Background In laboratory animals, the consumption of soy protein,rather than animal protein, decreases serum cholesterol concentrations,but studies in humans have been inconclusive. In this meta-analysisof 38 controlled clinical trials, we examined the relation betweensoy protein consumption and serum lipid concentrations in humans.
Methods We used a random-effects model to quantify the averageeffects of soy protein intake on serum lipids in the studieswe examined and used hierarchical mixed-effects regression modelsto predict variation as a function of the characteristics ofthe studies.
Results In most of the studies, the intake of energy, fat, saturatedfat, and cholesterol was similar when the subjects ingestedcontrol and soy-containing diets; soy protein intake averaged47 g per day. Ingestion of soy protein was associated with thefollowing net changes in serum lipid concentrations from theconcentrations reached with the control diet: total cholesterol,a decrease of 23.2 mg per deciliter (0.60 mmol per liter; 95percent confidence interval, 13.5 to 32.9 mg per deciliter [0.35to 0.85 mmol per liter]), or 9.3 percent; low-density lipoprotein(LDL) cholesterol, a decrease of 21.7 mg per deciliter (0.56mmol per liter; 95 percent confidence interval, 11.2 to 31.7mg per deciliter [0.30 to 0.82 mmol per liter]), or 12.9 percent;and triglycerides, a decrease of 13.3 mg per deciliter (0.15mmol per liter; 95 percent confidence interval, 0.3 to 25.7mg per deciliter [0.003 to 0.29 mmol per liter]), or 10.5 percent.The changes in serum cholesterol and LDL cholesterol concentrationswere directly related to the initial serum cholesterol concentration(P<0.001). The ingestion of soy protein was associated witha nonsignificant 2.4 percent increase in serum concentrationsof high-density lipoprotein (HDL) cholesterol.
Conclusions We found that the consumption of soy protein ratherthan animal protein significantly decreased serum concentrationsof total cholesterol, LDL cholesterol, and triglycerides.
Ingestion of vegetable protein in place of animal protein appearsto be associated with a lower risk of coronary heart disease1,2;this effect may reflect decreases in serum cholesterol concentrations.3The cholesterol-lowering effects of soy protein as comparedwith animal protein have been recognized in animals for morethan 80 years.4 Carroll reviewed the evidence that soy proteinproduced less hypercholesterolemia and less atherosclerosisin laboratory animals than animal protein.5 Although many clinicalinvestigators have examined the effects of soy protein on serumlipids in humans, the results have not been consistent6; consequently,the Nutrition Committee of the American Heart Association recentlyconcluded that soy protein decreases serum cholesterol concentrationsin rabbits but not in humans.7
Clinical investigators have used a variety of soy products,differing amounts of soy protein, differing criteria for selectingsubjects, and a variety of protocols. We performed a meta-analysisof these studies, since combining the results of multiple studiesof small or moderate size increases the statistical power broughtto bear on the research question and thus greatly enhances theprecision of estimates of effect. Our analysis indicated thatthe effects of soy protein in lowering serum cholesterol concentrationswere significantly related to the initial serum cholesterolvalues. The substitution of soy protein for animal protein producedsignificant decreases in serum concentrations of total cholesterol,low-density lipoprotein (LDL) cholesterol, and triglycerideswithout significantly affecting high-density lipoprotein (HDL)cholesterol concentrations.
Methods
Identification and Selection of Studies
We searched the medical literature for studies of the effectsof soy protein on serum cholesterol concentrations in humans;37 articles containing primary reports were identified.8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44Studies were selected for analysis if they had used isolatedsoy protein or textured soy protein; if they were controlledand had either a crossover or a parallel design; and if theyprovided initial (base line) values so that changes for eachstudy group could be calculated. Studies were excluded if therewas no control group8,11,14,25,27; if they used several sourcesof vegetable protein26; if whole soybeans rather than soy proteinwere used30; or if base-line values were not provided.22 Afterthese 8 articles were excluded, 29 articles remained in theanalysis.
Subgroup Analyses
Changes in serum lipid concentrations were analyzed in relationto the initial serum lipid values, the types of soy proteinused (isolated soy protein, textured soy protein, or a combination),the amount of soy protein ingested (in grams per day), the typeof diet (usual Western diet or low-fat and low-cholesterol diet),the age group of the subjects (adults or children), and thesimilarity of the control diet and the soy-containing diet (specifically,regarding weight change in the subjects and dietary intake offat, saturated fat, and cholesterol). Study diets were consideredto be similar in terms of weight change if the subjects' changein weight during consumption of the two diets did not differsignificantly. Study diets were considered to be similar interms of the intake of total dietary fat, saturated fat, andcholesterol if the reported values for the soy-containing andcontrol diets differed by less than 10 percent. When valueswere not reported for weight change, dietary fat, or cholesterolintake, these variables were assumed not to be similar.
Meta-Analysis
Summary results of each clinical trial and selected characteristicsof the study were tabulated for analysis. The estimate of theprincipal effect was defined as the mean difference (in milligramsper deciliter) between the change in lipid concentrations whenthe subjects ingested the soy-containing diet (final value minusinitial value) and the change when they ingested the controldiet (final value minus initial value). This difference is referredto as the net change. In additional meta-analyses we used onlythe mean difference attributed to the ingestion of soy protein.For the computation of pooled effects, each study was assigneda weight consisting of the reciprocal of its variance. Whenraw data were available, the variance for each study was calculatedseparately by computing the standard deviation of the differencesbetween paired observations for the change during the soy-containingdiet and the change during the control diet; the standard errorof the differences was then calculated. When raw data were unavailable,the variances of the difference were based on the reported standarddeviations for each measure and on either reported correlationcoefficients or reported results of paired t-tests for the changesduring the two diets.
Estimates of the average effect of soy protein on lipid valuesand 95 percent confidence intervals were calculated with modelsbased on both fixed-effects and random-effects assumptions.45,46Because substantial variability between observations was indicatedby preliminary tests for homogeneity, we have presented theresults of random-effects models calculated according to themethod of DerSimonian and Laird.47 The assumption of heterogeneityimplied by the use of random-effects models is plausible becauseof the diverse clinical settings and groups of subjects analyzed.
Predictive models were also developed to examine characteristicsof the studies that were hypothesized to influence the observedtreatment effects. For this purpose, two-stage mixed regressionmodels (fixed-effects and random-effects) were used.48,49 Predictivemodels were estimated by hierarchical linear modeling.50 Thisapproach models variation among studies as a function of thecharacteristics of the study that are hypothesized to affectthe response to treatment and a two-stage random component.Both net and unadjusted effects of the substitution of soy proteinfor animal protein served as outcome variables in alternativemodels. The set of predictors used for testing hypotheses inregression models was defined at the outset and was based ona preliminary review of the literature. Several alternativecoding strategies were evaluated in preliminary analyses. Ourfinal models included the set of predictors specified abovefor subgroup analyses. To establish overall levels of variabilityin treatment effects, our regression analysis began with theestimation of unconditional random-effects regression modelswithout predictors. In a second phase, predictors were enteredinto the models in bivariate and multiple-regression analyses.The degree of reduction in variance associated with each predictorwas calculated by comparing the components of variance in unconditionalmodels with those in conditional models containing predictors.50
Results
Characteristics of the Studies
Table 1 shows selected characteristics of the studies that metthe criteria for analysis. The 29 articles chosen included thefindings of 38 clinical studies; some articles reported datafor different subgroups of subjects from one study (e.g., thosewith normal and those with high cholesterol concentrations);others reported on two different clinical studies. The 38 clinicalstudies were analyzed independently. in 4 studies the subjectswere children, whereas in 34 they were adults. Most studiesincluded both men and women, but the data necessary to analyzeeffects of soy protein according to sex were not available.Most studies used random assignment with crossover design. Twentystudies used isolated soy protein, 15 used textured soy protein,and 3 used a combination of the two. Soy protein intake averaged47 g per day (range, 17 to 124); in 14 studies (37 percent)intake was <31 g per day.
In most studies the investigators attempted to provide similaramounts of total fat and saturated fat in the control and soy-containingdiets. In 14 studies the diets were similar to conventionalWestern diets in fat and cholesterol content (these were termed"usual" diets), and in 18 studies the diets were low in fatcontent (<30 percent of energy) and low in cholesterol content(<200 mg per day). In 29 studies the amounts of total fatand saturated fat were similar in the control and soy-containingdiets (i.e., they differed by less than 10 percent); 8 otherstudies were designed to provide similar total fat and saturatedfat intake but the similarity of the diets was not documented.In 20 studies cholesterol intake was similar in the two diets;9 other studies were designed to provide similar cholesterolintake but similarity was not documented.
All the studies except one37 were designed to maintain weight;34 studies reported similar weight changes for subjects ingestingthe control and soy-containing diets. In all, 19 studies hadcontrol and soy-containing diets that were similar with respectto intake of dietary fat (total and saturated), intake of dietarycholesterol, and weight change. These 19 studies are listedas "similar" in each of the last three columns of Table 1.
Changes in Serum Lipid Concentrations
The ingestion of diets containing soy protein, as compared withthe control diets, was accompanied by a significant reductionin serum concentrations of total cholesterol, LDL cholesterol,and triglycerides (Table 2). The net change (change during thesoy diet minus change during the control diet) in serum cholesterolconcentrations was a decrease of 23.2 mg per deciliter (0.60mmol per liter; 95 percent confidence interval for the decrease,13.5 to 32.9 mg per deciliter [0.35 to 0.85 mmol per liter]),or 9.3 percent. Of 38 studies, 34 (89 percent) reported a netdecrease and 4 (11 percent) reported a net increase in serumcholesterol concentrations.
Table 2. Net Change in Serum Lipids and Lipoprotein Concentrations in Subjects Ingesting the Soy-Containing Diets, as Compared with the Control Diets.
The net change in serum LDL cholesterol concentrations was adecrease of 21.7 mg per deciliter (0.56 mmol per liter; 95 percentconfidence interval for the decrease, 11.2 to 31.7 mg per deciliter[0.30 to 0.82 mmol per liter]), or 12.9 percent. Figure 1 illustratesthe net effects of the consumption of soy protein on serum LDLcholesterol concentrations as reported in 31 studies. Twenty-sixstudies (84 percent) reported a net reduction, four studies(13 percent) reported an increase, and one study (3 percent)reported no change.
Figure 1. Net Changes in Serum LDL Cholesterol Concentrations in 31 Clinical Trials of the Effects of Soy Protein on Serum Lipids.
These 31 trials presented data on LDL cholesterol for a total of 564 subjects. The values shown are the mean changes in LDL cholesterol concentrations while subjects received the diet containing soy protein minus the changes during the control diet, with 95 percent confidence intervals. A and B indicate separate studies reported in a single published article, listed here in the same order as in Table 1. To convert values to millimoles per liter, multiply by 0.02586.
Soy protein intake did not significantly affect serum HDL cholesterolconcentrations, but the net change was an increase of 2.4 percent.Serum very-low-density lipoprotein (VLDL) cholesterol concentrationswere not significantly altered by soy protein. The consumptionof soy protein significantly decreased serum triglyceride concentrations,by 13.3 mg per deciliter (0.15 mmol per liter; 95 percent confidenceinterval for the decrease, 0.3 to 25.7 mg per deciliter [0.003to 0.29 mmol per liter]), or 10.5 percent. Of 30 studies, 22(73 percent) reported a net decrease in serum triglyceride concentrations,whereas 8 (27 percent) reported an increase.
Effect of Initial Serum Lipid Concentrations
Table 3 summarizes the effects of various factors on changesin serum cholesterol concentrations. In the complete regressionmodel, the initial serum cholesterol concentration was the onlysignificant predictor of the change in the serum cholesterolconcentration (P<0.001). The relation between the initialserum cholesterol concentration and changes in serum cholesterolwas modeled as a quadratic polynomial function. The proportionreduction in variance among studies between conditional andunconditional models indicated that the base-line cholesterolconcentration accounted for approximately 77 percent of theoverall variance. However, significant heterogeneity continuedto be present in the model even after adjustment for hypothesizedpredictors of variation (variance component = 0.134, P<0.001).
Table 3. Fixed-Effects Estimates from the Regression Model Predicting Net Changes in Serum Cholesterol Concentrations as a Function of Characteristics of the Study.
Table 4 presents changes in serum cholesterol and LDL cholesterolconcentrations according to quartiles of the initial cholesterolconcentration. Subjects with normal cholesterol levels, whohad initial values below 200 mg per deciliter, had nonsignificantreductions of 3.3 percent while receiving the soy protein diet.Those with mild hypercholesterolemia, who had initial valuesof 200 to 255 mg per deciliter (5.2 to 6.6 mmol per liter),had nonsignificant reductions of 4.4 percent. Subjects withmoderate hypercholesterolemia, who had initial values of 259to 333 mg per deciliter (6.70 to 8.61 mmol per liter), had significantdecreases of 7.4 percent. Subjects with severe hypercholesterolemia,whose initial values were above 335 mg per deciliter (8.66 mmolper liter), had significant reductions of 19.6 percent.
Table 4. Changes in Serum Cholesterol and LDL Cholesterol Concentrations According to Quartiles of the Study Group for Initial Cholesterol Concentration.
The pattern of changes in serum LDL cholesterol concentrations,according to quartiles of the initial serum cholesterol values,was similar to the pattern for serum cholesterol concentrations:first quartile, a decrease of 7.7 percent; second quartile,a decrease of 6.8 percent; third quartile, a decrease of 9.8percent; and fourth quartile, a decrease of 24.0 percent. Changesin serum HDL cholesterol concentrations were similar for allquartiles. Changes in serum triglyceride concentrations weresignificantly related to the initial serum triglyceride concentrations(P<0.05). However, changes in individual quartile groupswere not statistically significant.
Effect of Other Variables
As shown in Table 3, the type of soy protein did not have asignificant effect on the net change in serum cholesterol concentrationsand accounted for only approximately 1.0 percent of the variance.The amount of soy protein in the diet was also not significant(P = 0.39) when net changes were assessed. The type of diet,although not statistically significant, accounted for approximately12.6 percent of the variance (P = 0.07); larger changes tendedto occur when the control diets were "usual" diets rather thanlow-fat and low-cholesterol diets. The results of studies ofadult subjects did not differ significantly from those of thefour studies of children; the age group of the subjects thushad a negligible effect on variance. The changes in the 19 studieswith similar diets in terms of fat and cholesterol intake andweight change did not differ significantly from the changesin the remaining studies, in which the diets were not similar;this factor accounted for negligible variance.
To examine the effects of the type and amount of soy proteinfurther, we performed a complete regression analysis using changesobserved with the soy diet alone instead of net changes (soydiet minus control diet) as the outcome variable. In this model,significant effects were obtained for the initial serum cholesterolconcentration (P<0.001; proportion of reduction accountedfor, 0.69) and the amount of soy protein (P = 0.02; proportionof reduction, 0.13). This model predicted that soy protein intakewould be associated with the following decreases in serum cholesterolconcentrations, after adjustment for the initial values andother variables: 25 g per day of soy protein, a decrease of8.9 mg per deciliter (0.23 mmol per liter); 50 g per day ofsoy protein, a decrease of 17.4 mg per deciliter (0.45 mmolper liter); and 75 g per day of soy protein, a decrease of 26.3mg per deciliter (0.68 mmol per liter). The type of soy protein(P = 0.16), the type of diet (P = 0.11), the age group of thesubjects (adults or children) (P = 0.39), and the similarityof the diets (P = 0.28) did not have significant effects onthis model.
Discussion
This analysis of 38 controlled clinical studies reported in29 scientific articles indicated that the replacement of animalprotein in the diet with soy protein was associated with a significantdecrease in serum cholesterol and LDL cholesterol concentrations.This was a fairly consistent finding, since decreases in serumcholesterol concentrations were reported in 34 of 38 studies;in the 4 studies15,20,23,36 that did not report such reductions,the subjects had fairly low initial serum cholesterol values(average, 185 mg per deciliter [4.78 mmol per liter]). Changesin serum lipid concentrations were independent of changes inbody weight and dietary intake of total fat, saturated fat,and cholesterol.
The strength and consistency of these observations are surprisingin the light of the conclusion of the Nutrition Committee ofthe American Heart Association that the "consumption of vegetableproteins leads to lower cholesterol levels than consumptionof animal proteins in rabbits but not in humans."7 This commentwas supported by only one study.51
Initial serum cholesterol concentrations had a powerful effecton changes in serum cholesterol and LDL cholesterol concentrationsand accounted for approximately 77 percent of the variance amongstudies. The amount of soy protein ingested had a significanteffect on serum cholesterol concentrations when the effectsof the soy diet were examined alone, without the effects ofthe control diet. Soy protein intake averaged 47 g per day,and 37 percent of the studies used 31 g per day or less. Theseobservations suggest that the daily consumption of 31 to 47g of soy protein can significantly decrease serum cholesteroland LDL cholesterol concentrations. After adjustment for initialserum cholesterol concentrations and other variables, the ingestionof 25 or 50 g of soy protein per day was estimated to decreaseserum cholesterol concentrations by 8.9 or 17.4 mg per deciliter,respectively. Persons with moderate or severe hypercholesterolemia(>250 mg per deciliter [6.46 mmol per liter]) should haveeven larger decreases in serum cholesterol concentrations whensoy protein replaces animal protein in the diet.
Soy protein products are widely available in supermarkets, andlower-fat soy products are easily obtainable. Persons with hypercholesterolemiacan achieve an intake of more than 30 g of soy protein per dayby consuming two to three servings of soy products daily. Theamount of soy protein in a single serving of various soy productsis as follows: 8 oz (226 g) of soy milk contains 4 to 10 g ofsoy protein; 4 oz (113 g) of tofu, 8 to 13 g; 1 oz (28 g) ofsoy flour, 10 to 13 g; 1 oz (28 g) of isolated soy protein,23 g; 1/2 cup (113 g) of textured soy protein, 11 g; and 3.2oz (91 g) of meat analogue, 18 g.52 Thus, substituting two cups(473 ml) of soy milk for regular milk and consuming one servingof meat analogue would provide approximately 30 g of soy proteinper day.
The mechanisms responsible for the effects of soy protein onserum lipoproteins are unknown6,44 and were not addressed inthis study. Carroll6 recently reviewed and discussed varioushypotheses. In experiments in animals, the amino acid compositionof the diet affects serum cholesterol concentrations; increasesin arginine are accompanied by decreases in serum cholesterolconcentrations.6 Although some studies suggest that alterationsin bile acid or cholesterol absorption may contribute to alteredcholesterol homeostasis,6 Fumagalli et al.18 found no differencesin the fecal excretion of bile acids or sterols by human subjects.Some observers, as discussed by Carroll,6 suggest that alterationsin the ratio of serum glucagon to serum insulin may affect hepaticcholesterol synthesis; others6,44 suggest that serum free thyroxineconcentrations may be higher when the diet contains soy protein.Huff and colleagues24 suggest that turnover of VLDL apoproteinB is increased in humans when soy protein is substituted formeat and dairy protein. Lovati and colleagues34 report thatthe LDL-receptor activity of monocytes is eight times greaterin human subjects receiving soy protein than in those eatingcontrol diets.
Setchell53 suggests that soy estrogens may contribute to thecholesterol-lowering effects of soy protein. Most soy proteinproducts contain soy estrogens (isoflavones or phytoestrogens),54which have weak estrogenic effects under certain circumstancesand antiestrogenic effects under others.55 The administrationof oral estrogens56 or the synthetic antiestrogen tamoxifen57decreases serum cholesterol and LDL cholesterol concentrations;soy estrogens may have similar actions. This suggestion is supportedin studies by Anthony and colleagues.58,59,60 In three studiesusing cynomolgus or rhesus monkeys, soy protein rich in soyestrogens favorably affected serum lipids, whereas soy proteinfrom which the soy estrogens had been extracted had a minimaleffect. These primate studies suggest that soy estrogens mayaccount for 60 to 70 percent of the hypocholesterolemic effectsof soy protein.
In summary, this meta-analysis of 38 studies indicates thatthe consumption of soy protein is associated with significantdecreases in serum cholesterol, LDL cholesterol, and triglycerideconcentrations and with a nonsignificant increase in serum HDLcholesterol concentrations. The decreases in serum cholesteroland LDL cholesterol concentrations were strongly related tothe subjects' initial serum cholesterol concentrations. Soyestrogens may be responsible for most of the hypocholesterolemiceffects of soy protein.
Supported in part by Protein Technologies International, St.Louis. Dr. Anderson is a member of the Health and NutritionAdvisory Group of Protein Technologies International.
Source Information
From the Metabolic Research Group, Veterans Affairs Medical Center and Department of Medicine (J.W.A.), the Department of Behavioral Science, College of Medicine (B.M.J.), and the Department of Nutritional Sciences (M.E.C.-N.), University of Kentucky, Lexington.
Address reprint requests to Dr. Anderson at the Medical Service, 111C, Veterans Affairs Medical Center, Leestown Rd., Lexington, KY 40511.
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Soy Protein and Serum Lipids
Krauss R. M., Chait A., Stone N. J., Anderson J. W., Johnstone B. M., Cook-Newell M. E.
Extract |
Full Text
N Engl J Med 1995;
333:1715-1716, Dec 21, 1995.
Correspondence
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Lin, Y., Meijer, G. W., Vermeer, M. A., Trautwein, E. A.
(2004). Soy Protein Enhances the Cholesterol-Lowering Effect of Plant Sterol Esters in Cholesterol-Fed Hamsters. J. Nutr.
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Jenkins, D. J., Kendall, C. W., Marchie, A., Jenkins, A. L, Augustin, L. S., Ludwig, D. S, Barnard, N. D, Anderson, J. W
(2003). Type 2 diabetes and the vegetarian diet. Am. J. Clin. Nutr.
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Zhang, X., Shu, X. O., Gao, Y.-T., Yang, G., Li, Q., Li, H., Jin, F., Zheng, W.
(2003). Soy Food Consumption Is Associated with Lower Risk of Coronary Heart Disease in Chinese Women. J. Nutr.
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Jenkins, D. J. A., Kendall, C. W. C., Marchie, A., Faulkner, D. A., Wong, J. M. W., de Souza, R., Emam, A., Parker, T. L., Vidgen, E., Lapsley, K. G., Trautwein, E. A., Josse, R. G., Leiter, L. A., Connelly, P. W.
(2003). Effects of a Dietary Portfolio of Cholesterol-Lowering Foods vs Lovastatin on Serum Lipids and C-Reactive Protein. JAMA
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Anderson, J. W.
(2003). Diet First, Then Medication for Hypercholesterolemia. JAMA
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Piersen, C. E.
(2003). Phytoestrogens in Botanical Dietary Supplements: Implications for Cancer. Integr Cancer Ther
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Sabate, J., Haddad, E., Tanzman, J. S, Jambazian, P., Rajaram, S.
(2003). Serum lipid response to the graduated enrichment of a Step I diet with almonds: a randomized feeding trial. Am. J. Clin. Nutr.
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Sesso, H. D, Gaziano, J M., Liu, S., Buring, J. E
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Chiba, H., Uehara, M., Wu, J., Wang, X., Masuyama, R., Suzuki, K., Kanazawa, K., Ishimi, Y.
(2003). Hesperidin, a Citrus Flavonoid, Inhibits Bone Loss and Decreases Serum and Hepatic Lipids in Ovariectomized Mice. J. Nutr.
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Kurzer, M. S.
(2003). Phytoestrogen Supplement Use by Women. J. Nutr.
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Bhathena, S. J., Ali, A. A., Haudenschild, C., Latham, P., Ranich, T., Mohamed, A. I., Hansen, C. T., Velasquez, M. T.
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Yancy, W. S. Jr, Westman, E. C., French, P. A., Califf, R. M.
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