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Soy and Cancer Prevention Abstracts

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AUTHOR: Hebert JR; Hurley TG; Olendzki BC; Teas J; Ma Y; Hampl JS
ADDRESS: Division of Preventive and Behavioral Medicine, University of Massachusetts Medical School, Worcester 01655, USA.
TITLE: Nutritional and socioeconomic factors in relation to prostate cancer mortality: a cross-national study
SOURCE: J Natl Cancer Inst (J9J), 1998 Nov 4; 90 (21): 1637-47
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
BACKGROUND: Large international variations in rates of prostate cancer incidence and mortality suggest that environmental factors have a strong influence on the development of this disease. The purpose of this study was to identify predictive variables for prostate cancer mortality in data from 59 countries. METHODS: Data on prostate cancer mortality, food consumption, tobacco use, socioeconomic factors, reproductive factors, and health indicators were obtained from United Nations sources. Linear regression models were fit to these data. The influence of each variable fit in the regression models was assessed by multiplying the regression coefficient b by the 75th (X75) and 25th (X25) percentile values of the variable. The difference, bX75 - bX25, is the estimated effect of the variable across its interquartile range on mortality rates measured as deaths per 100000 males aged 45-74 years. Reported P values are two-sided. RESULTS: Prostate cancer mortality was inversely associated with estimated consumption of cereals (bX75 - bX25 = -7.31 deaths; P = .001), nuts and oilseeds (bX75 - bX25 = -1.72 deaths; P = .003), and fish (bX75 - bX25 = -1.47 deaths; P = .001). In the 42 countries for which we had appropriate data, soy products were found to be significantly protective (P = .0001), with an effect size per kilocalorie at least four times as large as that of any other dietary factor. Besides variables related to diet, we observed an association between prostate cancer mortality rates and a composite of other health-related, sanitation, and economic variables (P = .003). CONCLUSIONS: The specific food-related results from this study are consistent with previous information and support the current dietary guidelines and hypothesis that grains, cereals, and nuts are protective against prostate cancer. The findings also provide a rationale for future study of soy products in prostate cancer prevention trials.



AUTHOR: Jacobsen BK; Knutsen SF; Fraser GE
ADDRESS: Institute of Community Medicine, University of Troms9, Norway.
TITLE: Does high soy milk intake reduce prostate cancer incidence?
The Adventist Health Study (United States)
SOURCE: Cancer Causes Control (A5R), 1998 Dec; 9 (6): 553-7
LANGUAGE: English
COUNTRY PUB.: NETHERLANDS
ABSTRACT:
OBJECTIVES: Recent experimental studies have suggested that isoflavones (such as genistein and daidzein) found in some soy products may reduce the risk of cancer. The purpose of this study was to evaluate the relationship between soy milk, a beverage containing isoflavones, and prostate cancer incidence. METHODS: A prospective study with 225 incident cases of prostate cancer in 12,395 California Seventh-Day Adventist men who in 1976 stated how often they drank soy milk. RESULTS: Frequent consumption (more than once a day) of soy milk was associated with 70 per cent reduction of the risk of prostate cancer (relative risk = 0.3, 95 percent confidence interval 0.1-1.0, p-value for linear trend = 0.03). The association was upheld when extensive adjustments were performed. CONCLUSIONS: Our study suggests that men with high consumption of soy milk are at reduced risk of prostate cancer. Possible associations between soy bean products, isoflavones and prostate cancer risk should be further investigated.



AUTHOR: Zheng W; Dai Q; Custer LJ; Shu XO; Wen WQ; Jin F; Franke AA
ADDRESS: School of Public Health and Cancer Center, University of South Carolina, Columbia 29203, USA.
TITLE: Urinary excretion of isoflavonoids and the risk of breast cancer.
SOURCE: Cancer Epidemiol Biomarkers Prev (BNJ), 1999 Jan; 8 (1): 35-40
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
Isoflavonoids are a group of biologically active phytochemicals that humans are exposed to mainly through soy food intake. Because of the similar chemical structure of these compounds and estradiol, it has been hypothesized that isoflavonoids may be related to the risk of breast cancer. Overnight urine samples from 60 incident breast cancer cases and their individually matched controls were assayed for urinary excretion rates of five major isoflavonoids (daidzein, genistein, glycitein, equol, and O- desmethylangolensin) and total phenols. These subjects were from a large population-based case-control study conducted in Shanghai, and urine samples from breast cancer cases were collected before any cancer therapy to minimize the potential influence of the disease and its sequelae on study results. Urinary excretion of total phenols and all individual isoflavonoids, particularly glycitein, was substantially lower in breast cancer cases than controls. For total isoflavonoids, the mean excretion was 13.95 nmol/mg creatinine (SD, 20.76 nmol/mg creatinine) for cases and 19.52 nmol/mg creatinine (SD, 25.36 nmol/mg creatinine) for controls (P for difference = 0.04). The case-control difference was more evident when median levels of these compounds were compared, with the median excretion of all major isoflavonoids being 50-65% lower in cases than in controls. Individuals in the highest tertile of daidzein, glycitein, and total isoflavonoids had about half the cancer risk of those in the lowest tertile. The adjusted odds ratio for breast cancer was 0.14 (95% confidence interval, 0.02- 0.88) for women whose urinary excretion of both phenol and total isoflavonoids was in the upper 50% compared with those in the lower 50%. The results from this study support the hypothesis that a high intake of soy foods may reduce the risk of breast cancer.



AUTHOR: Xu X; Duncan AM; Merz BE; Kurzer MS
ADDRESS: Department of Food Science and Nutrition, University of Minnesota, St. Paul 55108, USA.
TITLE: Effects of soy isoflavones on estrogen and phytoestrogen metabolism in premenopausal women.
SOURCE: Cancer Epidemiol Biomarkers Prev (BNJ), 1998 Dec; 7 (12): 1101-8
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
Isoflavones and lignans are soy phytoestrogens that have been suggested to be anticarcinogenic. The mechanisms by which they exert cancer-preventive effects may involve modulation of estrogen synthesis and metabolism. To evaluate this hypothesis, a randomized, cross-over soy isoflavone feeding study was performed in 12 healthy premenopausal women. The study consisted of three diet periods, each separated by a washout of approximately 3 weeks. Each diet period lasted for three menstrual cycles plus 9 days (averaging approximately 100 days), during which subjects consumed their habitual diets supplemented with soy protein powder providing 0.16 (control diet), 1.01, or 2.01 mg of total isoflavones per kg of body weight per day (10+/-1.1, 65+/-9.4, or 129+/-16 mg/day, respectively). A 72-h urine sample was collected during the midfollicular phase (days 7- 9) of the fourth menstrual cycle in each diet period. Urine samples were analyzed for 10 phytoestrogens and 15 endogenous estrogens and their metabolites by a capillary gas chromatography-mass spectrometry method. Urinary excretion of isoflavonoids and lignans significantly increased with increased isoflavone consumption. Compared with the control diet, increased isoflavone consumption decreased urinary excretion of estradiol, estrone, estriol, and total estrogens, as well as excretion of the hypothesized genotoxic estrogen metabolites, 16alpha- hydroxyestrone, 4-hydroxyestrone, and 4-hydroxyestradiol. Of importance are the observations of a significant increase in the 2-hydroxyestrone/16alpha-hydroxyestrone ratio and a decrease in the genotoxic/total estrogens ratio. These data suggest that soy isoflavone consumption may exert cancer- preventive effects by decreasing estrogen synthesis and altering metabolism away from genotoxic metabolites toward inactive metabolites.



AUTHOR: Messina MJ; Persky V; Setchell KD; Barnes S ADDRESS: National Cancer Institute, National Institutes of Health, Bethesda, MD. TITLE: Soy intake and cancer risk: a review of the in vitro and in vivo data. SOURCE: Nutr Cancer (O94), 1994; 21 (2): 113-31 LANGUAGE: English COUNTRY PUB.: UNITED STATES ABSTRACT: International variations in cancer rates have been attributed, at least in part, to differences in dietary intake. Recently, it has been suggested that consumption of soyfoods may contribute to the relatively low rates of breast, colon, and prostate cancers in countries such as China and Japan. Soybeans contain a number of anticarcinogens, and a recent National Cancer Institute workshop recommended that the role of soyfoods in cancer prevention be investigated. In this review, the hypothesis that soy intake reduces cancer risk is considered by examining relevant in vitro, animal, and epidemiological data. Soybeans are a unique dietary source of the isoflavone genistein, which possesses weak estrogenic activity and has been shown to act in animal models as an antiestrogen. Genistein is also a specific inhibitor of protein tyrosine kinases; it also inhibits DNA topoisomerases and other critical enzymes involved in signal transduction. In vitro, genistein suppresses the growth of a wide range of cancer cells, with IC50 values ranging from 5 to 40 microM (1-10 micrograms/ml). Of the 26 animal studies of experimental carcinogenesis in which diets containing soy or soybean isoflavones were employed, 17 (65%) reported protective effects. No studies reported soy intake increased tumor development. The epidemiological data are also inconsistent, although consumption of nonfermented soy products, such as soymilk and tofu, tended to be either protective or not associated with cancer risk; however, no consistent pattern was evident with the fermented soy products, such as miso. Protective effects were observed for both hormone- and nonhormone-related cancers. While a definitive statement that soy reduces cancer risk cannot be made at this time, there is sufficient evidence of a protective effect to warrant continued investigation.



AUTHOR: Thiagarajan DG; Bennink MR; Bourquin LD; Kavas FA
ADDRESS: Department of Food Science and Human Nutrition, Michigan State University, East Lansing 48824-1224, USA.
TITLE: Prevention of precancerous colonic lesions in rats by soy flakes, soy flour, genistein, and calcium.
SOURCE: Am J Clin Nutr (3EY), 1998 Dec; 68 (6 Suppl): 1394S-1399S
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
The main purpose of this research was to determine whether diets containing soy products would inhibit the early stages of azoxymethane-induced colon cancer in F344 rats. Additional objectives were to determine whether feeding starch instead of sucrose, feeding additional calcium (0.5% compared with 0.1%), or feeding a low-fiber powdered enteral formula would influence early colon carcinogenesis. Colon cancer was initiated with 2 injections of azoxymethane (15 mg/kg body wt) and a 12-wk dietary treatment period was started 1 wk after the second injection. Precancerous colon lesions were assessed as foci with aberrant crypts (FAC). The mean numbers of FAC were 133 [soy concentrate (low concentration of phytochemicals)], 111 (starch substituted for sucrose), 98 [full-fat soy flakes (whole soybeans)], 87 (defatted soy flour), 77 (0.015% genistein), and 70 (0.5% Ca). The soy flour and full-fat soy flake diets contained 0.049% genistein derivatives (primarily glycosides), but were less effective in inhibiting the formation of FAC than the diet containing 0.015% genistein (as the aglycone). Eating soybeans and soy flour may reduce the early stages of colon cancer.



AUTHOR: Le Marchand L; Hankin JH; Wilkens LR; Kolonel LN; Englyst HN; Lyu LC
ADDRESS: Etiology Program, University of Hawaii Cancer Research Center, Honolulu, USA.
TITLE: Dietary fiber and colorectal cancer risk.
SOURCE: Epidemiology (A2T), 1997 Nov; 8 (6): 658-65
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
We conducted a population-based case-control study among different ethnic groups in Hawaii to evaluate the role of various types and components of fiber, as well as micronutrients and foods of plant origin, on the risk of colorectal cancer. We administered personal interviews to 698 male and 494 female Japanese, Caucasian, Filipino, Hawaiian, and Chinese cases diagnosed during 1987-1991 with adenocarcinoma of the colon or rectum and to 1,192 population controls matched to cases by age, sex, and ethnicity. We used conditional logistic regression to estimate odds ratios, adjusted for caloric intake and other covariates. We found a strong, dose-dependent, inverse association in both sexes with fiber intake measured as crude fiber, dietary fiber, or nonstarch polysaccharides. We found inverse associations of similar magnitude for the soluble and insoluble fiber fractions and for cellulose and noncellulosic polysaccharides. This protective effect of fiber was limited to fiber from vegetable sources, with an odds ratio of 0.6 (95% confidence interval = 0.4-0.9) and 0.5 (95% confidence interval = 0.3-0.7) for the highest compared with the lowest quartile of intake for men and women, respectively. We found associations of the same magnitude for soluble and insoluble vegetable fiber, but no clear association with fiber from fruits or cereals. This pattern was consistent between sexes, across segments of the large bowel (right colon, left colon, and rectum), and among most ethnic groups. The effect of vegetable fiber may be independent of the effects of other phytochemicals, since the effect estimates remained unchanged after further adjustment for other nutrients. Intakes of carotenoids, light green vegetables, yellow-orange vegetables, broccoli, corn, carrots, bananas, garlic, and legumes (including soy products) were inversely associated with risk, even after adjustment for vegetable fiber. The data support a protective role of fiber from vegetables against colorectal cancer, which appears independent of its water solubility property and of the effects of other phytochemicals. The data also indicate that certain vegetables and fruits may be protective against this disease through mechanisms other than their fiber content.



AUTHOR: Adlercreutz H
ADDRESS: Folkhalsan Research Centre, Department of Clinical Chemistry, University of Helsinki, Finland.
TITLE: Epidemiology of phytoestrogens.
SOURCE: Baillieres Clin Endocrinol Metab (9JL), 1998 Dec; 12 (4): 605-23
LANGUAGE: English
COUNTRY PUB.: ENGLAND
ABSTRACT:
Epidemiological studies have revealed that high levels of lignans and isoflavonoids are frequently associated with low breast, prostate and colon cancer risk, as well as a low risk of coronary heart disease. These compounds seem to be cancer protective and/or are biomarkers of a 'healthy' diet. All soy protein products consumed by Asian populations have high concentrations of isoflavonoids. In other countries, such as Finland and Sweden, the lignan levels are higher in populations with the lowest risk because of a high consumption of whole-grain rye bread, berries and some vegetables. There is a strong association between fibre intake per kilogram body weight and lignan concentrations in body fluids. Breast cancer has been found to be associated with low lignan levels in the USA, Finland, Sweden and Australia. With regard to prostate and colon cancer, as well as coronary heart disease, the epidemiological data related to phytoestrogens are still very limited.



AUTHOR: Moyad MA
ADDRESS: Section of Urology, University of Michigan, Ann Arbor 48109- 0330, USA.
TITLE: Soy, disease prevention, and prostate cancer.
SOURCE: Semin Urol Oncol (CBS), 1999 May; 17 (2): 97-102
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
Population-based studies from around the world support the theory that soy products and their constituents, primarily the isoflavones or phytoestrogens, are partly responsible for the lower rates of certain chronic diseases in different areas of the world. Cardiovascular disease and hormonally induced cancers are just a few of the conditions lower in Asian countries that consume large quantities of soy per average person. Genistein, one of soy's individual phytoestrogens, has been found to inhibit numerous breast and prostate cancer cell lines. A limited amount of clinical evidence also points to a beneficial role of soy in reducing hormonal levels and exhibiting weak estrogen and antiestrogen-like qualities. Other phytoestrogens found in nature, such as lignans, may also have a future role in cancer. Collectively, these phytoestrogens, like genistein, have enough evidence to warrant their use in a number of clinical trials as a potential chemopreventive agent or adjunct to prostate cancer treatment.



AUTHOR: Li Y; Upadhyay S; Bhuiyan M; Sarkar FH
ADDRESS: Department of Pathology, Karmanos Cancer Institute at Wayne State University School of Medicine, Detroit, Michigan 48201, USA.
TITLE: Induction of apoptosis in breast cancer cells MDA-MB-231 by genistein.
SOURCE: Oncogene (ONC), 1999 May 20; 18 (20): 3166-72
LANGUAGE: English
COUNTRY PUB.: ENGLAND
ABSTRACT:
Breast cancer is the most common cancer among American women, whereas Asian women, who consume a traditional diet high in soy products, have a relatively low incidence. Genistein is a prominent isoflavonoid in soy products and has been proposed as the agent responsible for lowering the rate of breast cancer in Asian women. We investigated the effects of genistein on cell growth and apoptosis-related gene expression in breast cancer cells MDA-MB-231. We found up-regulation of Bax and p21WAF1 expressions and down- regulation of Bcl-2 and p53 expression in genistein-treated cells. Furthermore, DNA ladder formation, CPP32 activation, and PARP cleavage were observed after treatment with genistein, indicating apoptotic cell deaths. Flow cytometry with 7-amino actinomycin D staining showed that the number of apoptotic cells increased with longer treatment of genistein. From these results, we conclude that genistein inhibits the growth of MDA-MB-231 breast cancer cells, regulates the expression of apoptosis-related genes, and induces apoptosis through a p53-independent pathway. The up- regulation of Bax and p21WAF1 may be the molecular mechanisms by which genistein induces apoptosis, however, further definitive studies are needed. These results suggest that genistein may be a potentially effective chemopreventive or therapeutic agent against breast cancer.



AUTHOR: Davis JN; Singh B; Bhuiyan M; Sarkar FH
ADDRESS: Department of Cancer Biology, Wayne State University School of Medicine, Harper Hospital, Detroit Medical Center, MI, USA.
TITLE: Genistein-induced upregulation of p21WAF1, downregulation of cyclin B, and induction of apoptosis in prostate cancer cells.
SOURCE: Nutr Cancer (O94), 1998; 32 (3): 123-31
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
Increased soy consumption in Asian diets, resulting in increased serum isoflavone levels, has been associated with a decreased risk for prostate adenocarcinoma (PCa). The isoflavone genistein is believed to be the anticancer agent found in soy, and significant levels of genistein have been detected in human prostatic fluid, implicating the role of genistein in PCa prevention. Recent studies have demonstrated genistein's ability to inhibit cell growth and induce apoptosis in several cell lines; however, the molecular mechanisms of genistein's effect are not known. We have evaluated the mechanism by which genistein may inhibit PCa cell growth. Here we report that genistein inhibits PCa cell growth in culture in a dose-dependent manner, which is accompanied by a G2/M cell cycle arrest. Cell growth inhibition was observed with concomitant downregulation of cyclin B, upregulation of the p21WAF1 growth-inhibitory protein, and induction of apoptosis. Collectively, these results provide experimental evidence for a novel effect of genistein on cell cycle gene regulation, resulting in the inhibition of cell growth and ultimate demise of tumor cells.



AUTHOR: Fair WR; Fleshner NE; Heston W
ADDRESS: Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA.
TITLE: Cancer of the prostate: a nutritional disease?
SOURCE: Urology (WSY), 1997 Dec; 50 (6): 840-8
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
In summary, epidemiologic and laboratory evidence increasingly demonstrate that nutritional factors, especially reduced fat intake, soy proteins, vitamin E derivatives, and selenium, may have a protective effect against prostate cancer. The experimental observation that low-fat diets and soy protein extracts may influence the progression of established tumors, rather than inhibiting etiologic factors, is particularly intriguing because it may serve to help explain the paradox whereby the incidence of clinical prostate cancer shows wide geographic variation, yet the evidence persists that the incidence of microfocal tumors is essentially the same worldwide. These observations, plus the likelihood that nutrition trials are likely to have little in the way of toxicity that would preclude their completion, argue that such trials should be performed. It is estimated that 30% to 50% of human malignancies may be related to dietary factors, and although the feasibility of trials involving low-fat diets has been proved in ongoing trials for colon and breast cancer, no similar study exists for prostate malignancy. Critics of epidemiologic research argue that data derived from case- control studies are subject to recall bias and are thus artifactual. Indeed, many researchers now believe that the breast cancer-dietary fat hypothesis has been discredited. The major difference between the prostate cancer and breast cancer literature is the remarkable consistency of the cohort studies. In these studies, exposure is determined prospectively and is therefore free from recall bias. In this sense they more closely resemble a clinical trial. The majority of cohort studies involving dietary fat and breast cancer have been negative. We believe that these data justify large-scale trials in the area of prevention of prostate cancer. One such proposed study already submitted for National Institutes of Health funding from a consortium of centers is the Prostate Interventional Nutrition Study (PINS), modeled after the Women's Interventional Nutrition Study, which investigates the effect of low-fat diets in women receiving therapy for node-positive breast cancer. The PINS study will be limited to men who have detectable serum PSA levels but no other clinical evidence of disease after radical prostatectomy. All subjects will receive nutritional guidance, with randomization between a control arm receiving the currently recommended 30% fat diet and an interventional arm in which a 15% fat diet is supplemented with soy protein, vitamin E, and selenium. The end points for evaluation will be compared with progression based on changes in PSA and the time of onset of clinical, as opposed to biochemical, disease. Single-institution trials involving groups thought to be at high risk of developing clinical cancer--including men with persistently elevated PSA levels, two negative prostate biopsies, high-grade prostatic intraepithelial neoplasia on biopsy, and a strong family history of prostate cancer--are being initiated at MSKCC and other institutions. CONCLUSIONS: We have reviewed the evidence that nutritional factors play a role in the progression rate of prostate cancer and may help to explain the geographic variation in the incidence observed. However, without well-controlled prospective trials, the attractive hypothesis that nutrition plays a role in tumor progression remains simply an attractive hypothesis. To date, no definite proof of a preventive effect has been shown in a study that will withstand rigid scientific scrutiny. The opportunity exists, however, for the urologic community, working together with experts in the area of nutrition, not only to advance our understanding of prostate tumorigenesis, but to rebut those critics of modern medical technology who claim that we have ignored the total or holistic approach to healing. (ABSTRACT TRUNCATED)



AUTHOR: Goodman MT; Wilkens LR; Hankin JH; Lyu LC; Wu AH; Kolonel LN ADDRESS: Epidemiology Program, Cancer Research Center of Hawaii, University of Hawaii, Honolulu, USA.
TITLE: Association of soy and fiber consumption with the risk of endometrial cancer.
SOURCE: Am J Epidemiol (3H3), 1997 Aug 15; 146 (4): 294-306
LANGUAGE: English
COUNTRY PUB.: UNITED STATES
ABSTRACT:
The authors conducted a case-control study among the multi- ethnic population of Hawaii to examine the role of dietary soy, fiber, and related foods and nutrients on the risk of endometrial cancer. Endometrial cancer cases (n = 332) diagnosed between 1985 and 1993 were identified from the five main ethnic groups in the state (Japanese, Caucasian, Native Hawaiian, Filipino, and Chinese) through the rapid- reporting system of the Hawaii Tumor Registry. Population controls (n = 511) were selected randomly from lists of female Oahu residents and matched to cases on age (+/-2.5 years) and ethnicity. All subjects were interviewed using a diet history questionnaire that included over 250 food items. Non-dietary risk factors for endometrial cancer included nulliparity, never using oral contraceptives, fertility drug use, use of unopposed estrogens, a history of diabetes mellitus or hypertension, and a high Quetelet's index (kg/cm2). Energy intake from fat, but not from other sources, was positively associated with the risk of endometrial cancer. The authors also found a positive, monotonic relation of fat intake with the odds ratios for endometrial cancer after adjustment for energy intake. The consumption of fiber, but not starch, was inversely related to risk after adjustment for energy intake and other confounders. Similar inverse gradients in the odds ratios were obtained for crude fiber, non-starch polysaccharide, and dietary fiber. Sources of fiber, including cereal and vegetable and fruit fiber, were associated with a 29-46% reduction in risk for women in the highest quartiles of consumption. Vitamin A and possibly vitamin C, but not vitamin E, were also inversely associated with endometrial cancer, although trends were not strong. High consumption of soy products and other legumes was associated with a decreased risk of endometrial cancer (p for trend = 0.01; odds ratio = 0.46, 95% confidence interval 0.26-0.83) for the highest compared with the lowest quartile of soy intake. Similar reductions in risk were found for increased consumption of other sources of phytoestrogens such as whole grains, vegetables, fruits, and seaweeds. Ethnic-specific analyses were generally consistent with these results. The observed dietary associations appeared to be largely independent of other risk factors, although the effects of soy and legumes on risk were limited to women who were never pregnant or who had never used unopposed estrogens. These data suggest that plant-based diets low in calories from fat, high in fiber, and rich in legumes (especially soybeans), whole grain foods, vegetables, and fruits reduce the risk of endometrial cancer. These dietary associations may explain in part the reduced rates of uterine cancer in Asian countries compared with those in the United States.





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