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© 2007 American Society for Nutrition J. Nutr. 137:1974-1979, August 2007

Nutritional Epidemiology

Dietary Isoflavones May Protect against Prostate Cancer in Japanese Men1,2

Yoshie Nagata3, Tomoko Sonoda3,*, Mitsuru Mori3, Naoto Miyanaga4, Koji Okumura5, Ken Goto5, Seiji Naito5, Kiyohide Fujimoto6, Yoshihiko Hirao6, Atsushi Takahashi7, Taiji Tsukamoto7 and Hideyuki Akaza4

3 Department of Public Health, Sapporo Medical University School of Medicine, Chuo-ku, Sapporo, Hokkaido 060-8556, Japan; 4 Department of Urology, Institute of Clinical Medicine, Tsukuba University, Tsukuba, Ibaraki 305-8575, Japan; 5 Department of Urology, Faculty of Medicine, Kyushu University, Higashi-ku, Fukuoka 812-8582, Japan; 6 Department of Urology, Nara Medical University, Kashihara, Nara 634-8521, Japan; and 7 Department of Urology, Sapporo Medical University School of Medicine, Chuo-ku, Sapporo, Hokkaido 060-8556, Japan

* To whom correspondence should be addressed. E-mail: tsonoda{at}sapmed.ac.jp.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
We examined associations between nutritional and other lifestyle factors and the prevalence of prostate cancer in a case-control study of Japanese men. Two hundred patients and 200 age-matched controls (±5 y) were selected from 3 geographic areas of Japan. BMI, physical activity, occupation, family history of prostate cancer, and medical history were not associated with prostate cancer risk. Isoflavones and their aglycones (genistein and daidzein) were significantly associated with decreased risk. The odds ratio for the highest category (≥89.9 mg/d) compared with the lowest category (<30.5 mg/d) of isoflavone intake was 0.42 (95% CI = 0.24–0.72) and the linear trend was significant (P < 0.01). PUFA, (n-6) fatty acids, and magnesium were significantly associated with decreased risk but not after adjustment for isoflavone intake. Isoflavone intake was correlated with the intake of PUFA (r = 0.68, P < 0.001), (n-6) fatty acids (r = 0.69, P < 0.001), and magnesium (r = 0.56, P < 0.001), because soy products contain high levels of these nutrients. On the other hand, isoflavone significantly decreased the risk of prostate cancer regardless of adjustment by PUFA, (n-6) fatty acids or magnesium. In conclusion, our findings indicate that isoflavones might be an effective dietary protective factor against prostate cancer in Japanese men.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The age-standardized incidence rate of prostate cancer is lower in Japan (9.2/100,000 in Osaka prefecture in 1993–1997) than in other countries (e.g. 50.7/100,000 in Saarland, Germany, between 1993 and1997 and 44.4/100,000 in Oxford, England, during the same period) (1). However, the rates associated with Japanese immigrants in Hawaii is 62.1/100,000, which is ~6-fold higher than that in Japan (1) and the incidence of prostate cancer in Japan is gradually increasing. Thus, environmental factors such as dietary habits might play a major role in prostate cancer. The Japanese diet is high in soy products and fish. Soy includes substantial amounts of isoflavones, which are phytoestrogens. This case-control study evaluated the effects of isoflavones, fatty acids, vitamins, and minerals in the Japanese diet on prostate cancer risk. In addition, we examined whether physical activity, occupation, family history of prostate cancer, and medical history are associated with prostate cancer risk, because such associations in Japan had not been reported.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Participants. Surveys for this case-control study were performed in the Ibaraki, Nara, and Hokkaido areas. Two hundred cases with a confirmed histological diagnosis of adenocarcinoma of the prostate by prostate-specific antigen testing, digital rectal examination, and biopsies between 1996 and 2003 were used for analysis. A total of 80 cases from the Department of Urology of Tsukuba University Hospital in Ibaraki, 28 cases from the Department of Urology of Nara Medical College Hospital in Nara, and 92 cases from the Department of Urology of Sapporo Medical University Hospital in Hokkaido were included. The age range was 59–73 y. The stage distribution was as follows: 1 case of Stage 1, 131 cases of Stage 2, 44 cases of Stage 3, and 24 cases of Stage 4. The median and mode time between diagnosis and interview for this study were 3 and 2 mo, respectively.

A total of 200 controls were selected from the urology, oral surgery, ophthalmology, orthopedics, and dermatology departments of the same hospitals (or clinics in the same area as cases) and matched to each case by age (±5 y). Disease categories were benign kidney disorder, oral diseases, cataract, otitis media, and dermatosis. Exclusion criteria for controls were clinical history of benign prostatic hypertrophy, other prostatic diseases, malignant tumors, dietary restriction, or a serum prostate-specific antigen concentration of >4.0 µg/L.

The total sample size was 400, which was sufficient to detect an OR of 0.5 or 2.0 with 80% statistical power or more at 5% significance.

This study was approved by the ethics committee of each university. Physicians obtained informed consent from all subjects.

    Questionnaire. Fully trained staff interviewed both case and control participants in hospitals. The questionnaire included the following information: height, weight, cigarette smoking, physical activity, employment history, medical history, family (first and second degree) history of prostate cancer, and food items consumed. We used participants' height and weight to calculate their mean BMI from age 40 to 45 y and 1 y before diagnosis. Information on smoking habits included age when participant started, duration in years, and number of cigarettes smoked per day. Employment history included occupation 1 y before diagnosis and the job at which the participant worked for the longest period. Physical activity other than during working time included the type, period, mean frequency per month, and hours per occasion from age 40 to 45 y and 1 y before diagnosis. Employment history included the occupation held 1 y before diagnosis and the job at which the participant worked for the longest period. Medical history included questions about hypertension, diabetes, tuberculosis, heart disorder, stroke, sexually transmitted diseases, other infectious or lifestyle-related diseases, and vasectomy.

Interviewers questioned the participants in detail about their habitual diets, showing photographs of types and amounts of meals. The mean daily intakes of beverages and various foods including 11 soybean products during the 5 y before diagnosis was assessed using a semiquantitative FFQ that was a modification (with the authors' permission) of the questionnaire used in the Takayama study (2) in the Gifu prefecture. The validity of the Takayama study questionnaire was verified by Shimizu et al. (2). For men, the Pearson correlation coefficient for macronutrients between the questionnaire and 3-d records ranged from 0.45 to 0.51 in the Takayama study (2). We added 4 soy products to soybean items of the Takayama study. The following 12 food items were included in the questionnaire: tofu (soybean curd), natto (fermented soybeans), miso soup (soybean paste soup), okara (bean curd refuse), aburaage (fried bean curd), ganmodoki (fried bean curd with vegetables), kinako (soy flour), yuba (dried bean curd), tonyu (soybean milk), soy sauce, green soybeans, and bean sprouts.

Most participants in this study consumed a traditional Japanese diet consisting of fish, soy products, rice, and a little meat. Control subjects consumed 92.4 ± 79.8 g fish/d, 145.4 ± 94.8 g soy products/d, 279.3 ± 140.3 g rice/d, and 43.6 ± 30.1 g meat/d. Case subjects consumed 87.6 ± 63.0 g fish/d, 119.0 ± 75.6 g soy products/d, 299.6 ± 147.0 g rice/d, and 46.0 ± 28.7 g meat/d.

    Data analysis. We categorized BMI as <23.0 (normal), 23.0–24.9 (overweight), and ≥25.0 (obese). For physical activity, metabolic equivalent (MET) hours per week (MET-h/wk) were calculated for each participant. One MET equals ~3.5 mL·kg–1·min–1 of oxygen consumed, the cost of sitting at rest, with higher activity levels represented in multiples of this value. The various MET values provided by Ainsworth et al. (3) were used to estimate physical activity. The MET-h/wk were categorized into tertiles. Occupation was summarized in 4 categories based on major groups of the 2002 Census Occupational Classification (4). The OR of each occupation 1 y before diagnosis of prostate cancer and for the longest duration of employment was calculated using all other occupations and no employment as a reference category. Estimates of age-adjusted OR and 95% CI were calculated by conditional logistic regression models with adjustment for pack-years of smoking [cigarettes/(d x 20) x years of smoking] as a potential confounding factor, because some controls were selected from patients with smoking-related diseases, such as cataract (5) and oral disease (6,7).

The quantity of each nutrient included in each food item was obtained from the Standard Tables of Food Composition in Japan 2002. The nutrients we investigated were total isoflavones and their aglycones (genistein and daidzein), protein, carbohydrates, fatty acids (total fatty acids, SFA, monounsaturated fatty acids, PUFA, (n-6) fatty acids, and (n-3) fatty acids as a subcategory of PUFA), lycopene, vitamins (all carotenes, folate, vitamin K, thiamin, riboflavin, vitamin B-6, vitamin B-12, niacin, pantothenic acid, vitamin C, vitamin D, and vitamin E), and minerals (sodium, potassium, calcium, magnesium, selenium, zinc, and iron). Daily intake of each nutrient was calculated by adding the intake of food items and multiplying the portion size (in grams) by food frequency per day and was classified into quartiles (Q1–Q4) or other suitable categories on the basis of the distribution among control subjects. Estimates of age-adjusted OR, 95% CI, and linear trends of nutrient intake were calculated by conditional logistic regression models with adjustment for total energy intake, tobacco pack-years, and also isoflavone intake. Furthermore, total isoflavones and their aglycones were adjusted with PUFA, (n-6) fatty acids, or magnesium intakes. Median values in each category were entered into models for the linear trend tests.

The lowest category, with an OR of 1.00, was the reference category throughout the analyses. Analyses were performed with SPSS release 11.5.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
The OR for BMI, physical activity, industries, and family history of prostate cancer were not significant (all P-values > 0.1)(Table 1). Two of the 13 cases with family history of prostate cancer were both a father and a brother of prostate cancer patients. There was no association between medical history and prostate cancer risk (data not presented).


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  		TABLE 1 Risk of prostate cancer associated with BMI, physical activity, occupation, and family history in Japanese men

 
Total isoflavones, genistein, and daidzein were significantly associated with decreased risk of prostate cancer (Table 2). The OR for the fourth (Q4) vs. the first (Q1) category were 0.42 (95% CI = 0.24–0.72) for total isoflavones, 0.58 (95% CI = 0.34–0.97) for genistein, and 0.55 (95% CI = 0.32–0.93) for daidzein. Each linear trend also showed significantly decreasing risk (P < 0.05). The PUFA-adjusted OR and linear trend of total isoflavones showed significantly decreased risk (Table 2). The adjusted OR and linear trend of total isoflavones by (n-6) fatty acids and magnesium were similar (data not presented).


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  		TABLE 2 Risk of prostate cancer associated with isoflavone and aglycone intakes in Japanese men

 
PUFA and (n-6) fatty acids were significantly associated with decreased risk (Table 3). The OR for Q4 vs. Q1 was 0.44 (95% CI = 0.22–0.86) for PUFA and 0.53 (95% CI = 0.29–0.98) for (n-6) fatty acids. Each linear trend was significant (P < 0.05). The isoflavone-adjusted OR and linear trend of PUFA and (n-6) fatty acids did not show decreased risk (Table 3). Total, monounsaturated, and (n-3) fatty acids, SFA, and the ratio of (n-6):(n-3) fatty acids were not associated with prostate cancer risk (Table 3).


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  		TABLE 3 Risk of prostate cancer associated with fatty acid intakes in Japanese men

 
Magnesium was significantly associated with decreased risk (Table 4). The OR for Q4 vs. Q1 was 0.32 (95% CI = 0.16–0.66) and the P-value of the linear trend was <0.01. The isoflavone-adjusted OR and linear trend for magnesium showed no association (Table 4). Lycopene, vitamins (all carotenes, folate, vitamin B-12, vitamin C, vitamin D, and vitamin E), and selenium were not associated with prostate cancer risk (Table 4). The following other nutrients also were not associated with risk of prostate cancer: energy, protein, carbohydrates, sodium, potassium, vitamin K, thiamin, riboflavin, vitamin B-6, niacin, pantothenic acid, vitamin C, calcium, zinc, and iron (data not presented). Beverages (alcohol, coffee, black tea, and green tea) showed no association (data not presented).


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  		TABLE 4 Risk of prostate cancer associated with lycopene, vitamin, and mineral intakes in Japanese men

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Although it has been suggested that obesity and physical activity are associated with circulating testosterone levels (8,9), epidemiological studies have not provided strong evidence in prostate cancer (10). In this study, the prevalence of obesity may not have had enough statistical power for risk evaluation, because the frequency of obesity (BMI ≥25.0) in the Japanese population is low, with only 29.9% of controls having a BMI ≥25.0 1 y before diagnosis.

Occupational associations with prostate cancer are inconclusive except for farming (11). Positive associations between prostate cancer and farming were found in meta-analyses, although the excess risk was slight (12).

Many case-control studies (13–16) and cohort studies (17,18) have suggested that a family history of prostate cancer is associated with an increased risk of prostate cancer. In this study, a family history of prostate cancer showed no association. Our study may have had insufficient power to detect such an association, because the number of participants was relatively small and the age-adjusted incidence of prostate cancer is low in Japan. The required sample size would be 1600 for both cases and controls in this study.

The traditional Japanese diet includes many soy products, especially tofu and natto, which are rich in isoflavones (509 µg/g tofu and 1273 µg/g natto) (19) and, thus, the dietary isoflavone intake of the Japanese population is high. Serum phytoestrogen concentrations are higher among Japanese men and women than among those in Western countries. For example, the mean serum concentration of genistein in Japanese men is 492.7 nmol/L compared with 33.2 nmol/L in men from the UK) (20) and urinary excretion of phytoestrogens by Japanese is also high (21). In this study, control subjects consumed 67.0 mg isoflavone/d, which is ~200 times that in Sweden (22). Some epidemiological studies in Japan have suggested that the intake of soybean products may protect against prostate cancer (23,24). In the present study, the OR of ≥89.9 mg/d for <30.5 mg/d of isoflavone intake was 0.42 (95% CI = 0.24–0.72) and the linear trend was significant. These findings indicate that isoflavones indeed confer a protective effect against prostate cancer. Genistein and daidzein, which are aglycones of isoflavones, were associated with significant reductions in prostate cancer risk. However, the PUFA-adjusted OR and linear trend for genistein and daidzein did not show significant associations. The amounts of these aglycones compared with the amounts of total isoflavones in soy products may have been insufficient for risk evaluation. The proportion of aglycones in the isoflavones in each soybean product is different. The proportions of aglycones are below 15.0% in tofu, natto, aburaage, kinako, yuba, and tonyu, substantial amounts of which are consumed daily in Japan, but over 60% in miso and soy sauce, both of which are also consumed on a daily basis but in small amounts.

Many experimental studies have reported anticancer effects of isoflavones, and aglycones in particular, against prostate cancer; the mechanisms are thought to involve induction of apoptosis of prostate cancer cells (25–27) and growth inhibition by cell cycle arrest (28–30). In an intervention study, Dalais et al. (31) showed that men whose diets were high in phytoestrogens had reduced risks of prostate cancer development and progression. Recently, an adverse effect of isoflavones on normal hormone-related tissue was demonstrated; isoflavones promoted endometrial hyperplasia (32,33). In June 2006, the Food Safety Investigation Council in Japan (34) established an upper limit of isoflavone intake except from food sources at 30 mg/d for both men and women. The council contends that the Japanese population consumes sufficient isoflavones daily and does not need additional sources beyond the normal diet; in particular, the sensitivity of men to isoflavones may be higher than that of women, although adverse effects on the prostate have not been reported.

PUFA was mainly contained in the following foods in Japan: soy products, fish (mackerel, sardines, pacific saury, and horse mackerels, etc.), and vegetable oils. PUFA are classified into (n-3) and (n-6) fatty acids, with the former being found in fish, especially mackerel, sardines, and pacific saury. These are daily staples among Japanese people; the intake of fish per day among controls in this study was 92.4 g. MacLean et al. (35) noted that a large body of literature spanning numerous cohorts from many countries and with different demographic characteristics does not provide evidence to suggest a significant association between (n-3) fatty acids intake and prostate cancer incidence. In our study, the OR and the linear trend for (n-3) fatty acids were not significant. PUFA and (n-6) fatty acids are present in substantial amounts in soy, >10.0 g and >8.0 g, respectively, per 100 g of dried Japanese soy (Standard Tables of Food Composition in Japan) (36). Isoflavone intake was correlated with the intake of (n-6) fatty acids (r = 0.69; P < 0.001) and PUFA (r = 0.68; P < 0.001); therefore, the isoflavone-adjusted OR and linear trend of (n-6) fatty acids and PUFA showed no association. It was suggested that PUFA and (n-6) fatty acids were the insignificant risk factors depending on the intake of isoflavones in soy products.

Magnesium is present in substantial amounts in tofu, a type of soy product (>30 mg/100 g tofu according to by the Standard Tables of Food Composition in Japan) (36). Isoflavone intake was correlated with the intake of magnesium (r = 0.56; P < 0.001); therefore, the isoflavone-adjusted OR and linear trend for magnesium showed no association. Few reports have noted an association between magnesium intake and prostate cancer risk.

Other nutrients and beverages did not show significant associations with prostate cancer risk in this study. Many epidemiological studies have evaluated possible inverse associations of prostate cancer risk with lycopene (37), ß-carotene (38,39), vitamin E (40–42), and selenium (43,44), although epidemiologic evidence is still inconsistent.

We cannot deny the possibility of recall bias, because our study was retrospective in design. However, in conclusion, isoflavones might be an effective dietary protective factor against prostate cancer in Japanese men.


   FOOTNOTES
 
1 Supported by a Grant-in-Aid for Scientific Research on Priority Areas, Cancer A03-720 from the Japanese Ministry of Education, Culture, Sports, Science and Technology. Back

2 Author disclosures: Y. Nagata, T. Sonoda, M. Mori, N. Miyanaga, K. Okumura, K. Goto, S. Naito, K. Fujimoto, Y. Hirao, A. Takahashi, T. Tsukamoto, and H. Akaza, no conflicts of interest. Back

Manuscript received 4 January 2007. Initial review completed 8 February 2007. Revision accepted 9 June 2007.


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TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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