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Abstract
Aims To determine prevalence of pterygium, its role as main cause of unilateral and bilateral visual impairment and blindness and its impact on refractive errors from adults living in a high ultraviolet exposure area in the Brazilian Amazon Region.
Methods Cluster sampling was used in randomly selecting subjects ≥45 years of age from urban and rural areas of Parintins city. Eligible subjects were enumerated through a door-to-door household survey and invited for an eye exam including refraction. Pterygium was assessed considering location (nasal, temporal or both) and size (<3 mm or ≥3 mm reaching or not pupillary margin).
Results A total of 2384 persons were enumerated and 2041 (85.6%) were examined. Prevalence of pterygium was 58.8% (95% CI 53.8% to 63.7%) and associated with male gender (OR=1.63; 95% CI 1.37 to 1.94; p=0.001), while higher education was a protective factor (OR=0.63; 95% CI 0.44 to 0.92; p=0.018). Older age and rural residence were associated with pterygium ≥3 mm reaching or not pupillary margin, while higher education was a protective factor for pterygium ≥3 mm reaching pupillary margin. Prevalence of pterygium as cause of visual impairment and blindness was 14.3% and 3.9%, respectively. Significantly higher hyperopic refractive errors were found in eyes with pterygium ≥3 mm reaching or not pupillary margin.
Conclusions Pterygium was highly prevalent and the second cause of visual impairment and blindness after provision of refractive correction. Risk factors for pterygium were male gender, advanced age, lower education and rural residency. Strategies to provide pterygium early detection and proper management should be considered by healthcare authorities in this population.
- Pterygium
- Prevalence
- Blindness
- Visual Impairment
- Refractive Errors
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Introduction
Pterygium is a triangular dysplasia of bulbar conjunctiva characterised by a fibrovascular overgrowth from the limbo towards the cornea centre attributed to chronic ultraviolet (UV) B exposure.1–3 Clinical, epidemiological and laboratory studies indicate a multifactorial process leading to pterygium development.4 Besides UV light exposure, different risk factors contribute to its formation as heredity factors and chronic inflammation.5 Despite efforts to further characterise pterygium pathogenesis, the specific stimulus to pterygium development and progression remains unclear.2
Pterygium occurs all around the world, but there is an important variability on frequencies according to the population under study and their geographic location related to the equator line. The occurrence of pterygium is higher in the ‘pterygium belt’, a region located between the latitudes 40o north and south, and progressively decreases as the latitude increases.6–8
Despite a high prevalence in some areas, pterygium is not commonly associated as a potential cause of visual impairment and blindness.7 9 Specific studies in Southeast Asia and South America have demonstrated that bilateral pterygium can lead to blindness10 11 and, therefore, this condition deserves attention to achieve correct diagnosis and treatment.
Visual impairment usually occurs when pterygium causes changes in corneal biomechanics that lead to loss of transparency and curvature abnormalities resulting on important induced astigmatism.12 The corneal flattening induced by pterygium is associated with tractional forces and the pooling of tears at the pterygium apex.13 14
In Brazil, pterygium prevalence has been reported in specific populations as groups of native Brazilians,15 riverside communities from the Amazon16 and urban residents in a city of Southeast Brazil,17 with prevalence ranging from 5% to 41%. Nonetheless, visual impairment and blindness due to pterygium were not addressed in these studies.
The present data come from a population-based survey of visual impairment and blindness among adults in the city of Parintins located within the pterygium belt, the Brazilian Amazon Region Eye Survey (BARES).18 The purposes of the current study were: (A) to determine the prevalence of pterygium and possible sociodemographic factors associated with it, (B) to investigate pterygium as cause of unilateral and bilateral visual impairment and blindness and (C) to describe refractive errors in eyes with pterygium.
Methods
Study population
BARES is a population-based, cross-sectional epidemiological study designed to examine prevalence and causes of visual impairment and blindness in a non-institutionalised sample of Brazilian Amazonians adults.
According to the last census (2010),19 Parintins is a 102 718 inhabitants city located at 02°37′42″S and 56°44′09″’W, in the centre of the Brazilian Amazon Region. The UV index is a linear scale that calculates the UV incidence and its adverse effects on human tissues. A UV index higher than 11 represents a risk of harm from unprotected sun exposure. The North region of Brazil has a mean annual UV index of 12.5 being the highest of the country.20
The study population consisted of residents 45 years or older, living in 20 randomly selected clusters (14 urban and 6 rural, based on census criteria). Further details on sampling plan have been reported elsewhere.18 In brief, a door-to-door enumeration was performed, and eligible subjects (45 years of age and older residing for at least 6 months in Parintins city) were informed about the study and invited to participate in a clinical ophthalmic examination.
Ethical approval and informed consent
The institutional review board/ethics committees from Universidade Federal de São Paulo (UNIFESP) and from Universidade Federal do Amazonas (UFAM) approved the study protocol. The study was carried out in accordance to the tenets of the Declaration of Helsinki. Written informed consent was obtained from all participants after explanation of the nature and possible consequences of the study.
Sociodemographic data
The enumeration form included household address, phone number and a roster of those living in that home along with their sex, age and educational level. All eligible individuals were invited and scheduled for a detailed eye examination. Written informed consent was obtained at the examination site.
Clinical data
The examination protocol was similar to the one used in a previous study in Brazil, the São Paulo Eye Study.21 In-home eye examination was offered for those who could not come to the clinic.
Ophthalmic technologists measured from each eye presenting distance visual acuity (PVA), with spectacles if the participant presented with them, followed by uncorrected distance visual acuity (UCVA), using retroilluminated logarithm of the minimum angle of resolution tumbling E charts at 4 m distance. Best-corrected visual acuity (BCVA) was determined for each eye after automated and subjective refraction performed by ophthalmologists.
The eye examination included biomicroscopy, lens status, intraocular pressure measurement and fundus examination under dilation. Pterygium was classified by the ophthalmologist using the slit lamp considering: (A) occurrence (present or absent); (B) laterality (unilateral or bilateral); (C) location (nasal, temporal or both) and (D) size (<3 mm, ≥3 mm but not reaching pupillary margin or ≥3 mm reaching pupillary margin).
Individuals with different lesion severity in each eye were counted for prevalence calculation considering the most severe eye. Those with previous pterygium surgery signs through biomicroscopy were included for the corrected prevalence calculation.
At the end of the exam, the ophthalmologist had a 14-item list to determine the principal cause of visual impairment (presenting visual acuity 20/40 or worse) for each eye for distance vision.18
Impact of pterygium on visual status
To investigate the influence of pterygium on vision status, individuals with bilateral pterygium had visual acuity measurements categorised as: normal vision (≥20/32 in both eyes); unilateral visual impairment due to pterygium (<20/32 to ≥20/200 in the worse-seeing eye and ≥20/32 in the fellow eye); bilateral visual impairment due to pterygium (<20/32 to ≥20/200 in both eyes); unilateral blindness due to pterygium (<20/200 in the worse-seeing eye and ≥20/200 in the fellow eye); and bilateral blindness due to pterygium (<20/200 in both eyes).
The principal causes of visual impairment from each eye were analysed in order to also evaluate the impact of pterygium separately with visual acuity measurements categorised as: normal visual (≥20/32); moderate visual impairment (<20/32 to ≥20/63); visual impairment (<20/63 to ≥20/200); moderate blindness (<20/200 to ≥20/400); and severe blindness (<20/400).
Refractive errors
Refractive parameters obtained from computerised and subjective refractions were noted and compared among eyes without pterygium, with pterygium <3 mm, ≥3 mm not reaching pupillary margin and ≥3 mm reaching pupillary margin.
Statistical analysis
Statistical analyses were performed using Stata/SE Statistical Software, Release V.14.0, 2015.22 Frequency tables were used for descriptive analysis. The associations between categorical variables were evaluated through multiple logistic regressions. The association of continuous variables with categorical predictors was evaluated through analysis of variance. Post hoc Bonferroni analyses were performed to evaluate the results in different levels of covariables. Confidence intervals (CIs) for prevalence estimates and regression odds ratios (ORs) were calculated taking cluster sampling design effects into account. P values ≤0.05 were considered statistically significant.
Results
Of the 9931 residents from the selected clusters, 2384 (24.0%) were eligible for the study. Of these, 2041 completed an ophthalmic examination, representing a participation rate of 85.6%, whereas 335 (14.1%) did not show up for the clinical examination and 8 (0.3%) refused to participate. Demographic characteristics of the study population were described in detail previously.18 table 1 shows the distribution of sex, age and educational level of the participants from rural and urban areas.
Study population by sex, age and educational level in urban and rural areas
Prevalence of pterygium
Any type of pterygium in either eye was found in 1199 individuals representing an overall prevalence of 58.75% (95% CI: 53.82% to 63.67%). Unilateral pterygium was found in 398 individuals representing a prevalence of 19.50% (95% CI 17.81% to 21.19%) and bilateral pterygium was found in 801 individuals representing a prevalence of 39.25% (95% CI: 34.12% to 44.37%).
A total of 122 eyes of 92 (4.51%) participants presented signs of previous pterygium excision, and recurrence of disease was observed in 72 (78.26%). The remaining 20 participants operated but with no recurrence were considered for the calculation of corrected prevalence of 59.73% (95% CI: 54.96% to 64.49%).
Pterygium prevalence according to size taking into account age, sex, educational level and residence area are shown in table 2. Overall, 171 (14.3%) of the participants with pterygium in at least one eye (n=1199) had pterygium surgery indication. Details from the lesion size showed that 162 (36.6%) with pterygium ≥3 mm were referred for surgery, while 9 (1.2%) with pterygium <3 mm did.
Prevalence of pterygium according to socio-demographic factors
Multiple logistic regressions were used to investigate the association of pterygium with sociodemographic factors. Male gender (OR=1.63; 95% CI: 1.37 to 1.94; p=0.001) was associated with the presence of any type of pterygium in either eye, while higher education was a protective factor (OR=0.63; 95% CI: 0.44 to 0.92; p=0.018). Older age (OR=1.68; 95% CI: 1.09 to 2.59; p=0.021) and rural residency (OR=1.55; 95% CI: 1.12 to 2.15; p=0.011) were associated to pterygium ≥3 mm not reaching pupillary margin in either eye. Older age (OR=3.66; 95% CI: 1.89 to 7.11; p=0.001) and rural residence (OR=1.68; 95% CI: 1.02 to 2.77; p=0.044) were associated to pterygium ≥3 mm reaching pupillary margin, while higher education was a protective factor (OR=0.24; 95% CI: 0.06 to 0.99; p=0.049). table 3 shows the results of the regression for pterygium presence according to size.
Multiple logistic regression for pterygium presence adjusted for sex, age category, educational level and residence area
Most cases were bilateral (66.8%; 95% CI: 62.9% to 70.7%) with lesions smaller than 3 mm (68.9%; 95% CI: 66.9% to 70.9%) and located only nasally (78.1%; 95% CI: 76.3% to 79.9%). Multiple logistic regression shows that men were 1.51 times more likely to have bilateral pterygium than women (OR=1.51; 95% CI: 1.24 to 1.84; p<0.001).
Pterygium as cause of visual impairment and blindness
In 16 examined participants, reliable visual acuity measurements could not be obtained in either eye (nine with pterygium either eye and seven without pterygium). Therefore, the analysis regarding visual status and refractive error counted with a total of 2025 participants (4050 eyes).
Figure 1 shows the influence of pterygium on vision status of 824 individuals with bilateral pterygium. When considering bilateral visual status, 8.4% of individuals with bilateral pterygium had any level of visual impairment, while 34.9% had no visual impairment at all, and 54.7% were visually impaired/blind for other reason than pterygium.
Visual status of individuals with bilateral pterygium.
When analysing each eye separately, pterygium was assigned as the third PVA (<20/32) in 106 (4.43%) of 2393 eyes with impairment, following uncorrected refractive errors in 1384 (57.84%) eyes and cataract in 634 (26.49%).23 Overall, the prevalence of pterygium as the main cause of moderate visual impairment (n=28), visual impairment (n=62), moderate blindness (n=9) and severe blindness (n=7) were, respectively, 2.4%, 6.8%, 10.6% and 2.8%. Moderate visual impairment and visual impairment with pterygium as main cause were present in 90 eyes, with 59 showing pterygium ≥3 mm. In terms of moderate and severe blindness, pterygium was assigned as the main cause in 16 eyes, and all of them presented the disease ≥3 mm reaching pupillary margin.
Refractive errors
All the examined eyes went through automated and subjective refraction. The spherical and cylinder components data of these tests are shown in figure 2.
Spherical and cylindrical components of eyes with and without pterygium.
Using analysis of variance, pterygium was statistically associated with refractive error, considering both subjective (spherical component (F=36.63, p<0.001) and cylindrical component (F=103.24, p<0.001)) and automated refraction (spherical component (F=151.57, p<0.001) and cylindrical component (F=388.35, p<0.001)). Post hoc analysis of Bonferroni indicates that there was no significant difference (p=0.429) between eyes with pterygium <3 mm (mean spherical=0.83±0.05; mean cylindrical=−1.09±0.03) and eyes without pterygium (mean spherical=0.86±0.04; mean cylindrical=−1.01±0.02) in automated refraction. Similar results were found for subjective refraction with no significant difference (p=0.378) between eyes with pterygium <3 mm (mean spherical=0.53±0.05; mean cylindrical=−0.72±0.02) and eyes without pterygium (mean spherical=0.64±0.04; mean cylindrical=−0.66±0.02).
Eyes with pterygium ≥3 mm not reaching pupillary margin have shown a statistically greater (p<0.05) magnitude of refractive errors in both automated (mean spherical=2.89±0.14; mean cylindrical=−3.20±0.13) and subjective (mean spherical=1.44±0.09; mean cylindrical=−1.46±0.06) refraction when compared with eyes without pterygium or eyes with pterygium <3 mm.
Eyes with pterygium ≥3 mm reaching pupillary margin have shown a statistically greater (p<0.05) magnitude of refractive errors in both automated (mean spherical=4.88±0.95; mean cylindrical=−5.46±0.55) and subjective (mean spherical=1.35±0.27; mean cylindrical=−1.51±0.22) refraction when compared with eyes without pterygium, pterygium <3 mm or pterygium ≥3 mm not reaching pupillary margin.
Discussion
The strengths of this study were the large, randomly selected sample of participants and the fact that refraction was performed in all participants along with measurement of uncorrected, presenting and best-corrected visual acuity from each eye. Limitations included the distance and costly access to the city of Parintins, the fact that the whole survey had to be executed during only four visits to maximise the permanence of the study team, the transport of equipment and availability of infrastructure for the ophthalmic exam.
A high prevalence of pterygium was found in the studied population with around 60% of participants presenting lesions in either eye. Previous population-based studies performed in other low latitude regions as Indonesia, China, Myanmar and Japan have reported prevalence, respectively, of 48.7%, 33.0%, 19.6% and 30.8%.7 10 24 25
Although most studies performed in the equatorial region have shown a high prevalence of pterygium, low latitude associated with high UV exposure is not the only factor associated with the disease development. A study with 3280 adults 40 years and older from Singapore located at 1o N has found a prevalence of 12.1%, substantially lower than those described in other equatorial line region studies.26 The population profile is a determinant for the disease development so that people who have an indoor lifestyle tends to be less likely to develop pterygium as the direct ultraviolet exposure is reduced. The Singapore study dealt only with urban population explaining the lower prevalence found.
A study of pterygium among indigenous communities in the Brazilian Amazon found a prevalence of 36.6% in 265 residents living in the river margin and 5.0% in 359 living in the forest.15 Social behaviour, especially the rate of sun exposure, appears to be the main factor for the different rates between these two indigenous groups. Another study in Amazonian riverside communities has shown a prevalence of 41.1% in 659 adults older than 18 years old with 75.6% of cases presenting bilateral pterygium.16
A higher prevalence of pterygium greater or equal than 3 mm in rural residents was found in our study. A possible explanation is the lack of access for healthcare facilities in rural areas, since people living in urban areas could have a higher chance to treat and/or prevent the disease before its progression.
Males were more likely to develop pterygium than women corroborating previous studies in China, Indonesia, Singapore and Japan. 1,7,25-26 Lower education also showed up as a significant factor associated to the presence of pterygium. Higher prevalence in men is linked with higher UV exposure, since men are usually reported as outdoor workers. Similarly, those with lower education tend to have outdoor jobs and also have an increased UV exposure. However, those assumptions could not be properly evaluated on the present study as we did not have information regarding the occupation of the participants, but mainly in rural areas most of inhabitants were either fisherman or agricultural workers implying in outdoor lifestyle.
Pterygium is a progressive disease, and its growth is related to a dose–response profile, meaning that prolonged UV exposure leads to severity increase. In that sense, advanced age is expected to be associated with pterygium severity, as our data showed. Severe types of pterygium might be the result of untreated lesions with significant UV exposure along the years without proper protection.27 28 It is debatable whether pinguecula should be considered a risk factor for pterygium, mainly in unilateral pterygium cases.29 In our study, pinguecula was found in 355 (17.4%) subjects. Considering only unilateral pterygium cases (n=398), 94 (23.6%) subjects had pinguecula in the fellow eye.
A recent meta-analysis conducted to determine global prevalence and risk factors to development of pterygium has found an overall prevalence of 12%. In accordance with our study, older age, male sex and living in rural environments are the leading demographic risk factors for the development of pterygium. Other risk factors were outdoor occupation, sunlight exposure over 5 hours per day and alcohol consumption, whereas use of sunglasses and smoking showed up as protective factors, reinforcing that sociodemographic factors are associated with pterygium development and the individual’s lifestyle plays an important role in the disease natural history.30
Although pterygium pathogenesis is linked to UV exposure, recent molecular biology investigations have found genes and protein expression profile of pterygium greatly different from normal conjunctiva or cornea.31 It is hypothesised that genetic factors may interfere with the control of fibrovascular proliferation while UV light most likely only triggers pterygium development by inducing growth factors that in fact promote fibrovascular proliferation in predisposed individuals.5 Further studies should be performed to understand the mechanisms by which these genes and proteins are involved in pterygium.
When analysing the impact of bilateral pterygium on visual status, 34.7% of the individuals had no visual impairment, 56.9% had visual impairment due to other causes and only 8.4% presented any level of impairment with pterygium as the main cause, with the vast majority presenting pterygium ≥3 mm reaching or not pupillary margin.
The analysis of each eye separately indicates pterygium as the third more frequent cause of visual impairment and blindness when considering the PVA (4.4%) becoming the second more frequent cause considering the BCVA (10.5%).
A greater magnitude of spherical and cylindrical components of refraction was observed in eyes with more advanced pterygium. The high levels of astigmatism and hyperopia in these eyes occur due to tractional forces of contractile elements within the pterygium that leads to mechanical distortion and flattening of the cornea in its horizontal meridian resulting in hyperopic astigmatism.32 33 Eyes with pterygium smaller than 3 mm had similar refractive status than eyes without pterygium indicating that small lesions do not affect the cornea structure on the same way large lesions do. Previous studies have demonstrated the association of pterygium with astigmatism10 34 as supported by the present study. The induced astigmatisms have shown to increase proportionally to the severity of the lesion. Discrepancies between automated and subjective refraction were evident, especially in more severe cases due to the intolerance of high-power cylindric corrective lenses when performing subjective refraction.
In a population of adults located in the pterygium belt, this condition was highly prevalent and was the second main cause of visual impairment and blindness after provision of refractive correction. Males, advanced age, lower educational level and rural residency were risk factors for variable severity lesions. A hyperopic spherical and cylindrical shift was detected mainly in eyes with severe pterygium, supporting corneal changes caused by the disease. Strategies to provide early detection and proper management of pterygium should be considered by healthcare authorities in this population.
References
Footnotes
Contributors AB, AGF, SRS, NNF and SM contributed to the planning, conducting and reporting of the work described in the article. MHM, JMF, MCC, CCC, GCV, PYS, PHM, MJC, JMC, SSW, MC and RBJ contributed to conducting and reporting the work described in the article. All authors reviewed the manuscript.
Funding This work was supported by the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico – CNPQ, Brasilia, Brazil, Programa Ciencias sem Fronteiras (Grant # 402120/2012-4 to SRS, SM and JMF; research scholarships to SRS and RBJ); Fundacao de Amparo a Pesquisa do Estado de Sao Paulo, FAPESP, Sao Paulo, Brazil (Grant # 2013/16397-7 to SRS); SightFirst Program – Lions Club International Foundation (Grant #1758 to SRS), Instituto da Visão, IPEPO, São Paulo, SP, Brazil, Fundação Piedade Cohen, Manaus, AM, Brazil.
Competing interests None declared.
Patient consent for publication Not required.
Ethics approval The institutional review board/ethics committees from Universidade Federal de São Paulo and from Universidade Federal do Amazonas approved the study protocol.
Provenance and peer review Not commissioned; externally peer reviewed.
Data availability statement Data are available on request.
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