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The Jean Mayer U.S. Department of Agriculture Human Nutrition Research Center on Aging and the Gerald J. and Dorothy R. Friedman School of Nutrition Science and Policy at Tufts University, Boston, MA;
* American Cancer Society, Atlanta, GA;
Harvard Medical School and the Center for Ophthalmic Research, Brigham and Women’s Hospital, Boston, MA;
** The Channing Laboratory, Department of Medicine, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA; Departments of
Epidemiology and
Nutrition, Harvard School of Public Health, Boston, MA
4To whom correspondence should be addressed. E-mail: paul.jacques{at}tufts.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.5 using the Lens Opacification Classification System III. After adjusting for age, smoking, and other risk factors, women in the highest quartile category of HEI scores were significantly less likely to have nuclear opacities than those in the lowest category [odds ratio (OR) = 0.47; 95% CI: 0.26–0.84]. This association appeared to be stronger among nonusers of supplemental vitamin C (OR = 0.23; 95% CI: 0.10–0.52). Decreased prevalence odds of nuclear opacities were also observed with high intake of fruit (OR = 0.58; 95% CI: 0.32–1.05) and whole grains (OR = 0.64; 95% CI: 0.36–1.15). These results suggest that overall compliance with the Dietary Guidelines, as measured by the HEI, protects against nuclear opacities.
KEY WORDS: • Healthy Eating Index • dietary patterns • fruit • whole grains • cataract • aging
The chronic age-related diseases affecting Americans today, such as cardiovascular disease and diabetes, appear to be influenced by many different dietary components. Public health recommendations for chronic disease prevention usually attempt to summarize knowledge regarding myriad individual nutrients into a single, overall pattern of eating easily adopted by the general public. The Dietary Guidelines for Americans is one example of an attempt to advise the general U.S. population on the most effective dietary pattern to ensure health and prevent major chronic disease (1). However, few studies have examined the actual effectiveness of these guidelines as a whole in preventing disease (2,3).
Adherence to some or most of the Dietary Guidelines has been measured in a variety of ways. Some researchers examined the number of servings from select food groups in the Food Guide Pyramid (4) in an attempt to isolate the most important component of the diet in relation to nutritional or disease status (5–10). Others attempted to capture compliance with several of the guidelines simultaneously in a single measure (11–14). By comparing measures of diet quality, it may be possible to determine the following: 1) whether there are associations between the pattern recommended by the guidelines and disease outcomes, and 2) which parts of the guidelines, if any, are the most influential.
Age-related cataract is one chronic disease that may be influenced by diet (15). It represents a considerable public health burden, as the leading cause of visual disability in the United States and other developed countries (15). However, to our knowledge, no study has examined the effects of overall diet quality on any type of cataract. Therefore, we decided to examine the relation between dietary quality, as defined by the Dietary Guidelines, and the prevalence of age-related nuclear lens opacities, which are found in the oldest part of the lens and are most frequently related to nutrient intake.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In 1993, 1717 NHS participants were identified who were at least 52 y of age, resided in the Boston area, were free of diagnosed cancer other than nonmelanoma skin cancer, had complete dietary data, and had both eye lenses intact. These 1717 women were invited to participate in the Nutrition and Vision Project (NVP). Eight hundred ninety-five (52%) women returned the enclosed reply postcard indicating they were willing to participate in the study. To preserve their participation in the NHS, women who did not return the postcard were not contacted again. Of these volunteers, 603 were examined as part of the NVP between April 1993 and August 1995. Scheduling conflicts (due to work and travel) were the most common reason for failure to examine the 292 women who agreed to participate but were never seen.
Participants and nonparticipants were similar for many relevant characteristics (16), including age, alcohol consumption, BMI, reported summertime sunlight exposure, prevalence of hypertension, and vitamin C and multivitamin supplement use between 1980 and 1994. Participants reported fewer pack-years of smoking (17 pack-years) than nonparticipants (21 pack-years) and participants were also slightly more likely to have used vitamin E supplements between 1980 and 1994 (35%) than nonparticipants (29%). In addition, the percentage of women seeing an eye doctor in 1990 was 83% for those who did not participate and 85% for the participants.
Informed consent was obtained from all study participants, and all procedures were approved by the Human Investigations Review Committee at the New England Medical Center and the Human Research Committee at the Brigham and Women’s Hospital, both in Boston, MA.
Dietary assessment. Semiquantitative FFQs have been periodically sent to NHS participants at 2- to 4-y intervals since 1980. The 1980 FFQ listed 61 foods and beverages, as well as vitamin and mineral supplements. This original questionnaire was revised and expanded in 1984, 1986, and 1990 to include 126–136 items. A commonly used unit or portion size was specified for each item, and respondents indicated the usual frequency with which they had consumed that item during the past year. Nine responses were possible, ranging from "never or less than once per month" to "6 or more times per day." Additional questions regarding the use of fats and oils in cooking and the use of salt at the table and during cooking were included separately. Respondents were asked also to indicate the brand of breakfast cereal and multivitamin they usually used, if applicable. These questionnaires were examined previously for their reproducibility and validity (17–19). We also administered an additional 126-item FFQ as part of the NVP (1993–1995).
Measures of diet quality. Five indicators of diet quality were used to assess different aspects of adherence to the Dietary Guidelines for Americans, as described below. All measures of diet quality were based on data from the 1984, 1986, 1990, and 1993–1995 FFQs. The 1980 FFQ was not used because it contained only half as many food items as the subsequent questionnaires. All diet quality indicators were calculated from FFQs that reported daily energy intakes between 2512 and 14,947 kJ, and contained fewer than 70 items blank. The FFQs for all NVP participants in 1984 and 1993–95 met these criteria. Three 1986 FFQs and six 1990 FFQs did not meet these criteria and were excluded from analysis. For these 9 participants, all diet quality measures for the excluded FFQ (1986 or 1990) were calculated as the mean of the FFQs before and after the excluded one. For participants who met the inclusion criteria but left items blank, we assumed that the respondents rarely or never consumed the food item. This assumption should have little effect on our results because only 0.3% of food items were left blank for the women included in our analyses.
Fruit, vegetable, and whole grain intake.
The mean number of daily servings of fruits, vegetables, and whole grains was calculated from the 4 FFQs. These food groups make up the base of the food guide pyramid (4), and tend to be rich in many of the nutrients that have been associated with age-related nuclear cataract, such as vitamin C and carotenoids. Whole grain intake was calculated rather than all grains, because of the specific recommendation to consume several servings a day of whole grain products (4). Breakfast cereals specified on the FFQ were assigned to the whole grain category if they contained 25% whole grain or bran by weight (5,7).
Recommended Foods Score. The Recommended Foods Score (RFS), recently developed by Kant et al. (14) as a relatively simple measure of diet quality, summed the number of FFQ items participants consumed at least once a week, in any quantity, that qualified as recommended foods according to the Dietary Guidelines (e.g., fruits, vegetables, whole grains, low-fat dairy, fish, and lean meats). The highest possible score was 23 (14), using a 62-item FFQ. We adapted the original RFS for use with our longer questionnaires, with maximum scores ranging from 56 to 66, depending on the overall number of food items in the FFQ. A summary RFS was calculated as the mean RFS of the 4 FFQs, with a maximum overall score of 59. Like the original RFS, this adapted version reflects primarily the variety of fruit and vegetable consumption, because 75% of the recommended foods in the adapted version were fruits or vegetables.
Healthy Eating Index. We examined the concordance of participants’ diets with the totality of the Dietary Guidelines using the Healthy Eating Index (HEI), which was developed by the USDA to quantify overall adherence to the 1990 Dietary Guidelines (20). The construction of the original HEI was based on 24-h recalls and 2-d food records (13). McCullough and colleagues previously adapted the HEI for use with the Harvard FFQs (HEI-f) (2,3). HEI-f scores calculated from FFQs correlated well with those calculated using food records in a validation study in men (2).
The HEI-f is comprised of 10 equally weighted components (2,3). For each component, perfect adherence to the recommendation is given a score of 10. Less than perfect adherence is calculated proportionately, with a minimum score of 0. The component scores are summed to create an overall HEI-f score that ranges from 0 (worst) to 100 (best).
The first 5 components of the HEI-f, like the original HEI, measure compliance with the serving recommendations of the 5 food groups: grains (bread, cereal, rice, and pasta), vegetables (including potatoes), fruit (juice and whole fruit), milk (milk, yogurt, and cheese), and meat (meat, poultry, fish, dry beans, eggs, and nuts) (4). Recommended servings are age and sex specific. Before being assigned to food groups, the food items listed on all 4 FFQs were compared with the pyramid servings sizes, and multiplied by conversion factors if necessary, using the USDA food guide pyramid database (3,21). Each ingredient in mixed dishes was assigned a pyramid serving size, and allocated to the appropriate food group. Because the recommendations for age and sex categories are based on energy requirements, the HEI-f does not further adjust for total energy intake. In addition, the HEI-f does not assign extra points, nor subtract points, for exceeding the recommended number of servings in any given component.
The last 5 components of the HEI-f, regarding total fat, saturated fat, cholesterol, sodium, and variety, are not age or sex specific. The component scores for total fat, saturated fat, and cholesterol were assigned as described in the original HEI (3,13). The sodium component was scored differently because only the 1986 FFQ inquired about the use of salt during cooking. Therefore, for consistency, the sodium score for all 4 FFQs was determined from the cohort distribution of sodium intake by creating 11 equal quantile categories of energy-adjusted sodium intake, scored from 0 to 10, with 0 indicating the highest category of sodium intake, and 10 the lowest (3). The variety component was also scored on the basis of its distribution in the NVP cohort because the original HEI scored variety on the basis of the number of unique foods eaten over 3 d, which does not apply to the FFQ. The original HEI definitions of "unique foods" were used to group similar foods together, such as skim milk and whole milk (20). Participants in the highest quantile category of variety (i.e., those eating the greatest variety of foods) received a score of 10, whereas those in the lowest quantile category received a score of 0.
Assessment of lens status. All NVP participants received a detailed eye examination using standardized techniques. The examinations consisted of an ocular and medical history, Bailey Lovie test of visual acuity and manifest refraction, contrast sensitivity function and glare testing, external ocular examination, applanation tonometry, and a slit-lamp examination of the anterior chamber. Participants’ eyes were dilated to a minimum of 6 mm with phenylephrine and tropicamide after intraocular pressure measurements indicated it was safe to do so. The examiners did not know the nutrient status of the volunteers.
Color film slides of the nuclear region of the lens were taken with a Zeiss photo-slitlamp and Ektachrome 200 film. The Lens Opacity Classification System III (LOCS III) was used to measure the degree of nuclear opalescence (light scattering from the nucleus) (22). LOCS III is a subjective grading system that measures nuclear opacification on a decimal scale, using a set of 6 standard photographs. Possible grades range from 0.1 (clear) to 6.9 (most opaque) (22). LOCS III was validated in previous studies (22,23). As in earlier analyses of this data set (16), eyes are classified as having nuclear opacities if the nuclear opalescence grade is 2.5. The grade of 2.5 indicates an early stage of opacification that is not associated with clinical symptoms.
Potential confounders.
Information regarding known or suspected risk factors for nuclear cataract was obtained from the 1980 through 1994 biennial Nurses’ Health Study questionnaires. These factors included age, pack-years of cigarette smoking, history of hypertension (yes or no), reported summertime sunlight exposure in 1980 8 h/wk (yes or no), alcohol use based on the mean from 5 FFQs (g/d), duration of use of supplemental vitamin C (years), physical activity [in metabolic equivalent tasks (METs)/wk] from the NHS questionnaire preceding the NVP examination, and height (m) and weight (kg) as reported on the 1980 questionnaire. Height and weight values were used to calculate BMI (kg/m2).
Statistical analyses. Because prior knowledge of lens status could possibly affect dietary intake, we excluded 76 of the original 603 NVP participants who reported a history of cataract before their baseline eye exam in 1993–1995. Similarly, we excluded 22 women with a confirmed diagnosis of diabetes before their baseline eye exam to prevent the possibility that diabetes might modify the association between dietary quality and nuclear opacification. In addition, 19 women whose lens photographs were missing, upgradeable, or who had questionable nuclear lens data were not included in these analyses, nor were 7 additional participants who were missing covariate information. The final study sample included 479 women. The women included in the analyses were younger than those who were excluded from analyses, but they did not differ on any other subject characteristics such as BMI or the percentage that were current smokers, multivitamin supplement users, or had recently visited an eye doctor.
For each measure of diet quality, usual consumption over 
10 y was determined for each participant by calculating the mean from the 1984, 1986, 1990, and 1993–1995 FFQs. Quartile categories for each diet quality measure were established using data from all 603 participants, using the lowest (poorest quality) category as the reference category.
The characteristics of women with and without nuclear opacities were compared using t tests for continuous variables and 
2 tests for categorical variables. For all analyses relating nuclear opacities to measures of diet quality, eyes were the unit of analysis. Odds ratios (ORs) and 95% CI relating prevalence of nuclear opacities to each diet quality measure were estimated from logistic regression models using SAS GENMOD (unstructured) (SAS version 8.01, SAS Institute). SAS GENMOD is a generalized estimating equations method that adjusts the standard error of the model parameters for correlations due to repeated measurements on the same individuals, allowing for the use of eyes as the unit of analysis with correction for the correlation between fellow eyes. This approach has several advantages over standard logistic regression with individuals rather than eyes as the unit of analysis or separate logistic regression analyses of right and left eyes, including greater statistical power and precision of estimation, more interpretable regression coefficients, and less sensitivity to missing data on eyes (24,25). The diet quality variables were modeled as categorical variables for our primary analyses based on approximate quartile cutoff values using a class statement in SAS. P-values for the model parameters were used to assess the significance of the individual variables. The presence of a graded trend was assessed using each diet quality measure as a continuous variable in the logistic models.
We developed 3 different statistical models. The first included age and smoking, the 2 most widely accepted risk factors for nuclear cataract. The second model included additional covariates previously observed to be associated with opacities in this cohort (duration of vitamin C supplement use, alcohol intake, BMI, summer sunlight exposure and hypertension) and physical activity, which along with a healthy weight (assessed by BMI) are the nondietary components of the Dietary Guidelines for Americans. The third model included energy intake in addition to the covariates listed above.
As part of the HEI-f analyses, we also examined each of the 10 components of the HEI-f as continuous variables (0–10). One component at a time was entered into the full multivariable models to determine its association with prevalence of nuclear opacities, both alone and in the presence of the other 9 HEI-f components.
Because previous analyses in this cohort found an association between vitamin C use and prevalent nuclear lens opacities (26), and because supplement use often correlates with healthy dietary patterns (27,28), we tested for an interaction between vitamin C supplement use (yes/no) and each of the diet quality measures using the product of the dichotomous vitamin C variable and the continuous diet quality variables. Because of the small number of tests (n = 4) and our a priori hypothesis of an interaction between supplement use and health dietary patterns, we have not corrected our stated significance level to account for the number of interaction tests.
Unless otherwise noted, statistical significance refers to a 2-sided P-value < 0.05.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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10 y (Table 1). After adjusting for age, differences in high blood pressure and energy intake were no longer significant; in addition, women with opacities were more likely to have had greater sun exposure (8 h/wk outdoors in the summer) in 1980 and to have lower HEI-f scores.
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0.70).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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High intake of whole grain products and fruits was also inversely related to nuclear opacities, although the results were only marginally significant. Neither high levels of vegetable intake nor consumption of a wide variety of guideline-recommended foods was related to the prevalence of nuclear opacities. However, these null associations may be due to a lack of statistical power. Although we had >80% power to detect a risk ratio of 0.5 for all of the measures of diet quality, we had more limited power to detect risk ratios 0.6.
To our knowledge, this is the first study to report on the association between adherence to the Dietary Guidelines for Americans and nuclear lens opacities. Previous studies of nuclear cataract identified many nutrients that appear to be protective (15,29–32). Most of these nutrients are antioxidants, found primarily in fruits, vegetables, and whole grains. However, the levels of these nutrients in the diet and blood varied across study populations, as did the strength of their reported benefits. Although the Dietary Guidelines for Americans aim to promote health and protect against disease without the use of supplements, it is unknown whether such a diet actually provides sufficient amounts of nutrients to protect against nuclear cataract, or whether the required levels can be obtained from supplements only.
A few researchers have attempted to address this issue, at least in part, by looking at the effects of fruit and vegetable intake on nuclear cataract, or at specific vegetables rich in particular nutrients (33–35). Although Mares-Perlman et al. (33) did not find fruit and vegetable intake in general to be associated with nuclear opacities in women, they did find a significant relation with spinach intake. In general, spinach has been the food item most consistently associated with both nuclear opacities (33–35) and with opacities in any location (36–39). Intake of fruits and vegetables in general has also been related to cataract in any location in 1 case-control study (40). Because the Dietary Guidelines do not recommend consuming any one fruit or vegetable over another, we did not examine intake of specific foods. However, iceberg lettuce, potatoes (baked, boiled, or mashed, not including fried), and tomatoes contributed most to total vegetable intake in all quartile categories in the NVP, and oranges, orange juice, apples, and bananas were the greatest contributors to fruit intake in all quartile categories of fruit (data not shown). Our results did suggest a possible benefit of increased fruit consumption, which, unlike the HEI findings, was not modified by vitamin C supplement use.
However, the Dietary Guidelines recommend more than just fruits and vegetables. Whole grain intake is also encouraged, and recent studies suggest that increased consumption of whole grains may protect against heart disease and stroke (5,7,41). Because coronary heart disease was recently found to be associated with cataract extraction in the NHS cohort (42), we were particularly interested in the possible association between whole grain intake and nuclear opacities. We found that the prevalence of nuclear opacities was reduced only among women in the highest quartile category of whole grain intake [median (range), 2.2 (1.8–6.6) servings/d].
The Dietary Guidelines have always stressed the importance of eating a variety of foods to obtain sufficient amounts of the myriad nutrients and nonnutritive compounds necessary for optimal health (1,43). Although it was designed as a measure of overall diet quality, we believe that the RFS may also be considered a measure of dietary variety to some extent because higher scores are obtained by eating a greater number of different food items. Kant et al. (14) found that a high RFS was associated with decreased risk of mortality in women. Because several studies have reported a relation between cataract and mortality (42,44–47), we hypothesized that the prevalence of nuclear opacities would be lower among women with a high RFS. Instead, we found that women in the highest quartile category of RFS were no less likely to have nuclear opacities than those in the lowest category of RFS.
As important as individual foods and food groups may be to health, the multiple recommendations made by the Dietary Guidelines imply that several aspects of the diet are important for optimal health. Accordingly, the HEI was devised as a stand-alone gauge of diet quality, with no one component any more or less important than the others (13). Nevertheless, as a secondary analysis, we examined the individual HEI components to determine whether any of the recommendations appeared more important with respect to the risk of nuclear opacities. Although we found significant inverse trends for the milk, fruit, and variety components, it is important to note that the strongest association was observed for the HEI-f overall, rather than with any of the individual components, supporting the idea that the association between risk of nuclear opacities and adherence to the Dietary Guidelines results from multiple aspects of a healthy eating pattern, rather than a single component, such as fruit intake.
We demonstrated previously in this same study population that duration of vitamin C supplement use is associated with a reduced prevalence of nuclear opacities (26), which is what prompted us to examine the potential for an interaction between our measures of diet quality and vitamin C supplement use. Although no association was found between the HEI-f and nuclear opalescence in vitamin C supplement users, we are hesitant to conclude that vitamin C supplement use alone can substitute for a healthy diet to reduce the risk of nuclear opacities because the interaction between the HEI-f and vitamin C supplement use was only marginally significant and vitamin C supplement use did not modify the associations between nuclear opacification and any of the other measures of diet quality. Nonetheless, our results suggest that consumption of a healthy diet alone, as measured by the HEI-f, without use of supplemental vitamin C, may protect against nuclear opacities.
We presented our analyses both with and without energy in the model because of the potential implications of energy adjustment for our analyses. As previously noted, energy intake was addressed within the HEI. However, we examined energy as a covariate because people who consume more food may more easily achieve higher HEI scores, and energy adjustment helps address this concern (although energy, per se, is not believed to be a risk factor for cataract). In general, the results were similar with and without the inclusion of energy in the model.
The Alternate Healthy Eating Index was proposed by McCullough and colleagues (48) in an attempt to address some of the limitations of the HEI and the U.S. Dietary Guidelines. It does not directly measure adherence to the current guidelines; rather, it suggests more specific recommendations for major chronic disease risk reduction (e.g., cardiovascular disease) based on the current literature. Further research is warranted to determine whether such alternate dietary recommendations offer the same or greater protection against age-related cataract.
We believe that there are many strengths, and a few potential limitations, to our methods and approach. A major strength of this study is that all nutrient intake data were assessed before the eye examinations. In addition, women with previously diagnosed cataract were excluded from the analyses, and a previous study of this population found no difference in visual acuity between participants with and without nuclear opacities (16). These design features limit an important potential source of differential bias due to diet change or differential reporting of diet by the women based on the knowledge of their lens status. Another strength of this study was the use of multiple dietary assessments over a period 10 y to characterize usual dietary intake to reduce nondifferential bias associated with misclassification of our dietary exposures, which otherwise might limit our ability to detect relations between diet quality and nuclear opacities.
One potential weakness of the study is our focus on relatively early amounts of lens opacification. This restricts us from making inferences about more advanced, clinically relevant forms of cataract. Nevertheless, our findings should be applicable to more advanced nuclear lens opacities because it was demonstrated that 50% of nuclear opacities graded as 2 using the LOCS III classification system progress significantly over a 5-y period (49). Another potential weakness of this study is the fairly low participation of eligible subjects. Although 52% of the eligible sample agreed to participate, only 35% actually participated, largely due to difficulties in scheduling. Although this has the potential to introduce bias due to selection or self-selection of study participants, our study sample allowed us the opportunity to assess this potential because of the large amounts of data routinely collected on these women as part of the NHS. There were no differences in the characteristics of participants and nonparticipants that would indicate a potential for bias. Moreover, the exclusion of women with known cataract, as noted above, would also limit the ability for low participation to introduce bias.
In summary, we found that a diet in concordance with the Dietary Guidelines for Americans, as measured by the HEI-f, was associated with a decreased prevalence of nuclear lens opacities in women. Separate analyses suggested that increased consumption of fruit and whole grains may possibly be beneficial, although less strongly than the HEI-f. However, consumption of a large number of USDA-recommended food items, without reference to food group or quantity, does not appear to be related to prevalence of nuclear opacities in women. These results suggest that an overall high quality diet, such as that recommended by the U.S. Dietary Guidelines, may prevent or delay nuclear lens opacities in women.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Financial support for this project was provided by the U.S. Department of Agriculture, under agreement No. 58-1950-9-001 and the National Research Initiative Competitive Grant Program grant nos. 98-01023 and 92–37200-7704; Brigham Surgical Group; research grants EY-09611, CA-40356, and R01-13250 from the National Institutes of Health; NIH training grant T32 AG00209; and by grants from Roche Vitamins and Fine Chemicals Division, Kemin Foods and the Florida Department of Citrus. Any opinions, findings, conclusion, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.
3 Present address: Departments of Nutritional Sciences and Ophthalmology and Visual Sciences, University of WI-Madison, Madison, WI.
5 Abbreviations used: HEI, Healthy Eating Index; HEI-f, Healthy Eating Index for food-frequency questionnaires; LOCS III, Lens Opacity Classification System III; METs, metabolic equivalent tasks; NHS, Nurses’ Health Study; NVP, Nutrition and Vision Project; OR, odds ratio; RFS, Recommended Foods Score.
Manuscript received 17 November 2003. Initial review completed 17 December 2003. Revision accepted 28 April 2004.
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