Ophthalmic Epidemiology, 2014; 21(6): 378–383 ! Informa Healthcare USA, Inc. ISSN: 0928-6586 print / 1744-5086 online DOI: 10.3109/09286586.2014.967359
ORIGINAL ARTICLE
Prevalence of and Risk Factors for Pterygia in a Rural Northern Chinese Population Zhijian Li1*, Shubin Wu1*, Jieying Mai1, Keke Xu1, Ying Sun2, Zhen Song1, Di Jin1, Haijing Wang1, and Ping Liu1
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
1
Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, China and 2Department of Ophthalmology, Second Hospital of Heilongjiang Province, Harbin, China
ABSTRACT Purpose: To determine the prevalence of and associated risk factors for pterygia development in a highlatitude-dwelling Northern Chinese population. Methods: A prospective population-based survey was conducted between November 2008 and July 2009. A stratified, clustered, randomized sampling procedure was used to select 8445 subjects, aged 18 years, all with diagnosed, graded pterygia. Risk factors associated with the occurrence of pterygia were evaluated according to logistic regression models. Results: A total of 8445 residents (aged 18–94 years) from the Heilongjiang Province, China, participated in the study. Of these, 208 (2.5%) had at least one diagnosed pterygium. The prevalence of bilateral pterygia was 1.2% (95% confidence interval, CI, 1.0–1.4%). According to multivariable analysis, pterygia were significantly more likely to occur in persons aged 70–94 years than in those aged 18–39 years (odds ratio, OR, 29.0, 95% CI 13.6–61.6, p50.01). Pterygia were significantly associated with male sex (OR 1.9, 95% CI 1.4–2.6, p50.01) and outdoor work (OR 1.8, 95% CI 1.2-2.6, p50.01). Multivariable analysis indicated that pterygia were not associated with smoking status (OR 1.0, 95% CI 0.8–1.4) or alcohol intake (OR 1.0, 95% CI 0.7–1.4, p40.05). Conclusions: This study details the occurrence of and risk factors for pterygia in a Chinese population residing in a rural, high-latitude, cold-climate area of Northern China. The primary risk factors for pterygia were age, male sex, and outdoor work. Keywords: Cold climate, population-based, prevalence, pterygium, risk factor
INTRODUCTION
previously reported prevalences of unilateral and bilateral pterygia to be 3.7% and 2.6%, respectively, in Southern Harbin, a rural population-based sample.4 Persons residing in rural areas spend considerable time outdoors during daylight hours and are thus exposed to high levels of ultraviolet (UV) light.5 Despite the known occupational and environmental risk factors encountered by large rural populations, little is known of the eye health of such populations. In this study, we present pterygia prevalence in a rural population of Heilongjiang Province, Northern China.
Pterygia are common pathologic ophthalmic conditions of unknown etiopathogenesis.1 Pterygia characteristically appear as fleshy growths on the conjunctival and corneal surfaces, where they cause ocular irritation and visual disturbances. Despite these last conditions, however, their cosmetic lack of appeal is typically the main concern of patients. Pterygia occur across multiethnic populations, with widely varying prevalence rates (1.2–23.4%).2,3 We
Received 16 November 2013; Revised 31 July 2014; Accepted 2 August 2014; Published online 9 October 2014 *These two authors contributed equally in the preparation of this manuscript. Correspondence: Ping Liu, Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, 23 Youzheng Street, Harbin, China. E-mail: [email protected] Zhijian Li, Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, 23 Youzheng Street, Harbin, China. E-mail: [email protected]
378
Pterygium in a Rural Northern Chinese Population
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
MATERIALS AND METHODS The present study is a population-based, ophthalmologic survey of all age groups living in the rural Heilongjiang Province of Northern China. The population of this county was chosen for its relative stability and because it epitomizes the demographics and socioeconomic characteristics of a Northern Chinese rural population. The surveyed area, with a total population of 360,000 persons, 20,000 of whom live in rural areas (2007 census), is located in central Heilongjiang Province, an area characterized by cold temperatures (average 2.9 C yearly), lower elevation (200 m above sea level), and farming communities. In 2007, a typical farmer’s average annual income was CN¥4132 (US$656) in Heilongjiang Province and CN¥3880 (US$626) in Mingshui County. The male to female ratio was 108.5:100 in Heilongjiang Province and 106.4:100 in Mingshui County.6
Sampling Strategy Mingshui County located in central Heilongjiang Province, China, was selected as the survey location. The methodology used in this study has been described in detail elsewhere.7 In brief, sample size was determined by estimating the prevalence of bilateral blindness (51%) among people of all ages in Mingshui County, within a 25% error bound by a 95% confidence interval (CI). This number was then adjusted by cluster design effects (1.8) to compensate for the multistage (as opposed to simple random sampling) method. Assuming an examination response rate of 90%, the final number of survey participants required for the study was 10,953. The sampling design made use of village-based clusters of approximately equal size (n = 1000 people). Villages 41500 persons were subdivided into more than one cluster, using streets as boundaries between clusters. When geographically practical, villages of 5800 persons were combined. A total of 281 clusters, ranging in size from 761 to 1200 persons, were defined geographically. Of these, 12 clusters (n = 11,787 persons) were randomly chosen for inclusion in the survey. The study was conducted between November 2008 and July 2009.
Questionnaire Designated ophthalmologists provided training to the registrars. Following their training, registrars visited every household in the selected village, recording basic information for each of the inhabitants. A structured questionnaire was used to assess basic demographics, including name, age, sex, locality, marital status, history of agricultural work, number !
2014 Informa Healthcare USA, Inc.
379
of hours per day spent outdoors in the sun currently and number of hours per day spent outdoors in the sun 5 years ago, perceived health status, smoking status, alcohol consumption, and level of education. Information on any previous surgeries, as well as the reason why patients had not undergone recommended surgeries, was also recorded. A person was categorized as engaging in outdoor activity if his/her average outdoor activity was 4 hours per day during the past 5 years. Alcohol consumption was categorized as having or not having a habit of alcohol consumption. Participants were also categorized according to smoking habit into three groups as follows: (a) non-smoker, (b) former smoker (a person who had smoked regularly in the past 10 years and had quit smoking at least 1 year before the date of the interview), and (c) current smokers (a person who now smokes any tobacco product either daily or occasionally). Former and current smokers were assigned to ever smoker status and non-smokers were assigned to never smoker status. A final list of eligible participants was created, after which details of the eye examination were explained to each eligible participant, who was then given a referral slip with the time and location for a clinical eye examination. This investigation followed the tenets of the Declaration of Helsinki and was approved by the Research Ethics Board of the First Hospital, Harbin Medical University, Harbin, Heilongjiang, China.
Ocular Examination The 1-month survey was completed by local village doctors and a Residence Administrative Committee officer familiar with the local community. Clinical eye examinations were conducted by two different teams, each consisting of seven ophthalmologists. Each ophthalmologist received special training in study procedures in order to document clinical findings in a standardized manner. Examination sites were typically located at village clinics, schools, or halls. Those not willing to participate in examinations, either at home or at the examination site after a minimum of three visits were considered refusals. Inhabitants who lived in a village for 56 months were excluded from the study. A standardized ophthalmic examination, consisting of presenting visual acuity (VA) and bestcorrected distance visual acuity, intraocular pressure, non-cycloplegic automated refraction (RM-8000B, Topcon Corporation, Tokyo, Japan), and basic ophthalmic assessments, was performed. A logarithmic VA chart (Precision Vision, La Salle, IL, USA) was used to measure VA in each eye. The smallest line that could be read with one or no errors at a distance of
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
380 Z. Li et al. 4 m, using five tumbling-E letters in each row, was recorded. If no letters from the chart could be identified, VA was determined by counting fingers, hand movements, and light (or no light) perception. The basic ophthalmic examination also included an external eye examination, anterior segment examination by slit-lamp biomicroscopy, and fundus examination by direct ophthalmoscopy. Bilateral blindness was defined as presenting VA 520/400 in the better eye. Bilateral visual impairment was defined as presenting VA 520/60 but 20/400 in the better eye. Unilateral blindness was defined as blind in one eye but with presenting VA 20/60 in the fellow eye. Unilateral visual impairment was defined as visual impairment in one eye but VA 20/60 in the fellow eye.8 A diagnosis of pterygium was given if a characteristic raised fleshy growth, crossing the corneoscleral limbus and encroaching onto the clear cornea, was present9 or if pterygium surgery had been performed previously. Pterygia were graded according to size and severity: Stage I, head of the pterygium not extending beyond the middle line between the limbus and the center of the cornea; Stage II, head of the pterygium extending further than stage I, but not over the margin of the pupil; Stage III, head of the pterygium extending into the pupillary area.10,11 A subject was defined as ‘‘positive’’ for pterygia if at least one lesion was confirmed in either eye.
Data Analysis The prevalence of pterygium was analyzed. A multivariable-adjusted logistic regression model was used to investigate the association between pterygia and age, sex, education, smoking, and alcohol intake. The 95% CI for the prevalence of pterygium and p values for the adjusted odds ratio (OR) were calculated after adjusting for clustering effects (1.8) associated with the sampling design. Significance was assigned at a p50.05 level for all parameters. Data were entered into a Microsoft Access database. Statistical analyses were performed using SPSS software version 15 (SPSS Inc, Chicago, IL, USA).
RESULTS There were 11,787 eligible residents, of whom 10,384 (88.1%) were examined. Subjects ranged in age from 1–94 years, with a mean age of 35.8 ± 19.4 years for men and 36.8 ± 18.7 years for women. A total of 673 women (48.0%) and 730 men (52.0%) chose not to participate in the survey. Of these, 483 were not at home and 920 refused. There were no significant differences between participants and non-participants with regard to distribution of males and females
TABLE 1. Distribution of sex, age, and educational level of study participants, Mingshui County, Heilongjiang Province, China. Variable
Male n (%)
Age, years 18–39 40–49 50–59 60–69 70–94
2027 892 691 417 269
(52.0) (49.1) (48.5) (51.5) (54.3)
Educational level, years 0–5 2262 (58.9) 6–13 2034 (44.1) Total 4296 (50.8)
Female n (%) 1873 924 734 392 226
(48.0) (50.9) (51.5) (48.5) (45.8)
1575 (41.1) 2574 (58.9) 4149 (49.2)
All n (%) 3900 1816 1425 809 495
(46.1) (21.5) (16.9) (9.6) (5.8)
3837 (45.4) 4608 (55.6) 8445 (100.0)
(51.7 vs 52.0%; 48.3 vs 48.0%, respectively, p = 0.8); age (15.4 vs 15.0%, 23.2 vs 22.8%, 17.6 vs 16.2%, 17.5 vs 17.0%, 13.7 vs 14.0%, 7.8 vs 9.9%, and 4.8 vs 5.1% for the 0–15, 16–29, 30–39, 40–49, 50–59, 60–69, and 70 years age groups, respectively, p = 0.2); and education (19.3 vs 18.0%, 32.6 vs 34.0%, and 48.1 vs 48.0% for 0, 1–6, and 7–13 years of education, respectively, p = 0.4).7 Of the 10,384 participants who were examined, 1939 were excluded from the study population, including those aged 518 years (due to the rare prevalence of pterygia) and those in whom no record of pterygia could be obtained. Distributions of sex, age, and level of education are shown in Table 1. The prevalence of pterygium was 2.5% (95% CI 2.2– 2.8%). A total of 208 persons (n = 308 eyes) were diagnosed with pterygia in at least one eye. Pterygia were equally common in left and right eyes (1.9 vs 1.7%, respectively). The prevalence of bilateral pterygia was 1.2% (95% CI 1.0–1.4%). For those aged 40 years, the overall prevalence of pterygia was 2.2% (95% CI 1.8–2.6%; bilateral 2.1%, 95% CI 1.7–2.5% and unilateral 4.2%, 95% CI 3.6–4.8%). The incidence of pterygia increased in frequency among the elderly (0.3%, 1.4%, 4.1%, 7.3%, and 11.3% in the 18–39, 40–49, 50–59, 60-69, and 70-year age groups, respectively). No participant had undergone previous pterygium surgery. Two people were blind in both eyes as a result of pterygial extension onto the cornea and the resulting occlusion of the visual axis. Among the 308 eyes with 1 pterygium, 179 eyes (58.1%) were graded as Stage I, 96 eyes (31.2%) as Stage II, and 33 eyes (10.7%) as Stage III. The prevalence of pterygia in at least one eye according to age, sex, education, outdoor work, smoking, and alcohol consumption is shown in Table 2. Pterygia were significantly more likely to occur in the 70–94 years age group than in the 18–39 years age group. The age-adjusted OR for men was 1.7 (95% CI 1.3–2.2, p50.01). Furthermore, the prevalence of pterygia was higher among people with higher education levels (age-adjusted OR 1.5, 95% CI 1.0–2.4, p = 0.08) and among those who had ever smoked Ophthalmic Epidemiology
Pterygium in a Rural Northern Chinese Population TABLE 2. Correlation between presence of pterygia and risk factors in the multivariable-adjusted logistic regression model, Heilongjiang Province, China.
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Variable Age group, years 18–39 40–49 50–59 60–69 70–94 Sex Female Male Education, years 8–13 5–7 0–4 Outdoor work No Yes Smoking status Never smoker Ever smoker Alcohol intake No Yes
Age-adjusted OR (95% CI) 1 1.6 2.3 8.8 46.5
Multivariable-adjusted OR (95%CI)
(1.1–2.3)a (1.5–3.5)b (5.4–14.4)b (23.5–92.1)b
1 1.5 2.8 6.3 29.0
(1.0–2.2)a (1.9–4.1)b (3.7–10.8)b (13.6–61.6)b
1 1.7 (1.3–2.2)b
1 1.9 (1.4–2.6)b
1 1.4 (1.0–1.9) 1.5 (1.0–2.4)
1 1.5 (1.1–2.2)a 1.8 (1.1–3.0)a
1 1.9 (1.3–2.9)b
1 1.8 (1.2–2.6)a
1 1.1 (0.8–1.4)
1 1.0 (0.8– 1.4)
1 1.0 (0.7–1.4)
1 1.0 (0.7–1.4)
CI, confidence interval; OR, odds ratio a p50.05; bp50.01
(age-adjusted OR 1.1, 95% CI 0.8–1.4, p = 0.67). The remaining variable (alcohol intake) was not associated with occurrence of pterygia (p = 0.85). A multivariable logistic regression model adjusting for all variables found to be significantly associated with pterygia showed that there was a significantly increased risk of pterygia with age, sex, and outdoor activity of 4 hours/day during the past 5 years, but not with smoking status or alcohol intake (Table 2). The risk of having pterygia for the 70–94 years age group was 29 times higher than for the 18–39 years age group, whereas extensive time spent outdoors conferred a 1.9 times increased risk. The multivariable-adjusted OR for men was 1.9 (95% CI 1.4–2.6, p50.01). Pterygia were not associated with smoking in the model (multivariable-adjusted OR 1.0, 95% CI 0.8–1.4).
DISCUSSION In 2006, the cross-sectional prevalence Southen Harbin Eye Study of blindness focused mainly on eye diseases that resulted in blindness. Although the prevalence and risk factors for pterygia were reported in that study,4 it is highly likely that the results were subject to numerous biases resulting from the population analyzed (ages 50 years) and limited relevant risk factors (Table 3). The present study differs from the Southern Harbin Eye Study in several respects, !
2014 Informa Healthcare USA, Inc.
381
TABLE 3. Comparison of the present study in Heilongjiang Province to the Southern Harbin Eye Study. Factor
Present study
Southern Harbin Eye Study
Average temperature 2.9 C 4.5 C in survey area Distance from central 182 70 city, km Participants, n 8445 5057 Age, years 42.3 (range 18–94) 60.5 (range 50–96) Prevalence of pterygia At least one eye, % 2.5 6.4 Bilateral, % 1.2 2.6 Outdoor work + Unspecified Alcohol intake + Unspecified +, risk factor for pterygia
e.g. representative population surveyed, age range of population, and survey methods. The 2.5% prevalence rate determined in our study is lower than those reported in most studies of Chinese individuals10,12–14 (Table 4), and is even lower than those reported for similar populations, e.g. South Koreans (South National Health and Nutrition Examination Survey, 5.4%),15 Chinese (Handan Eye Study, 7.1%),16 Tibetans (14.49%),17 and Americans (North Carolina, 23.3%).4 These data are especially significant considering that our screening involved all available inhabitants aged 18 years and that our respondents were relatively young (average age 42.3 years). Large pterygia (stages II, III) have significant effects on VA due to the lesions’ extension onto the cornea and astigmatism. In the present study, 96 eyes (31.2%) were stage II, and 33 (10.7%) were stage III. It is our understanding that many patients with pterygium do not submit to the operation due to a fear of surgery and/or of recurrence. Further work, particularly involving patient education, is essential for ameliorating patient fears. Although a previous study did not find age to be significantly associated with the occurrence of pterygia,18 we did find such an association in the present study. In addition, similar findings were recently described in the Multiethnic Population Study of Asians (Beijing-based) and Mongolian populations.1,11,12 Also consistent with several studies,1,19 we observed a trend towards an increasing prevalence of pterygia in persons with lower educational levels. Multivariable analysis indicated a significant association of pterygia with lower education. An association between educational level and prevalence of pterygia is possibly attributable to the variety of occupations associated with educational levels and outdoor (exposure to sunlight) activities. An association between sex and formation of pterygia is controversial. Some reports indicate that pterygia are more prevalent among men (all age
382 Z. Li et al. TABLE 4. Prevalence and risk factors for pterygia in various population-based surveys in Chinese populations.
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Prevalence of pterygium, % Year
Study location
Age, years
Sample size, n
2001 2012
Singapore22 Yunnan, China14
40+ 50+
2225 2133
2010 2013 2009 2007
Beijing, China12 Handan, China16 Nei Monggol, China1 Tibet, China17
55+ 30+ 40+ 40+
37,067 6885 2486 2632
2013 2014
Harbin China4 Present Study
50+ 40+
5057 4546
Unilateral
Bilateral
At least one eye 7.0 39.0 5.91 4.8 17.9 14.5
3.7 2.1
groups).3,10 In contrast, there are also reports indicating higher prevalence rates among women.9,17 Still other studies found no correlation between pterygia and sex.1,19 In the present study, the prevalence of pterygia was higher in men than in women. This controversy may reflect variations in the study populations as well as the extent to which each population’s sexes differ in outdoor activities and sun exposure. In the present study, outdoor work was significantly associated with the occurrence of pterygia (p50.001). A considerable number of persons are involved in agriculture in the area covered in our survey. The outdoor nature of these occupations likely increases the cumulative exposure to UV radiation. Asokan and colleagues20 used the well-established Melbourne visual impairment project model21 to calculate UV exposure. These investigators found that those with higher lifetime UV exposures were 3 times more likely to develop pterygia, findings similar to those found in an epidemiological study conducted in Victoria.21 Consistent with a study of pterygia in a Chinese population,22 our survey showed that pterygia were not associated with smoking in the model. Even so, other study indicates that smokers are less likely to develop pterygia.23 The possible mechanism by which smoking is protective is unclear. A Spanish study indicated that alcohol consumption had a significant effect on the prevalence of pinguecula, but not pterygia. The increased oxidative stress resulting from alcohol use might favor development of the degenerative changes associated with pinguecula, but not the proliferative processes that occur in pterygia.24 In our study, multivariable analysis indicated that alcohol intake had no effect on the prevalence of pterygia. In conclusion, the prevalence of pterygia was found to be 2.5% in a Northern Chinese population. Risk factors include age, education, sex (male), and outdoor work. Dissemination of awareness about the use
2.6 2.2
6.4 4.2
Risk factors Age, male sex, poor education Age, female sex, lower education, outdoor work Age, male sex, low latitude Age, male sex Age, lower education Age, female sex, not using spectacles, lower education status, low socioeconomic status Male sex, smoking Age, male sex, outdoor work, alcohol intake
of protective spectacles and appropriate headgear is expected to help to reduce the risk of developing pterygia.
ACKNOWLEDGMENTS We acknowledge local government officials and the workers at the local township clinics for their painstaking and enthusiastic work. We thank the Mingshui People’s Hospital for its organizational support. We are also grateful to the participants for their generous participation in the survey.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. The study was supported by the post-doctoral fund of China (LRB2011-484),the postdoctoral ScienceResearch Foundation (LBH-Q12043), the Special Fund of Harbin Technological Innovation.(Contract No. 2013RFXYJ004), and Nature Science Foundation of Heilongjiang Province, China (D201254).
REFERENCES 1. Lu J, Wang Z, Lu P, et al. Pterygium in an aged Mongolian population: a population-based study in China. Eye 2009; 23:421–427. 2. Solomon A, Pires RT, Tseng SC. Amniotic membrane transplantation after extensive removal of primary and recurrent pterygia. Ophthalmology 2001;108:449–460. 3. McCarty CA, Fu CL, Taylor HR. Epidemiology of pterygium in Victoria, Australia. Br J Ophthalmol 2000;84: 289–292. 4. Li Z, Cui H. Prevalence and associated factors for pterygium in a rural adult population (the Southern Harbin Eye Study). Cornea 2013;32(6):806–809. Ophthalmic Epidemiology
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Pterygium in a Rural Northern Chinese Population 5. Taylor SL, Coates ML, Vallejos Q, et al. Pterygium among Latino migrant farmworkers in North Carolina. Arch Environ Occup Health 2006;61(1):27–32. 6. Heilongjiang Province Bureau of Statistics. Announcement of the Heilongjiang Province Bureau of Statistics on Revision in 2007. from: http://www.hlj.stats.gov.cn. [last accessed 29 Dec 2008]. 7. Zhang Y, Wang H, Liu J, et al. Prevalence of blindness and low vision: a study in the rural Heilongjiang Province of China. Clin Exp Ophthalmol 2012;40(5):484–489. 8. World Health Organization. ICD-10. International Statistical Classification of Diseases and Related Health Problems, 10th Revision. In: Johnson GJ, Minassian DC, Weale R, eds. The epidemiology of eye disease. London: Chapman & Hall Medical, 1998. 8–30. 9. Taylor HR, West SK, Rosenthal FS, et al. Corneal changes associated with chronic UV irradiation. Arch Ophthalmol 1989;107:1481–1484. 10. Wu K, He M, Xu J, et al. Pterygium in aged county population in Doumen, China. Yan Ke Xue Bao 2002;18: 181–184. 11. Tan CS, Lim TH, Koh WP, et al. Epidemiology of pterygium on a tropical island in the Riau Archipelago. Eye 2006;20: 908–912. 12. Liang Q, Xu L, Jin X, et al. Epidemiology of pterygium in aged rural population of Beijing, China. Chin Med J 2010; 123(13):1699–1701. 13. Ang M, Li X, Wong W, et al. Prevalence of and racial differences in pterygium: a multiethnic population study in Asians. Ophthalmology 2012;119(8):1509–1515. 14. Zhong H, Cha X, Wei T, et al. Prevalence of and risk factors for pterygium in rural adult Chinese populations of the Bai nationality in Dali: the Yunnan Minority Eye Study. Invest Ophthalmol Vis Sci 2012;53(10):6617–6621.
!
2014 Informa Healthcare USA, Inc.
383
15. Yoon KC, Mun GH, Kim SD, et al. Prevalence of eye diseases in South Korea: data from the Korea National Health and Nutrition Examination Survey 2008–2009. Korean J Ophthalmol 2011;25(6):421–433. 16. Sun LP, Lv W, Liang YB, et al. The prevalence of and risk factors associated with pterygium in a rural adult Chinese population: the Handan Eye Study. Ophthalmic Epidemiol 2013;20(3):148–154. 17. Lu P, Chen X, Kang Y, et al. Pterygium in Tibetans: a population-based study in China. Clin Experiment Ophthalmol 2007;35(9):828–833. 18. Paula JS, Thorn F, Cruz AA. Prevalence of pterygium and cataract in indigenous populations of the Brazilian Amazon rain forest. Eye (Lond) 2006;20(5):533–536. 19. Luthra R, Nemesure B, Wu S-Y, et al. Frequency and risk factors for pterygium in the Barbados Eye Study. Arch Ophthalmol 2001;119:1827–1832. 20. Asokan R, Venkatasubbu RS, Velumuri L, et al. Prevalence and associated factors for pterygium and pinguecula in a South Indian population. Ophthalmic Physiol Opt 2012; 32(1):39–44. 21. McCarty CA, Lee SE, Livingston PM, et al. Ocular exposure to UV-B in sunlight: the Melbourne visual impairment project model. Bull World Health Organ 1996; 74:353–360. 22. Wong TY, Foster PJ, Johnson GJ, et al. The prevalence and22 risk factors for pterygium in an adult Chinese population in Singapore: the Tanjong Pagar survey. Am J Ophthalmol 2001;131:176–183. 23. West S, Mun˜oz B. Prevalence of pterygium in Latinos: Proyecto VER. Br J Ophthalmol 2009;93(10):1287–1290. 24. Viso E, Gude F, Rodrı´guez-Ares MT. Prevalence of pinguecula and pterygium in a general population in Spain. Eye (Lond) 2011;25(3):350–357.
ORIGINAL ARTICLE
Prevalence of and Risk Factors for Pterygia in a Rural Northern Chinese Population Zhijian Li1*, Shubin Wu1*, Jieying Mai1, Keke Xu1, Ying Sun2, Zhen Song1, Di Jin1, Haijing Wang1, and Ping Liu1
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
1
Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, China and 2Department of Ophthalmology, Second Hospital of Heilongjiang Province, Harbin, China
ABSTRACT Purpose: To determine the prevalence of and associated risk factors for pterygia development in a highlatitude-dwelling Northern Chinese population. Methods: A prospective population-based survey was conducted between November 2008 and July 2009. A stratified, clustered, randomized sampling procedure was used to select 8445 subjects, aged 18 years, all with diagnosed, graded pterygia. Risk factors associated with the occurrence of pterygia were evaluated according to logistic regression models. Results: A total of 8445 residents (aged 18–94 years) from the Heilongjiang Province, China, participated in the study. Of these, 208 (2.5%) had at least one diagnosed pterygium. The prevalence of bilateral pterygia was 1.2% (95% confidence interval, CI, 1.0–1.4%). According to multivariable analysis, pterygia were significantly more likely to occur in persons aged 70–94 years than in those aged 18–39 years (odds ratio, OR, 29.0, 95% CI 13.6–61.6, p50.01). Pterygia were significantly associated with male sex (OR 1.9, 95% CI 1.4–2.6, p50.01) and outdoor work (OR 1.8, 95% CI 1.2-2.6, p50.01). Multivariable analysis indicated that pterygia were not associated with smoking status (OR 1.0, 95% CI 0.8–1.4) or alcohol intake (OR 1.0, 95% CI 0.7–1.4, p40.05). Conclusions: This study details the occurrence of and risk factors for pterygia in a Chinese population residing in a rural, high-latitude, cold-climate area of Northern China. The primary risk factors for pterygia were age, male sex, and outdoor work. Keywords: Cold climate, population-based, prevalence, pterygium, risk factor
INTRODUCTION
previously reported prevalences of unilateral and bilateral pterygia to be 3.7% and 2.6%, respectively, in Southern Harbin, a rural population-based sample.4 Persons residing in rural areas spend considerable time outdoors during daylight hours and are thus exposed to high levels of ultraviolet (UV) light.5 Despite the known occupational and environmental risk factors encountered by large rural populations, little is known of the eye health of such populations. In this study, we present pterygia prevalence in a rural population of Heilongjiang Province, Northern China.
Pterygia are common pathologic ophthalmic conditions of unknown etiopathogenesis.1 Pterygia characteristically appear as fleshy growths on the conjunctival and corneal surfaces, where they cause ocular irritation and visual disturbances. Despite these last conditions, however, their cosmetic lack of appeal is typically the main concern of patients. Pterygia occur across multiethnic populations, with widely varying prevalence rates (1.2–23.4%).2,3 We
Received 16 November 2013; Revised 31 July 2014; Accepted 2 August 2014; Published online 9 October 2014 *These two authors contributed equally in the preparation of this manuscript. Correspondence: Ping Liu, Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, 23 Youzheng Street, Harbin, China. E-mail: [email protected] Zhijian Li, Department of Ophthalmology, First Affiliated Hospital, Harbin Medical University, 23 Youzheng Street, Harbin, China. E-mail: [email protected]
378
Pterygium in a Rural Northern Chinese Population
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
MATERIALS AND METHODS The present study is a population-based, ophthalmologic survey of all age groups living in the rural Heilongjiang Province of Northern China. The population of this county was chosen for its relative stability and because it epitomizes the demographics and socioeconomic characteristics of a Northern Chinese rural population. The surveyed area, with a total population of 360,000 persons, 20,000 of whom live in rural areas (2007 census), is located in central Heilongjiang Province, an area characterized by cold temperatures (average 2.9 C yearly), lower elevation (200 m above sea level), and farming communities. In 2007, a typical farmer’s average annual income was CN¥4132 (US$656) in Heilongjiang Province and CN¥3880 (US$626) in Mingshui County. The male to female ratio was 108.5:100 in Heilongjiang Province and 106.4:100 in Mingshui County.6
Sampling Strategy Mingshui County located in central Heilongjiang Province, China, was selected as the survey location. The methodology used in this study has been described in detail elsewhere.7 In brief, sample size was determined by estimating the prevalence of bilateral blindness (51%) among people of all ages in Mingshui County, within a 25% error bound by a 95% confidence interval (CI). This number was then adjusted by cluster design effects (1.8) to compensate for the multistage (as opposed to simple random sampling) method. Assuming an examination response rate of 90%, the final number of survey participants required for the study was 10,953. The sampling design made use of village-based clusters of approximately equal size (n = 1000 people). Villages 41500 persons were subdivided into more than one cluster, using streets as boundaries between clusters. When geographically practical, villages of 5800 persons were combined. A total of 281 clusters, ranging in size from 761 to 1200 persons, were defined geographically. Of these, 12 clusters (n = 11,787 persons) were randomly chosen for inclusion in the survey. The study was conducted between November 2008 and July 2009.
Questionnaire Designated ophthalmologists provided training to the registrars. Following their training, registrars visited every household in the selected village, recording basic information for each of the inhabitants. A structured questionnaire was used to assess basic demographics, including name, age, sex, locality, marital status, history of agricultural work, number !
2014 Informa Healthcare USA, Inc.
379
of hours per day spent outdoors in the sun currently and number of hours per day spent outdoors in the sun 5 years ago, perceived health status, smoking status, alcohol consumption, and level of education. Information on any previous surgeries, as well as the reason why patients had not undergone recommended surgeries, was also recorded. A person was categorized as engaging in outdoor activity if his/her average outdoor activity was 4 hours per day during the past 5 years. Alcohol consumption was categorized as having or not having a habit of alcohol consumption. Participants were also categorized according to smoking habit into three groups as follows: (a) non-smoker, (b) former smoker (a person who had smoked regularly in the past 10 years and had quit smoking at least 1 year before the date of the interview), and (c) current smokers (a person who now smokes any tobacco product either daily or occasionally). Former and current smokers were assigned to ever smoker status and non-smokers were assigned to never smoker status. A final list of eligible participants was created, after which details of the eye examination were explained to each eligible participant, who was then given a referral slip with the time and location for a clinical eye examination. This investigation followed the tenets of the Declaration of Helsinki and was approved by the Research Ethics Board of the First Hospital, Harbin Medical University, Harbin, Heilongjiang, China.
Ocular Examination The 1-month survey was completed by local village doctors and a Residence Administrative Committee officer familiar with the local community. Clinical eye examinations were conducted by two different teams, each consisting of seven ophthalmologists. Each ophthalmologist received special training in study procedures in order to document clinical findings in a standardized manner. Examination sites were typically located at village clinics, schools, or halls. Those not willing to participate in examinations, either at home or at the examination site after a minimum of three visits were considered refusals. Inhabitants who lived in a village for 56 months were excluded from the study. A standardized ophthalmic examination, consisting of presenting visual acuity (VA) and bestcorrected distance visual acuity, intraocular pressure, non-cycloplegic automated refraction (RM-8000B, Topcon Corporation, Tokyo, Japan), and basic ophthalmic assessments, was performed. A logarithmic VA chart (Precision Vision, La Salle, IL, USA) was used to measure VA in each eye. The smallest line that could be read with one or no errors at a distance of
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
380 Z. Li et al. 4 m, using five tumbling-E letters in each row, was recorded. If no letters from the chart could be identified, VA was determined by counting fingers, hand movements, and light (or no light) perception. The basic ophthalmic examination also included an external eye examination, anterior segment examination by slit-lamp biomicroscopy, and fundus examination by direct ophthalmoscopy. Bilateral blindness was defined as presenting VA 520/400 in the better eye. Bilateral visual impairment was defined as presenting VA 520/60 but 20/400 in the better eye. Unilateral blindness was defined as blind in one eye but with presenting VA 20/60 in the fellow eye. Unilateral visual impairment was defined as visual impairment in one eye but VA 20/60 in the fellow eye.8 A diagnosis of pterygium was given if a characteristic raised fleshy growth, crossing the corneoscleral limbus and encroaching onto the clear cornea, was present9 or if pterygium surgery had been performed previously. Pterygia were graded according to size and severity: Stage I, head of the pterygium not extending beyond the middle line between the limbus and the center of the cornea; Stage II, head of the pterygium extending further than stage I, but not over the margin of the pupil; Stage III, head of the pterygium extending into the pupillary area.10,11 A subject was defined as ‘‘positive’’ for pterygia if at least one lesion was confirmed in either eye.
Data Analysis The prevalence of pterygium was analyzed. A multivariable-adjusted logistic regression model was used to investigate the association between pterygia and age, sex, education, smoking, and alcohol intake. The 95% CI for the prevalence of pterygium and p values for the adjusted odds ratio (OR) were calculated after adjusting for clustering effects (1.8) associated with the sampling design. Significance was assigned at a p50.05 level for all parameters. Data were entered into a Microsoft Access database. Statistical analyses were performed using SPSS software version 15 (SPSS Inc, Chicago, IL, USA).
RESULTS There were 11,787 eligible residents, of whom 10,384 (88.1%) were examined. Subjects ranged in age from 1–94 years, with a mean age of 35.8 ± 19.4 years for men and 36.8 ± 18.7 years for women. A total of 673 women (48.0%) and 730 men (52.0%) chose not to participate in the survey. Of these, 483 were not at home and 920 refused. There were no significant differences between participants and non-participants with regard to distribution of males and females
TABLE 1. Distribution of sex, age, and educational level of study participants, Mingshui County, Heilongjiang Province, China. Variable
Male n (%)
Age, years 18–39 40–49 50–59 60–69 70–94
2027 892 691 417 269
(52.0) (49.1) (48.5) (51.5) (54.3)
Educational level, years 0–5 2262 (58.9) 6–13 2034 (44.1) Total 4296 (50.8)
Female n (%) 1873 924 734 392 226
(48.0) (50.9) (51.5) (48.5) (45.8)
1575 (41.1) 2574 (58.9) 4149 (49.2)
All n (%) 3900 1816 1425 809 495
(46.1) (21.5) (16.9) (9.6) (5.8)
3837 (45.4) 4608 (55.6) 8445 (100.0)
(51.7 vs 52.0%; 48.3 vs 48.0%, respectively, p = 0.8); age (15.4 vs 15.0%, 23.2 vs 22.8%, 17.6 vs 16.2%, 17.5 vs 17.0%, 13.7 vs 14.0%, 7.8 vs 9.9%, and 4.8 vs 5.1% for the 0–15, 16–29, 30–39, 40–49, 50–59, 60–69, and 70 years age groups, respectively, p = 0.2); and education (19.3 vs 18.0%, 32.6 vs 34.0%, and 48.1 vs 48.0% for 0, 1–6, and 7–13 years of education, respectively, p = 0.4).7 Of the 10,384 participants who were examined, 1939 were excluded from the study population, including those aged 518 years (due to the rare prevalence of pterygia) and those in whom no record of pterygia could be obtained. Distributions of sex, age, and level of education are shown in Table 1. The prevalence of pterygium was 2.5% (95% CI 2.2– 2.8%). A total of 208 persons (n = 308 eyes) were diagnosed with pterygia in at least one eye. Pterygia were equally common in left and right eyes (1.9 vs 1.7%, respectively). The prevalence of bilateral pterygia was 1.2% (95% CI 1.0–1.4%). For those aged 40 years, the overall prevalence of pterygia was 2.2% (95% CI 1.8–2.6%; bilateral 2.1%, 95% CI 1.7–2.5% and unilateral 4.2%, 95% CI 3.6–4.8%). The incidence of pterygia increased in frequency among the elderly (0.3%, 1.4%, 4.1%, 7.3%, and 11.3% in the 18–39, 40–49, 50–59, 60-69, and 70-year age groups, respectively). No participant had undergone previous pterygium surgery. Two people were blind in both eyes as a result of pterygial extension onto the cornea and the resulting occlusion of the visual axis. Among the 308 eyes with 1 pterygium, 179 eyes (58.1%) were graded as Stage I, 96 eyes (31.2%) as Stage II, and 33 eyes (10.7%) as Stage III. The prevalence of pterygia in at least one eye according to age, sex, education, outdoor work, smoking, and alcohol consumption is shown in Table 2. Pterygia were significantly more likely to occur in the 70–94 years age group than in the 18–39 years age group. The age-adjusted OR for men was 1.7 (95% CI 1.3–2.2, p50.01). Furthermore, the prevalence of pterygia was higher among people with higher education levels (age-adjusted OR 1.5, 95% CI 1.0–2.4, p = 0.08) and among those who had ever smoked Ophthalmic Epidemiology
Pterygium in a Rural Northern Chinese Population TABLE 2. Correlation between presence of pterygia and risk factors in the multivariable-adjusted logistic regression model, Heilongjiang Province, China.
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Variable Age group, years 18–39 40–49 50–59 60–69 70–94 Sex Female Male Education, years 8–13 5–7 0–4 Outdoor work No Yes Smoking status Never smoker Ever smoker Alcohol intake No Yes
Age-adjusted OR (95% CI) 1 1.6 2.3 8.8 46.5
Multivariable-adjusted OR (95%CI)
(1.1–2.3)a (1.5–3.5)b (5.4–14.4)b (23.5–92.1)b
1 1.5 2.8 6.3 29.0
(1.0–2.2)a (1.9–4.1)b (3.7–10.8)b (13.6–61.6)b
1 1.7 (1.3–2.2)b
1 1.9 (1.4–2.6)b
1 1.4 (1.0–1.9) 1.5 (1.0–2.4)
1 1.5 (1.1–2.2)a 1.8 (1.1–3.0)a
1 1.9 (1.3–2.9)b
1 1.8 (1.2–2.6)a
1 1.1 (0.8–1.4)
1 1.0 (0.8– 1.4)
1 1.0 (0.7–1.4)
1 1.0 (0.7–1.4)
CI, confidence interval; OR, odds ratio a p50.05; bp50.01
(age-adjusted OR 1.1, 95% CI 0.8–1.4, p = 0.67). The remaining variable (alcohol intake) was not associated with occurrence of pterygia (p = 0.85). A multivariable logistic regression model adjusting for all variables found to be significantly associated with pterygia showed that there was a significantly increased risk of pterygia with age, sex, and outdoor activity of 4 hours/day during the past 5 years, but not with smoking status or alcohol intake (Table 2). The risk of having pterygia for the 70–94 years age group was 29 times higher than for the 18–39 years age group, whereas extensive time spent outdoors conferred a 1.9 times increased risk. The multivariable-adjusted OR for men was 1.9 (95% CI 1.4–2.6, p50.01). Pterygia were not associated with smoking in the model (multivariable-adjusted OR 1.0, 95% CI 0.8–1.4).
DISCUSSION In 2006, the cross-sectional prevalence Southen Harbin Eye Study of blindness focused mainly on eye diseases that resulted in blindness. Although the prevalence and risk factors for pterygia were reported in that study,4 it is highly likely that the results were subject to numerous biases resulting from the population analyzed (ages 50 years) and limited relevant risk factors (Table 3). The present study differs from the Southern Harbin Eye Study in several respects, !
2014 Informa Healthcare USA, Inc.
381
TABLE 3. Comparison of the present study in Heilongjiang Province to the Southern Harbin Eye Study. Factor
Present study
Southern Harbin Eye Study
Average temperature 2.9 C 4.5 C in survey area Distance from central 182 70 city, km Participants, n 8445 5057 Age, years 42.3 (range 18–94) 60.5 (range 50–96) Prevalence of pterygia At least one eye, % 2.5 6.4 Bilateral, % 1.2 2.6 Outdoor work + Unspecified Alcohol intake + Unspecified +, risk factor for pterygia
e.g. representative population surveyed, age range of population, and survey methods. The 2.5% prevalence rate determined in our study is lower than those reported in most studies of Chinese individuals10,12–14 (Table 4), and is even lower than those reported for similar populations, e.g. South Koreans (South National Health and Nutrition Examination Survey, 5.4%),15 Chinese (Handan Eye Study, 7.1%),16 Tibetans (14.49%),17 and Americans (North Carolina, 23.3%).4 These data are especially significant considering that our screening involved all available inhabitants aged 18 years and that our respondents were relatively young (average age 42.3 years). Large pterygia (stages II, III) have significant effects on VA due to the lesions’ extension onto the cornea and astigmatism. In the present study, 96 eyes (31.2%) were stage II, and 33 (10.7%) were stage III. It is our understanding that many patients with pterygium do not submit to the operation due to a fear of surgery and/or of recurrence. Further work, particularly involving patient education, is essential for ameliorating patient fears. Although a previous study did not find age to be significantly associated with the occurrence of pterygia,18 we did find such an association in the present study. In addition, similar findings were recently described in the Multiethnic Population Study of Asians (Beijing-based) and Mongolian populations.1,11,12 Also consistent with several studies,1,19 we observed a trend towards an increasing prevalence of pterygia in persons with lower educational levels. Multivariable analysis indicated a significant association of pterygia with lower education. An association between educational level and prevalence of pterygia is possibly attributable to the variety of occupations associated with educational levels and outdoor (exposure to sunlight) activities. An association between sex and formation of pterygia is controversial. Some reports indicate that pterygia are more prevalent among men (all age
382 Z. Li et al. TABLE 4. Prevalence and risk factors for pterygia in various population-based surveys in Chinese populations.
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Prevalence of pterygium, % Year
Study location
Age, years
Sample size, n
2001 2012
Singapore22 Yunnan, China14
40+ 50+
2225 2133
2010 2013 2009 2007
Beijing, China12 Handan, China16 Nei Monggol, China1 Tibet, China17
55+ 30+ 40+ 40+
37,067 6885 2486 2632
2013 2014
Harbin China4 Present Study
50+ 40+
5057 4546
Unilateral
Bilateral
At least one eye 7.0 39.0 5.91 4.8 17.9 14.5
3.7 2.1
groups).3,10 In contrast, there are also reports indicating higher prevalence rates among women.9,17 Still other studies found no correlation between pterygia and sex.1,19 In the present study, the prevalence of pterygia was higher in men than in women. This controversy may reflect variations in the study populations as well as the extent to which each population’s sexes differ in outdoor activities and sun exposure. In the present study, outdoor work was significantly associated with the occurrence of pterygia (p50.001). A considerable number of persons are involved in agriculture in the area covered in our survey. The outdoor nature of these occupations likely increases the cumulative exposure to UV radiation. Asokan and colleagues20 used the well-established Melbourne visual impairment project model21 to calculate UV exposure. These investigators found that those with higher lifetime UV exposures were 3 times more likely to develop pterygia, findings similar to those found in an epidemiological study conducted in Victoria.21 Consistent with a study of pterygia in a Chinese population,22 our survey showed that pterygia were not associated with smoking in the model. Even so, other study indicates that smokers are less likely to develop pterygia.23 The possible mechanism by which smoking is protective is unclear. A Spanish study indicated that alcohol consumption had a significant effect on the prevalence of pinguecula, but not pterygia. The increased oxidative stress resulting from alcohol use might favor development of the degenerative changes associated with pinguecula, but not the proliferative processes that occur in pterygia.24 In our study, multivariable analysis indicated that alcohol intake had no effect on the prevalence of pterygia. In conclusion, the prevalence of pterygia was found to be 2.5% in a Northern Chinese population. Risk factors include age, education, sex (male), and outdoor work. Dissemination of awareness about the use
2.6 2.2
6.4 4.2
Risk factors Age, male sex, poor education Age, female sex, lower education, outdoor work Age, male sex, low latitude Age, male sex Age, lower education Age, female sex, not using spectacles, lower education status, low socioeconomic status Male sex, smoking Age, male sex, outdoor work, alcohol intake
of protective spectacles and appropriate headgear is expected to help to reduce the risk of developing pterygia.
ACKNOWLEDGMENTS We acknowledge local government officials and the workers at the local township clinics for their painstaking and enthusiastic work. We thank the Mingshui People’s Hospital for its organizational support. We are also grateful to the participants for their generous participation in the survey.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. The study was supported by the post-doctoral fund of China (LRB2011-484),the postdoctoral ScienceResearch Foundation (LBH-Q12043), the Special Fund of Harbin Technological Innovation.(Contract No. 2013RFXYJ004), and Nature Science Foundation of Heilongjiang Province, China (D201254).
REFERENCES 1. Lu J, Wang Z, Lu P, et al. Pterygium in an aged Mongolian population: a population-based study in China. Eye 2009; 23:421–427. 2. Solomon A, Pires RT, Tseng SC. Amniotic membrane transplantation after extensive removal of primary and recurrent pterygia. Ophthalmology 2001;108:449–460. 3. McCarty CA, Fu CL, Taylor HR. Epidemiology of pterygium in Victoria, Australia. Br J Ophthalmol 2000;84: 289–292. 4. Li Z, Cui H. Prevalence and associated factors for pterygium in a rural adult population (the Southern Harbin Eye Study). Cornea 2013;32(6):806–809. Ophthalmic Epidemiology
Ophthalmic Epidemiol Downloaded from informahealthcare.com by Selcuk Universitesi on 01/29/15 For personal use only.
Pterygium in a Rural Northern Chinese Population 5. Taylor SL, Coates ML, Vallejos Q, et al. Pterygium among Latino migrant farmworkers in North Carolina. Arch Environ Occup Health 2006;61(1):27–32. 6. Heilongjiang Province Bureau of Statistics. Announcement of the Heilongjiang Province Bureau of Statistics on Revision in 2007. from: http://www.hlj.stats.gov.cn. [last accessed 29 Dec 2008]. 7. Zhang Y, Wang H, Liu J, et al. Prevalence of blindness and low vision: a study in the rural Heilongjiang Province of China. Clin Exp Ophthalmol 2012;40(5):484–489. 8. World Health Organization. ICD-10. International Statistical Classification of Diseases and Related Health Problems, 10th Revision. In: Johnson GJ, Minassian DC, Weale R, eds. The epidemiology of eye disease. London: Chapman & Hall Medical, 1998. 8–30. 9. Taylor HR, West SK, Rosenthal FS, et al. Corneal changes associated with chronic UV irradiation. Arch Ophthalmol 1989;107:1481–1484. 10. Wu K, He M, Xu J, et al. Pterygium in aged county population in Doumen, China. Yan Ke Xue Bao 2002;18: 181–184. 11. Tan CS, Lim TH, Koh WP, et al. Epidemiology of pterygium on a tropical island in the Riau Archipelago. Eye 2006;20: 908–912. 12. Liang Q, Xu L, Jin X, et al. Epidemiology of pterygium in aged rural population of Beijing, China. Chin Med J 2010; 123(13):1699–1701. 13. Ang M, Li X, Wong W, et al. Prevalence of and racial differences in pterygium: a multiethnic population study in Asians. Ophthalmology 2012;119(8):1509–1515. 14. Zhong H, Cha X, Wei T, et al. Prevalence of and risk factors for pterygium in rural adult Chinese populations of the Bai nationality in Dali: the Yunnan Minority Eye Study. Invest Ophthalmol Vis Sci 2012;53(10):6617–6621.
!
2014 Informa Healthcare USA, Inc.
383
15. Yoon KC, Mun GH, Kim SD, et al. Prevalence of eye diseases in South Korea: data from the Korea National Health and Nutrition Examination Survey 2008–2009. Korean J Ophthalmol 2011;25(6):421–433. 16. Sun LP, Lv W, Liang YB, et al. The prevalence of and risk factors associated with pterygium in a rural adult Chinese population: the Handan Eye Study. Ophthalmic Epidemiol 2013;20(3):148–154. 17. Lu P, Chen X, Kang Y, et al. Pterygium in Tibetans: a population-based study in China. Clin Experiment Ophthalmol 2007;35(9):828–833. 18. Paula JS, Thorn F, Cruz AA. Prevalence of pterygium and cataract in indigenous populations of the Brazilian Amazon rain forest. Eye (Lond) 2006;20(5):533–536. 19. Luthra R, Nemesure B, Wu S-Y, et al. Frequency and risk factors for pterygium in the Barbados Eye Study. Arch Ophthalmol 2001;119:1827–1832. 20. Asokan R, Venkatasubbu RS, Velumuri L, et al. Prevalence and associated factors for pterygium and pinguecula in a South Indian population. Ophthalmic Physiol Opt 2012; 32(1):39–44. 21. McCarty CA, Lee SE, Livingston PM, et al. Ocular exposure to UV-B in sunlight: the Melbourne visual impairment project model. Bull World Health Organ 1996; 74:353–360. 22. Wong TY, Foster PJ, Johnson GJ, et al. The prevalence and22 risk factors for pterygium in an adult Chinese population in Singapore: the Tanjong Pagar survey. Am J Ophthalmol 2001;131:176–183. 23. West S, Mun˜oz B. Prevalence of pterygium in Latinos: Proyecto VER. Br J Ophthalmol 2009;93(10):1287–1290. 24. Viso E, Gude F, Rodrı´guez-Ares MT. Prevalence of pinguecula and pterygium in a general population in Spain. Eye (Lond) 2011;25(3):350–357.
