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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:797-800, March 2003

Nutritional Epidemiology
Research Communication

Soy Product Intake Is Inversely Associated with Serum Homocysteine Level in Premenopausal Japanese Women1

Chisato Nagata2, Hiroyuki Shimizu, Rieko Takami*, Makoto Hayashi*, Noriyuki Takeda{dagger} and Keigo Yasuda{dagger}

Department of Public Health, Gifu University School of Medicine, Gifu 500-8705, Japan; * Internal Medicine of Matsunami General Hospital, Gifu, Japan; and {dagger} The Third Department of Internal Medicine, Gifu University School of Medicine, Gifu 500-8705, Japan

2To whom correspondence should be addressed. E-mail: chisato{at}cc.gifu-u.ac.jp.


   ABSTRACT
TOP
 ABSTRACT
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Soybeans, which are an excellent source of folate, vitamin B-6 and minerals, may reduce serum homocysteine level. However, there is a possibility that dietary soy raises the serum homocysteine level because isoflavones, which are weak estrogens contained in soybeans, may exert antiestrogenic effects in a high estrogen environment, such as in premenopausal women. The present study examined a cross-sectional relationship between soy product intake and serum homocysteine level in 201 premenopausal Japanese women. Intakes of soy products, folate, methionine and vitamins B-6 and B-12 were estimated by a semiquantitative food frequency questionnaire. Folate status was also assessed by measuring serum folate. Soy product intake in terms of soy protein as well as soy isoflavone intake was modestly but significantly inversely associated with serum homocysteine level (r = -0.15, P = 0.04) after controlling for covariates. Soy product intake was also significantly positively correlated with serum folate (r = 0.15, P = 0.04). Although it is unclear the extent to which each component of soy, such as folate and isoflavones, is associated with the serum homocysteine concentration, this biochemical complex appears to have a favorable effect on homocysteine metabolism in premenopausal women.

KEY WORDS: • soybeans • isoflavones • homocysteine • premenopausal women

An elevated blood homocysteine concentration has been shown to be an independent risk factor for cardiovascular disease (1 ). Several studies have identified factors that are associated with homocysteine level in the general population (2 –10 ). Established determinants of blood homocysteine include folate and vitamin B-12 status and serum creatinine concentration (10 ); this is expected because they serve as cofactors in the enzymatic pathway of homocysteine metabolism (11 ).

A recent study reported by Bazzano et al. (12 ) has shown that the consumption of legumes, which are high in bean protein, was significantly inversely associated with the risk of coronary heart disease. Soybeans are an excellent source of folate. It is possible that soy intake reduces the serum homocysteine concentration, which can lead to a decreased risk of coronary heart disease. However, there is a possibility that soy intake raises the serum homocysteine concentration because soybeans are also a unique dietary source of a group of phytochemicals called isoflavones. Although isoflavones are structurally similar to estrogens, it is hypothesized that isoflavones exert antiestrogenic effects in a high estrogen environment, such as in premenopausal women, and estrogenic effects in a low estrogen environment, such as in postmenopausal women (13 ). Blood homocysteine concentration is related to estrogen status. Premenopausal women or women who are on hormone replacement therapy have lower homocysteine concentrations than postmenopausal women (14 ,15 ). Therefore, soy or isoflavone intake in premenopausal women may hinder the beneficial effect of their endogenous estrogen status on homocysteine concentration.

To our knowledge, two intervention studies that examined the effects of soy protein on serum biomarkers have included measurements of serum homocysteine in diabetic subjects (16 ) and hypercholesterolemic subjects (17 ). In both studies, there was a decreased plasma homocysteine concentration with soy protein intake compared with casein intake, suggesting a novel, possibly antiatherosclerotic effect of dietary soy. However, the subjects of these studies were men or postmenopausal women. Also, the differences in amino acid composition, including that of methionine, one of the principal dietary precursors of homocysteine, of casein and soy protein may account for the findings.

In the present cross-sectional study, we examined the relationship between soy intake and serum homocysteine concentration in premenopausal Japanese women considering folate, methionine, vitamin B-6 and vitamin B-12 status. A recent update of the Japanese food composition tables enabled us to measure dietary intakes of folate and vitamins B-6 and B-12.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Subjects for this study were participants in a health check-up program provided by a general hospital in Gifu, Japan, between September 1996 and August 1997. A total of 291 premenopausal women agreed to participate and completed a self-administered questionnaire that asked about demographic characteristics, smoking and drinking habits, diet, exercise and past medical and reproductive histories (the response rate was 95.7%). To be considered premenopausal, a woman had to have had at least one natural menstrual cycle in the previous 12 mo. Women who had experienced surgical menopause >3 mo before the study were considered to be postmenopausal. To obtain complete data, a nurse epidemiologist interviewed those who returned the questionnaire with incomplete information.

Diet was assessed by a semiquantitative food-frequency questionnaire. The women were asked to indicate the average frequency that they consumed 169 food items during the year before the study and the usual serving size of each item. We included nine food items for soy products (miso soup, tofu, deep-fried tofu, fried bean curd, dried bean curd, fermented soy beans, houba-miso, soymilk and boiled soybeans). Soy product intake, as the total amount (g/d) of soy products, was calculated as the sum of these nine food items. Soy protein intake (g/d) was also calculated as the sum of the protein included in these food items. Isoflavone intake (mg/d) from soy products was estimated using isoflavone concentration in these soy foods (18 ). The intakes of foods and nutrients were estimated from the frequency of ingestion and portion size using the Japanese Standard Tables of Food Composition, fourth and fifth editions, published by the Science and Technology Agency of Japan (19 ). The Japanese food composition tables are incomplete for amino acid compositions of some foods. When the values were missing for a certain food, they were substituted by those of another nutritionally comparable food. Detailed information on the questionnaire, including its validity and reproducibility, has been described (20 ,21 ). For example, the Spearman correlation coefficient comparing estimates of soy product intake from this questionnaire with the estimates from 12 daily diet records kept over a 1-y period was 0.71. The corresponding figures for folate, methionine and vitamins B-6 and B-12 were 0.45, 0.61, 0.59 and 0.24, respectively.

A fasting blood sample was collected from each subject between 9 and 10 AM. The samples were stored at -80°C until assayed. Serum homocysteine was determined by HPLC using the fluorescent conjugate (22 ). Serum folate was measured with a radioassay (23 ). Serum creatinine was determined with standard automated clinical chemistry laboratory technique (24 ). All measurements were conducted at SRL, Inc. (Tokyo, Japan). The intra-assay and interassay CVs were 1.1% and 3.5% for homocysteine, 7.5% and 11.1% for folate and 1.3% and 2.3% for creatinine, respectively.

This study was approved by the local institutional review board.

For statistical analysis, we excluded women who were taking hormone replacement therapy or other hormones (n = 11) and who had a history of cancer (n = 10), ischemic heart disease (n = 1) and endogenous diseases such as diabetes mellitus (n = 9). Of the 260 eligible women, serum creatinine concentrations were measured for 207 women who chose program courses including this measurement; 201 had sufficient sera available for the measurement of serum folate and homocysteine. Their ages ranged from 20 to 54 y.

Spearman correlation coefficients were used to calculate the associations of dietary soy with serum homocysteine and folate. Intakes of soy products and the individual nutrient were log-transformed and adjusted for total energy intake using the method proposed by Willett (25 ). Previous studies have suggested that age, body size, education, smoking, alcohol use, coffee consumption and serum creatinine concentrations are associated with blood homocysteine concentration. The effects of these potential confounders were examined by including them into the models as covariates. Significant difference was declared at P = 0.05. All of the statistical analyses were performed using SAS programs (26 ).


   RESULTS
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
The characteristics of the study subjects are given in Table 1 ; 187 (93.0%) women were married, and 12 (6.0%) women were current smokers.


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  		TABLE 1 Selected characteristics of 201 premenopausal Japanese women1

 
The correlation between soy product intake and serum homocysteine concentration was marginally significant (r = -0.13, P = 0.07), but soy protein and soy isoflavone intakes were significantly inversely correlated with serum homocysteine concentration after controlling for age and total energy intake (r = -0.15, P = 0.04 and r = -0.14, P = 0.04, respectively) (Table 2 ). Additional adjustment for height and weight, years of education, pack-years of cigarette smoking, alcohol and coffee intakes and serum creatinine concentration did not alter the results. Intakes of vitamin B-6 and folate were significantly inversely correlated with serum homocysteine concentration after controlling for covariates (r = -0.17, P = 0.02 and r = -0.17, P = 0.02, respectively), and the correlation for vitamin B-12 was of marginal significance (r = -0.14, P = 0.07). Serum folate was strongly inversely correlated with serum homocysteine concentration (r = -0.46, P = 0.0001).


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  		TABLE 2 Spearman correlation coefficients for serum homocysteine with intakes of soy products, methionine and vitamins B-6 and B-12 and folate status in premenopausal Japanese women1

 
The correlations between folate status and intakes of soy protein, methionine and vitamins B-6 and B-12 are shown in Table 3 . Total soy product and soy isoflavone intakes were omitted from the table because these variables were highly correlated with soy protein intake (r = 0.94 and r = 0.995, respectively). The correlations among dietary soy protein, folate and vitamin B-6 were strong. The estimated means ± SD of folate and vitamin B-6 intakes derived from soy products were 64.1 ± 45.0 µg/d and 0.10 ± 0.06 mg/d, respectively.


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  		TABLE 3 Spearman correlation coefficients between intakes of soy protein, methionine and vitamins B-6 and B-12 and folate status in premenopausal Japanese women1

 
Further adjustment for folate or vitamin B-6 intake attenuated the correlations between soy intake variables and serum homocysteine concentration (for soy protein intake, r = -0.07, P = 0.34 and r = -0.08, P = 0.27 after additional adjustment for folate and vitamin B-6, respectively). Adjustment for serum folate also attenuated the correlations between soy protein and serum homocysteine (r = -0.10, P = 0.19).


   DISCUSSION
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
We observed that a high intake of soy protein or isoflavones was modestly but significantly associated with a decreased serum homocysteine concentration in premenopausal women. In accordance with other studies (3 ,5 ,7 –10 ), serum homocysteine concentration was significantly inversely correlated with dietary and serum folate, and the strong correlation with serum folate concentration suggests that serum folate is an important determinant of serum homocysteine. Vitamin B-6 also plays a role in homocysteine transsulfuration and catabolism (11 ). We observed a significant inverse correlation between vitamin B-6 intake and serum homocysteine. Similar results have been reported in some studies (10 ,27 ,28 ). However, the correlation with vitamin B-6 was attenuated (r = -0.07) after additional adjustment for serum folate.

Soy intake was significantly inversely correlated with serum folate, and an adjustment for folate status or dietary vitamin B-6 attenuated the correlation between soy intake variables and serum homocysteine. This may suggest that the folate or vitamin B-6 contained in soy products accounts for the apparent association between dietary soy and serum homocysteine concentration. However, it is possible that some other components of soybeans are related to decreased serum homocysteine concentration. Soy products are also rich in minerals, such as iron, zinc, calcium, phosphorus and potassium. The dietary or plasma concentration of these minerals has been inversely associated with serum homocysteine concentration in some studies (3 ,28 ) as well as in the present study (data not shown). Because of strong correlations among intakes of folate, vitamins and minerals when soy products are consumed, it is difficult to associate specific components of soybeans with a decreased serum homocysteine concentration. It is also impossible to entirely rule out confounding with serum folate or intake of folate, vitamin B-6, minerals or other nutrients as an explanation of our finding.

We speculated that the presence of folate or vitamin B-6, if not other components in soybeans, might offset the homocysteine concentration raising effect of soy isoflavones. However, we considered whether soy isoflavones can increase the serum homocysteine concentration in premenopausal women through the antiestrogenic effect. Studies on endogenous estrogen and homocysteine concentrations are scarce. Wouters et al. (29 ) have reported that plasma homocysteine concentration after methionine loading was negatively correlated with serum estradiol concentration. Our previous cross-sectional and intervention studies have shown that soy intake decreases serum estrogen concentrations in premenopausal women (20 ,30 ). However, a decreased serum estrogen concentration may not necessarily lead to a decrease in homocysteine concentration. Considering that the observed correlation between soy isoflavone intake and serum homocysteine concentration was attenuated but remained inverse after adjustment for folate status, we cannot rule out the possibility that dietary soy has an estrogenic effect on homocysteine metabolism in premenopausal women.

Although the present study had limitations in terms of inferring to what extent each component of soy products, such as folate and isoflavones is related to serum homocysteine concentration, we obtained results that do not indicate a homocysteine concentration raising effect of this biochemical complex in premenopausal women. The results instead suggested a favorable effect of soy products as a food group in regard to homocysteine metabolism. There is growing interest in the potential health effects of soy or soy isoflavones. It is worth focusing on this food group to study both the risks and benefits of soy isoflavones. In addition, recent studies on diet and cardiovascular disease risk factors, such as hypertension, have considered the benefits of foods instead of emphasizing single nutrients (31 ). Although soybeans and soy products are biochemically complex, information about relationships of this food group to diseases or health-related conditions would help consumers to make healthy food choices.

In the present study, the estrogen status of some women may be similar to that of postmenopausal women. Inclusion of these women may have favored the inverse correlation between soy intake and serum homocysteine concentration. However, restricting the study subjects to women who were aged 50 y old or younger and had had a menstrual cycle in the past 3 mo (n = 187) did not substantially alter the results (r = -0.14, P = 0.06 for total soy products, r = -0.15, P = 0.04 for soy protein and r = -0.15, P = 0.046 for soy isoflavone in relation to serum homocysteine concentration).

Our dietary questionnaire was designed to measure an individual’s relative intakes of foods and nutrients rather than absolute values. The intakes of folate and vitamins B-6 and B-12 may have been overestimated by the questionnaire because in the validity study, these estimates from the questionnaire were 15% (for vitamin B-12) to 26% (for folate) higher than those estimated from the 12 daily diet records over 1 y. On the other hand, the data presented for soy products may have been underestimated because soy product intake estimated from the questionnaire was 20% lower than that estimated from the 12 daily diet records. Although we estimated that 12.3% of total folate intake and 5.9% of total vitamin B-6 intake would be derived from soy products in our study subjects, these values are very likely to be underestimates.

We could not measure serum estrogen concentrations because blood samples were not drawn from the subjects on the same day of their menstrual cycle. Tallova et al. (32 ) reported a change in blood homocysteine concentration during the menstrual cycle. In the present study, adjustment for the day of blood draw in relation to the menstrual cycle did not substantially alter the results (r = -0.13, P = 0.08 for total soy products, r = -0.14, P = 0.046 for soy protein and r = -0.14, P = 0.06 for soy isoflavones in relation to serum homocysteine concentration). To our knowledge, none of the previous studies on lifestyle and homocysteine concentration in premenopausal women have included the measurements of serum estrogens. Interrelationships among dietary soy and endogenous estrogen and homocysteine concentrations should be elucidated in future studies.


   FOOTNOTES
 
1 Supported in part by grant from the Ministry of Education, Science, Sports and Culture of Japan. Back

Manuscript received 28 September 2002. Initial review completed 25 October 2002. Revision accepted 21 November 2002.


   LITERATURE CITED
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 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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