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ORIGINAL RESEARCH COMMUNICATION |
1 From the Department of Community and Family Medicine and The School of Public Health, The Chinese University of Hong Kong, Shatin, Hong Kong (SZ and SCH), and the School of Public Health, Peking University, Beijing (SZ)
2 Supported by the Centre of Research and Promotion of Women's Health. 3 Address reprint requests to SC Ho, Department of Community and Family Medicine and The School of Public Health, The Chinese University of Hong Kong, 4th Floor, School of Public Health, Prince of Wales Hospital, Shatin, NT, Hong Kong. E-mail: suzanneho{at}cuhk.edu.hk.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Objective: We conducted a meta-analysis to identify and quantify the effects of soy protein containing isoflavones on the lipid profile.
Design: Twenty-three eligible randomized controlled trials published from 1995 to 2002 were identified from the PUBMED database (National Library of Medicine, Bethesda, MD). Weighted mean effect sizes were calculated for net changes in serum lipid concentrations by using fixed-effect or random-effect models. Pre-specified subgroup analyses were performed to explore the influence of covariates on net lipid change.
Results: Soy protein with isoflavones intact was associated with significant decreases in serum total cholesterol (by 0.22 mmol/L, or 3.77%), LDL cholesterol (by 0.21 mmol/L, or 5.25%), and triacylglycerols (by 0.10 mmol/L, or 7.27%) and significant increases in serum HDL cholesterol (by 0.04 mmol/L, or 3.03%). The reductions in total and LDL cholesterol were larger in men than in women. Initial total cholesterol concentrations had a powerful effect on changes in total and HDL cholesterol, especially in subjects with hypercholesterolemia. Studies with intakes >80 mg showed better effects on the lipid profile. The strongest lowering effects of soy protein containing isoflavones on total cholesterol, LDL cholesterol, and triacylglycerol occurred within the short initial period of intervention, whereas improvements in HDL cholesterol were only observed in studies of >12 wk duration. Tablets containing extracted soy isoflavones did not have a significant effect on total cholesterol reduction.
Conclusions: Soy protein containing isoflavones significantly reduced serum total cholesterol, LDL cholesterol, and triacylglycerol and significantly increased HDL cholesterol, but the changes were related to the level and duration of intake and the sex and initial serum lipid concentrations of the subjects.
Key Words: Soy protein containing isoflavones • total cholesterol • high-density-lipoprotein cholesterol • HDL cholesterol • low-density-lipoprotein cholesterol • LDL cholesterol • triacylglycerols • meta-analysis • randomized controlled trials
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Isoflavones are considered to be natural selective estrogen receptor modulators (3). Animal experiments have indicated that the serum lipid-lowering properties of soy protein are related primarily to the presence of isoflavones (4, 5). Two observational studies reported associations between habitual isoflavone intake and cardiovascular disease risk factors, including an abnormal lipid profile, in postmenopausal women in the United States (6, 7). Population-based studies in Asian populations have noted the potential beneficial effects of habitual soy protein intake on lipid profiles (8, 9). Although many clinical trials in humans have examined the effects of soy protein containing intact or depleted isoflavones on lipid profiles, most used small sample sizes and were of short-term duration. The results have not been consistent. Moreover, Greaves et al (10) were unable to achieve the plasma lipid-lowering effects of soy protein when the amount of isoflavones contained in soy protein was added to a diet containing casein and lactalbumin. A study using monkeys further contradicted the notion that isoflavones are responsible for the lipid-lowering effect of soy (11). The plasma lipid-lowering effect seen with soy containing isoflavones could not be restored by returning the whole alcohol extract or its isoflavones to isoflavone-depleted soy. However, alcohol extraction of isoflavones also degrades the protein and active peptides that may be important in cholesterol metabolism or in its interactions with isoflavones in modulating cholesterol metabolism. A recent proteomic investigation of ethanol and non-ethanol-treated soy protein products showed considerable variability in soy protein composition and isoflavone concentrations (12).
Clinical investigators have used a variety of isolated soy proteins; differing concentrations of isoflavones, trial lengths, and criteria for selecting subjects; and a variety of protocols. In the present meta-analysis, we attempted to combine the results of multiple studies with small or moderate sample sizes to increase their statistical power and enhance the precision of the estimates of the effects of soy protein containing isoflavones or isoflavone extracts on changes in lipid concentrations.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Meta-analysis
The summary results of each clinical trial and selected characteristics of the study were tabulated for analysis. The estimate of the principal effect was defined as the mean difference (net change in mmol/L) between the change in lipid concentrations among the subjects ingesting the soy protein containing isoflavones or isoflavone extracts (final value minus initial value) and that among the subjects consuming the control diet. For the computation of pooled effects, each study was assigned a weight consisting of the reciprocal of its variance. When raw data were available, the variance for each study was calculated separately by computing the SD of the differences between paired observations for the change during the diet of soy protein containing isoflavones or isoflavone extracts and the change during the control diet; the SE of the differences was then calculated. When raw data were unavailable, the variances of the difference were based on the reported SDs for each measure and on either reported correlation coefficients or reported results of paired t tests for the changes during the 2 diets.
Estimates of the average effect of soy protein containing isoflavones on lipid values and 95% CIs were calculated by using both fixed-effect and random-effect models. If the test for homogeneity was significant, we present the results of the random-effect models (36). Otherwise, estimated results based on a fixed-effect model are presented. To avoid duplication of data derived from the same subjects from studies with multiple time points, only endpoints for the longest duration were used.
The assumption of heterogeneity implied by the use of random-effects models is plausible because of differences in amounts of soy protein containing isoflavones, study durations, initial lipid concentrations, and the presence of other covariates. To explore the possible influence of those covariates on net lipid change, we further conducted a series of pre-specified subgroup analyses based on biological plausibility and the literature. Finally, to examine potential publication bias, we plotted the SEs of the studies against their corresponding effect size. REVMAN 4.1 software (Cochrane Collaboration, Oxford, United Kingdom) was applied to this meta-analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. These articles included the findings of 52 comparisons based on subgroup analysis according to participant characteristics, different concentrations and types of isoflavones contained in soy protein or as isoflavone extracts, and different lengths of intervention. Overall, 1381 subjects were included in the meta-analysis. Eleven studies focused on women, and half of these were studies of postmenopausal women (14, 15, 17–19, 25, 27, 28, 32–34). Three studies focused on men (13, 30, 35), and the remaining studies included both sexes (16, 20–24, 26, 29, 31). In 9 studies with 27 comparisons, the subjects had hypercholesterolemia at baseline (14, 18, 19, 22, 23, 26, 30, 31, 35) according to the definitions of the original study. The subjects' initial total cholesterol concentrations are listed in the table. Most studies used a parallel randomized design. Sixteen studies used isolated soy protein containing isoflavones, 3 used tablets containing extracted isoflavones (18, 21, 27), and 3 used textured soy food (13, 15, 28). Isoflavone concentrations contained in soy protein averaged 80 mg/d (median: 70.5 mg; range: 3–185 mg). The trials varied in length from 3 to 26 wk, with a median duration of 8 wk. Three trials observed the effects of soy protein containing isoflavones on lipid profiles at multiple time points (14, 17, 31). Most control groups received casein or whey. In 3 trials (13, 19, 35), the control group received meat or milk. Methods for general dietary control during the trial period were available for these studies. In most studies, the investigators attempted to provide similar amounts of total fat and saturated fat in the intervention and control diets. In 12 studies, the diets were similar to conventional Western diets in fat and cholesterol contents (these were termed "usual" diets). In 7 studies, the diets followed NCEP Step I or Step II diets with low fat (<30% of energy) and low cholesterol (<200 mg/d) contents (14, 16, 22, 27, 30, 31, 35). In the remaining 4 trials, standard or modified diets were applied to maintain weight. All the studies reported similar weight changes for subjects ingesting the intervention or the control diets.
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). Overall, soy protein containing isoflavones decreased total cholesterol by 0.22 mmol/L (95% CI: –0.29, –0.16), or by 3.77%.
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). The pooled estimate of the effects of intake of soy protein containing isoflavones on LDL cholesterol was a decrease of 0.21 mmol/L (95% CI: –0.30, –0.13), or 5.25%.
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). The pooled estimate of the effect of isoflavone intake on triacylglycerol was a decrease of 0.109 mmol/L (95% CI: –0.16, –0.05), or 7.27%.
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). The overall pooled estimate of the effect of soy protein containing isoflavones was 0.04 mmol/L for HDL cholesterol (95% CI: 0.00, 0.07), or 3.03%. These results are summarized in Table 2.
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. The results were more marked in men than in women, with net decreases of 0.26 and 0.16 mmol/L, respectively. Subjects with hypercholesterolemia had greater reductions of total cholesterol than did normal subjects. The total cholesterol concentrations of the former decreased by 0.25 mmol/L (95% CI: –0.33, –0.17) and those of the latter decreased by 0.17 mmol/L (95% CI: –0.25, –0.08). There was also a greater reduction of total cholesterol in pre- and perimenopausal women (–0.22 mmol/L; P < 0.05) than in postmenopausal women (–0.13 mmol/L; P = 0.06). Subjects consuming low-fat and low-cholesterol diets had greater reductions in total cholesterol than did subjects following a usual diet [–0.26 mmol/L (95% CI: –0.33, –0.18) and –0.16 mmol/L (95% CI: –0.24, –0.07), respectivelyrs]. Total cholesterol decreased to a larger extent in subjects with daily consumption of 
80 mg of isoflavones contained in soy protein than in those ingesting lesser amounts. In contrast, there was a negative dose-response relation between the duration of intervention and the reduction of serum cholesterol.
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, only the amount of soy protein containing isoflavones was independently associated with the change in total cholesterol. Furthermore, on the basis of quartile of initial total cholesterol concentration, no significant dose-response trend was observed in the net change of lipid profile (Table 5). There was a reduction in total cholesterol in the soy protein containing isoflavones groups compared with either the casein or the isoflavone-depleted soy protein groups. No significant difference was found between the isoflavone-depleted soy protein groups and the controls. Tablets containing extracted soy isoflavones did not show significant effects on total cholesterol reduction in 3 trials.
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–8, respectively. The reduction of LDL cholesterol was more significant in men than in women, with respective net changes of –0.30 and –0.14 mmol/L. Initial lipid concentrations did not appear to significantly influence changes in LDL cholesterol or triacylglycerol. However, soy protein containing isoflavones had a significant effect on HDL cholesterol among subjects with hypercholesterolemia (0.10 mmol/L). The beneficial effect of soy protein containing isoflavones on HDL cholesterol was also observed in postmenopausal women, particularly among those with hypercholesterolemia. Low-fat and low-cholesterol diets were useful for increasing HDL cholesterol and reducing LDL cholesterol. However, for hypercholesterolemic individuals consuming a usual Western diet, the intake of soy isoflavones alone seemed to have no significant effect on HDL cholesterol (0.03 mmol/L; P = 0.3) or triacylglycerol (–0.07 mmol/L; P = 0.4). An intake of >80 mg/d had a greater effect on lipid profiles, with a net increase of HDL cholesterol of 0.10 mmol/L and net reduction in LDL cholesterol of 0.33 mmol/L.
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Compared with casein, the intake of soy protein containing isoflavones was beneficial for improving lipid profiles. Compared with isoflavone-depleted soy protein, intake of soy protein containing isoflavones markedly decreased the LDL-cholesterol concentration, with a net change of –0.15 mmol/L (95% CI: –0.27, –0.03), but had no significant effect on HDL cholesterol or triacylglycerol. Tablets were not effective in producing a net change in serum lipid values.
Publication bias
The funnel plot of the effects on total cholesterol by SE in 51 comparisons of soy protein containing isoflavones indicated no significant publication bias (data not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The substantial heterogeneity among individual studies implies that the effects of soy protein containing isoflavones on lipid concentrations are not uniform. We found larger reductions in total cholesterol and LDL cholesterol in men than in women and larger reductions in premenopausal women than in postmenopausal women. Sex differences in lipid profiles in response to soy protein containing isoflavones have not been specifically investigated in previous studies or meta-analyses (1). These findings of sex differences concur with observational studies in populations with a wide range of soy intake. Ho et al (8) reported that in the Hong Kong Chinese population, soy intake is negatively correlated with total cholesterol and LDL cholesterol in men and young women but not in women aged 50 y. A nonsignificant association between soy intake and serum lipids is also reported in postmenopausal Japanese women (37). A recent study in Syrian F1B hybrid hamsters observed sex differences in plasma lipid responses to soy protein containing isoflavones or depleted in isoflavones (38).
Serum cholesterol values are negatively associated with estradiol (39) and increase in women who are approaching menopause or are menopausal (40, 41). van Beresteijn et al (41) noted that the cessation of ovulation was associated with a major increase of 19% in the serum total cholesterol concentration. Menopause has also been found to be associated with feedback insensitivity to estrogens (42). Therefore, the mild estrogenic effect of the present dosages of 40–80 mg isoflavones/d or from usual intake in Asian populations may be inadequate to counteract the dramatic postmenopausal increase in cholesterol. Further studies on the optimal dosages and effects of isoflavones on lipid metabolism in postmenopausal women would be required.
Initial serum cholesterol concentrations had a powerful effect on changes in lipid concentrations. As found in the previous meta-analysis by Anderson et al (1), the beneficial effects of soy on lipid profiles are more marked in subjects with hypercholesterolemia. Although lower concentrations of isoflavones contained in soy protein, on the order of 40 mg/d, still have effects on total cholesterol and LDL cholesterol, values >80 mg/d have better effects on lipid profiles. In the moderate and low-isoflavone protein products, the protein may have been degraded with extraction of the isoflavones.
The most significant lowering effects of soy protein containing isoflavones on total and non-HDL cholesterol occurred within the initial short period of isoflavone exposure. However, the extent of the lipid-lowering effect decreased as the duration of the intervention increased. The inverse relation between net changes and duration of intervention is unclear. It may imply a physiologic adaptation mechanism to more prolonged supplementation. It could also be related to "diet fatigue" and thus less attention paid to the diet or lower product adherence in prolonged periods of intervention. However, the sustained increase in HDL cholesterol is encouraging for public health, because it provides evidence that soy protein containing isoflavones at least improves the protective component of the lipid profile.
Compared with soy protein depleted in isoflavones, the isolated soy protein containing isoflavones had a significant effect on total cholesterol and LDL cholesterol, although the reduction was smaller. This finding implies that the net changes in the lipid profile could be partially attributable to the isoflavones contained in soy protein.
The 3 studies of tablets containing purified soy isoflavones in amounts ranging from 55 to 150 mg reported no significant cholesterol-lowering effects. Clarkson et al (43) speculated on 3 scenarios to explain the lack of cholesterol-lowering effects of purified isoflavone tablets. First, alcohol extraction may have removed the responsible active agent; second, the isoflavones may have been inactivated during the process of purification; and third, some enabling factor in soy protein may be required for the beneficial effects of isoflavones on lipids. Therefore, phytoestrogen-rich foods, rather than extracted soy isoflavones, should be recommended. Databases on the isoflavone content of foods have been developed (44, 45). Most soybean products, such as mature soybeans, roasted soybeans, soy flour, and textured soy protein, are excellent sources of isoflavones and provide 5.1–5.5 mg total isoflavones/g soy protein. Green soybeans (3.3 mg/g) and tempeh (3.1 mg/g) are intermediate sources of isoflavones. Tofu, isolated soy protein, and some types of soymilk provide 2 mg isoflavones/g soy protein. Examples of foods containing 
40 mg isoflavones include 456 g soymilk (2 cups), 120 g uncooked tofu, 73 g uncooked green soybeans, 20 g soy flour (1/4 cup), and 20 g roasted soybeans (46).
The mechanisms responsible for the effects of soy isoflavones on the lipid profile are still being explored (47). Isoflavones contained in intact soy protein may serve as a natural selective estrogen receptor modulator and exert an effect on lipid metabolism through their biological similarities to estrogens and estrogen-receptor-dependent gene expressions (42, 43, 48). Other possible mechanisms of soy protein containing isoflavones may include their effects on hepatic lipase activity and adipose tissue (49), although substantive evidence of these effects has yet to be produced. Resent studies have also suggested that soy protein peptide chains may up-regulate LDL receptors and induce gene expression of several enzymes and proteins important in lipid metabolism (14, 50–52). In addition, studies have reported that soy protein peptides may regulate cholesterol homeostasis in Hep G2 cells (53). Moreover, the amino acid profile may also differ from that of animal protein with consumption of a soy protein diet. As such, the hypocholesterolemic effect of soy protein is likely to be dependent on the presence of soy protein with isoflavones intact.
In summary, this meta-analysis of 23 trials indicates that the consumption of soy protein containing isoflavones is associated with significantly decreased serum total cholesterol, LDL-cholesterol, and triacylglycerol concentrations and with a significant increase in serum HDL-cholesterol concentrations. The changes in lipid concentrations were strongly related to the subjects' sex, initial serum lipid concentrations, and dietary pattern. Higher concentrations of isoflavones contained in soy protein have larger effects on lipid changes. Longer-term intake of soy protein containing isoflavones can improve HDL-cholesterol concentrations, but the effects on total cholesterol, LDL cholesterol and triacylglycerol are less consistent. Tablets containing soy-extracted isoflavones alone seem ineffective in modifying lipid concentrations.
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ACKNOWLEDGMENTS |
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SZ was responsible for the literature search, data analyses, and writing of the manuscript. SCH was responsible for formulating the research question, interpreting the data and results, and writing the manuscript.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Y. Ma, D. Chiriboga, B. C. Olendzki, R. Nicolosi, P. A. Merriam, and I. S. Ockene Effect of Soy Protein Containing Isoflavones on Blood Lipids in Moderately Hypercholesterolemic Adults: A Randomized Controlled Trial J. Am. Coll. Nutr., August 1, 2005; 24(4): 275 - 285. [Abstract] [Full Text] [PDF]
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