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Department of Family and Preventive Medicine, University of California, San Diego, CA
2To whom correspondence should be addressed. E-mail: dgoodman{at}ucsd.edu.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • cardiovascular risk factors • isoflavones • lipids • lipoproteins • soy • humans
|
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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2
3
4
5)
. Many postmenopausal women, however,
either cannot or will not comply with HRT regimens
(6
7
8
9
10)
.
Isoflavones, a group of biologically active compounds found in soybeans
and other legumes, bind to estrogen receptor sites and have weak
estrogenic effects (11
12
13)
. Clinical trials have shown
that soy supplementation is associated with a reduction in lipids and
lipoproteins in hypercholesterolemic (14
15
16
17)
and
nonhypercholesterolemic subjects (16)
, a reduction in
systolic and diastolic blood pressure (18)
, and an
improvement in biomarkers of lipid peroxidation (19)
and
vascular reactivity (20)
. On the basis of these studies,
scientific and lay literature have touted the benefits of isoflavones
and soy consumption. Few previous studies, however, have examined the
effects of usual, unsupplemented dietary isoflavone consumption on
heart disease risk factors. To our knowledge, only one
cross-sectional study in Japanese men and women has examined the
effect of typical, unsupplemented dietary soy intake on total serum
cholesterol level (21)
; no previous studies have examined
the effects on other heart disease risk factors.
The purpose of this study was to describe the variations in pattern of daily dietary isoflavone intake by ethnicity and other behavioral and demographic characteristics. We also examined the cross-sectional association between usual dietary isoflavone intake and CVD risk factors including lipids and lipoproteins, body mass index (BMI), blood pressure and glucose metabolism in a sample of 208 postmenopausal, Southern Californian women.
|
SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3 mo, and not currently using
lipid-lowering drugs, antidiabetic medications, tamoxifen, or soy
protein or herbal supplements. Women with a history of uncontrolled
hypertension, stroke or transient ischemic attack, cancer diagnosed <5
y ago, or myocardial infarction within 6 mo were excluded from the
study. A total of 210 postmenopausal women were enrolled in the SHE
study. This study was approved by the University of California, San
Diego Institutional Review Board.
At the screening visit, women responded to a standardized
questionnaire, which ascertained information about demographic
characteristics including age, ethnicity and educational level. Women
were also queried about their cigarette smoking history, frequency of
alcohol use and physical activity (exercise 3 times per week or more),
gynecologic history, including age at menopause, and the use of
selected medications. Medication use was validated by examination of
prescriptions or pills brought to the clinic for that purpose. Blood
samples for lipid and lipoprotein levels were obtained by venipuncture
after a requested 12-h fast. Lipids were measured in a Centers for
Disease Control-standardized Lipid Research Clinic laboratory.
Plasma total cholesterol and triglyceride levels were measured using
enzymatic techniques, and HDL cholesterol was measured by precipitating
the other lipoproteins with heparin and manganese chloride according to
the standardized procedures of the LRC Manual (22)
. LDL
cholesterol was calculated using the Friedwald formula
(23)
.
The baseline visit occurred 
1 mo after the screening visit. Diet was
assessed using the self-administered and validated Block
Food-Frequency Questionnaire (24
,25)
. The Block
Food-Frequency Questionnaire asks participants to report usual
frequency of consumption during the past year for a list of foods.
Included in this list are tofu, bean curd and meat substitutes made
from soy. In addition, participants were asked about the amount and
frequency of consumption of five common foods containing isoflavones,
specifically, miso soup, soy milk or other soy beverages, green tea,
bean sprouts and soy sauce in cooking or added at the table. Dietary
questionnaires were scored by Block Dietary Systems; soy database
values were obtained from a compendium of literature values
(26)
. Height and weight were measured with subjects
wearing light-weight clothing and no shoes; BMI (calculated as
kg/m2) was used as an estimate of obesity. Waist
and hip girths were measured in centimeters over single-thickness
clothing with the participant standing. Waist was measured both at the
bending point (point marked when participant naturally bends forward
and measured after participant has realigned to an upright position)
and at the narrowest circumference. Hip circumference was measured both
at the iliac crest and at the largest circumference. Both waist and hip
measures were highly correlated (r > 0.90;
P < 0.001) and the former in each instance was used to
calculate waist-to-hip ratio. Blood pressure was measured twice using
the Hypertension Detection and Follow-up Program protocol
(27)
with a mercury sphygmomanometer after the participant
had been seated quietly for at least 5 min. An average of the two blood
pressure measurements was used in the analyses. A 75-g oral glucose
tolerance test was administered between 0830 and 1100 h after a
requested 12-h fast. Plasma glucose and insulin levels were measured by
a glucose oxidase assay (2300 STAT PLUS) and human insulin-specific
RIA (28)
, respectively, before and 2 h after the
glucose load.
There were 209 women who completed the baseline diet questionnaire and had lipid and lipoprotein levels, blood pressure, glucose, insulin, and anthropometric data available from the baseline visit for analysis. After exclusion of one woman who reported isoflavone intake >4 SD above the mean, there were 208 women who form the focus of this report.
Data were analyzed using SAS and SAS/STAT (29)
. Because
risk factors, including total cholesterol (C), HDL-C, LDL-C,
triglycerides, and fasting and 2-h postchallenge glucose and insulin
showed a slightly skewed distribution, analyses were performed using
log-transformed data. To aid in the interpretation of results,
untransformed data are presented; however, all P-values are
based on log-transformed data. ANOVA for continuous variables and
2 tests for categorical variables were used to
test for significant differences in demographic and behavioral
characteristics by category of genistein intake. Analysis of covariance
was used to adjust mean risk factor levels by BMI and compare adjusted
means by daily genistein consumption. Linear trends across tertiles of
genistein were tested using linear contrasts in analysis of covariance
models. Multiple regression analysis was used to assess the independent
association between daily genistein intake (as a continuous variable)
and CVD risk factors while controlling for major covariates (age, BMI,
ethnicity, total energy intake/d, total dietary fat intake/d, total
dietary fiber intake/d and total dietary protein intake/d). ß
represents the change in risk factor for every 100 µg/d
dietary intake of genistein, daidzein or isoflavones. All analyses were
repeated using daidzein consumption and combining genistein and
daidzein to approximate total isoflavone intake. All
P-values are two-tailed. Statistical significance was
defined as P < 0.05. Values are means ± SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Consumption of genistein ranged from none to 13.9 mg/d with an average
of 1.3 ± 2.4 mg/d. Table 1
shows the distribution of demographic and behavioral characteristics by
categorical daily genistein intake. As shown, there were no significant
differences in age, years postmenopausal, education level, smoking,
alcohol intake, total energy intake, total dietary fiber, protein,
total fat or saturated fat intake, or exercise by level of daily
genistein consumption (P > 0.05); however, Asian women
were significantly most likely to report genistein consumption >1.0
mg/d.
|
. Mean BMI and waist circumference were significantly smaller in the
group with highest daily genistein consumption compared with those that
did not consume genistein (P < 0.05). Women who
reported moderate genistein intake tended to have lower systolic blood
pressure than women who did not consume genistein-containing foods
(P < 0.10). In addition, women with moderate and high
genistein consumption had significantly improved HDL-C
(P 
0.05) and fasting insulin levels (P
0.05 and P < 0.10, respectively) compared with
those who did not consume genistein (P-trend = 0.06 and
0.07 for HDL-C and insulin, respectively). No other significant
differences by genistein intake were seen for the other measured CVD
risk factors, including diastolic blood pressure, total cholesterol,
triglycerides, fasting and 2-h glucose, or 2-h insulin. Repeating the
analyses and substituting daidzein or total isoflavones (approximated
by addition of genistein and daidzein) did not change these findings.
Repeat analysis after excluding the 12 women of Asian or Pacific
Islander ethnicity did not alter these results.
|
. Genistein, daidzein and total isoflavone intake were significantly and
positively associated with HDL-C level (P = 0.05,
0.008, and 0.03, respectively) and inversely associated with 2-h
insulin concentration (P = 0.04, 0.05, and 0.05,
respectively). Associations of borderline significance were also found
between fasting insulin level and genistein (P = 0.09)
and total isoflavones (P = 0.10). Results were not
affected by substitution of waist circumference for BMI or additional
adjustment for total daily protein, fiber, or fat intake. Repeating
analysis but dichotomizing by total cholesterol level into > or
< 6.5 mmol/L yielded similar associations.
|
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Although the dietary isoflavone-body composition and dietary
isoflavone-insulin relationships have not been evaluated
previously, clinical trial data have reported a reduced insulin
response to oral glucose challenge in hyperlipidemic patients given a
soy protein supplement (30)
. In addition, sex
hormone–binding globulin level, which increases with soy consumption
in postmenopausal women (31
,32)
, is inversely associated
with total body fat (33)
, impaired glucose tolerance and
type II diabetes (34)
.
Only one previous study evaluated the association between usual dietary
soy intake and total cholesterol levels (21)
. In contrast
to the present study which found no effect, Nagata et al.
(21)
observed an inverse association between daily dietary
soy intake and total serum cholesterol in a population-based sample
of Japanese men and women. These contradictory results may be due to
differences in mean dietary isoflavone intake between the two
populations or the lack of adjustment for replacement estrogen use in
the study of Nagata et al.
To our knowledge, the present study is the first to evaluate the
relation between usual dietary isoflavone intake and
lipoproteins. Although previous intervention trials in subjects with
hypercholesterolemia have also shown significant decreases in total
cholesterol and LDL-C levels and significant increases in HDL-C
level with soy protein supplementation (14
15
16)
, studies
in subjects with normal cholesterol levels have had conflicting results
(18
,35
36
37
38)
. In this study, stratification by total
cholesterol level (6.5 mmol/L vs. >6.5 mmol/L) did not alter the
results. However, <16% of this population had total cholesterol
levels >6.5 mmol/L.
This study has a number of limitations. The Block Food-Frequency
Questionnaire assesses the major sources of isoflavones as well as
other sources such as meat substitutes made from soy and processed
foods; these include hot dogs, bologna and other lunch meats that may
contain soy. This study added five soy products to the original,
validated diet questionnaire. Therefore, it is unlikely that any
important source of isoflavones was missed. However, measurement error
associated with nutrient estimates from the food-frequency
questionnaire could occur. It has been reported that measurement errors
from dietary food-frequency questionnaires are typically
underestimates of risk (39)
. Therefore, any true
association would be stronger than that reported. Second, because this
study recruited volunteers interested in joining a dietary soy
supplementation study, selection bias may exist. However, mean
cholesterol levels in age-stratified analyses (45–55 y, 5.5
mmol/L; 55–64 y, 5.7 mmol/L) were similar to those from another
published cohort (40)
. Last, it is possible that
additional as yet unidentified factors that covary with isoflavone
exposure, or a component of soy other than genistein or daidzein may be
the active compound(s) responsible for the observed increase in
HDL-C and decrease in insulin levels. Although genistein and
daidzein represent the major phytochemicals found in soy products,
other components found in soy, such as saponins, have also been
reported to decrease cholesterol (11)
.
Usual isoflavone consumption was relatively low in this study. Subjects were screened to ensure they were not supplementing themselves with high doses of isoflavones, especially within the month before their screening visit. The fact that associations were observed even with this relatively low level of isoflavone consumption suggests that the effects of isoflavone supplement use on body fat and insulin may be much greater than those observed here.
In sum, results of this study suggest a protective cardiovascular effect of usual, unsupplemented, dietary isoflavone intake on obesity, HDL cholesterol, and fasting and postchallenge insulin in postmenopausal women. Additional studies are warranted to further evaluate the cardioprotective mechanisms of isoflavone action via changes in lipids, body fat and insulin.
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FOOTNOTES |
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3 Abbreviations used: BMI, body mass index; C, cholesterol; CVD, cardiovascular disease; HRT, hormone replacement therapy; SHE, Soy Health Effects Study.
Manuscript received October 18, 2000. Initial review completed November 22, 2000. Revision accepted January 8, 2001.
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Y. T. van der Schouw, L. Sampson, W. C. Willett, and E. B. Rimm The Usual Intake of Lignans but Not That of Isoflavones May Be Related to Cardiovascular Risk Factors in U.S. Men J. Nutr., February 1, 2005; 135(2): 260 - 266. [Abstract] [Full Text] [PDF]
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S. Kim, I. Sohn, Y. S. Lee, and Y. S. Lee Hepatic Gene Expression Profiles Are Altered by Genistein Supplementation in Mice with Diet-Induced Obesity J. Nutr., January 1, 2005; 135(1): 33 - 41. [Abstract] [Full Text] [PDF]
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M. S Rosell, P. N Appleby, E. A Spencer, and T. J Key Soy intake and blood cholesterol concentrations: a cross-sectional study of 1033 pre- and postmenopausal women in the Oxford arm of the European Prospective Investigation into Cancer and Nutrition Am. J. Clinical Nutrition, November 1, 2004; 80(5): 1391 - 1396. [Abstract] [Full Text] [PDF]
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E. Nikander, A. Tiitinen, K. Laitinen, M. Tikkanen, and O. Ylikorkala Effects of Isolated Isoflavonoids on Lipids, Lipoproteins, Insulin Sensitivity, and Ghrelin in Postmenopausal Women J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3567 - 3572. [Abstract] [Full Text] [PDF]
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 J. Tuomilehto, G. Hu, S. Bidel, J. Lindstrom, and P. Jousilahti Coffee Consumption and Risk of Type 2 Diabetes Mellitus Among Middle-aged Finnish Men and Women JAMA, March 10, 2004; 291(10): 1213 - 1219. [Abstract] [Full Text] [PDF]
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X. Zhang, X. O. Shu, Y.-T. Gao, G. Yang, Q. Li, H. Li, F. Jin, and W. Zheng Soy Food Consumption Is Associated with Lower Risk of Coronary Heart Disease in Chinese Women J. Nutr., September 1, 2003; 133(9): 2874 - 2878. [Abstract] [Full Text] [PDF]
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 A. Naaz, S. Yellayi, M. A. Zakroczymski, D. Bunick, D. R. Doerge, D. B. Lubahn, W. G. Helferich, and P. S. Cooke The Soy Isoflavone Genistein Decreases Adipose Deposition in Mice Endocrinology, August 1, 2003; 144(8): 3315 - 3320. [Abstract] [Full Text] [PDF]
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S. C. Blum, S. N. Heaton, B. M. Bowman, M. Hegsted, and S. C. Miller Dietary Soy Protein Maintains Some Indices of Bone Mineral Density and Bone Formation in Aged Ovariectomized Rats J. Nutr., May 1, 2003; 133(5): 1244 - 1249. [Abstract] [Full Text] [PDF]
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C. L Frankenfeld, R. E Patterson, N. K Horner, M. L Neuhouser, H. E Skor, T. F Kalhorn, W. N Howald, and J. W Lampe Validation of a soy food-frequency questionnaire and evaluation of correlates of plasma isoflavone concentrations in postmenopausal women Am. J. Clinical Nutrition, March 1, 2003; 77(3): 674 - 680. [Abstract] [Full Text] [PDF]
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S. J Bhathena and M. T Velasquez Beneficial role of dietary phytoestrogens in obesity and diabetes Am. J. Clinical Nutrition, December 1, 2002; 76(6): 1191 - 1201. [Abstract] [Full Text] [PDF]
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 V. Jayagopal, P. Albertazzi, E. S. Kilpatrick, E. M. Howarth, P. E. Jennings, D. A. Hepburn, and S. L. Atkin Beneficial Effects of Soy Phytoestrogen Intake in Postmenopausal Women With Type 2 Diabetes Diabetes Care, October 1, 2002; 25(10): 1709 - 1714. [Abstract] [Full Text] [PDF]
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 M. S. Anthony Phytoestrogens and Cardiovascular Disease: Where's the Meat? Arterioscler Thromb Vasc Biol, August 1, 2002; 22(8): 1245 - 1247. [Full Text] [PDF]
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Y. T. van der Schouw, A. Pijpe, C. E.I. Lebrun, M. L. Bots, P. H.M. Peeters, W. A. van Staveren, S. W.J. Lamberts, and D. E. Grobbee Higher Usual Dietary Intake of Phytoestrogens Is Associated With Lower Aortic Stiffness in Postmenopausal Women Arterioscler Thromb Vasc Biol, August 1, 2002; 22(8): 1316 - 1322. [Abstract] [Full Text] [PDF]
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S. Lyou, E. Hirano, K. Tujioka, Y. Mawatari, K. Hayase, S. Okuyama, and H. Yokogoshi Dietary Genistein Affects Brain Protein Synthesis Rates in Ovariectomized Female Rats J. Nutr., July 1, 2002; 132(7): 2055 - 2058. [Abstract] [Full Text] [PDF]
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E. Rohrdanz, S. Ohler, Q.-H. Tran-Thi, and R. Kahl The Phytoestrogen Daidzein Affects the Antioxidant Enzyme System of Rat Hepatoma H4IIE Cells J. Nutr., March 1, 2002; 132(3): 370 - 375. [Abstract] [Full Text] [PDF]
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