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Myopia and Incident Cataract and Cataract Surgery: The Blue Mountains Eye Study

¹ From the Department of Ophthalmology, and the ² Department of Public Health and Community Medicine, University of Sydney, Sydney, Australia.

	Abstract

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PURPOSE. To assess whether an association exists between myopia and incident cataract and cataract surgery in an older population-based cohort study.

METHODS. The Blue Mountains Eye Study examined 3654 participants aged 49 years or more during 1992 to 1994 and then 2334 (75.1%) of the survivors after 5 years. A history of using eyeglasses for clear distance vision was obtained. Objective refraction was performed with an autorefractor, followed by subjective refraction with a logarithm of minimum angle of resolution (logMAR) chart. Emmetropia was defined as a spherical equivalent refraction between +1 D and -1 D, hyperopia as more than +1 D, and myopia as less than -1 D. Slit lamp and retroillumination lens photographs were graded for presence of cortical, nuclear, or posterior subcapsular cataract, according to the Wisconsin Cataract Grading System. Generalized estimating equation models analyzed data by eye.

RESULTS. There was a statistically significant association between high myopia (-6 D or less) and incident nuclear cataract (odds ratio [OR] 3.3, 95% confidence interval [CI] 1.5–7.4). Incident posterior subcapsular cataract was associated with any myopia (OR 2.1, 95% CI 1.0–4.8), moderate to high myopia (-3.5 D or less, OR 4.4, 95% CI 1.7–11.5), and use of distance glasses before age 20 (OR 3.0, 95% CI 1.0–9.3), after adjustment for multiple potential confounders, including severity of nuclear opacity. Incident cataract surgery was significantly associated with any myopia (OR 2.1, 95% CI 1.1–4.2) as well as moderate (-3.5 to more than -6D; OR 2.9, 1.2–7.3) and high myopia (OR 3.4, 95% CI 1.0–11.3).

CONCLUSIONS. These epidemiologic data provide some evidence of an association between myopia and incident cataract and cataract surgery, after adjustment for multiple confounders and severity of nuclear opacity. These data support other cross-sectional and longitudinal population-based findings.

	Introduction

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Myopia is relatively common in older populations, with reports indicating prevalence rates ranging from 15% (in those 49 years and older)¹ to 38.7% (in those aged 40–79 years).² Cataract is also common in older age groups, with increasing age associated with increased prevalence^{3 4} and incidence.⁵ High myopia is known to be associated with cataract,⁶ and a relationship between myopia and cataract has been suggested.^{7 8} Other reports reject the association with myopia, instead explaining that a trend to myopia is the direct consequence of the presence of nuclear cataract.⁹

To date, few population-based studies have attempted to assess the association between myopia and cataract. Cross-sectional data from the Blue Mountains Eye Study have provided such evidence, showing an association between myopia and both nuclear and posterior subcapsular cataract.¹⁰ The cross-sectional association between myopia and nuclear cataract was supported by data from the Beaver Dam Eye Study.¹¹ The longitudinal data from Beaver Dam, however, noted increased incident nuclear cataract, and possibly incident cortical cataract, in hyperopic eyes. In that study no relationship was found between myopia and 5-year incident cataract, but a higher incidence of cataract surgery was reported in myopes.¹²

A laboratory-based study identified reduced antioxidant properties in myopic eyes compared with those with typical age-related cataract.¹³ Increased levels of lipid peroxidation by-products have been found in cataractous lenses and in the vitreous of myopes compared with control subjects and nonmyopic cataractous lenses.^{13 14} An association was also shown between the degree of retinal lipid peroxidation and lens opacity in rodents.¹⁵ These studies provide a plausible explanation for the association between myopia and cataract and suggest that increasing myopia may be related to increasing damage to rod outer segments, which could lead to potentially cataractous by-products.

Our purpose in the present report is to assess the association between myopia and incident cataract and cataract surgery in a group of older Australians for whom baseline and follow-up information had been collected over a 5-year interval. These data could add further epidemiologic evidence to the debate about whether an association exists between myopia and cataract and may serve to guide laboratory-based studies in the search for biological explanations of cataract risk factors.

	Methods

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The Blue Mountains Eye Study is a population-based study of vision and common eye diseases in an urban population aged 49 years or older, resident in two postal codes of the Blue Mountains region, west of Sydney, Australia. The baseline survey methods and procedures have been described.^{16 17} The study was approved by the Western Sydney Area Health Service Human Ethics Committee and signed, informed consent was obtained from all participants. The research was conducted according to the recommendations of the Declaration of Helsinki. During 1992 to 1994 at the baseline examinations, 3654 (82.4%) of the 4433 eligible residents aged 49 to 97 years were assessed. Five-year follow-up examinations were conducted during 1997 to 1999, when 2334 (75.1%) of the survivors were reexamined. Of those not seen, 383 (12.3%) had moved from the area, and 394 (12.7%) refused the examination.

Questionnaire and Definitions
An interviewer-administered questionnaire enabled documentation of a detailed general medical and ocular history, as well as general demographic information. A history of myopia was sought by asking each participant whether he or she currently wore glasses to see clearly in the distance (including bifocals or multifocals), or had previously done so. If worn, the participant was asked at what age glasses were first used for clear distance vision. Data from this question were used only for participants with eyes having a measured myopic refractive error at baseline. Objective refraction was performed with an autorefractor (model 530; Humphrey, San Leandro, CA). This was followed by subjective refraction according to the Beaver Dam Eye Study modification of the Early Treatment Diabetic Retinopathy Study (ETDRS) protocol using a logarithm of minimum angle of resolution (logMAR) chart.^{17 18}

Baseline refraction data were used for analyses. The baseline refractive state was defined as the spherical equivalent refraction (SER), calculated by the algebraic addition of the best corrected spherical refraction and half the cylindrical refraction. Emmetropia was defined as a SER between +1 D and -1 D, hyperopia as more than +1 D, and myopia less than -1 D. Myopia was further classified as low (less than -1 D to more than -3.5 D), moderate (-3.5 D or less to more than -6 D) and high (-6 D or less). For those known to be myopic at baseline, the age at which distance glasses were first worn was used as a proxy for the onset and therefore duration of myopia. Hyperopia was also divided into low (greater then +1 D to less than +2 D), moderate (+2 D to less than +4 D), and high categories (+4 D or greater).

Participants were asked whether they smoked or consumed alcohol and whether oral or inhaled steroids had been prescribed in the past. They were asked whether they had angina (also described as "chest pain from your heart"), stroke, diabetes, or hypertension diagnosed by a doctor. Systolic and diastolic blood pressure was measured with the subject seated, before the use of any eye drops. Hypertension was defined either by history and/or a systolic measurement above 160 mm Hg and/or a diastolic measurement above 95 mm Hg. Diabetes was defined either by history or a fasting blood glucose level of 7.0 mmol/L or more. All blood samples were collected at a subsequent visit and later analyzed at Westmead Hospital. Sun-related skin damage was estimated by a clinical examiner on a four-point scale (none, mild, moderate, and severe) by assessing the arms, hands, and face.¹⁹ Participants had their weight (after removal of shoes and heavy clothing) and height measured. Body mass index was calculated as weight/height squared in kilograms per square meter, with obesity defined as a body mass index of 30 or greater. Higher educational achievement was defined as attainment of a qualification (certificate, diploma, or degree) after leaving school.

Cataract Grading
Cataract was documented by both slit lamp (Topcon SL-7e camera; Topcon Optical Co., Tokyo, Japan) and retroillumination (CT-R cataract camera; Neitz Instrument Co., Tokyo, Japan) lens photographs. Details of the photographic technique and grading^{3 16} used in the Blue Mountains Eye Study have been reported. The grading closely followed the Wisconsin Cataract Grading System,²⁰ with good agreement found for assessments of both inter- and intragrader reliability.³ History of past cataract surgery was confirmed at both the examination and photographic grading. At the follow-up study, graders were masked to baseline cataract status.

Presence of nuclear, cortical, and posterior subcapsular cataract was assessed in each eye.²⁰ Presence and severity of nuclear cataract was defined on a five-level scale by comparison with a set of four standard slit lamp photographs. Participants with nuclear grades 1 to 3 at baseline who developed nuclear grade level 4 or 5 at 5-year follow-up were defined as having incident nuclear cataract. The percentage area involved by cortical or posterior subcapsular cataract in each eye was calculated from the estimated percentage area involved in each of nine segments of the lens divided by a grid.²⁰ Participants with less than 5% cortical opacity at baseline who then developed 5% or more of the total lens area involved at follow-up were defined as having incident cortical cataract. Participants with no posterior subcapsular cataract at baseline with the presence of any posterior subcapsular cataract at follow-up were defined as having incident posterior subcapsular cataract. The definitions of each of these incident cataract types were not mutually exclusive.

Statistical Analysis
Because refraction is eye specific, analyses were run according to eye rather than subject. These were performed with all eyes combined using a generalized estimating equation method described by Zeger et al.²¹ and Liang and Zeger.²² This method allows data from both eyes to be used while accounting for the correlation between the two eyes of a single subject. Cataract was analyzed as a dichotomous variable. Because age is strongly associated with cataract incidence⁵ and both increased cataract prevalence^{3 4 23 24 25} and incidence^{5 26} has been noted in women, all odds ratios are age- and sex-adjusted, unless otherwise stated. For comparison, logistic regression analyses were also performed in right and then left eyes for both hyperopia and myopia. All presented results are from multivariate models that adjust for the same potential confounders as found in the tables, including level of nuclear opacity.

The variables included in multivariate generalized estimating equation models varied by cataract type. Variables considered for inclusion were: age (categorically), sex, smoking (ever versus never), current alcohol consumption (drinks per week), ever used inhaled steroids, dark brown iris color, educational achievement, sun exposure (none versus any sun-related skin damage), obesity, severity of nuclear opacity (levels 1–5), and history of diabetes, hypertension, stroke, or angina. Each model included only variables associated with that cataract type, either from our own age- and sex-adjusted incident analyses or from reports for prevalent or incident cortical,^{25 27 28 29 30} nuclear,^{25 27 29 31 32} or posterior subcapsular cataract,²⁵ as well as for cataract surgery.²⁵

Statistical analysis was performed on computer (Statistical Analysis System, ver. 6.12; SAS Institute Inc, Cary, NC). P < 0.05 was used to indicate statistical significance. Odds ratio (OR) and 95% confidence interval (CI) are presented.

	Results

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Over the 5-year period, nuclear cataracts developed in 593 (23.4%) eyes, cortical in 350 (9.8%) eyes, and posterior subcapsular in 100 (2.5%) eyes, according to data from both eyes. During this same period, 211 (4.7%) eyes underwent cataract surgery. Baseline aphakia, pseudophakia, or enucleation was present in 139 (3.0%) eyes, which were excluded from these analyses. The reported data refer to participants who attended both examinations and had gradable photographs from both visits. Approximately 8.7% of eyes had missing baseline and/or follow-up data for cortical or posterior subcapsular cataract, because photographs were ungradable or were not taken. A higher proportion (35.7%) had missing data for grading of nuclear cataract, predominantly because of an intermittent camera malfunction, as described in our previous report.³ There were no significant differences, however, between participants with and without gradable photographs.³

Of participants who returned for the 5-year examination, baseline refraction data were available on 4663 (99.9%) eyes, including 2218 (47.6%) emmetropic, 1925 (41.3%) hyperopic, and 520 (11.2%) myopic eyes. The myopic eyes included 330 (63.5%) with low myopia, 115 (22.1%) with moderate myopia, and 75 (14.4%) eyes with high myopia. Information about the age at which distance glasses were first worn was available for 464 eyes of participants with myopia (89.2%). In 52.6%, the age was 40 years more, in 25.6% between ages 20 and 39 years and in 21.8%, before 20 years. The hyperopic eyes included 961 (49.9%) with low hyperopia, 836 (43.4%) with moderate hyperopia, and 128 (6.6%) with high hyperopia.

Baseline characteristics of participants in the 5-year follow-up examination who were included in any analyses and survivors of the baseline examination who did not attend follow-up are shown in Table 1 . There were no statistically significant differences (P < 0.05) between these two groups. Of the 2334 participants in both examinations, 56 were not included in any analyses (44 because of nongradable photographs at baseline and 12 because of nongradable photographs at follow-up).

	Discussion

Top Abstract Introduction Methods Results Discussion References

An important limitation of this report is that using the age at which distance glasses were first worn as a proxy for onset of myopia does not take into account the many factors that impact on the decision to start wearing glasses. As pointed out by Wong et al.¹¹ in the Beaver Dam Eye Study report on the relationship between refractive errors and incident cataract, poor memory and interpretation of this question may be relevant factors and may have played a role in the reported inconsistencies between a history of wearing distance glasses, the age at first wearing, and prevalent age-related cataract.^{11 33}

Similarly, the decision to undergo cataract surgery, particularly on a second eye, takes into account many factors other than severity of cataract. In our effort to counter the possibility that statistically significant associations with myopia may have been due to the presence of baseline nuclear cataract, interpretation of those adjusted results was limited by the fact that a significant proportion of participants had missing baseline data for nuclear cataract because of random camera malfunction (so reducing the power of our analyses). Our definitions of incident cortical and nuclear cataract may also pose a limitation. Presence of less than 5% baseline cortical opacity and baseline nuclear grades 1 to 3 were not considered to be cataract. Although we sought to encompass a level of clinically significant cataract to define cataract incidence, inclusion of any baseline cataract may have had a minor influence on our findings.

Strengths of our study include its high participation rate from a well-defined urban residential population. Information was collected about a large number of potential confounders as well as detailed information on refractive status.¹ Documentation of cataract status, based on reproducible grading of lens photographs according to the Wisconsin System, is a further strength. Graders of the prospective lens photographs were masked to refractive state and so could not be influenced by selection bias.

The development of age-related cataract is widely known to be associated with a myopic shift in refraction, principally by progression of the level of opacity within the lens nucleus.⁹ The Visual Impairment Project demonstrated a strong cross-sectional association between myopia and nuclear opacity,^{24 34} as did the Barbados Eye Survey.³⁵ In the 5-year examinations of the Beaver Dam Eye Study, participants with the highest levels of nuclear opacity at baseline were more likely to have a myopic shift in refraction.³⁶

As cataract is frequently mixed, it is reasonable to adjust for the level of nuclear opacity when examining the impact of myopia on development of other cataract types. Our study indicates that myopia was related to incident posterior subcapsular cataract (as well as incident cataract surgery), after taking into account the effects both from multiple confounders plus the level of nuclear opacity. Adjustment for level of nuclear opacity, however, may be less important in assessing longitudinal associations, as we used the baseline refractive state to evaluate the impact of refractive error on development of cataract over time. The moderately strong relationship found between incident posterior subcapsular cataract and either moderate or high myopia at baseline argues that myopic shift may not be a relevant influence. It could be expected that further cataract-associated myopic shifts would be of a low magnitude.

The apparent relationship found in our study between duration of myopia and both incident posterior subcapsular cataract and incident surgery provides further support for a true association between myopia and this cataract type. This was seen for both longer-duration subgroups, but was strongest and statistically significant only in the fully adjusted model for those myopic subjects who reported wearing glasses for the longest period.

Apart from the association found with posterior subcapsular cataract, our data provide no evidence for a relationship between myopia, or other refractive error, and cortical cataract. Incident nuclear cataract was unrelated to baseline low or moderate magnitude myopia, but a relationship was found with high myopia, after adjustment for confounders. A weak relationship was observed between incident nuclear cataract and moderate hyperopia. There was, however, no statistically significant relationship with any hyperopia, and the odds ratios in the hyperopia categories did not show a dose–response relationship, suggesting that this finding could be spurious.

Although our prevalence findings suggested a protective influence of hyperopia for posterior subcapsular cataract,¹⁰ this was not supported longitudinally, either in our current data or from the Beaver Dam Eye Study data.¹¹ the Beaver Dam findings reported a significant trend (P = 0.02) for increasing myopia and higher prevalence of posterior subcapsular cataract. This was not, however, supported by their incidence data. In contrast, our longitudinal data supported the cross-sectional associations found with any myopia or high myopia and in persons with onset of myopia in their youth.

Small posterior subcapsular opacities may cause significant visual disturbance because of their central location in the visual axis. Because these opacities thus have a propensity to progress to cataract surgery relatively quickly compared with nuclear or cortical opacities, it seems reasonable to consider incident cataract surgery as a surrogate for the development of posterior subcapsular cataract. The number of incident posterior subcapsular cataract cases may also be limited because of varying thresholds for cataract surgery.

The Beaver Dam Eye Study found a statistically significant association between baseline myopia and 5-year incident cataract surgery,^{11 12} as well as a significant trend (P = 0.003) for the relationship between increasing levels of myopia and increased incidence of cataract surgery.¹¹ Our longitudinal results provide strong support for this finding, with significant associations present between myopia at all levels and in all models examined, apart from low myopia in the multivariate model that adjusted for severity of nuclear cataract.

Our finding of a link between myopia and cataract is supported by data from several other studies.^{2 24 37 38 39 40 41} The Visual Impairment Project reported a statistically significant association between myopia (defined as 1 D) and cortical, nuclear, and posterior subcapsular cataract.^{24 37} The Melton Mowbray Eye Study reported a higher prevalence of cataract in myopes.³⁸ Participants who had worn eye glasses before age 20 (used as an indicator for myopia) had a higher relative risk (RR) for nuclear cataract in the Longitudinal Study of Cataract (RR 1.37, 95% CI 0.97–1.95),⁴⁰ and a higher risk of development of mixed cataract in the Lens Opacities Case–Control Study (OR 1.44, 95% CI 1.06–1.94).³⁹ In an Oxfordshire case–control study of patients who had had cataract surgery and control subjects aged between 50 and 79 years,⁴² a statistically significant increased risk of cataract was found in participants with a history of childhood myopia (RR 1.68, 95% CI 1.2–2.4). In several reports in which the records of patients who had undergone cataract surgery were reviewed,^{7 8} myopes were found to be more likely to undergo surgery than nonmyopes.

Biological plausibility of this association has been provided by a number of laboratory-based studies. Development of cataract in myopic lenses has been shown to be related to oxidative changes in lens proteins,⁴³ with glutathione a potential inhibitor of this oxidation.⁴⁴ Compared with healthy control subjects, cataractous lenses had lower levels of glutathione, with the lowest levels found in myopic lenses.¹³ Increased levels of malondialdehyde (MDA) have been found in cataractous lenses and in the vitreous of myopes compared with control subjects and nonmyopic cataract lenses.^{13 14} Because MDA is a breakdown product of lipid peroxidation, the vitreous finding suggests a retinal source. Rod outer segments are particularly susceptible to lipid peroxidation because of the high concentration of polyunsaturated lipid in their membranes.

One study has shown a correlation between degree of retinal lipid peroxidation and extent of lens damage.¹⁵ A subsequent study has shown a correlation between the level of thiobarbituric acid reactive substances (also indicating lipid peroxidation) in the subretinal fluid of patients who undergo retinal detachment surgery and the degree of myopia.⁴⁵ These results suggest that increasing myopia may be related to increasing damage of rod outer segments and that by-products of this process may affect various ocular structures, including the lens. This could explain the higher prevalence and incidence, particularly of posterior subcapsular cataract and nuclear cataract, in myopic eyes.

Myopia increases the risk of glaucoma^{35 46} as well as retinal detachment, myopic retinal degeneration, visual impairment, and blindness.⁴⁷ The present study builds on our earlier finding¹⁰ in suggesting that myopia may increase the risk of posterior subcapsular cataract, one of the important predictors of cataract surgery. This finding is potentially important, given the increasing prevalence of myopia in East Asia,^{48 49} the United States,⁵⁰ and elsewhere.⁵¹

In this study, we assessed the association between baseline refraction and the 5-year incidence of cataract and cataract surgery. We have been able to provide epidemiologic evidence to confirm the previously noted increased risk of posterior subcapsular cataract in eyes with high myopia. We have also provided evidence to support the hypothesis that this type of cataract may develop more frequently in eyes with lower levels of myopia. These longitudinal data support our cross-sectional findings as well as the findings from some, but not all,¹¹ population-based reports. Previously, this association was considered because of the myopic shift from increasing nuclear opacity and was thought unlikely to be causally related.³⁷ Our data suggest the possibility of a causal relationship. Although some laboratory-based studies support a plausible biological basis, further studies are needed.

	Footnotes

 
Supported by Australian National Health and Medical Research Council Grant 974159, and the Westmead Millennium and Save Sight Institutes, University of Sydney.

Submitted for publication November 16, 2001; revised April 18, 2002; accepted April 26, 2002.

Commercial relationships policy: N.

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. 1734 solely to indicate this fact.

Corresponding author: Paul Mitchell, Department of Ophthalmology (Centre for Vision Research), University of Sydney, Westmead Hospital, Hawkesbury Road, Westmead, NSW 2145, Australia; paulmi{at}westgate.wh.usyd.edu.au.

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