. The whys of patient education. Semin Oncol Nurs. 1991;7(2):79-86.
3. Glimelius B, Birgegård G, Hoffman K, Kvale G, Sjödén PO. Information to and communication with cancer patients: improvements and psychosocial correlates in a comprehensive care program for patients and their relatives. Patient Educ Couns. 1995;25(2):171-182.
4. Harris KA. The informational needs of patients with cancer and their families. Cancer Pract. 1998;6(1):39-46.
5. Jensen AB, Madsen B, Andersen P, Rose C. Information for cancer patients entering a clinical trial--an evaluation of an information strategy. Eur J Cancer. 1993;29A(16):2235-2238.
6. Wells ME, McQuellon RP, Hinkle JS, Cruz JM. Reducing anxiety in newly diagnosed cancer patients: a pilot program. Cancer Pract. 1995;3(2):100-104.
7. Diaz JA, Griffith RA, Ng JJ, Reinert SE, Friedmann PD, Moulton AW. Patients’ use of the Internet for medical information. J Gen Intern Med. 2002;17(3):180-185.
8. Fox S, Duggan M. Health Online 2013. Pew Research Center’s Internet and American Life Project. www.pewinternet.org/~/media//Files/Reports/PIP_HealthOnline.pdf. Published January 15, 2013. Accessed November 18. 2014.
9. Schwartz KL, Roe T, Northrup J, Meza J, Seifeldin R, Neale AV. Family medicine patients’ use of the Internet for health information: a MetroNet study. J Am Board Fam Med. 2006;19(1):39-45.
10. Basch EM, Thaler HT, Shi W, Yakren S, Schrag D. Use of information resources by patients with cancer and their companions. Cancer. 2004;100(11):2476-2483.
11. Huang GJ, Penson DF. Internet health resources and the cancer patient. Cancer Invest. 2008;26(2):202-207.
12. Metz JM, Devine P, Denittis A, et al. A multi-institutional study of Internet utilization by radiation oncology patients. Int J Radiat Oncol Biol Phys. 2003;56(4):1201-1205.
13. Peterson MW, Fretz PC. Patient use of the internet for information in a lung cancer clinic. Chest. 2003;123(2):452-457.
14. Satterlund MJ, McCaul KD, Sandgren AK. Information gathering over time by breast cancer patients. J Med Internet Res. 2003;5(3):e15.
15. Tustin N. The role of patient satisfaction in online health information seeking. J Health Commun. 2010;15(1):3-17.
16. Van de Poll-Franse LV, Van Eenbergen MC. Internet use by cancer survivors: current use and future wishes. Support Care Cancer. 2008;16(10):1189-1195.
17. Ziebland S, Chapple A, Dumelow C, Evans J, Prinjha S, Rozmovits L. How the internet affects patients’ experience of cancer: a qualitative study. BMJ. 2004;328(7439):564.
18. Committee on Health Literacy, Board on Neuroscience and Behavioral Health, Institute of Medicine. Nielsen-Bohlman L, Panzer AM, Kindig DA, eds. Health Literacy: A Prescription to End Confusion. Washington, DC: National Academies Press; 2004. Available at: www.nap.edu/openbook.php?record_id=10883. Accessed November 18, 2014.
19. Kutner M, Greenberg E, Ying J, Paulsen C. The Health Literacy of America’s Adults: Results from the 2003 National Assessment of Adult Literacy. NCES 2006-483. US Department of Education. Washington, DC: National Center for Education Statistics; 2006. Available at: www.nces.ed.gov/pubs2006/2006483.pdf. Accessed November 18, 2014.
20. How to write easy-to-read health materials. MedlinePlus website. www.nlm.nih.gov/medlineplus/etr.html. Updated February 13, 2013. Accessed November 18, 2014.
21. Ellimoottil C, Polcari A, Kadlec A, Gupta G. Readability of websites containing information about prostate cancer treatment options. J Urol. 2012;188(6):2171-2175.
22. Friedman DB, Hoffman-Goetz L, Arocha JF. Health literacy and the World Wide Web: comparing the readability of leading incident cancers on the Internet. Med Inform Internet Med. 2006;31(1):67-87.
23. Hoppe IC. Readability of patient information regarding breast cancer prevention from the Web site of the National Cancer Institute. J Cancer Educ. 2010;25(4):490-492.
24. Misra P, Kasabwala K, Agarwal N, Eloy JA, Liu JK. Readability analysis of internet-based patient information regarding skull base tumors. J Neurooncol. 2012;109(3):573-580.
25. Stinson JN, White M, Breakey V, et al. Perspectives on quality and content of information on the internet for adolescents with cancer. Pediatr Blood Cancer. 2011;57(1):97-104.
26. Badarudeen S, Sabharwal S. Readability of patient education materials from the American Academy of Orthopaedic Surgeons and Pediatric Orthopaedic Society of North America web sites. J Bone Joint Surg Am. 2008;90(1):199-204.
27. Bluman EM, Foley RP, Chiodo CP. Readability of the Patient Education Section of the AOFAS Website. Foot Ankle Int. 2009;30(4):287-291.
28. Polishchuk DL, Hashem J, Sabharwal S. Readability of online patient education materials on adult reconstruction Web sites. J Arthroplasty. 2012;27(5):716-719.
29. Sabharwal S, Badarudeen S, Unes Kunju S. Readability of online patient education materials from the AAOS web site. Clin Orthop. 2008;466(5):1245-1250.
30. Vives M, Young L, Sabharwal S. Readability of spine-related patient education materials from subspecialty organization and spine practitioner websites. Spine. 2009;34(25):2826-2831.
31. Wang SW, Capo JT, Orillaza N. Readability and comprehensibility of patient education material in hand-related web sites. J Hand Surg Am. 2009;34(7):1308-1315.
32. Lam CG, Roter DL, Cohen KJ. Survey of quality, readability, and social reach of websites on osteosarcoma in adolescents. Patient Educ Couns. 2013;90(1):82-87.
33. Tumors. Quinn RH, ed. OrthoInfo. American Academy of Orthopaedic Surgeons website. http://orthoinfo.aaos.org/menus/tumors.cfm. Accessed November 18, 2014.
34. Sarcoma specialists. Sarcoma Alliance website. sarcomaalliance.org/sarcoma-centers. Accessed November 18, 2014.
35. LaCoursiere SP, Knobf MT, McCorkle R. Cancer patients’ self-reported attitudes about the Internet. J Med Internet Res. 2005;7(3):e22.
36. Test your document’s readability. Microsoft Office website. office.microsoft.com/en-us/word-help/test-your-document-s-readability-HP010148506.aspx. Accessed November 18, 2014.
37. Kincaid JP, Fishburne RP, Rogers RL, Chissom BS. Derivation of new readability formulas (Automated Readability Index, Fog Count and Flesch Reading Ease Formula) for Navy enlisted personnel. Naval Technical Training Command. Research Branch Report 8-75. www.dtic.mil/dtic/tr/fulltext/u2/a006655.pdf. Published February 1975. Accessed November 18, 2014.
38. Coleman M, Liau TL. A computer readability formula designed for machine scoring. J Appl Psychol. 1975;60(2):283-284.
39. Fry E. Fry’s readability graph: clarifications, validity, and extension to Level 17. J Reading. 1977;21(3):242-252.
40. Chall JS, Dale E. Manual for the New Dale-Chall Readability Formula. Cambridge, MA: Brookline Books; 1995.
41. Gunning R. The Technique of Clear Writing. Rev. ed. New York, NY: McGraw-Hill; 1968.
42. Powers RD, Sumner WA, Kearl BE. A recalculation of four adult readability formulas. J Educ Psychol. 1958;49(2):99-105.
43. McLaughlin GH. SMOG grading—a new readability formula. J Reading. 1969;22,639-646.
44. Raygor L. The Raygor readability estimate: a quick and easy way to determine difficulty. In: Pearson PD, Hansen J, eds. Reading Theory, Research and Practice. Twenty-Sixth Yearbook of the National Reading Conference. Clemson, SC: National Reading Conference Inc; 1977:259-263.
45. Krempec J, Hall J, Biermann JS. Internet use by patients in orthopaedic surgery. Iowa Orthop J. 2003;23:80-82.
46. Beall MS, Golladay GJ, Greenfield ML, Hensinger RN, Biermann JS. Use of the Internet by pediatric orthopaedic outpatients. J Pediatr Orthop. 2002;22(2):261-264.
47. Beall MS, Beall MS, Greenfield ML, Biermann JS. Patient Internet use in a community outpatient orthopaedic practice. Iowa Orthop J. 2002;22:103-107.
48. Davis TC, Bocchini JA, Fredrickson D, et al. Parent comprehension of polio vaccine information pamphlets. Pediatrics. 1996;97(6 Pt 1):804-810.
49. Apter AJ, Wan F, Reisine S, et al. The association of health literacy with adherence and outcomes in moderate-severe asthma. J Allergy Clin Immunol. 2013;132(2):321-327.
50. Baker DW, Parker RM, Williams MV, Clark WS. Health literacy and the risk of hospital admission. J Gen Intern Med. 1998;13(12):791-798.
51. Berkman ND, Sheridan SL, Donahue KE, Halpern DJ, Crotty K. Low health literacy and health outcomes: an updated systematic review. Ann Intern Med. 2011;155(2):97-107.
52. Bevan JL, Pecchioni LL. Understanding the impact of family caregiver cancer literacy on patient health outcomes. Patient Educ Couns. 2008;71(3):356-364.
53. Corey MR, St Julien J, Miller C, et al. Patient education level affects functionality and long term mortality after major lower extremity amputation. Am J Surg. 2012;204(5):626-630.
54. Davis TC, Arnold C, Berkel HJ, Nandy I, Jackson RH, Glass J. Knowledge and attitude on screening mammography among low-literate, low-income women. Cancer. 1996;78(9):1912-1920.
55. Davis TC, Williams MV, Marin E, Parker RM, Glass J. Health literacy and cancer communication. CA Cancer J Clin. 2002;52(3):134-149.
56. Freedman RB, Jones SK, Lin A, Robin AL, Muir KW. Influence of parental health literacy and dosing responsibility on pediatric glaucoma medication adherence. Arch Ophthalmol. 2012;130(3):306-311.
57. Peterson NB, Dwyer KA, Mulvaney SA, Dietrich MS, Rothman RL. The influence of health literacy on colorectal cancer screening knowledge, beliefs and behavior. J Natl Med Assoc. 2007;99(10):1105-1112.
58. Peterson PN, Shetterly SM, Clarke CL, et al. Health literacy and outcomes among patients with heart failure. JAMA. 2011;305(16):1695-1701.
59. Rosas-salazar C, Apter AJ, Canino G, Celedón JC. Health literacy and asthma. J Allergy Clin Immunol. 2012;129(4):935-942.
60. Song L, Mishel M, Bensen JT, et al. How does health literacy affect quality of life among men with newly diagnosed clinically localized prostate cancer? Findings from the North Carolina-Louisiana Prostate Cancer Project (PCaP). Cancer. 2012;118(15):3842-3851.
61. Williams MV, Davis T, Parker RM, Weiss BD. The role of health literacy in patient-physician communication. Fam Med. 2002;34(5):383-389.
62. Badarudeen S, Sabharwal S. Assessing readability of patient education materials: current role in orthopaedics. Clin Orthop. 2010;468(10):2572-2580.
63. Doak CC, Doak LG, Friedell GH, Meade CD. Improving comprehension for cancer patients with low literacy skills: strategies for clinicians. CA Cancer J Clin. 1998;48(3):151-162.
64. Doak CC, Doak LG, Root JH. Teaching Patients With Low Literacy Skills. 2nd ed. Philadelphia, PA: JB Lippincott Company; 1996.
65. Kemp EC, Floyd MR, McCord-Duncan E, Lang F. Patients prefer the method of “tell back-collaborative inquiry” to assess understanding of medical information. J Am Board Fam Med. 2008;21(1):24-30.
66. Kripalani S, Bengtzen R, Henderson LE, Jacobson TA. Clinical research in low-literacy populations: using teach-back to assess comprehension of informed consent and privacy information. IRB. 2008;30(2):13-19.
67. Centers for Disease Control and Prevention. Simply Put: A Guide For Creating Easy-to-Understand Materials. 3rd ed. Atlanta, GA: Strategic and Proactive Communication Branch, Centers for Disease Control and Prevention, US Dept of Health and Human Services; 2009.
68. National Institutes of Health, National Cancer Institute. Clear & Simple: Developing Effective Print Materials for Low-Literate Readers. Devcompage website. http://devcompage.com/wp-content/uploads/2010/12/Clear_n_Simple.pdf Published March 2, 1998. Accessed December 1, 2014.
69. Weiss BD. Health Literacy and Patient Safety: Help Patients Understand. 2nd ed. Chicago, IL: American Medical Association and AMA Foundation; 2007:35-41.
70. Dale E, O’Rourke J. The Living Word Vocabulary. Newington, CT: World Book-Childcraft International, 1981.
71. Word suggestions. Plain Language website. www.plainlanguage.gov/howto/wordsuggestions/index.cfm. Accessed November 18, 2014.
72. Rivers K. Initiative aims to enhance patient communication materials. Reporter: Vanderbilt University Medical Center’s Weekly Newspaper. April 28, 2011. http://www.mc.vanderbilt.edu/reporter/index.html?ID=10649. Accessed November 18, 2014.
73. Ewing’s sarcoma. OrthoInfo. American Academy of Orthopaedic Surgeons website. http://orthoinfo.aaos.org/topic.cfm?topic=A00082. Last reviewed September 2011. Accessed November 18, 2014.
1. Piredda M, Rocci L, Gualandi R, Petitti T, Vincenzi B, De Marinis MG. Survey on learning needs and preferred sources of information to meet these needs in Italian oncology patients receiving chemotherapy. Eur J Oncol Nurs. 2008;12(2):120-126.
2. Fernsler JI, Cannon CA. The whys of patient education. Semin Oncol Nurs. 1991;7(2):79-86.
3. Glimelius B, Birgegård G, Hoffman K, Kvale G, Sjödén PO. Information to and communication with cancer patients: improvements and psychosocial correlates in a comprehensive care program for patients and their relatives. Patient Educ Couns. 1995;25(2):171-182.
4. Harris KA. The informational needs of patients with cancer and their families. Cancer Pract. 1998;6(1):39-46.
5. Jensen AB, Madsen B, Andersen P, Rose C. Information for cancer patients entering a clinical trial--an evaluation of an information strategy. Eur J Cancer. 1993;29A(16):2235-2238.
6. Wells ME, McQuellon RP, Hinkle JS, Cruz JM. Reducing anxiety in newly diagnosed cancer patients: a pilot program. Cancer Pract. 1995;3(2):100-104.
7. Diaz JA, Griffith RA, Ng JJ, Reinert SE, Friedmann PD, Moulton AW. Patients’ use of the Internet for medical information. J Gen Intern Med. 2002;17(3):180-185.
8. Fox S, Duggan M. Health Online 2013. Pew Research Center’s Internet and American Life Project. www.pewinternet.org/~/media//Files/Reports/PIP_HealthOnline.pdf. Published January 15, 2013. Accessed November 18. 2014.
9. Schwartz KL, Roe T, Northrup J, Meza J, Seifeldin R, Neale AV. Family medicine patients’ use of the Internet for health information: a MetroNet study. J Am Board Fam Med. 2006;19(1):39-45.
10. Basch EM, Thaler HT, Shi W, Yakren S, Schrag D. Use of information resources by patients with cancer and their companions. Cancer. 2004;100(11):2476-2483.
11. Huang GJ, Penson DF. Internet health resources and the cancer patient. Cancer Invest. 2008;26(2):202-207.
12. Metz JM, Devine P, Denittis A, et al. A multi-institutional study of Internet utilization by radiation oncology patients. Int J Radiat Oncol Biol Phys. 2003;56(4):1201-1205.
13. Peterson MW, Fretz PC. Patient use of the internet for information in a lung cancer clinic. Chest. 2003;123(2):452-457.
14. Satterlund MJ, McCaul KD, Sandgren AK. Information gathering over time by breast cancer patients. J Med Internet Res. 2003;5(3):e15.
15. Tustin N. The role of patient satisfaction in online health information seeking. J Health Commun. 2010;15(1):3-17.
16. Van de Poll-Franse LV, Van Eenbergen MC. Internet use by cancer survivors: current use and future wishes. Support Care Cancer. 2008;16(10):1189-1195.
17. Ziebland S, Chapple A, Dumelow C, Evans J, Prinjha S, Rozmovits L. How the internet affects patients’ experience of cancer: a qualitative study. BMJ. 2004;328(7439):564.
18. Committee on Health Literacy, Board on Neuroscience and Behavioral Health, Institute of Medicine. Nielsen-Bohlman L, Panzer AM, Kindig DA, eds. Health Literacy: A Prescription to End Confusion. Washington, DC: National Academies Press; 2004. Available at: www.nap.edu/openbook.php?record_id=10883. Accessed November 18, 2014.
19. Kutner M, Greenberg E, Ying J, Paulsen C. The Health Literacy of America’s Adults: Results from the 2003 National Assessment of Adult Literacy. NCES 2006-483. US Department of Education. Washington, DC: National Center for Education Statistics; 2006. Available at: www.nces.ed.gov/pubs2006/2006483.pdf. Accessed November 18, 2014.
20. How to write easy-to-read health materials. MedlinePlus website. www.nlm.nih.gov/medlineplus/etr.html. Updated February 13, 2013. Accessed November 18, 2014.
21. Ellimoottil C, Polcari A, Kadlec A, Gupta G. Readability of websites containing information about prostate cancer treatment options. J Urol. 2012;188(6):2171-2175.
22. Friedman DB, Hoffman-Goetz L, Arocha JF. Health literacy and the World Wide Web: comparing the readability of leading incident cancers on the Internet. Med Inform Internet Med. 2006;31(1):67-87.
23. Hoppe IC. Readability of patient information regarding breast cancer prevention from the Web site of the National Cancer Institute. J Cancer Educ. 2010;25(4):490-492.
24. Misra P, Kasabwala K, Agarwal N, Eloy JA, Liu JK. Readability analysis of internet-based patient information regarding skull base tumors. J Neurooncol. 2012;109(3):573-580.
25. Stinson JN, White M, Breakey V, et al. Perspectives on quality and content of information on the internet for adolescents with cancer. Pediatr Blood Cancer. 2011;57(1):97-104.
26. Badarudeen S, Sabharwal S. Readability of patient education materials from the American Academy of Orthopaedic Surgeons and Pediatric Orthopaedic Society of North America web sites. J Bone Joint Surg Am. 2008;90(1):199-204.
27. Bluman EM, Foley RP, Chiodo CP. Readability of the Patient Education Section of the AOFAS Website. Foot Ankle Int. 2009;30(4):287-291.
28. Polishchuk DL, Hashem J, Sabharwal S. Readability of online patient education materials on adult reconstruction Web sites. J Arthroplasty. 2012;27(5):716-719.
29. Sabharwal S, Badarudeen S, Unes Kunju S. Readability of online patient education materials from the AAOS web site. Clin Orthop. 2008;466(5):1245-1250.
30. Vives M, Young L, Sabharwal S. Readability of spine-related patient education materials from subspecialty organization and spine practitioner websites. Spine. 2009;34(25):2826-2831.
31. Wang SW, Capo JT, Orillaza N. Readability and comprehensibility of patient education material in hand-related web sites. J Hand Surg Am. 2009;34(7):1308-1315.
32. Lam CG, Roter DL, Cohen KJ. Survey of quality, readability, and social reach of websites on osteosarcoma in adolescents. Patient Educ Couns. 2013;90(1):82-87.
33. Tumors. Quinn RH, ed. OrthoInfo. American Academy of Orthopaedic Surgeons website. http://orthoinfo.aaos.org/menus/tumors.cfm. Accessed November 18, 2014.
34. Sarcoma specialists. Sarcoma Alliance website. sarcomaalliance.org/sarcoma-centers. Accessed November 18, 2014.
35. LaCoursiere SP, Knobf MT, McCorkle R. Cancer patients’ self-reported attitudes about the Internet. J Med Internet Res. 2005;7(3):e22.
36. Test your document’s readability. Microsoft Office website. office.microsoft.com/en-us/word-help/test-your-document-s-readability-HP010148506.aspx. Accessed November 18, 2014.
37. Kincaid JP, Fishburne RP, Rogers RL, Chissom BS. Derivation of new readability formulas (Automated Readability Index, Fog Count and Flesch Reading Ease Formula) for Navy enlisted personnel. Naval Technical Training Command. Research Branch Report 8-75. www.dtic.mil/dtic/tr/fulltext/u2/a006655.pdf. Published February 1975. Accessed November 18, 2014.
38. Coleman M, Liau TL. A computer readability formula designed for machine scoring. J Appl Psychol. 1975;60(2):283-284.
39. Fry E. Fry’s readability graph: clarifications, validity, and extension to Level 17. J Reading. 1977;21(3):242-252.
40. Chall JS, Dale E. Manual for the New Dale-Chall Readability Formula. Cambridge, MA: Brookline Books; 1995.
41. Gunning R. The Technique of Clear Writing. Rev. ed. New York, NY: McGraw-Hill; 1968.
42. Powers RD, Sumner WA, Kearl BE. A recalculation of four adult readability formulas. J Educ Psychol. 1958;49(2):99-105.
43. McLaughlin GH. SMOG grading—a new readability formula. J Reading. 1969;22,639-646.
44. Raygor L. The Raygor readability estimate: a quick and easy way to determine difficulty. In: Pearson PD, Hansen J, eds. Reading Theory, Research and Practice. Twenty-Sixth Yearbook of the National Reading Conference. Clemson, SC: National Reading Conference Inc; 1977:259-263.
45. Krempec J, Hall J, Biermann JS. Internet use by patients in orthopaedic surgery. Iowa Orthop J. 2003;23:80-82.
46. Beall MS, Golladay GJ, Greenfield ML, Hensinger RN, Biermann JS. Use of the Internet by pediatric orthopaedic outpatients. J Pediatr Orthop. 2002;22(2):261-264.
47. Beall MS, Beall MS, Greenfield ML, Biermann JS. Patient Internet use in a community outpatient orthopaedic practice. Iowa Orthop J. 2002;22:103-107.
48. Davis TC, Bocchini JA, Fredrickson D, et al. Parent comprehension of polio vaccine information pamphlets. Pediatrics. 1996;97(6 Pt 1):804-810.
49. Apter AJ, Wan F, Reisine S, et al. The association of health literacy with adherence and outcomes in moderate-severe asthma. J Allergy Clin Immunol. 2013;132(2):321-327.
50. Baker DW, Parker RM, Williams MV, Clark WS. Health literacy and the risk of hospital admission. J Gen Intern Med. 1998;13(12):791-798.
51. Berkman ND, Sheridan SL, Donahue KE, Halpern DJ, Crotty K. Low health literacy and health outcomes: an updated systematic review. Ann Intern Med. 2011;155(2):97-107.
52. Bevan JL, Pecchioni LL. Understanding the impact of family caregiver cancer literacy on patient health outcomes. Patient Educ Couns. 2008;71(3):356-364.
53. Corey MR, St Julien J, Miller C, et al. Patient education level affects functionality and long term mortality after major lower extremity amputation. Am J Surg. 2012;204(5):626-630.
54. Davis TC, Arnold C, Berkel HJ, Nandy I, Jackson RH, Glass J. Knowledge and attitude on screening mammography among low-literate, low-income women. Cancer. 1996;78(9):1912-1920.
55. Davis TC, Williams MV, Marin E, Parker RM, Glass J. Health literacy and cancer communication. CA Cancer J Clin. 2002;52(3):134-149.
56. Freedman RB, Jones SK, Lin A, Robin AL, Muir KW. Influence of parental health literacy and dosing responsibility on pediatric glaucoma medication adherence. Arch Ophthalmol. 2012;130(3):306-311.
57. Peterson NB, Dwyer KA, Mulvaney SA, Dietrich MS, Rothman RL. The influence of health literacy on colorectal cancer screening knowledge, beliefs and behavior. J Natl Med Assoc. 2007;99(10):1105-1112.
58. Peterson PN, Shetterly SM, Clarke CL, et al. Health literacy and outcomes among patients with heart failure. JAMA. 2011;305(16):1695-1701.
59. Rosas-salazar C, Apter AJ, Canino G, Celedón JC. Health literacy and asthma. J Allergy Clin Immunol. 2012;129(4):935-942.
60. Song L, Mishel M, Bensen JT, et al. How does health literacy affect quality of life among men with newly diagnosed clinically localized prostate cancer? Findings from the North Carolina-Louisiana Prostate Cancer Project (PCaP). Cancer. 2012;118(15):3842-3851.
61. Williams MV, Davis T, Parker RM, Weiss BD. The role of health literacy in patient-physician communication. Fam Med. 2002;34(5):383-389.
62. Badarudeen S, Sabharwal S. Assessing readability of patient education materials: current role in orthopaedics. Clin Orthop. 2010;468(10):2572-2580.
63. Doak CC, Doak LG, Friedell GH, Meade CD. Improving comprehension for cancer patients with low literacy skills: strategies for clinicians. CA Cancer J Clin. 1998;48(3):151-162.
64. Doak CC, Doak LG, Root JH. Teaching Patients With Low Literacy Skills. 2nd ed. Philadelphia, PA: JB Lippincott Company; 1996.
65. Kemp EC, Floyd MR, McCord-Duncan E, Lang F. Patients prefer the method of “tell back-collaborative inquiry” to assess understanding of medical information. J Am Board Fam Med. 2008;21(1):24-30.
66. Kripalani S, Bengtzen R, Henderson LE, Jacobson TA. Clinical research in low-literacy populations: using teach-back to assess comprehension of informed consent and privacy information. IRB. 2008;30(2):13-19.
67. Centers for Disease Control and Prevention. Simply Put: A Guide For Creating Easy-to-Understand Materials. 3rd ed. Atlanta, GA: Strategic and Proactive Communication Branch, Centers for Disease Control and Prevention, US Dept of Health and Human Services; 2009.
68. National Institutes of Health, National Cancer Institute. Clear & Simple: Developing Effective Print Materials for Low-Literate Readers. Devcompage website. http://devcompage.com/wp-content/uploads/2010/12/Clear_n_Simple.pdf Published March 2, 1998. Accessed December 1, 2014.
69. Weiss BD. Health Literacy and Patient Safety: Help Patients Understand. 2nd ed. Chicago, IL: American Medical Association and AMA Foundation; 2007:35-41.
70. Dale E, O’Rourke J. The Living Word Vocabulary. Newington, CT: World Book-Childcraft International, 1981.
71. Word suggestions. Plain Language website. www.plainlanguage.gov/howto/wordsuggestions/index.cfm. Accessed November 18, 2014.
72. Rivers K. Initiative aims to enhance patient communication materials. Reporter: Vanderbilt University Medical Center’s Weekly Newspaper. April 28, 2011. http://www.mc.vanderbilt.edu/reporter/index.html?ID=10649. Accessed November 18, 2014.
73. Ewing’s sarcoma. OrthoInfo. American Academy of Orthopaedic Surgeons website. http://orthoinfo.aaos.org/topic.cfm?topic=A00082. Last reviewed September 2011. Accessed November 18, 2014.