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Original Research Communication |
1 From the Clinical Nutrition and Risk Factor Modification Center (DJAJ, CWCK, TP, DF, and EV) and the Division of Endocrinology and Metabolism, Department of Medicine (PWC, LAL, and RGJ), St Michael’s Hospital, Toronto; the Departments of Nutritional Sciences (DJAJ, CWCK, EV, SCC, LAT, and RGJ), Biochemistry (PWC), and Laboratory Medicine and Pathobiology (PWC), Faculty of Medicine, University of Toronto; and the Laboratory Services Division, University of Guelph, Canada (C-JCJ).
2 Supported by the Natural Sciences and Engineering Research Council of Canada (Ottawa) and Loblaw Brands Ltd (Toronto). Loblaw Brands Ltd, Yves Veggie Cuisine Inc (Vancouver, Canada), Protein Technologies International (St Louis), Sanitarium Pt, Sydney, Australia), Soy City Foods (Toronto), La Soyarie (Hull, Quebec), First Line Seeds (Guelph, Canada), and Advantage Seed Growers and Processors (Lucknow, Canada) generously developed and donated the soyfoods, soy-protein isolates, and high- and low-isoflavone soybeans used in the study. DJAJ is a Canada Research Chair in Nutrition and Metabolism funded by the federal government of Canada.
3 Address reprint requests to DJA Jenkins, Clinical Nutrition and Risk Factor Modification Center, St Michael’s Hospital, 61 Queen Street East, Toronto, Ontario M5C 2T2, Canada. E-mail: cyril.kendall{at}utoronto.ca.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The objective was to determine the effects of high- and low-isoflavone soy-protein foods on both lipid and nonlipid risk factors for coronary artery disease (CAD).
Methods: Forty-one hyperlipidemic men and postmenopausal women participated in a study with three 1-mo diets: a low-fat dairy food control diet and high- (50 g soy protein and 73 mg isoflavones daily) and low- (52 g soy protein and 10 mg isoflavones daily) isoflavone soyfood diets. All 3 diets were very low in saturated fat (< 5% of energy) and cholesterol (< 50 mg/d). Fasting blood samples were drawn and blood pressure was measured at the start and end of each diet.
Results: No significant differences were seen between the high- and low-isoflavone soy diets. Compared with the control diet, however, both soy diets resulted in significantly lower total cholesterol, estimated CAD risk, and ratios of total to HDL cholesterol, LDL to HDL cholesterol, and apolipoprotein B to A-I. No significant sex differences were observed, except for systolic blood pressure, which in men was significantly lower after the soy diets than after the control diet. On the basis of blood lipid and blood pressure changes, the calculated CAD risk was significantly lower with the soy diets, by 10.1 ± 2.7%.
Conclusion: Substitution of soyfoods for animal products, regardless of isoflavone concentration, reduces the CAD risk because of both modest reductions in blood lipids and reductions in oxidized LDL, homocysteine, and blood pressure.
Key Words: Soy protein • isoflavones • diet • cardiovascular disease risk • blood lipids • oxidized LDL • homocysteine • blood pressure
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mammalian estrogens are also thought to confer a range of cardiovascular benefits, including favorable effects on the blood lipid profile (23), improved antioxidant status (24), improved vascular reactivity (25), and possibly lower blood pressure (26). Most recently, elevated homocysteine concentrations, unrelated to significant changes in vitamin status, were reported in postmenopausal women (27), suggesting that estrogens may play a role in homocysteine metabolism.
We therefore assessed the effect of feeding soyfoods either high or low in isoflavones, as weak plant-derived estrogenic compounds (14), on a range of cardiovascular risk factors in hyperlipidemic men and postmenopausal women. Our research has focused on feeding soyfoods that are available in the supermarket and health food store (18,28,29). Our present study involved a range of different types of soy products made from tofu and soy-protein isolate that were consumed as part of the diet, not as an experimental beverage containing soy-protein isolate to be taken as a supplement, as was the case in many other studies. Furthermore, the soyfoods we used were components of diets that were very low in saturated fat.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Subjects
Healthy hyperlipidemic men (n = 37) and postmenopausal women (n = 36) were recruited by newspaper advertisement and from patients attending the Risk Factor Modification Center, St Michael’s Hospital (Toronto). Eighteen subjects withdrew either before or after randomization but before starting the first phase, and 14 withdrew during or after completing 1–2 study phases. Five subjects quit for reasons directly related to the study: dislike of dairy foods (n = 1), dislike of soyfoods (n = 1), tired of eating soy (n = 1), belief that the soy flavoring caused bladder irritation (n = 1), and constipation (n = 1). Of the subjects that withdrew, most (n = 9) did so for reasons unrelated to the study: work-related reasons (n = 4), personal or family-health reasons (n = 4), and loss of interest (n = 1). Forty-one subjects (23 men and 18 women) completed all 3 phases of the study. The subjects had a mean (± SE) age of 62 ± 2 y and a body mass index (in kg/m2) of 25.3 ± 0.5. All subjects had elevated LDL-cholesterol concentrations (> 4.1 mmol/L) on initial assessment. Before the start of the study, 8 subjects had elevated triacylglycerol concentrations (> 2.3 mmol/L; range: 2.76–4.77 mmol/L). None of the subjects had clinical or biochemical evidence of diabetes or liver or renal disease, and none were taking hypolipidemic agents. Five women were receiving hormone replacement therapy and 3 were taking levothyroxine. Five men were taking 1 or 2 of the following medications: ß-blocking agents (n = 2), angiotensin-converting-enzyme (EC 3.4.15.1) inhibitors (n = 1), an angiotensin II receptor blocker with a calcium channel blocker (n = 1), and a calcium channel blocker alone (n = 1). Four women were taking these drugs: an angiotensin II receptor blocker (n = 1), a calcium channel blocker (n = 2), and a calcium channel blocker with an angiotensin-converting-enzyme inhibitor (n = 1). The dosages of all medications were held constant throughout the study. Subjects were also asked to maintain their habitual level of physical activity throughout all 3 study phases. The study was approved by the Ethics Committee of the University of Toronto and St Michael’s Hospital, and informed consent was obtained from all subjects.
Diets
During the study phases, the subjects consumed self-selected National Cholesterol Education Program Step II diets in which the main protein-containing foods [meats, fish, dairy foods, eggs, nuts (eg, peanut butter), and legumes] were replaced during the control phase with low-fat dairy products: skim milk, yogurt, cottage cheese, very low-fat Hoop cheese (Western Creamery, Toronto), cheese made with skim milk (NutriSpring Farms, Dundas, Canada), and egg substitute (Egg Beaters; Lipton’s, Toronto). During the high- and low-isoflavone soy phases, the main protein-containing foods were replaced with low-fat soymilk (0.1% fat; Sanitarium Pt, Sydney, Australia); soy hot dogs, breakfast links, soy burgers, and cold cuts (Yves Veggie Cuisine, Vancouver, Canada); tofu nuggets (Soy City Foods, Toronto); and tofu burgers (La Soyarie, Hull, Canada). These products were made from either alcohol-washed or nonalcohol-washed soy-protein isolate (Protein Technologies International, St Louis) or from tofu that was made from soybeans selected for their very high or very low isoflavone content (First Line Seeds, Guelph, Canada; Advantage Seed Growers and Processors, Lucknow, Canada). The nutrient profiles of the dairy and soyfood substitutes were balanced for fatty acid composition and dietary cholesterol intake by adding butter (group mean: 11 g/wk) and one egg (53 g/wk) per 8.4-MJ (2000-kcal) soy diet. For the control diet, fatty acid balance was achieved with the use of an 8-g/d oil mixture providing 0.3 g soy oil/d, 1.9 g safflower oil/d, 4.0 g corn oil/d, and 1.7 g canola oil/d. The foods provided were designed to represent 20% of the subjects’ estimated daily total energy intake (31) and contributed 
13.5% of energy as protein, expressed as a percentage of the daily recorded energy intake (Table 1
). Analyses of isoflavones as aglycones in the soyfoods indicated that the mean daily intake of isoflavones for the 41 subjects was 10 ± 0 mg/d during the low-isoflavone soy phase and 73 ± 3 mg/d during the high-isoflavone soy phase.
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Compliance was assessed on the basis of the 7-d diet histories, the completed weekly checklists of foods eaten, and the amount of uneaten food returned at the clinic visits, which were weighed and recorded. Every effort was made to ensure that subjects maintained their body weights throughout the study; appropriate advice was given as necessary at each clinic visit.
Measurements
Fasting body weight, blood samples, and blood pressure measurements were obtained at the start and end of each 4-wk diet phase. The subjects were asked to fast overnight for 12–14 h. Blood pressure was taken, after the subjects sat for 15–20 min, from the nondominant arm by the same 3 observers throughout the study with the use of a standard 52 cm x 14 cm cuff. Twenty-four–hour urine samples were collected during the last week of each phase. Urine samples were collected into 4-L plastic containers that contained no preservatives and were returned to the laboratory by courier on the morning of completion to be measured, portioned, and stored at -70 °C until analyzed.
Seven-day weighed diet histories were recorded before each phase and during week 4 of each phase and were checked by a dietitian to ensure accuracy.
The palatability of the foods provided was assessed at the conclusion of the study by asking subjects to rate the foods on a semantic scale of 0–10, where 0 was very distasteful, 5 was neutral, and 10 was very appetizing.
Analyses
Serum, stored at –70°C, was analyzed according to the Lipid Research Clinics protocol (32) for total cholesterol, triacylglycerol, and HDL cholesterol after dextran sulfate–magnesium chloride precipitation (33). All samples from a given subject were analyzed in the same batch. LDL cholesterol was calculated with the use of the Friedewald equation (34). Serum apolipoprotein A-I and B were measured by nephelometry (35), and lipoprotein(a) was measured with a commercial enzyme-linked immunosorbent assay (Macra Lp(a) Kit; Trinity Biotech USA, Jamestown, NY).
Total L-homocysteine was measured in citrated plasma, stored at –70 °C, that had been refrigerated at 4 °C for 1.5 h before separation with the use of fluorescence polarization immunoassay (IMx homocysteine assay; Axis-Shield, Oslo).
Oxidized LDL was measured in serum stored at –70 °C as conjugated dienes in the LDL fraction after isolation of LDL particles by precipitation with buffered heparin at their isoelectric point (36). The results were expressed as total serum conjugated dienes in the LDL fraction (37).
Dietary isoflavone concentrations were measured as 3 aglycones (genistein, daidzein, and glycitein) in foods, which had been freeze-dried. After acid hydrolysis of the endogenous isoflavones, aglycones in alcoholic extracts were identified and quantitated by HPLC (38,39) with the use of a 600E multisolvent delivery system with a photodiode array detector monitoring at 200–350 nm (Waters, Marlborough, MA) and with a Nova Pak C18 column (5 µm, 150 mm x 3.9 mm internal diameter; Waters) equipped with a C18 guard column. Appropriate isoflavone standards were analyzed. Biochanin A was used as an internal standard, with recovery values ranging from 80% to 100%. Urinary metabolites of isoflavones (genistein, daidzein, glycitein, equol, and o-desmethylangolensin) were measured by HPLC after enzymatic hydrolysis in the first group of subjects to complete the study (n = 24) (39). Chromatographs were obtained from the 3-dimensional array by using a photodiode array detector at 258 nm to allow assessment of common regions of relatively high absorbance for daidzein, genistein, and flavone—the added recovery standard.
Freeze-dried soy and dairy foods were analyzed in the laboratory by using methods of the Association of Official Analytical Chemists for fat and protein (40) and fiber (41) with available carbohydrate calculated as the difference between the sample weight and the weight of moisture, ash, fiber, fat, and protein. The fatty acid composition was determined by gas chromatography (42). Diet histories were assessed by using a computer program based on US Department of Agriculture data (43), data from food labels, and data from the results of foods analyzed in the laboratory. The percentages of soluble and insoluble fiber were derived from published data (44).
Statistical analysis
The results are expressed as means ± SEs. The isoflavone effect was assessed by comparing the 3 treatments with the use of analysis of covariance with a Tukey adjustment to determine the significance of differences between treatments (45). The statistical model included week 4 values as the response variable, treatment and sequence as the main effects, treatment x sex as the interaction term, a random subject effect nested within sex by sequence, and baseline as a covariate. For the urinary excretion data, because pretreatment samples were not collected, analysis of variance was used with week 4 values as the response variable, treatment and sequence as the main effects, and a subject effect nested within sex by sequence. Sex was not included because none of the women whose urine was analyzed took high-isoflavone soy in the first phase followed by low-isoflavone soy in the second phase. It was therefore not possible to use both sex and sequence in the same model. Nevertheless, similar results were obtained when the sex x diet interaction term was substituted for sequence in the model. To assess the effect of soy protein, the high- and low-isoflavone data were combined, because the 2 soy treatments produced similar results, and compared with the control data by using the CONTRAST test in SAS (45). Weights of -0.5 were assigned to each of the combined soy treatments and weights of 1.0 to the single control treatment. Student’s t test for paired data (two tailed) was used to assess the significance of the percentage changes from baseline to week 4 for individual treatments. CAD risk was calculated by using the ratio of total to HDL cholesterol and systolic blood pressure in the Framingham cardiovascular disease risk assessment equation (46). SAS version 8 software was used for all statistical analyses (45).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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).
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). No significant differences in blood lipid responses were seen between the low- and high-isoflavone soy phases, but both were lower than values during the control phase for total cholesterol (P = 0.016 and P = 0.045, respectively), total:HDL cholesterol (P = 0.001 and P = 0.018), LDL:HDL cholesterol (P = 0.001 and P = 0.004), apolipoprotein B:A-I (P = 0.010 and P = 0.002), and estimated CAD risk (P < 0.001 and P = 0.033) (Table 2
). In addition, LDL cholesterol (P = 0.024) and apolipoprotein B (P = 0.020) were also lower during the high-isoflavone soy phase than during the control phase. LDL cholesterol and apolipoprotein B were also lower during the low-isoflavone soy phase than during the control phase, but not significantly so (P = 0.077 and P = 0.076, respectively).
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Because of the lack of significant differences in results between the high- and low-isoflavone soy phases and to assess the effect of soy protein, the combined results for the high- and low-isoflavone soy phases were compared directly with the control data by using the CONTRAST test (Table 2). LDL cholesterol (P = 0.006), apolipoprotein B (P = 0.005), homocysteine (P = 0.044), and oxidized LDL (P = 0.030) assessed as conjugated dienes in the LDL fraction in the whole group and systolic blood pressure in the men only (P = 0.002) were lower during the soy phases than during the control phase. In addition, the reductions in total cholesterol (P = 0.003), in the lipid and lipoprotein ratios (P < 0.001), and in the estimated CAD risk (P < 0.001) were in line with what was reported above for the comparisons between the 3 phases individually. The percentage change in conjugated dienes from baseline in men and women during each phase is shown in Figure 2.
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. Total urinary isoflavone outputs during the control and low- and high-isoflavone soy phases were 2.1 ± 0.7, 11.3 ± 3.1, and 41.3 ± 4.8 mg/d, respectively. The urinary isoflavone output was significantly greater during the high-isoflavone soy phase than during the other 2 phases (P < 0.001), which were not significantly different from each other.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Many studies have assessed the effects of high- and low-isoflavone intakes either as soy supplements or as isoflavone extracts (5,6,8,10,19). In general, when the effects of increased isoflavone intakes on blood lipids have been seen in humans, the isoflavones have been associated with soy proteins (5,6,8,10). Lipid-lowering effects have generally not been seen in humans fed isoflavones separated from the soy protein by extraction (19), but other benefits have been shown, including increased vascular compliance of benefit to CAD risk reduction (19). Furthermore, some studies have noted altered endocrine activity with soy feeding (47), whereas other have not (48). Our own study failed to show a benefit of high- compared with low-isoflavone intakes, and it is possible that either a larger number of subjects or a higher soy isoflavone intake would be required to show such differences (8,10). However, our studies indicated that even low-isoflavone soy-protein foods may have the additional benefits reported for soy, including antioxidant activity (15), lower homocysteine concentrations (22), and blood pressure reduction (20).
Our studies were different from many studies reported in the literature in that we used a wide range of soyfoods to substitute for the sources of animal protein normally eaten in the diet. The proportion of vegetable to animal protein in the soy diets was relatively high, 96% of the total protein consumed. This aspect of the diet may be relevant in considering suggestions that the nature of the protein and the amino acid composition of the diet are important for cholesterol lowering and possibly other effects (2,12,13). Furthermore, the wide range of soyfoods used, with some made from tofu and the remainder made from soy-protein isolate, supports the generalization that soyfoods are effective regardless of the starting material (11). Very low saturated fat intakes were used because a reduction in dietary saturated fat remains a primary objective of a cholesterol-lowering diet. It was therefore important to show that soy had an effect in improving the blood lipid profile even after dietary saturated fat intakes were reduced maximally. Others have noted greater reductions in LDL cholesterol but the saturated fat intakes in the diets they used were higher (4–8,10).
We conclude that soy-protein foods, regardless of their isoflavone content, may improve many lipid and nonlipid risk factors for CAD and thus justify the use of soyfoods as part of a dietary strategy to reduce CAD risk. Further studies are required to determine whether all these benefits can be achieved by taking soy as a supplement or whether it is better to substitute soy for animal-protein foods, ie, Is there an optimal ratio of vegetable to animal proteins to maximize the soy effect (1)? Certainly the displacement of saturated fat and cholesterol in the diet with soyfoods may result in the extra dietary advantage of cholesterol lowering, as has been suggested for dietary fiber (49).
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ACKNOWLEDGMENTS |
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REFERENCES |
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), low-isoflavone soy (
), and high-isoflavone soy (
) groups. *,**Significantly different from the control group: *P < 0.05, **P < 0.01. n = 41.
