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American Journal of Clinical Nutrition, Vol. 87, No. 6, 1899-1905, June 2008
© 2008 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

Antioxidant nutrient intake and the long-term incidence of age-related cataract: the Blue Mountains Eye Study1,2,3,4

Ava Grace Tan, Paul Mitchell, Victoria M Flood, George Burlutsky, Elena Rochtchina, Robert G Cumming and Jie Jin Wang

1 From the Department of Ophthalmology, Centre for Vision Research, Westmead Millennium Institute, University of Sydney, Sydney, NSW, Australia (AGT, PM, VMF, GB, ER, and JJW); the Human Nutrition Unit, Department of Molecular and Microbial Biosciences (VMF) and the School of Public Health, University of Sydney, Sydney, NSW, Australia (RGC); and Centre for Eye Research Australia, Department of Ophthalmology, University of Melbourne, Melbourne, Australia (JJW)

2 Presented in abstract form at the Association for Research in Vision and Ophthalmology 2007 annual meeting; Fort Lauderdale, FL; May 2007.

3 Supported by the Australian National Health & Medical Research Council, Canberra, Australia (grants 932085, 974159, and 211069).

4 Address reprint requests to JJ Wang, Centre for Vision Research, Westmead Millennium Institute, University of Sydney, Sydney, NSW, Australia. E-mail: jiejin_wang{at}wmi.usyd.edu.au.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Oxidative stress has been implicated in cataractogenesis. Long-term intake of antioxidants may offer protection against cataract.

Objective: We investigated relations between antioxidant nutrient intakes measured at baseline and the 10-y incidence of age-related cataract.

Design: During 1992–1994, 3654 persons aged ≥49 y attended baseline examinations of the Blue Mountains Eye Study (82.4% response). Of these persons, 2464 (67.4%) participants were followed ≥1 time after the baseline examinations (at either 5 or 10 y). At each examination, lens photography was performed and questionnaires were administered, including a 145-item semiquantitative food-frequency questionnaire. Antioxidants, including β-carotene, zinc, and vitamins A, C, and E, were assessed. Cataract was assessed at each examination from lens photographs with the use of the Wisconsin Cataract Grading System. Nuclear cataract was defined for opacity greater than standard 3. Cortical cataract was defined as cortical opacity ≥ 5% of the total lens area, and posterior subcapsular (PSC) cataract was defined as the presence of any such opacity.

Results: Participants with the highest quintile of total intake (diet + supplements) of vitamin C had a reduced risk of incident nuclear cataract [adjusted odds ratio (OR): 0.55; 95% CI: 0.36, 0.86]. An above-median intake of combined antioxidants (vitamins C and E, β-carotene, and zinc) was associated with a reduced risk of incident nuclear cataract (OR: 0.51; 95% CI: 0.34, 0.76). Antioxidant intake was not associated with incident cortical or PSC cataract.

Conclusion: Higher intakes of vitamin C or the combined intake of antioxidants had long-term protective associations against development of nuclear cataract in this older population.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Oxidative stress has long been implicated in the development of age-related cataract (1-5). Hydrogen peroxide present in the aqueous can give rise to reactive oxygen species (ROS) (6, 7), such as superoxides and hydroperoxides (8), which can damage lens components, such as crystallin proteins, lens fiber membranes, and lipids, leading to lens opacities (1, 9-12).

The relation between antioxidants and cataract formation is not well established. Observational population-based and case-control studies have reported inconsistent results (13), and clinical trials showed little benefit from vitamin supplementation either on preventing or reducing progression of age-related cataract (13-17).

The development of age-related cataract is a slow process, and the effects of environmental and lifestyle factors would be unlikely to be detected in the short term. Our study therefore aimed to investigate relations between antioxidant nutrient intake measured at baseline and the long-term (cumulative 10 y) incidence of age-related cataract in the Blue Mountains Eye Study.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The Blue Mountains Eye Study (BMES) is a population-based cohort study of vision, common eye, and systemic conditions in a population aged ≥49 y, living in a defined 2-postcode region west of Sydney, Australia. At baseline (1992–1994), 3654 (82.4% of eligible) persons participated. Surviving participants were invited to attend follow-up examinations after 5 (1997–1999) and 10 (2002–2004) y.

Survey methods and procedures were previously described (18, 19). Briefly, all participants underwent a detailed eye examination, including retinal and lens photography, and interviewer-administered questionnaires to collect medical and demographic history. Written informed consent was obtained from all participants. The study was conducted according to the recommendations of the Declaration of Helsinki, and approval was obtained from the Western Sydney Area Health Service Human Research Ethics Committee. The same procedures were used at each of the 3 examinations.

Cataract grading
Cataract was assessed with the use of retroillumination (Neitz CT-R; Neitz Instruments, Tokyo, Japan) and slit-lamp (Topcon SL-7e; Topcon Optical, Tokyo, Japan) lens photographs. Details of the photographic and grading procedures used at all 3 examinations were previously described (19). Nuclear cataract was determined by comparing participant slit-lamp photographs against a set of 4 standards. Nuclear opacity greater than Wisconsin standard photograph number 3 was defined as nuclear cataract. Cortical and posterior subcapsular (PSC) cataract types were assessed by laying a grid over the anterior and posterior retroillumination photographs in turn and estimating the percentage area involved for each cataract type. Typically, cortical cataract is graded from the anterior photograph, and PSC cataract is graded from the posterior photograph. The total area of opacity involved was calculated for each eye. Cortical opacity was considered present for total areas ≥ 5%. PSC cataract was considered present if any such opacity was present. The presence of an intraocular lens implant or the absence of the lens was confirmed from the retroillumination or slit-lamp photographs and classified as cataract surgery. For participants without gradable lens photographs, self-reported past history of cataract surgery was confirmed from the eye examination. Eyes without a particular cataract type at baseline were considered at risk of that cataract type and so were included in the assessment of incident cataract. Both inter- and intragrader reliability of the cataract grading was high (20).

Measurement of nutrient intakes
Participants were asked to complete a 145-item self-administered food-frequency questionnaire (FFQ), modified for the Australian diet and vernacular from a Willett FFQ (21), that detailed food consumption, including portion size estimates and frequency. The FFQ also included questions on the use of dietary supplements. The use of the FFQ for the BMES was validated with weighed food records, with Spearman correlation coefficients > 0.50 for most nutrients (22). Nutrient intakes were calculated with the use of the Australian Tables of Food Composition 1990 (23) and the US Department of Agriculture Carotenoid Food Composition database. Dietary intakes were energy adjusted with the use of the residual method of Willett and Stampfer (24). Energy-adjusted total antioxidant intake, from both diet and supplements, for β-carotene, zinc, and vitamins A, C, and E was calculated (25). Median intakes from diet and supplements for the BMES population were 6692 µg for β-carotene, 1897 µg retinol equivalents for vitamin A, 202.3 mg for vitamin C, 8.0 mg for vitamin E, and 11.9 mg for zinc.

Statistical analyses
Energy-adjusted total nutrient intakes (from diet and supplements) were divided into quintiles. Associations between quintiles of nutrient intake and the incidence of each cataract type were assessed with the use of discrete logistic regression (26) (PHREG procedure in SAS; SAS Institute, Cary, NC). This model, similar to Cox regression modeling (except that the time to event information is not continuous), allowed us to incorporate information from either or both discrete time points of the follow-up visits (5 or 10 y). With the use of this model, participants who attended only at the 5-y follow-up visit could also contribute information. We adjusted for age, sex, hypertension, smoking, diabetes, education, and use of inhaled steroids. Infurther analyses to determine associations between vitamin C from major dietary sources only and incident cataract, further adjustment for the use of vitamin C supplements was included in the model to assess whether the association with dietary vitamin C was independent of supplement use. Multivariable adjusted odds ratios (ORs) are presented with 95% CIs. To assess the combined antioxidant intake, different combinations of the antioxidants studied were analyzed with the use of antioxidant intake scores. These scores were determined by the median intakes of each nutrient; below median intakes of each antioxidant studied were scored 0 (low-intake group), above median intakes of each antioxidant were scored 2 (high-intake group), and participants who had a combination of above and below median intakes of the antioxidants were scored 1 (reference group). To assess the association between the combined antioxidant intakes and incident cataract independent of vitamin C, additional adjustment for vitamin C was performed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of the 3654 baseline participants, 2897 (79.2%) had usable FFQs, and 2464 (67.4%) participants were followed ≥1 time after their baseline examinations, at either 5- or 10-y examinations. Of these participants, 2174 (88.2%) phakic participants, ie, participants with their natural lens intact, had usable FFQs. After excluding those with the corresponding cataract type at baseline and with missing or ungradable photographs, and those who had undergone cataract surgery since baseline, 1094 participants were free from nuclear cataract and were therefore at risk of nuclear cataract. Similarly, 1535 participants were at risk of cortical cataract and 1724 were at risk of PSC cataract. After excluding participants with missing or ungradable photographs plus those who could not be accurately classified in relation to cataract surgery by their examination or self-reported surgery, 2075 participants were at risk of cataract surgery.

The baseline characteristics of all participants followed after baseline examinations with and without incident cataract are compared in Table 1Go. Participants with incident nuclear cataract were more likely to be older, women, past smokers, or to have diabetes and hypertension at baseline, whereas participants with incident cortical cataract were more likely to be older, women, and to have hypertension at baseline. Participants with incident PSC cataract were more likely to be older and to have used inhaled steroids at baseline. Participants who had cataract surgery during follow-up were more likely to be older, men, and to have had hypertension but were less likely to be a smoker at baseline. A comparison between participants examined and participants who declined or were lost to follow-up was reported previously (20), with nonparticipants being younger, more likely to smoke, and to have diabetes. For participants who were followed, those who completed the FFQ were slightly younger, more likely to be past smokers, and to have higher job prestige than those who did not complete the FFQ (25). When comparing energy-adjusted antioxidant intakes of participants and nonparticipants, the latter group had lower intakes of dietary iron and vitamin E (25).


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  		TABLE 1. Comparison of baseline characteristics between participants with and without incident cataract at the follow-up visits1

 
Increasing vitamin C consumption was associated with a significantly reduced 10-y risk of incident nuclear cataract (P for trend = 0.045; Table 2Go). A similar but nonsignificant trend was observed for vitamins A and E and zinc (Table 2Go). Incident cortical or PSC cataract or cataract surgery was not significantly associated with the consumption of any antioxidants at baseline (Table 2Go).


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  		TABLE 2. Associations between baseline energy-adjusted antioxidant intake (from diet and supplements), by quintile (Q), and the 10-y incidence of different cataract types and cataract surgery1

 
Above median intakes of combined antioxidants were associated with a reduced risk of all cataract types plus cataract surgery, although some associations were not statistically significant (Table 3Go). The combined intake of vitamin C plus other antioxidants showed a protective association with long-term incidence of nuclear cataract (Table 3Go). After adjusting for vitamin C, above median intakes of vitamin E, β-carotene, and zinc also showed a protective association for incident nuclear cataract (Table 3Go).


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  		TABLE 3. Associations between combined antioxidant intakes (from diet and supplements) and the 10-y incidence of cataract and cataract surgery1

 
In the BMES population, the main dietary sources of vitamin C (percentage contribution per capita) were from vegetables of the Brassica variety (includes cabbage, cauliflower, broccoli, and brussel sprouts), potatoes, citrus fruit, and fruit juices. Further analysis with these main dietary sources showed that increasing consumption of fruit juice was associated with a decreased risk of incident nuclear cataract (P for trend = 0.017; Table 4Go).


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  		TABLE 4. Associations between main dietary sources of vitamin C, by quintile (Q), and incident nuclear cataract1

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This prospective population-based study provides evidence of long-term beneficial association between antioxidants, mainly vitamin C (either alone or in combination with other antioxidants), and nuclear cataract development, a well-known biological marker of aging. Earlier observational (27-37) and intervention (15, 16, 38, 39) studies have provided inconsistent evidence about the development of cataract in relation to antioxidant nutrient intake(s) or serum antioxidant concentrations. A number of prospective population-based studies (40-44), however, showed positive associations between antioxidant intake and reduced incidence or progression of nuclear cataract.

Higher intakes of vitamin C from diet, supplements, or both or higher serum concentrations of vitamin C were associated with a lower prevalence of nuclear cataract (29, 32-35, 40, 43). Increasing intakes of vitamin C, recorded 13–15 y before lens examination, was reported to be associated with a reduced prevalence of nuclear cataract in the Nurses Health Study cohort (31). Although vitamin C intake was inversely associated with the 5-y incidence of nuclear cataract in the Beaver Dam Eye Study, this inverse association was observed only in subjects who either smoked or were hypertensive (41). Baseline data from the Italian-American Clinical Trial of Nutritional Supplements and Age-related Cataract showed that higher plasma concentrations of vitamin C were associated with a reduced prevalence of nuclear cataract (35). Our findings are in keeping with these previous studies and are supported by the known antioxidant property of vitamin C and our current understanding of cataractogenesis.

The free-radical theory of aging proposed by Harman (45) in the 1950s suggested that ROSs are an integral component of the aging process. Accumulation of oxygen radicals leads to aging and disease (46-48), and oxidative stress was implicated in cataractogenesis (1-5). ROSs, including superoxide, hydrogen peroxide, and hydroxy radicals, are products of normal metabolic processes or ultraviolet radiation, which affects the lens on a daily basis. Lens components (crystallin proteins, lens fibers, and lipids) are susceptible to ROS damage (1, 9-12), which presumably accelerates nuclear cataractogenesis (9, 10).

Vitamin C is well known for its antioxidant properties. It is an efficient ROS scavenger and absorbs ultraviolet radiation (49). Vitamin C is found in high concentrations within the lens, aqueous humor, and vitreous humor of humans (50). It was shown that mice fed a diet supplemented with ascorbate did not develop cataract (51). Other experimental in vitro or in vivo studies have also shown that lenses with high concentrations of vitamin C, either in the culture medium or aqueous humor, were protected from oxidative damage (50, 52).

The BMES population is a healthy older population with relatively high intakes of fruit and vegetables and fairly healthy diet habits (53). Around one-third of the BMES population was taking vitamin supplements at the baseline examination (28), with a median vitamin C intake of 500 mg among supplement consumers. The main dietary sources of vitamin C in this population were from Brassica vegetables, potatoes, citrus fruit, and fruit juices. We found a significant protective association between increasing consumption of fruit juices and incident nuclear cataract but not for citrus fruit separately. A higher concentration and bioavailability of vitamin C in fruit juice compared with citrus fruit could explain this difference in our findings. The total antioxidant capacity of fruit and fruit juices was shown to mostly come from the juice fractions (54). Consumption of orange juice was also shown to significantly increase plasma vitamin C concentration (55).

Our finding of benefit against nuclear cataract from the combined intakes of antioxidants (vitamins C and E, β-carotene, and zinc) suggests possible synergism afforded by multiple antioxidant nutrients, together with vitamin C. It was suggested that vitamins C and E can act synergistically (56). With the help of glutathione, vitamin C is able to regenerate vitamin E after it scavenges free radicals (56-58). β-carotene and vitamin E can also convert destructive singlet oxygen to "normal oxygen" (58, 59). Zinc is an essential cofactor for endogenous antioxidant enzymes such as superoxide dismutase (60). Improved protection against ROSs from multiple antioxidants was suggested (58).

Data from the baseline of the current cohort study documented protection against nuclear cataract among persons using multivitamins (28). Similar findings were reported from other studies (31-33, 40, 43). The Beaver Dam Eye Study observed a lower incidence of nuclear cataract among persons using multivitamins for ≥10 y (44). A beneficial effect on nuclear cataract was also found with multivitamin use in the Roche European American Cataract Trial (38), the Dysplasia Trial of the Linxian Cataract Studies (17), and with the use of Centrum in the Age-Related Eye Disease Study (16). No significant beneficial effect on the 7-y risk of any cataract type, however, was found in the Age-Related Eye Disease Study for people using a high-dose formulation of vitamins C and E, β-carotene, and zinc (15).

Strengths of this study include its high participation rate, use of similar examination and cataract grading procedures at all 3 examinations, and the use of a validated FFQ to estimate nutrient intakes. Limitations of this study are the reduced number of nuclear cataract cases available for the assessment of nuclear cataract, because of a random camera error. This is unlikely to have resulted in any major bias (61). Although we accounted formany of the known factors influencing cataract, other influences from possible unidentified confounding factors cannot be ruled out. Because of the number of associations investigated, the possibility that chance could explain these findings cannot be excluded.

In conclusion, higher intakes of vitamin C, alone or in combination with other antioxidants, had a protective association with the long-term (10 y) incidence of nuclear cataract in this population-based cohort. These findings support the hypothesis that diet and supplement intakes of vitamin C and other antioxidants may exert age-related ocular benefits, as well as beneficial effects on aging itself.


   ACKNOWLEDGMENTS
 
The authors’ responsibilities were as follows—PM, JJW, and RGC: study conception and design; AGT and VMF: data acquisition; GB and ER: performed statistical analyses; AGT, VMF, and JJW: interpretation of study findings; AGT: wrote the first draft of the manuscript; all authors critically reviewed and contributed to the final version of the manuscript. None of the authors had a personal or financial conflict of interest.


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 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication November 7, 2007. Accepted for publication March 5, 2008.




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