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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:1937-1942, June 2003

Nutritional Epidemiology

Risk of Human Ovarian Cancer Is Related to Dietary Intake of Selected Nutrients, Phytochemicals and Food Groups

Susan E. McCann2, Jo L. Freudenheim, James R. Marshall* and Saxon Graham

Department of Social and Preventive Medicine, University at Buffalo, Buffalo, NY 14214 and * Division of Population Science and Cancer Prevention, Roswell Park Cancer Institute, Buffalo, NY 14263

2To whom correspondence and reprint requests should be addressed. E-mail: mccann{at}acsu.buffalo.edu.


   ABSTRACT
TOP
 ABSTRACT
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Intakes of specific nutrients and food groups have been shown previously to be related to ovarian cancer risk, but no studies, to our knowledge, have emphasized the effect of phytochemical intakes on this cancer. We conducted a case-control study of diet and ovarian cancer in western New York involving 124 primary, histologically confirmed ovarian cancer cases and 696 population-based controls, frequency matched to cases on age and county of residence. Diet was assessed with a detailed food-frequency questionnaire. Nutrient and phytochemical intakes were calculated from published food composition data. The odds ratios (OR) and 95% CI for risk of ovarian cancer with each nutrient, phytochemical and food group were estimated with unconditional logistic regression adjusting for age, education, total months menstruating, difficulty becoming pregnant, oral contraceptive use, menopausal status and energy intake. Compared with women in the lowest quintile of intake, reduced risks were observed for women in the highest quintile of intake of dietary fiber (OR 0.43, 95% CI, 0.20–0.94), total carotenoids (OR 0.33, 95% CI, 0.16–0.68), stigmasterol (OR 0.42, 95% CI, 0.20–0.87), total lignans (OR 0.43, 95% CI, 0.21–0.85), vegetables (OR 0.47, 95% CI, 0.23–0.97) and poultry (OR 0.45, 95% CI, 0.22–0.92). These results support a protective effect on ovarian cancer of phytoestrogen intakes, and our results support the hypothesis that a plant-based diet may be important in reducing risks of hormone-related neoplasms.

KEY WORDS: • diet • flavonoids • ovarian neoplasms • phytoestrogens • phytosterols

The literature concerning the relationship between dietary components and ovarian cancer is limited. In general, reduced risks of ovarian cancer have been associated with higher intakes of dietary fiber, vitamin A, ß-carotene, fruits and vegetables (1–12), and fruit and vegetable intakes during adolescence (13), whereas increased risks have been associated with higher intakes of total fat and animal fat, cholesterol and lactose intakes, meat, eggs and whole milk (8,11,14–17). The mechanisms by which diet could affect the etiology of ovarian cancer include modulation of endogenous hormones (18–24), antioxidant activity or other anticarcinogenic mechanisms (25).

Recent research has identified food components (phytochemicals) that may have important anticarcinogenic activities. These include phytoestrogens, phytosterols and flavonoids. Phytoestrogens, including isoflavones (primarily from soy) and lignans (fruits, vegetables, grains and seeds), have been shown to possess estrogenic as well as antiestrogenic activity (26). Phytosterols are plant compounds found in food oils that are structurally similar to cholesterol. These compounds could affect endogenous hormone levels through alterations in bile acid metabolism and estrogen reabsorption, or through competition with cholesterol as a substrate for steroid hormone synthesis (27). Flavonoids (found in fruits and vegetables), such as quercetin, have been shown to possess potent antioxidant, antibacterial, antithrombotic, antiinflammatory and anticarcinogenic properties (28,29).

To our knowledge, the relationship between phytochemical intake and ovarian cancer has not been investigated previously. The aim of this study was to investigate the relationship of selected nutrients, other food components including phytochemicals, and food groups with risk of ovarian cancer in a case-control study conducted in western New York.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
The present study utilized data obtained as part of a series of case-control studies of diet and cancer of the breast, endometrium, ovary and prostate in western New York (1986–1991). The methods were described in detail elsewhere (30–32). The study protocol was approved by the Institutional Review Board of the University at Buffalo and informed consent was obtained from all participants. Briefly, women in this study included 124 incident, primary, histologically confirmed cases of ovarian carcinoma identified in women between the ages of 40 and 85 y. The mean number of months between diagnosis and interview for cases was 2.59 (median = 2.00); 93% were interviewed within 6 mo of diagnosis. Controls from the complete case-control series (breast, endometrium and ovary; n = 696) were frequency matched to cases on age (± 5 y) and county of residence and were randomly selected from driver’s license lists for women <65 y of age and from Health Care Finance Administration lists for women >=65 y of age.

Data were collected during a detailed in-person interview by trained nurse interviewers and included questions on diet, reproductive history, family history of cancer, medical history, health habits such as cigarette smoking and physical activity, and other lifestyle and occupational factors. Diet in the 12-mo period 2 y before the interview was queried with an extensive food-frequency questionnaire (FFQ) that included questions for portion size for each food, seasonality of use and food preparation methods. Although the FFQ used in this study was not validated in this population, it is comparable in structure to widely used and extensively validated instruments such as those used by the National Cancer Institute and Harvard University’s Nurse’s Health Study, and thus is likely to possess comparable validity.

Nutrient intakes from foods and beverages were calculated using food composition data from the USDA and published food composition tables (33–35). Vitamin supplement intake was not assessed. ß-Sitosterol, campesterol, stigmasterol, total phytosterols and the flavonoids, quercetin and kaempferol, were calculated using published food composition data compiled by Pillow et al. (36). Dietary intakes of total lignan precursors were calculated as the sum of secoisolariciresinol and matairesinol using the method of de Kleijn et al. (37). Isoflavone intake was not assessed because soy foods were not queried.

Statistical analyses.

Analyses were conducted using SPSS for Windows (Chicago, IL), and all statistical tests were considered significant at P < 0.05. Descriptive characteristics of cases and controls were compared with Student’s t tests for continuous variables and {chi}2 for categorical variables. Odds ratios (OR) and 95% CI for risk of ovarian cancer associated with the following nondietary risk factors was estimated with unconditional logistic regression: BMI [kg/m2] (>27.5 vs. <=27.5), cigarette smoking (never, former, current), pregnancy (never, ever), fertility problems (no, yes, never attempted pregnancy), total months menstruating (median cutpoint), oral contraceptive use (never, ever) and hormone replacement therapy (never, ever).

We considered the following dietary components: total energy (kJ), carbohydrates (g), protein (g), fat (g), saturated fat (g), monounsaturated fat (g), polyunsaturated fat (g), cholesterol (mg), alcohol (g), dietary fiber (g), vitamin C (mg), folate (µg), total carotenoids (mg), and the phytochemicals ß-sitosterol (mg), campesterol (mg), stigmasterol (mg), total phytosterols (mg), total lignan precursors (secoisolariciresinol and matairesinol) (µg), quercetin (µg), and kaempferol (µg). Finally, risk of ovarian cancer associated with monthly grams of intake of fruits, vegetables, grain products, red meat, poultry, fats, snacks and dairy were estimated. Each dietary variable was categorized into quintiles on the basis of the distribution in the controls, and risk in each quintile estimated referent to the lowest quintile of intake. For these analyses, the OR and 95% CI were calculated with unconditional logistic regression adjusting for age, education, total months menstruating, difficulty becoming pregnant, oral contraceptive use, menopausal status and total energy intake.


   RESULTS
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 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Compared with controls, cases were older, had less education, had a greater number of total months menstruated, were more likely to be postmenopausal, more likely to have had difficulty becoming pregnant, and, consequently, they had somewhat lower parity than controls (Table 1). Although not significant, cases were somewhat less likely to have ever been pregnant (P = 0.08). Cases also were less likely to have ever used oral contraceptives (P = 0.09), but more likely to have used hormone replacement therapy (P = 0.37) and less likely to be current smokers (P = 0.48). No differences were observed between cases and controls for BMI, age at menarche or age at first birth.


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  		TABLE 1 Descriptive characteristics of women with and without ovarian cancer, Western New York Diet Study (1986–1991)1

 
Among nutrient and food group intakes, cases consumed significantly less total carotenoids and more snacks than did controls (Table 2). Compared with controls, cases also tended to have slightly higher mean intakes of energy (P = 0.19), carbohydrate (P = 0.20), protein (P = 0.46), total and specific fats (P = 0.12, 0.12, 0.27, 0.38, total, saturated, monounsaturated, and polyunsaturated fats, respectively), and cholesterol (P = 0.24), and somewhat lower mean intakes of alcohol (P = 0.32), dietary fiber (P = 0.73), folate (P = 0.69) and total lignan precursors (P = 0.09).


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  		TABLE 2 Intakes of selected nutrients and phytochemicals of women with and without ovarian cancer in the Western New York Diet Study (1986–1991)1

 
The primary food sources for the phytosterols included black tea, peanuts and peanut butter, and margarine (data not shown). For the flavonoids, quercetin and kaempferol, the major food sources included tea, tomato sauce, vegetable soup, onions, apples and applesauce, broccoli and strawberries. Top contributors to the lignan precursors, secoisolariciresinol and matairesinol, included decaffeinated and caffeinated coffee, carrots, cucumbers and strawberries.

Consistent with previous literature, reduced ovarian cancer risks were observed for women who had ever been pregnant compared with those who had never been pregnant (OR 0.64, 95% CI, 0.39–1.06, P = 0.081) and for ever use of oral contraceptives compared with never use (OR 0.72, 95% CI, 0.49–1.06, P = 0.093) (Table 3). Similarly, increased risks were observed for women reporting problems becoming pregnant (OR 1.61, 95% CI, 1.03–2.51), or who had never attempted pregnancy (OR 3.07, 95% CI, 1.29–7.35) and for longer duration of exposure to menstruation (OR 1.77, 95% CI, 1.19–2.63). No associations with risk were observed for ovarian cancer and BMI, cigarette smoking or hormone replacement therapy.


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  		TABLE 3 Odds ratios (OR) and 95% CI for risk of ovarian cancer with nondietary risk factors among women in the Western New York Diet Study (1986–1991)1

 
We observed a substantial reduction in risk associated with the highest vs. lowest quintile of dietary fiber intake (OR 0.43, 95% CI, 0.20–0.94) and total carotenoids (OR 0.33, 95% CI, 0.16–0.68) (Table 4). Risk was not associated with intakes of other nutrients or food groups.


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  		TABLE 4 Odds ratios (OR) and 95% CI for risk of ovarian cancer with daily intakes of selected nutrients among women in the Western New York Diet Study (1986–1991)1

 
Among the phytochemicals examined (Table 5), reduced ovarian cancer risks were observed for the highest vs. lowest intakes of stigmasterol (OR 0.42, 95% CI, 0.20–0.87) and total lignan precursors (OR 0.43, 95% CI, 0.21–0.85). Risk did not appear to be related to intakes of the other phytosterols, total phytosterols or the flavonoids quercetin or kaempferol. Adjustment for possible confounding nutrients such as dietary fiber and folate had no effect on these estimates (data not shown)


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  		TABLE 5 Odds ratios (OR) and 95% CI for risk of ovarian cancer with selected phytochemicals among women in the Western New York Diet Study (1986–1991)1

 
For summary examinations of diet, we also estimated risk of ovarian cancer associated with monthly intakes of selected food groups (Table 6). Consistent with the finding of reduced risks associated with dietary fiber and carotenoid intakes, we observed a substantial decrease in risk for women in the highest vs. lowest quintile of vegetable intake (OR 0.47, 95% CI, 0.23–0.97). Reduced risks were also observed for the highest intakes of poultry (OR 0.45, 95% CI, 0.22–0.92), but risk did not appear to be related to fruits, grain products, red meat, fats, snacks or dairy products.


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  		TABLE 6 Odds ratios (OR) and 95% CI for risk of ovarian cancer with monthly intakes of selected food groups among women in the Western New York Diet Study (1986–1991)1

 

   DISCUSSION
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Although ovarian cancer is a relatively uncommon neoplasm, accounting for an estimated 4% of cancer cases among women in 2002, mortality from this cancer is high (38). Ovarian cancer is not easy to detect, making early diagnosis difficult. Therefore, identification of modifiable factors contributing to its etiology is important in reducing the incidence of this highly fatal neoplasm. Previously identified risk factors have been related to hormonal factors. Reduced ovarian cancer risks have been associated with oral contraceptive use and fewer menstrual cycles (consequent to greater parity), whereas increased risks have been associated with difficulties becoming pregnant and hormone replacement therapy (39,40). Consistent with the previous literature, we found reductions in risks for women who had ever been pregnant vs. never pregnant and for oral contraceptive use. We also observed increased risks among women reporting difficulty becoming pregnant or who had never become pregnant.

Investigations of dietary factors in the etiology of ovarian cancer have been limited. One of the mechanisms by which diet could affect ovarian cancer risk is through modulation of endogenous hormone levels. Relationships between diet and endogenous hormone levels have been fairly well established, with lower levels of estrone and estradiol levels reported for women consuming vegetarian diets compared with omnivorous diets (18,19,24). Furthermore, it has been demonstrated that endogenous hormone levels can be modified through changes in dietary intake (20–23). In this study we found significantly reduced risks associated with poultry and vegetable intake and related nutrients, especially dietary fiber and lignans. These findings are consistent with previous investigations (1–12) and provide further evidence that a healthy diet may at least contribute to the etiology of this neoplasm.

Interestingly, although we observed reductions in risk associated with higher dietary fiber and lignan intakes, risk was not related to higher intakes of grain products. Among grains, both dietary fiber and lignans are found predominantly in the bran portion of whole grains, which is removed in the refining process. In the western New York population, consumption of whole grain foods is low, and the primary contributors to lignan intakes in these data were coffee, carrots, cucumbers and strawberries, not grains. On the other hand, the findings for dietary fiber and lignans are consistent with the observed reduced risks associated with vegetable intake.

To our knowledge, this is the first study to investigate the effect of phytochemical intakes on ovarian cancer risk. In these data, we observed important reductions in risk associated with the highest quintiles of intake of stigmasterol and total lignans. Phytosterols have been shown to affect cholesterol metabolism, which could ultimately affect steroidogenesis (27). Plant lignans are phytoestrogens metabolized in the mammalian gut to form enterolactone and enterodiol, compounds with estrogenic as well as antiestrogenic activities (41). Reduced risks of breast cancer, another hormonally related cancer, have been associated with higher urinary excretion of lignans, although risks associated with dietary lignan intake have been inconsistent (42–44). Part of the observed effects of high lignan intakes might be explained by higher intakes of plant foods in general; however, adjustment for possibly confounding nutrients such as dietary fiber and folate had no effect on our observed estimates. Our results strengthen the hypothesis that the phytoestrogen lignans may be important contributors to the effect of diet for this and other hormone-related cancers.

On the other hand, we observed no association in risk with higher intakes of the flavonoids quercetin and kaempferol in these data. The hormonal etiology of ovarian cancer is fairly well established; flavonoids are potent antioxidants. Although it is possible that oxidative mechanisms might be important in some portion of the development or progression of ovarian neoplasms, it is likely that the hormonal mechanisms are more pronounced. Conversely, we were limited in our investigation of flavonoid intakes. Food composition data were available only for quercetin and kaempferol; there are >400 flavonoids present in the food supply (28). Although quercetin and kaempferol are strongly represented in plant foods, it is possible that we are not sufficiently estimating the true effect of flavonoids in these analyses.

An important limitation of our study is the small number of cases available for analyses, possibly reducing the generalizability of our results. Although this may have reduced the precision of our estimates, we observed both dietary and nondietary risk factors in these data that were similar to those reported in larger studies. Furthermore, even with categorization of dietary variables into quintiles, our estimates were fairly stable, and the confidence limits not overly wide. It is unlikely that a larger sample size would change our observed associations, but rather would strengthen the precision of the estimates.

As is common to all case-control studies, there may have been biased reporting of dietary intake and other data. The mean number of months between diagnosis and interview was short (2.59) and diet was queried for the 12-mo period 2 y before diagnosis. Furthermore, we observed both dietary and nondietary risk factors in these data similar to those reported in the literature. It is unlikely that bias was a serious problem in these analyses.

Food composition data for the phytochemicals examined in this study have been, until more recently, fairly limited. It is possible that we are underestimating true intakes of these compounds. However, for estimation of risk associated with diet, ranking of individuals on intake is more important than estimation of actual intake, especially given that we are interested in usual long-term diet. The error in intake estimation is likely to be random, and not associated with case-control status in these data.

Our study provides additional evidence that diet may play an etiologic role in ovarian cancer, and is the first, to our knowledge, to report an association with phytoestrogen intakes. The evidence toward a protective effect of a plant-based diet on hormone-related cancers continues to accumulate. Our continuing challenge will be in the design and implementation of strategies to encourage population-based changes toward this dietary pattern.


   FOOTNOTES
 
1 Supported in part by grants 2T32CA009051 and CA89123–01A1 from the National Cancer Institute. Back

Manuscript received 31 January 2003. Initial review completed 10 March 2003. Revision accepted 28 March 2003.


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