The Association of Consumption of Fruits/Vegetables With Decreased Risk of Glaucoma Among Older African-American Women in the Study of Osteoporotic Fractures




Purpose


To explore the association between consumption of fruits and vegetables and the presence of glaucoma in older African-American women.


Design


Cross-sectional study.


Methods


Disc photographs and suprathreshold visual fields were obtained from the 662 African-American participants in the Study of Osteoporotic Fractures. Masked, trained readers graded all discs, and 2 glaucoma specialists reviewed photographs and visual fields. The Block Food Frequency Questionnaire assessed food consumption. Relationships between selected fruit/vegetable/nutrient consumption and glaucoma were evaluated using logistic regression models after adjusting for potential confounders.


Results


After excluding women missing Food Frequency Questionnaire and disc data, 584 African-American women (88.2% of total African-American cohort) were included. Glaucoma was diagnosed in at least 1 eye in 77 subjects (13%). Women who ate 3 or more servings/day of fruits/fruit juices were 79% (odds ratio [OR] = 0.21; 95% confidence interval [CI]: 0.08–0.60) less likely to have glaucoma than women who ate less than 1 serving/day. Women who consumed more than 2 servings/week of fresh oranges (OR = 0.18; 95% CI: 0.06–0.51) and peaches (OR = 0.30; 95% CI: 0.13–0.67) had a decreased odds of glaucoma compared to those consuming less than 1 serving/week. For vegetables, >1 serving/week compared to ≤1 serving/month of collard greens/kale decreased the odds of glaucoma by 57% (OR = 0.43; 95% CI: 0.21–0.85). There was a protective trend against glaucoma in those consuming more fruit/fruit juices ( P = .023), fresh oranges ( P = .002), fresh peaches ( P = .002), and collard greens/kale ( P = .014). Higher consumption of carrots ( P = .061) and spinach ( P = .094) also showed some associations. Individual nutrient intake from food sources found protective trends with higher intakes of vitamin A ( P = .011), vitamin C ( P = .018), and α-carotene ( P = .021), and close to statistically significant trends with β-carotene ( P = .052), folate ( P = .056), and lutein/zeaxanthin ( P = .077).


Conclusion


Higher intake of certain fruits and vegetables high in vitamins A and C and carotenoids may be associated with a decreased likelihood of glaucoma in older African-American women. Randomized controlled trials are needed to determine whether the intake of specific nutrients changes the risk of glaucoma.


Presently, the only treatment shown to prevent progression of glaucoma is lowering of intraocular pressure (IOP), although it does not prevent progression and/or onset in all patients. A primary prevention strategy for glaucoma is highly desirable. Epidemiologic studies on antioxidants, ingested through diet and supplements, have suggested benefit on the risk of multiple diseases, including late age-related macular degeneration, cataract, cardiovascular disease, and cancers, although data are still needed from randomized controlled trials for cataracts, cardiovascular disease, and cancer. In vitro evidence suggests that oxidative stress may contribute to the etiology and progression of glaucoma via apoptosis and extracellular matrix remodeling of the trabecular meshwork and lamina cribosa. It is biologically feasible that antioxidants found in the diet through fruits and vegetables may modify the risk of glaucoma development and/or progression.


We previously investigated associations between diet and glaucoma in a random sample of women from the Study of Osteoporotic Fractures. Some associations, such as that between green leafy vegetables and glaucoma, appeared stronger in the African-American subgroup; however, the number of African-American women in the sample was very small (n = 144, 12.5% of study population). In this study, we further investigated a possible association between glaucoma and the consumption of fruits and vegetables in the entire cohort of African-American women aged 65 and older (n = 662) participating in the Study of Osteoporotic Fractures. The association between the antioxidant constituents of fruits and vegetables and glaucoma was also examined.


Methods


Setting and Subjects


The subjects and setting of the Study of Osteoporotic Fractures have been previously described. Institutional Review Board approvals were obtained from the participating institutions prior to this study in order to review de-identified data that had been collected as part of the Study of Osteoporotic Fractures. The characteristics of the entire study population have been described in earlier reports.


Glaucoma (Outcome Measurement) Ascertainment


The ascertainment of glaucoma has been previously described. In brief, optic nerve images were obtained with a Canon nonmydriatic camera (Canon CR – 45UAF 45-degree autofocus nonmydriatic camera; Canon Inc, Kanagawaken, Japan) through a pharmacologically dilated pupil. Visual field testing was performed on each eye using the Humphrey Field Analyzer suprathreshold 76-point 30-degree visual field test (Carl Zeiss Meditec, Dublin, California). Photographs were graded by 2 masked, trained photograph graders. The visual fields and photographs of all women with a cup-to-disc ratio of 0.6 or greater (n = 118), asymmetry between vertical cup-to-disc ratios of 0.2 or greater (n = 93), discrepancy greater than 0.1 between photograph graders on the grading of cup-to-disc ratios (n = 161), and/or discrepancy in notation of focal thinning/notching of the neuroretinal rim between photograph graders (n = 62), along with a 5% random sample of the women with cup-to-disc ratios less than 0.6 (n = 36), were evaluated by a masked, trained glaucoma specialist (J.G.). The optic nerves were diagnosed as glaucomatous based on diffuse or localized thinning of the neuroretinal rim and loss of retinal nerve fiber layer. Visual field loss was defined as the presence of at least 1 missing point on the suprathreshold test. A second glaucoma specialist (A.C.) reviewed all optic nerves diagnosed with glaucoma and glaucoma suspect, along with the 5% random sample for confirmation of the diagnosis.


Measurement of Fruit/Vegetable Consumption and Antioxidant Intake


Consumption of fruits and vegetables was assessed using the 1995 Block Food Frequency Questionnaire. The Block questionnaire is a validated, self-administered diet questionnaire developed from the National Health and Nutrition Survey III (or NHANES III) that asks for average frequency of food intake over the last year. Participants completed the questionnaire just before their clinical visit. Block Dietary Data Systems (Berkeley, California, USA) calculated nutrition summary variables based on questionnaire responses, including daily intake of vitamins, fat, protein, carbohydrates, and nutrients obtained from all food sources (not including intake from supplements).


Statistical Analysis


Excluded from the analysis were women with incomplete questionnaires or unknown glaucoma status, because of ungradable or absent photographs. The distribution of selected fruit and vegetable items was examined in the total study population. In the analysis, consumption of individual items was categorized into frequency categories reflective of their different frequency distributions on the questionnaires filled out by participants. The number of participants consuming a certain item may not add up to the total study population because of incomplete responses for the item. For further details see reference .


Because it is presumably the constituents (eg, vitamins, minerals) of fruits and vegetables that confer a protective effect, the major nutrient components of fruits and vegetables were determined. The total intake of calories, fat, protein, and carbohydrate were also calculated based on the consumption of all food. The relationships of both food items and nutrients to the risk of glaucoma were examined individually using logistic regression models, adjusted for potential confounders. The potential confounders were chosen based on their clinical relevance and evidence from the literature, and are seen in Table 1 . Because of the skewed distribution of antioxidant intake, intakes were categorized into either tertiles or quartiles, depending on where easily recognized cut-offs were seen. The lowest tertile or quartile of intake formed the reference category. Trend P values were determined from the multiple logistic regression models of the odds of glaucoma adjusting for the potential confounders listed above. Trend P values indicate whether a dose-response effect exists when consuming a higher amount of food items or nutrients.



TABLE 1

Characteristics of African-American Women Who Had Known Glaucoma Status and Completed Block Food Frequency Questionnaire in the Study of Osteoporotic Fractures Year-10 Clinic Visit (N = 584)






































































































































































Characteristics All Women (N = 584) N (%) or Mean ± SD Women With Glaucoma (N = 77) N (%) or Mean ± SD Women Without Glaucoma (N = 507) N (%) or Mean ± SD P Value
Study sites .543 a
Baltimore 137 (23.5%) 15 (19.5%) 122 (24.1%)
Minneapolis 146 (25.0%) 18 (23.4%) 128 (25.3%)
Pittsburgh 157 (26.9%) 20 (26.0%) 137 (27.0%)
Portland 144 (24.7%) 24 (31.2%) 120 (23.7%)
Age (y)
Mean ± SD 75.3 ± 5.1 77.0 ± 5.5 75.1 ± 5.0 .003 b
65–74 295 (50.5%) 30 (39.0%) 265 (52.3%) .065 a
75–79 172 (29.5%) 25 (32.5%) 147 (29.0%)
80–84 84 (14.4%) 14 (18.2%) 70 (13.8%)
85–94 33 (5.7%) 8 (10.4%) 25 (4.9%)
Education (y)
Mean ± SD 12.1 ± 3.2 12.1 ± 3.5 12.1 ± 3.1 .939 b
<12 y 192 (33.2%) 23 (29.9%) 169 (33.7%) .675 a
12 y 187 (32.3%) 24 (31.2%) 163 (32.5%)
>12 y 200 (34.5%) 30 (39.0%) 170 (33.9%)
Current smoker 48 (8.3%) 6 (7.9%) 42 (8.3%) 1.00 a
At least 1 alcoholic drink in past 30 d 154 (26.4%) 19 (24.7%) 135 (26.7%) .782 a
Walking for exercise 212 (36.5%) 19 (25.0%) 193 (38.2%) .030 a
Body mass index (kg/m 2 )
Mean ± SD 30.2 ± 6.0 31.2 ± 6.2 30.0 ± 6.0 .098 b
Self-rated health status .414 a
Good or excellent 419 (71.9%) 52 (67.5%) 367 (72.5%)
Fair or poor 164 (28.1%) 25 (32.5%) 139 (27.5%)
Self-report of diabetes 101 (17.3%) 12 (15.6%) 89 (17.6%) .748 a
Self-report of hypertension 370 (63.5%) 43 (55.8%) 327 (64.6%) .162 a

SD = standard deviation; y = year.

The number of participants may not add up to 584 due to missing data for some characteristics.

a Fisher exact test.


b t test.



A power calculation was performed at the start of this study based on the results of previous analysis of 1155 Study of Osteoporotic Fractures participants that included only 144 African-American participants. Drawing on the results of that study, where some relationships appeared stronger in the African-American cohort, one of the key distinctions anticipated to occur was between subjects reporting less than 1 serving of spinach per week and those reporting at least 1 serving per week. With assumed alternate prevalence rates for glaucoma between 10% and 12% and intake of less than 1 serving per week or between prevalence rates of 2% and 3% with more than 1 serving per week, study power was calculated to lie between 95% and 99.9%, assuming at least 500 patients with gradable photos. All statistical analyses were performed using SAS version 9.1 statistical software (SAS institute, Cary, North Carolina, USA).




Results


Study Population


Among the 662 African-American women in the cohort, glaucoma status could not be determined in 68 women because of missing or ungradable disc photographs (10.3%; 47 with unknown status bilaterally and 21 with unknown status unilaterally with a normal fellow eye). Additionally, there were 13 women (1.9%) for whom we did not have Food Frequency Questionnaire data; 3 of them also had unknown glaucoma status. Thus, the final study population consisted of 584 women (88.2% of the original African-American cohort). There were no statistically significant differences in baseline characteristics among the 78 women excluded from analyses (data not shown).


The characteristics of the study population are described in Table 1 .


Prevalence of Glaucoma


Among the 584 women in the analysis, 77 (13.2%) were diagnosed with glaucoma in at least 1 eye. Glaucoma was bilateral in 32 women and unilateral in 39, and there were 6 women with glaucoma in 1 eye but unknown status in the fellow eye.


Relationship Between Fruit/Vegetable Intake and Glaucoma: Adjusted Analyses


Fruit and vegetable consumption varied among study participants, with a somewhat even spread across the various frequency categories ( Table 2 ). In analyses adjusted for potential confounders ( Table 2 ), the odds of having glaucoma were decreased by 79% (odds ratio [OR] = 0.21; 95% confidence interval [CI] = 0.08–0.60) in women who consumed 3 or more servings per day of all fruits and fruit juices compared to those who consumed less than 1 serving per day (trend P = .023). Compared to the reference group (<1 serving per day of fruit), those women consuming 2 servings per day and at least 1 serving per day had a 37% (OR = 0.63; 95% CI = 0.32–1.24) and 65% (OR = 0.35; 95% CI = 0.18–0.70) decreased odds of glaucoma, respectively. Of the individual fruits analyzed, women consuming greater amounts of fresh oranges (OR = 0.18; CI = 0.06–0.51; P = .002) and fresh peaches (OR = 0.30; CI = 0.13–0.67; P = .002) were 82% and 70% less likely to have glaucoma, respectively. The frequencies compared for these fruits were more than 2 servings per week compared to less than 1 serving per week. Consumption of apples/applesauce, bananas, orange juice, or canned/dried peaches did not show any statistically significant benefits or harms with relation to glaucoma and there were no significant trends with higher consumption.



TABLE 2

Associations Between Selected Fruits and Vegetable Consumptions and Glaucoma Among African-American Women Who Had Known Glaucoma Status and Completed Block Food Frequency Questionnaire in the Study of Osteoporotic Fractures Year-10 Clinic Visit (N = 584)
































































































































































































































































































Average Intake of Fruits/Vegetables N (%) OR (95% CI) a
All fruits and fruit juices
<1 serving per day 121(21%) 1.00 (referent)
1 serving per day 216 (37%) 0.35 (0.18–0.70)
2 servings per day 157 (27%) 0.63 (0.32–1.24)
≥3 servings per day 90 (15%) 0.21 (0.08–0.60)
Trend P value .023
All vegetables
<1 serving per day 62 (11%) 1.00 (referent)
1 serving per day 202 (35%) 0.95 (0.39–2.28)
2 servings per day 178 (30%) 1.02 (0.41–2.53)
≥3 servings per day 142 (24%) 0.97 (0.37–2.54)
Trend P value .965
Fresh apple
<1 serving per week 171 (34%) 1.00 (referent)
1 serving per week 57 (11%) 0.32 (0.10–1.02)
2 servings per week 99 (20%) 0.84 (0.40–1.77)
>2 servings per week 171 (34%) 0.52 (0.26–1.05)
Trend P value .137
Fresh banana
<1 serving per week 95 (17%) 1.00 (referent)
1–2 servings per week 117 (21%) 0.73 (0.31–1.75)
3–6 servings per week 228 (41%) 1.02 (0.48–2.15)
≥1 serving per day 112 (20%) 1.05 (0.44–2.48)
Trend P value .661
Fresh orange
<1 serving per week 153 (39%) 1.00 (referent)
1 serving per week 42 (11%) 0.83 (0.28–2.48)
2 servings per week 85 (22%) 0.70 (0.30–1.61)
>2 servings per week 111 (28%) 0.18 (0.06–0.51)
Trend P value .002
Orange juice
≤1 serving per week 191 (33%) 1.00 (referent)
3 servings per week to <1 serving per day 185 (32%) 0.77 (0.41–1.44)
≥1 serving per day 205 (35%) 0.79 (0.42–1.47)
Trend P value .448
Fresh peach
<1 serving per week 156 (36%) 1.00 (referent)
1 serving per week 60 (14%) 0.86 (0.38–1.98)
2 servings per week 84 (19%) 0.42 (0.17–1.02)
>2 servings per week 134 (31%) 0.30 (0.13–0.67)
Trend P value .002
Canned/dried peach
<1 serving per month 239 (41%) 1.00 (referent)
1 serving per month to <1 serving per week 183 (32%) 1.07 (0.60–1.91)
≥1 serving per week 157 (27%) 0.65 (0.33–1.28)
Trend P value .258
Fresh carrot
≤1 serving per month 85 (16%) 1.00 (referent)
>1 serving per month to <1 serving per week 136 (26%) 1.23 (0.54–2.83)
1 serving per week 105 (20%) 0.81 (0.32–2.05)
>1 serving per week 190 (37%) 0.57 (0.24–1.34)
Trend P value .061
Spinach (cooked or raw)
≤1 serving per month 129 (29%) 1.00 (referent)
>1 serving per month to <1 serving per week 125 (28%) 1.19 (0.57–2.46)
1 serving per week 96 (22%) 0.62 (0.26–1.45)
>1 serving per week 96 (22%) 0.54 (0.22–1.35)
Trend P value .094
Green salad
<1 serving per week 141 (27%) 1.00 (referent)
1 serving per week 86 (17%) 1.43 (0.62–3.30)
2 servings per week 84 (16%) 1.28 (0.52–3.14)
>2 servings per week 210 (40%) 1.02 (0.48–2.17)
Trend P value .909
Green collards/kale
≤1 serving per month 178 (30%) 1.00 (referent)
>1 serving per month to <1 serving per week 162 (28%) 0.45 (0.24–0.88)
1 serving per week 85 (15%) 0.48 (0.22–1.09)
>1 serving per week 159 (27%) 0.43 (0.21–0.85)
Trend P value .014

CI = confidence interval; OR = odds ratio.

The number of participants consuming a certain item may not add up to the total study population because of incomplete responses for the item.

a Based on multiple logistic regression models of the odds of glaucoma adjusting for potential confounders including study sites, age, education, smoking status, alcohol consumption, walking for exercise, body mass index, self-rated health status, presence of self-reported diabetes, and presence of self-reported hypertension.



The odds of having glaucoma were not affected by consumption of 3 or more servings of vegetables per day compared to less than 1 serving (OR = 0.97; CI = 0.37–2.54; trend P = .965). However, consumption of more than 1 serving per week of green collards/kale decreased the odds of having glaucoma by 57% (OR = 0.43; CI = 0.21–0.85) compared to consuming less than 1 serving per month (trend P = .014). Eating greater amounts of spinach and fresh carrots came close to showing a statistically significant protective trend (trend P = .094 and P = .061, respectively). Higher green salad consumption showed no protective or harmful trend.


Relationship Between Individual Nutrient Intake and Glaucoma


After adjusting for potential confounders, the highest quartiles or tertiles of intake of the following nutrients were associated with decreased odds of having glaucoma: vitamin C 70% less likely (trend P = .018), vitamin A 63% less likely (trend P = .011), and α-carotene 54% less likely ( P = .021) ( Table 3 ). The trend results for higher dietary intake of β-carotene (trend P = .052), folate (trend P = .056), and lutein/zeaxanthin (trend P = .077) were very close to being statistically significant. Higher intake levels of vitamins B1, B2, B3, B6, D, E, lycopene, and potassium were not associated with statistically significant increased or decreased odds of having glaucoma. Intake of increasing calories per day, total carbohydrate, total protein ( Table 3 ), and total fat ( Table 4 ) also showed no trend or effect on the odds of glaucoma.



TABLE 3

Associations Between Selected Intake of Nutrients From Food Consumptions and Glaucoma Among African-American Women Who Had Known Glaucoma Status and Completed Block Food Frequency Questionnaire in the Study of Osteoporotic Fractures Year-10 Clinic Visit (N = 584)
















































































































































































































































































































































































































































Average Daily Intake of Nutrients From Food N (%) OR (95% CI) a
Vitamin A (RE)
<800 155 (27%) 1.00 (referent)
800–1099 135 (23%) 1.35 (0.69–2.65)
1100–1499 146 (25%) 0.93 (0.47–1.86)
≥1500 148 (25%) 0.37 (0.15–0.90)
Trend P value .011
Vitamin B (folate) (μg)
<180 163 (28%) 1.00 (referent)
180–229 136 (23%) 0.61 (0.30–1.22)
230–299 128 (22%) 0.70 (0.35–1.40)
≥300 157 (27%) 0.47 (0.22–0.96)
Trend P value .056
Vitamin B1 (thiamin) (mg)
<1 238 (41%) 1.00 (referent)
1–1.4 243 (42%) 0.65 (0.37–1.14)
≥1.5 103 (18%) 0.84 (0.41–1.72)
Trend P value .455
Vitamin B2 (riboflavin) (mg)
<1 129 (22%) 1.00 (referent)
1–1.3 160 (27%) 0.77 (0.38–1.57)
1.4–1.8 162 (28%) 0.73 (0.35–1.50)
≥1.9 133 (23%) 0.75 (0.35–1.62)
Trend P value .529
Vitamin B3 (niacin) (mg)
<11 135 (23%) 1.00 (referent)
11–14 166 (28%) 0.71 (0.36–1.40)
15–18 153 (26%) 0.61 (0.29–1.26)
≥19 130 (22%) 0.64 (0.30–1.38)
Trend P value .251
Vitamin B6 (mg)
<1.1 152 (26%) 1.00 (referent)
1.1–1.3 159 (27%) 0.72 (0.37–1.43)
1.4–1.6 112 (19%) 0.88 (0.43–1.83)
≥1.7 161 (28%) 0.65 (0.32–1.32)
Trend P value .299
Vitamin C (mg)
<60 128 (22%) 1.00 (referent)
60–99 179 (31%) 0.37 (0.18–0.76)
100–139 147 (25%) 0.58 (0.29–1.14)
≥140 130 (22%) 0.30 (0.13–0.70)
Trend P value .018
Vitamin D (IU)
<70 138 (24%) 1.00 (referent)
70–119 153 (26%) 0.76 (0.38–1.53)
120–179 151 (26%) 0.61 (0.29–1.30)
≥180 142 (24%) 0.91 (0.45–1.83)
Trend P value .915
Vitamin E (A-TE)
<5 135 (23%) 1.00 (referent)
5–6.9 163 (28%) 1.22 (0.61–2.44)
7–8.9 140 (24%) 1.00 (0.47–2.12)
≥9 146 (25%) 0.76 (0.35–1.66)
Trend P value .327
Alpha-carotene (μg)
<200 226 (39%) 1.00 (referent)
200–399 176 (30%) 0.69 (0.38–1.26)
≥400 182 (31%) 0.45 (0.23–0.88)
Trend P value .021
Beta-carotene (μg)
<2000 157 (27%) 1.00 (referent)
2000–3199 144 (25%) 0.61 (0.31–1.20)
3200–4799 137 (23%) 0.54 (0.27–1.11)
≥4800 146 (25%) 0.46 (0.22–0.95)
Trend P value .052
Cryptoxanthin (μg)
<60 163 (28%) 1.00 (referent)
60–99 134 (23%) 1.26 (0.63–2.51)
100–149 157 (27%) 0.98 (0.50–1.94)
≥150 130 (22%) 0.62 (0.28–1.36)
Trend P value .171
Lutein/zeaxanthin (μg)
<1400 152 (26%) 1.00 (referent)
1400–2199 130 (22%) 0.44 (0.21–0.90)
2200–3999 160 (27%) 0.42 (0.21–0.84)
≥4000 142 (24%) 0.43 (0.21–0.88)
Trend P value .077
Lycopene (μg)
<400 158 (27%) 1.00 (referent)
400–799 150 (26%) 0.70 (0.35–1.43)
800–1199 124 (21%) 0.69 (0.32–1.48)
≥1200 152 (26%) 0.94 (0.47–1.87)
Trend P value .917
Potassium (mg)
<1700 154 (26%) 1.00 (referent)
1700–2099 132 (23%) 0.75 (0.36–1.55)
2100–2699 146 (25%) 0.70 (0.34–1.44)
≥2700 152 (26%) 0.83 (0.41–1.70)
Trend P value .670
Total calories (Kcal)
<1100 172 (29%) 1.00 (referent)
1100–1399 133 (23%) 0.72 (0.35–1.51)
1400–1799 161 (28%) 0.87 (0.44–1.71)
≥1800 118 (20%) 1.06 (0.51–2.18)
Trend P value .786
Total protein (g)
<40 130 (22%) 1.00 (referent)
40–54 157 (27%) 0.47 (0.22–0.99)
55–69 142 (24%) 0.77 (0.38–1.58)
≥70 155 (27%) 0.65 (0.32–1.34)
Trend P value .460
Total carbohydrate (g)
<120 126 (22%) 1.00 (referent)
120–159 167 (29%) 0.69 (0.34–1.40)
160–209 154 (26%) 0.72 (0.35–1.48)
≥210 137 (23%) 0.75 (0.35–1.59)
Trend P value .613

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Jan 12, 2017 | Posted by in OPHTHALMOLOGY | Comments Off on The Association of Consumption of Fruits/Vegetables With Decreased Risk of Glaucoma Among Older African-American Women in the Study of Osteoporotic Fractures

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