Evaluating Pterygium Severity a Survey of Corneal Specialists

Evaluating Pterygium Severity A Survey of Corneal Specialists

J. Daniel Twelker, O.D., F.A.A.O., Ian L. Bailey, M.S., O.D., Mark J. Mannis, M.D., F.A.C.S., and William A. Satariano, Ph.D.

Purpose. Accurate and reliable evaluation techniques are essential mon in the periequatorial region ± 40° latitude.3 The primary risk for clinical and epidemiologic studies. This survey of corneal spe- factor for the development of pterygium is believed to be increased cialists was designed to lay a foundation for the further develop- exposure to ultraviolet light,4–6 although other risk factors have ment of methods for evaluating and staging pterygium. Methods. been implicated. There are several theories of the pathogenesis of In a self-administered, mailed questionnaire, 213 corneal special- pterygium.7–12 Further clinical and epidemiologic studies of pter- ists rated the importance of nine symptoms, nine signs, and nine ygium patients could help us to better understand its etiology and clinical tests for the severity of primary pterygium. Severity was defined as the present need for surgical intervention. Results. The natural history. However, such studies would be improved if there most important factors for determining primary pterygium severity were better-defined methods of evaluation. This survey lays the were the extent of encroachment onto the cornea, decreased visual foundation for developing criteria for evaluating pterygia by ask- acuity, restricted ocular motility, and increased rate of growth. ing corneal specialists which symptoms, signs, and tests they con- Many patient symptoms were rated as moderately to highly im- sider important in determining the severity of primary pterygium. portant. The questionnaire was shown to have good response reliability by test–retest comparisons. Cronbach’s ␣ was 0.89, which indicates very good internal consistency reliability. Conclusion. MATERIALS AND METHODS The survey identifies the priorities of experts in determining the severity of pterygium. More precise and clearly defined evaluation We developed a short, self-administered confidential question- methods will enhance future clinical and epidemiologic studies of naire, which included two sections. The first section was a 27-item pterygium. The ranked list of pterygium signs, symptoms, and tests list of nine symptoms, nine signs, and nine clinical tests related to can serve as a guide for developing pterygium evaluation methods primary pterygium. We selected these 27 items from a review of in the future. There is a need for a method that accurately and precisely quantifies the distance of pterygium encroachment onto the literature, consultation with several corneal specialists who the cornea and the pterygium progression rate. Furthermore, there were not included in the survey sample, and a 36-item pilot survey is a need for an assessment of patient symptoms. completed by primary eye-care practitioners. We asked corneal Key Words: Cornea–Corneal specialist—Evaluation—Measure- specialists to rate the importance of each item to the severity of ment—Pterygium. primary pterygium. Severity was defined as the present need for surgical intervention. The rating scale ranged from 1 to 10, with 1 being “not important” and 10 being “extremely important.” The second section solicited information about the respondents and A pterygium is a raised, triangular-shaped growth of abnormal included years of practice, mode of practice, and other demo- ocular tissue that extends horizontally from the bulbar conjunctiva, graphic information. across the limbus, and onto the cornea, usually from the nasal The University of California, Berkeley, Committee for the Pro- side.1 As this abnormal tissue invades the superficial cornea, it tection of Human Subjects reviewed and approved the protocol for destroys Bowman’s layer through fibrovascular ingrowth.2 Clini- this study. cal manifestations of pterygium can include increased regular and We mailed the questionnaire and a self-addressed, stamped re- irregular astigmatism, corneal-surface irregularities, and decreased turn envelope to 300 members of the Castroviejo Society, an in- visual acuity. Patients often report blur, distortion, redness, tearing, ternational organization of corneal surgeons. The 300 corneal spe- foreign-body sensation, and poor cosmesis. cialists represent the entire membership of the Castroviejo Society, Pterygia can be found throughout the world, but are more com- except for one member who was excluded because he is a co- investigator. Four weeks after the initial mailing, we sent a reminder postcard to all nonrespondents. Six weeks later, we sent Submitted April 14, 1999. Revision received June 23, 1999. Accepted July 6, 1999. another identical questionnaire and self-addressed, stamped return From the School of Optometry, University of California, Berkeley, envelope to the remaining nonrespondents, followed 3 weeks later Berkeley (J.D.T., I.L.B.); Department of Ophthalmology, University of by another reminder postcard. After 20 weeks, 213 (71%) corneal California, Davis, Davis (M.J.M.); and School of Public Health, University specialists had responded to the questionnaire. of California, Berkeley, Berkeley (W.A.S.), California, U.S.A. Address correspondence and reprint requests to Dr. J.D. Twelker, School To evaluate the survey’s test–retest repeatability, we mailed an of Optometry, University of California, Berkeley, 360 Minor Hall, Berke- abridged version of the survey to 60 randomly selected respon- ley, CA 94720-2020. E-mail: [email protected] dents several weeks after they had returned their completed ques-

292 EVALUATING PTERYGIUM SEVERITY 293 tionnaires. Forty-five (75%) respondents completed and returned third column presents the median of the responses, but this does the second questionnaire. not convey the richness of information that was gathered in the survey. The fourth column of Table 2 presents the Rasch estimate in log-odds units, or logits. We used BIGSTEPS,14 a Rasch-model RESULTS computer program, to obtain the Rasch estimate of item impor- 15 Profile of Respondents tance. The Rasch model uses a probabilistic model based on the difference between importance of item and rater’s decision crite- The mean number of years as a corneal specialist was 16 years, ria.16 BIGSTEPS uses an iterative estimation process to construct with a standard deviation of 8 years. Fifty-nine percent reported the Rasch estimate from the responses of a set of persons to a set working primarily in private-practice settings, 27% in teaching of items. Our data fit the Rasch model well, resulting in estimates hospitals, and 11% in research. Corneal specialists reported seeing of item importance that lie on an interval scale. a mean of 55 primary pterygium patients per year, with a standard The advantage of the Rasch estimate is that the distance between deviation of 68 patients per year. The median was 30 patients per each item estimate is meaningful. For example, because “de- year, and the range extended from four patients per year in the creased best corrected VA” was 1.14 logits and “increased distor- Northeastern United States to 500 in India, with 22% of the re- tion” was 0.57 logits, ‘decreased best corrected VA” was judged to spondents seeing >100 primary pterygium patients per year. be about twice as important as “increased distortion.” For this Of the 300 corneal specialists on the mailing list, 10 (3%) prac- survey, the mean, median, and Rasch estimates all led to similar ticed in the Northwestern United States, 43 (14%) in the South- conclusions. western United States, 134 (45%) in the Northeastern United We separated the responses into five groups according to geo- States, 77 (26%) in the Southeastern United States, and 36 (12%) graphic area and compared the responses for each of the 27 indi- in 19 countries outside of the United States. The return rates were cators of pterygium severity. For 24 of the 27 items, there was no similar among the geographic regions, and were 70, 81, 70, 70, and difference in the response between the five groups (p value ranged 64%, respectively. Although the return rate was highest in the between 0.18 and 0.96, Kruskal–Wallis equality of populations Southwestern United States (81%) and lowest in the 19 countries rank test). For the item “abnormal corneal topography,” there was outside of the United States (64%), this difference was not statis- borderline statistical significance for a difference between groups ס p ;3.08 ס tically significant at the 95% confidence level (␹2 Kruskal–Wallis equality of populations rank ,0.06 ס p value) 0.08). test). The corneal specialists of the Northwestern United States The corneal specialists reported performing a mean of 16 sur- appeared to rate the importance of “abnormal corneal topography” gical interventions for primary pterygium per year, with a standard and median ,10 ס (higher than the other four groups [median (NW deviation of 21 per year. The distribution was skewed, with a p < 0.05 for all pairwise comparisons, rank-sum ;8 ס (all others) median of 10 surgeries per year with a range from 0 in several test]. For the item “increased size by patient report,” there was locations to 160 in India. The most commonly reported surgical borderline statistical significance for a difference between groups procedure for primary pterygium was excision and conjunctival Kruskal–Wallis equality of populations rank ,0.06 ס p value) transplant (58%), followed by excision and sliding conjunctival test). The corneal specialists of the 19 other countries appeared to flap (19%), simple excision (13%), excision and beta radiation rate the importance of “increased size by patient report” lower than (4%), excision and mitomycin C (4%), and other surgical proce- -and me ,6 ס (the other four groups [median (19 other countries dures (2%). Table 1 shows the proportion of respondents that per- ,p values < 0.05 for all pairwise comparisons ;8 ס (dian (all others formed each type of surgical procedure, separated into the five rank-sum test]. For the item “pterygium inflammation,” there was geographic regions. ס a difference between the responses of the five groups (p value 0.01, Kruskal–Wallis equality of populations rank test). The cor- Indicators of Pterygium Severity neal specialists of the 19 other countries rated the importance of Table 2 shows each item’s importance ranked from highest to “pterygium inflammation” lower than the other four groups [me- median ;7 ס (median (SW, NE, SE ;6 ס (lowest. The first and second columns present the item mean and dian (19 other countries p values < 0.05 for all pairwise comparisons, rank-sum ;9 ס (standard deviations. The mean and standard deviation are not nec- (NW essarily the appropriate summary statistics for data on a “1–10” test]. rating scale, which is an ordinal scale. According to Stevens,13 parametric statistics such as means and standard deviations should Survey Reliability not be used with ordinal scales, for these statistics imply a knowl- Table 3 shows the results of the test–retest repeatability study. edge of something more than the relative rank-order of data. The Eleven of 12 items showed excellent correlation between the first

TABLE 1. Type of surgical procedure for the excision of primary pterygium, separated by geographic region

Proportion of respondents in each region Other Procedure NW SW NE SE countries Simple excision 0.29 0.11 0.10 0.13 0.22 Excision and sliding conjunctival flap 0.43 0.14 0.18 0.20 0.17 Excision and conjunctival transplant 0.14 0.57 0.63 0.52 0.48 Excision and beta-radiation 0.00 0.06 0.04 0.00 0.09 Excision and mitomycin C 0.00 0.03 0.02 0.07 0.04 Other procedure 0.00 0.03 0.01 0.04 0.00

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TABLE 2. Item importance from highest to lowest

Mean Standard Median Rasch score Items rating deviation rating (logits) 1. Length of encroachment 9.33 1.14 10 1.18 2. Decreased best-corrected VA 9.30 1.42 10 1.14 3. Restricted ocular motility 9.15 1.47 10 0.99 4. Increased rate of growth 8.80 1.48 9 0.72 5. Increased distortion 8.52 2.06 9 0.57 6. Increased astigmatism 8.35 1.59 9 0.48 7. Increased blur 8.20 2.19 9 0.40 8. Distortion of keratometry mires 7.74 2.05 8 0.21 9. Change in refractive error 7.73 1.78 8 0.21 10. Increased size by patient report 7.48 1.94 8 0.10 11. Abnormal corneal topography 7.38 2.27 8 0.07 12. Pterygium area 6.96 1.98 7 −0.06 13. Pterygium inflammation 6.94 1.87 7 −0.06 14. Increased ocular discomfort 6.76 1.98 7 −0.12 15. Increased photophobia 6.47 2.17 7 −0.21 16. Pterygium thickness 6.31 2.09 7 −0.26 17. Incr. foreign-body sensation 6.30 2.06 6 −0.25 18. Poor cosmesis by patient report 6.29 2.18 7 −0.27 19. Pterygium vascularization 6.12 2.16 6 −0.31 20. Incr. redness by patient report 6.05 2.11 6 −0.32 21. Increased burning 5.94 2.16 6 −0.35 22. Fluorescein dye staining 5.50 2.23 6 −0.47 23. Rose bengal dye staining 5.12 2.38 5 −0.56 24. Abnormal tear-film tests 5.02 2.26 5 −0.58 25. Subepithelial infiltrates at cap 4.96 2.48 5 −0.63 26. Decreased translucency 4.73 2.35 5 −0.66 27. Presence of Stocker line 3.70 2.46 3 −0.96 and second response (p value <0.05, Spearman rank correlation We explored the possibility that respondents with more experi- test). Only “length of encroachment onto cornea” showed a statis- ence in pterygium evaluation might show different response char- tically significant difference between the two responses (Spearman acteristics. We separated the 213 respondents into three subgroups, Although it is statistically significant, 121 who reported examining 0–50 pterygium patients a year, 46 .(0.18 ס p value ;0.21 ס ␳ this difference does not have practical significance for this survey, who reported examining 51–100 patients a year, and 38 respon- given that the median of the first response is 10 and the second dents who reported examining >100 patients a year. We calculated response is 9, which both indicate ratings of “extremely impor- the median for all three subgroups for each of the 27 variables. tant.” Moreover, this result is probably due more to a “ceiling There was no difference between the three levels of experience in effect” of the 1–10 response scale rather than a lack of correspon- evaluating pterygium (p values >0.05 for all 27 parameters, dence in the respondent’s opinions. Based on these results, the Kruskal–Wallis equality of populations rank test). It appears that, survey appears to be a reliable instrument. regardless of the amount of reported experience in examining pter- Cronbach’s coefficient ␣ measures internal consistency reliabil- ygium patients, the corneal specialists were consistent in their ity among the 27 items to form a single scale of importance. The ratings. Cronbach’s ␣ for this study was 0.89, as computed by Stata statistics and data-analysis package,17 indicating that an estimated DISCUSSION 11% of the observed variance is due to error in measurement. This indicates that the survey shows very good internal consistency The most commonly reported surgical procedures for the exci- reliability. sion of primary pterygium were excision and conjunctival trans-

TABLE 3. Test–retest repeatability

Medians Spearman rank correlations Items 1st 2nd ␳ p Value Increased blur 9 8 0.53 <0.01 Increased distortion 9 8 0.44 <0.01 Increased burning 6 6 0.69 <0.01 Poor cosmesis by patient report 7 7 0.57 <0.01 Length of encroachment 10 9 0.21 0.18a Pterygium inflammation 7 7 0.45 <0.01 Presence of Stocker line 3 3 0.60 <0.01 Subepithelial infiltrates at cap 5 4 0.40 <0.01 Decreased best corrected VA 10 9 0.58 <0.01 Abnormal tear-film tests 5 5 0.55 <0.01 Fluorescein dye staining 6 6 0.43 <0.01 Increased rate of growth 9 9 0.34 <0.05

a For “length of encroachment,” the correlation between the first and second ratings was not statistically significant at the 95% confidence level, but probably due more to the truncated 1–10 response scale than to a lack of correlation between ratings.

Cornea, Vol. 19, No. 3, 2000 EVALUATING PTERYGIUM SEVERITY 295 plant (58%), excision and sliding conjunctival flap (19%), and All of these parameters can be evaluated by well-established in- simple excision (13%). Beta radiation and mitomycin C were not strumentation and methods. commonly used. In 1991, ophthalmologists who practice in Inflammation and vascularization were rated moderately impor- Queensland, Australia, most commonly reported using simple ex- tant to primary pterygium severity. These parameters are more cision with the “mobilisation of conjunctiva and suturing conjunc- difficult to assess. A grading protocol using standardized photo- tival free edges together plus thiotepa” (23%).18 Simple excision graphic plates might make it easier to assess these parameters, and (21%) and simple excision plus thiotepa (15%) also were com- better assessment methods could possibly elevate the importance monly reported. In 1998, ophthalmologists who practice in Victo- of these parameters. ria, Australia, most commonly reported using simple “excision Translucency of the lesion was rated of low importance in leaving bare sclera followed by beta radiation” (57%).19 Simple evaluating pterygium severity. Interestingly, Tan and co-workers24 excision leaving bare sclera (15%) and excision and autologous found that nontranslucency, or fleshiness of the pterygium tissue, conjunctival transplantation (11%) also were commonly reported. is a significant risk factor for recurrence after bare sclera excision. As presented in Table 2, “length of encroachment” was rated the They describe a simple grading system to classify pterygium mor- most important indicator of pterygium severity. The closer the phology based on the relative translucency of the pterygium tissue. pterygium approaches the center of the cornea and pupillary area, Based on their reports, relative translucency still merits attention. the more likely the patient will have visual consequences, whether As an indicator of pterygium severity, corneal specialists rated they be from induced astigmatism, corneal irregularities, or direct tear-film tests relatively low in importance. Part of the reason for obscuration of the pupil. This result is consistent with the current this may that the results of common tear-film tests such as Shirm- scientific literature. Lin and Stern20 showed a significant correla- er’s and tear break-up time are not considered to be reproduc- tion between the extension of pterygium onto the cornea and the ible.25,26 A recent study, however, reported that two noninvasive amount of induced astigmatism. Ophthalmologists in Queensland, tear break-up methods (the HIR-CAL grid-modified keratometer Australia, reported the pterygium size as the most important indi- and the Mengher-Tonge xeroscope) were repeatable.27 However, cation for surgical treatment of pterygium.18 Ophthalmologists in these two methods are not commonly used in clinical settings. Victoria, Australia, reported that the feature most likely to lead to The association between pterygium and dry eye is equivocal. a change in treatment was the size of the pterygium.19 Taylor28 performed Schirmer test, rose bengal staining, examina- “Decreased best-corrected visual acuity,” secondary to pteryg- tion of the marginal tear strip, and tear break-up time on 30 Aus- ium, was rated the second most important parameter of pteryg- tralians of Aboriginal descent and compared the results with those ium severity. This is not surprising, given that visual acuity is of 101 Australians of European descent. The tests failed to show almost always measured, is used to monitor disease progression, any association between tear-film abnormalities and the presence and is seen as a primary indicator of the patient’s functional status. of pterygium. Goldberg and David29 tested both patients with pter- There are already well-documented methods for measuring visual ygia and controls in the Bantu population of South Africa. They acuity.21 concluded that Schirmer’s and fluorescein break-up time tests The third most important indicator of pterygium severity was were inadequate. Their results did not support an association be- “restricted ocular motility,” secondary to pterygium. We should tween pterygium and dry eye. Kadayifcilar et al.,30 on the other note, however, that a pterygium must be quite severe to restrict hand, found significant abnormalities in the tear break-up time, ocular motility, and it is rare for a patient to progress to this mucus fern patterns, and marginal tear strip in eyes with pter- advanced stage. There are well-described methods of assessing ygium. ocular motility.22 However, this measure will probably not be relevant to the assessment of most cases of pterygium. The fourth most important indicator of pterygium severity was CONCLUSION “increased rate of growth.” Pterygium progression rate is certainly a marker of pterygium activity. The progression rate influences The results of this survey demonstrate that corneal specialists clinical decisions about the frequency of follow-up examination are in good agreement about which signs, symptoms, and clinical visits, medical treatment, and surgical intervention. Good quanti- tests are most important in the evaluation of pterygium severity. fication of progression rate demands high precision in the mea- For many of the parameters that were rated moderately to highly surement of the length of encroachment onto the cornea. important to the severity of pterygium severity, there are no well- All of the patient symptoms due to pterygium (patient report of defined methods for quantifying these clinical findings. To en- increased distortion, increased blur, increased size, increased ocu- hance epidemiologic and natural history studies of pterygium, lar discomfort, increased photophobia, increased foreign-body sen- there should be convenient, accurate, and reliable systems of mea- sation, poor cosmesis, increased redness, and increased burning) surement. In particular, accurate and precise measurement meth- were rated moderately to highly important to pterygium severity. ods should be used for determining the extent of encroachment and Assessment of patients’ symptoms can be a valuable evaluation the rate of progression of pterygium and for the evaluation of tool. Investigators of other anterior-segment diseases, such as dry patient symptoms. Continuing efforts to develop and standardize eye and keratoconjunctivitis,23 found symptom-based question- evaluation methods for pterygium should lead to a better under- naires to be very helpful. Ophthalmologists in Queensland, Aus- standing of its etiology and prevention. tralia, reported that symptoms due to pterygium were among the most important indications for surgical treatment.18 Acknowledgment: We thank the corneal specialists of the Castroviejo Society. We appreciate the statistical consultation services of Steve Moore Increased astigmatism, distortion of keratometry mires, change of the American Academy of Ophthalmology. This research was supported in refractive error, and abnormal corneal topography were all rated by the National Eye Institute Grant K23-EY00372 (National Institutes of highly important to determining the severity of primary pterygium. Health, Bethesda, MD).

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REFERENCES 16. Wright BD, Stone MH. Best test design: Rasch measurement. Chi- cago: MESA Press, 1979. 1. Adamis AP, Starck T, Kenyon KR. The management of pterygium. 17. Stata, version 6.0. Stata Corporation, 702 University Drive East, Col- Ophthalmol Clin North Am 1990;3:611. lege Station, TX 77840, U.S.A. Copyright 1984–1999. 2. Jaros PA, DeLuise VP. Pinguecula and pterygia. Surv Ophthalmol 18. Sebban A, Hirst LW. Treatment of pterygia in Queensland. Australian 1988;33:41–9. and New Zealand. J Ophthalmol 1991;19:123–7. 3. Cameron ME. Pterygium throughout the world. Springfield, IL: 19. Snibson GR, Luu CD, Taylor HR. Pterygium surgery in Victoria: a Thomas, 1965. survey of ophthalmologists. AustNZJOphthalmol 1998;26:271–6. 4. Mackenzie FD, Hirst LW, Battistutta D, Green A. Risk analysis in the 20. Lin A, Stern G. Correlation between pterygium size and induced cor- development of pterygia. Ophthalmology 1992;99:1056–61. neal astigmatism. Cornea 1998;17:28–30. 5. Moran DJ, Hollows FC. Pterygium and ultraviolet radiation: a positive 21. Ferris FL, Bailey IL. Standardizing the measurement of visual acuity correlation. Br J Ophthalmol 1984;68:343–6. for clinical research studies. Ophthalmology 1996;103:181–2. 6. Taylor HR, West SK, Rosenthal FS, Munoz B, Newland HS, Emmett 22. Jampolsky AA. Simplified approach to strabismus diagnosis. In: EA. Corneal changes associated with chronic UV irradiation. Arch Burian HM, Dunlap EA, Dyer JA, et al. eds. Symposium on strabis- Ophthalmol 1989;107;1481–4. mus, transactions of the New Orleans Academy of Ophthalmology. St. 7. Taylor HR. Aetiology of climatic droplet keratopathy and pterygium. Louis: CV Mosby, 1971;49–50. Br J Ophthalmol 1980;64:154–63. 23. McMonnies CW. Key questions in a dry eye history. JAmOptom 8. Pinkerton OD, Hokama Y, Shigemura LA. Immunologic basis for the Assoc 1986;57:512–7. pathogenesis of pterygium. Am J Ophthalmol 1984;98:225–8. 24. Tan DTH, Chee SP, Dear KBG, Lim ASM. Effect of pterygium mor- 9. Hill JC, Maske R. Pathogenesis of pterygium. Eye 1989;3:218–26. phology on pterygium recurrence in a controlled trial comparing con- 10. Kwok LS, Coroneo MT. A model for pterygium formation. Cornea junctival autografting with bare sclera excision. Arch Ophthalmol 1994;13:219–24. 1997;115:1235–40. 11. Cullen AP, Oriowo OM, Voison AC. Anterior eye focusing of periph- 25. Holly FJ, Lemp MA. Tear physiology and dry eyes. Surv Ophthalmol eral ultraviolet and visible radiation albedo. Clin Exp Optom 1997;80: 1977;22:69–87. 80–6. 26. Vanley GT, Leopold IH, Gregg TH. Interpretation of tear film 12. Dushku N, Reid TW. p53 expression in altered limbal basal cells of breakup. Arch Ophthalmol 1977;95:445–8. pingueculae, pterygia, and limbal tumors. Curr Eye Res 1997;16: 27. Madden RK, Paugh JR, Wang C. Comparative study of two non- 1179–92. invasive tear film stability techniques. Curr Eye Res 1994;13:263–9. 13. Stevens SS. On the theory of scales of measurement. Science 1946; 28. Taylor HR. Studies on the tear film in climatic droplet keratopathy and 103:677–80. pterygium. Arch Ophthalmol 1980;98:86–8. 14. Linacre JM, Wright BD. BIGSTEPS Rasch-model computer program. 29. Goldberg L, David R. Pterygium and its relationship to the dry eye in Chicago: MESA Press, 1995. the Bantu. Br J Ophthalmol 1976;60:720–1. 15. Rasch G. Probabilistic models for some intelligence and attainment 30. Kadayifcilar SC, Orhan M, Irkec M. Tear functions in patients with tests. Chicago: MESA Press, 1980. pterygium. Acta Ophthalmol Scand 1998;76:176–9.

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