European Journal of Clinical Nutrition (2000) 54, 14±19 ß 2000 Macmillan Publishers Ltd. All rights reserved 0954±3007/00 $15.00 www.nature.com/ejcn
Effects of soy as tofu vs meat on lipoprotein concentrations
E Ashton1 and M Ball1*
1School of Biological Sciences, Deakin University, Victoria, Australia
Objectives: To investigate the effect of replacing lean meat with a soy product, tofu, on serum lipoprotein concentrations. Study and design: Randomized cross-over dietary intervention study. Subjects: Forty-two free-living healthy males aged 35 ± 62 y completed the dietary intervention. Three additional subjects were non-compliant and excluded prior to analysis. Interventions: A diet containing lean meat (150 g=d) was compared with one with 290 g=d tofu in an isocaloric and isoprotein substitution. Both diet periods were 1 month, and fat intake was carefully controlled. Results: Seven-day diet records showed the two diets were similar in energy, macronutrients and ®bre. Total cholesterol (mean difference 0.23 mmol=l, 95% CI 0.02, 0.43; P 0.03) and triglycerides (mean difference 0.15 mmol=l, 95% CI 0.02, 0.31; P 0.017) were signi®cantly lower on the tofu diet than the lean meat diet. However, HDL-C was also signi®cantly lower on the tofu diet (mean difference 0.08 mmol=l, 95% CI 0.02, 0.14; P 0.01) although the LDL-C:HDL-C ratio was similar. Conclusion: The effect on HDL-C and the small LDL-C reduction differ from some other studies, where fat was often less controlled, and the comparison was of soy as textured protein or soymilk against casein. This suggests a differential effect of the various proteins compared to the soy may in¯uence the ®ndings. In practice, the replacement of meat with tofu would usually be associated with a decrease in saturated fat and an increase in polyunsaturated fat and this should enhance any small bene®ts due to the soy protein. Sponsor: Deakin University with some contribution from a Commonwealth Department of Veterans Affairs research grant. Descriptors: soy protein; tofu; lipoproteins European Journal of Clinical Nutrition (2000) 54, 14±19
Introduction 1994; Goldberg et al, 1982; Verrillo et al, 1985; Jenkins et al, 1989; Sirtori et al, 1977; Descovich et al, 1980; Carroll Asian populations generally consume large amounts of soy et al, 1978) to determine the effects of substituting soy for products compared with populations eating Western diets, animal protein, usually as milk, on plasma lipid concentra- as well as consuming less fat and having higher vegetable tions. These investigations have shown differing results: intake (Hodgson et al, 1996; Roberts, 1995; Erdman & however, the majority found that soy protein was associated Fordyce, 1989). Asian populations also have lower inci- with decreased TC and LDL-C concentrations and varying dences of coronary heart disease (CHD), which is a major effects on TG and HDL-C. Subjects with hypercholester- cause of death in Western countries, including Australia. olaemia prior to the dietary intervention generally had a Many of the identi®ed risk factors for CHD, particularly greater response to soy compared with mildly hypercho- raised plasma total cholesterol (TC) and low-density lipo- lesterolaemic and normocholesterolaemic subjects, who protein cholesterol (LDL-C), raised triglycerides (TG) and had little or no response (Bakhit et al, 1994; Goldberg et low levels of high-density lipoprotein cholesterol (HDL-C), al, 1982; Descovich et al, 1980; Carroll et al, 1978). are in¯uenced by dietary factors and can be modi®ed by However, in some of these studies the ®ndings could not dietary changes (Ascherio & Willett, 1995; Dwyer, 1995). be attributed speci®cally to the effect of the soy protein, as Many studies indicate a positive relationship between the comparison diet often had different amounts of energy dietary intake of animal protein and TC levels (Carroll, from fat (Jenkins et al, 1989), different polyunsaturated 1991; Forsythe et al, 1986), and some studies have shown fatty acid (PUFA) to saturated fatty acid (SAFA) ratio an inverse relationship between the intake of soy protein (PUFA : SAFA ratio; Sirtori et al, 1977; Descovich et al, and TC (Nagata et al, 1998; Potter et al, 1996; Sirtori et al, 1980), and dietary cholesterol (Verrillo et al, 1985). In 1995). Dietary studies have been performed in both animals some studies subjects also experienced weight changes (Atwal et al, 1997; Woodward & Carroll 1985; Forsythe between the diets (Jenkins et al, 1989), which could have et al, 1980; Park & Liepa, 1982) and humans (Bakhit et al, affected the plasma lipids (Ernst et al, 1997; Lehmann et al, 1995; Anderson et al, 1956). *Correspondence: M Ball, School of Biological Sciences, Deakin Anderson et al (1995), in a meta-analysis of 38 clinical University, 221 Burwood Highway, Burwood, Victoria 3125, Australia. E-mail: [email protected]. studies (34 in adults), assessed the effects of soy protein on Guarantor: M Ball. lipoprotein levels. They found the mean effect was a Contributors: EA was involved in day to day running of study and subject 0.60 mmol=l decrease in TC, 0.56 mmol=l decrease in recruitment, dietary and laboratory analysis, statistical analysis and writing LDL-C, and a 0.15 mmol=l decrease in TG, with no of the paper. MB was involved in design of the study, supervision of the signi®cant effect on HDL-C. The majority of the studies running of the study including dietary and laboratory analysis, and writing of the paper. considered were small: 92% with less than 25 subjects, and Received 18 March 1999; revised 28 June 1999; accepted 16 July 1999 in 24% of the studies the dietary fat was not kept constant Soy vs meat and lipoprotein concentrations E Ashton and M Ball 15 or was not mentioned. In only 22 of the 38 studies were the were then randomly assigned to a study diet for 1 month, soy protein diet and animal protein diet considered similar after which they returned to their habitual diet for a 2-week by the author's criteria of total fat and SAFA being within `washout' period before undertaking the second diet for 1 10% and with no signi®cant weight change between diets. month. Twenty-one subjects completed the sequence of These 22 studies had similar results to the 38. However, a lean meat followed by tofu diet and 21 subjects completed difference in fat of less than 10% could still in¯uence the the tofu then lean meat diet sequence. lipoprotein levels (Howell et al, 1997). Also the PUFA: The diets were designed to be similar in energy, protein, SAFA ratio was generally not mentioned or taken into fat, carbohydrate, alcohol and dietary ®bre, with only the consideration, yet this has an inverse effect on TC con- source of protein changing from an animal source to plant centrations (Forsythe et al, 1986; Descovich et al, 1980; source. Subjects consumed similar vegetarian breakfasts, Sirtori et al, 1979; Meredith et al, 1989). As soy protein is lunches and snacks on both diets. During the meat diet naturally higher in PUFA than animal protein and animal subjects consumed 150 g (raw weight) of cooked lean red protein contains more monounsaturated fatty acids meat, with all visible fat removed, each day. PUFA (MUFA) and SAFA than soy protein, diets which do not margarine, 15 g, was prescribed. Subjects avoided all soy compensate for this in the design will actually have quite products during this diet. The tofu diet was designed to different fatty acid pro®les. replace 90 ± 100% of the animal protein with 290 g of tofu. Most studies of soy protein vs animal protein on lipids and To minimize the differences in MUFA, PUFA and SAFA CHD risk factors have compared isolated soy protein or between the two diets, 5 g of butter, 5 g of lard and 8 ml of textured soy protein vs casein in a milk product. We are olive oil were also prescribed daily on the tofu diet. All tofu unaware of any human studies comparing the effect of soy as was supplied from Blue Lotus Foods P=L (Kilsyth, Aus- tofu and meat as the sole protein replacement. The present tralia). The tofu and fats were supplied free, and recipes study was designed to investigate the effect on plasma and specially prepared tofu biscuits were also supplied to lipoproteins of substituting tofu, for meat, while carefully help subjects consume the tofu if required. To standardize controlling the dietary fat intake and other dietary factors. the lean meat consumed all subjects were counselled by a dietitian on the cut of meat allowed, the amount to be consumed, and instructions on how to prepare the meat. Methods and materials Subjects were also provided with an extensive list of Subjects acceptable and unacceptable meats. Dietary counselling Forty-®ve healthy male volunteers aged 34 ± 62 y (mean was provided weekly to help with dietary manipulation age 45.8) with no symptoms or prior diagnosis of CHD and to assess and improve compliance. All subjects were were recruited via newspaper articles, radio announcements instructed to maintain their usual exercise patterns for the and direct personal communications. All volunteers were duration of the study. Subjects were instructed to advise the initially screened by telephone conversation followed by a investigators if they felt hungry or satis®ed and if they formal interview. Exclusion criteria included use of any experienced any weight change. During the last week of medication that affects blood lipids or blood pressure, a each diet the subjects completed a 7 d diet record, using body mass index > 35 kg=m2, TC concentration > 7.5 accurate scales, or household measures when weighing was mmol=l, and TG concentration > 6.0 mmol=l. Of the 45 not possible (Edington et al, 1989). All diets were coded subjects three were excluded prior to analysis due to and analysed using System for Online Dietary Analysis noncompliance. (SODA) version 5 (Cottesloe, Australia) using NUTTAB Deakin University Ethics Committee approved the study 91 database with updated nutrient composition of the tofu protocol, and informed written consent was obtained from and margarine used. each participant. Height and weight were measured at commencement of the study, and weight, in light clothing and no shoes, was Study and design measured on accurate digital scales at the end of both diet The study was designed to compare the effects of two diets periods. A 24 h urine collection was performed at the end of using a randomized crossover design, as shown in Figure 1. both diet periods to measure the urinary excretion of the Prior to commencement of the dietary intervention, all iso¯avones genistein and daidzein. Venous blood was subjects were given detailed written and verbal instructions collected into vacutainers without anticoagulant during on how to accurately complete a weighed food record and the baseline period and twice at the end of each diet were instructed to record their habitual diet for 7 d, includ- period 3 ± 4 d apart and after an overnight fast. Blood was ing two weekend days. Subjects were provided with scales allowed to coagulate for 1 h and then spun at 4C for 20 accurate to 1 g and household measuring equipment, such min at 3000 rpm. All serum was aliquotted and stored at as spoons and graduated cups. This gave subjects practice 7 80C, and all analyses were carried out in the same run. on completing a food record and provided details of the subject's normal energy intake, and pattern of food con- Laboratory analysis sumption to aid in manipulating their diet. The subjects TC, TG and HDL-C were measured using an enzymtic colorimetric test using Boehringer Mannheim Kits (Mann- heim, Germany) on a Hitachi 704 autoanalyser (Tokyo, Meat Diet (4 weeks) ? Washout (2 weeks) Japan). LDL-C was calculated using Friedewald's equation ? Tofu Diet (4 weeks) (Friedewald et al, 1972). The following serum cholesteryl Habitual diet ester fatty acids were measured on samples from 11 subjects on both the lean meat and tofu diet by gas Tofu Diet (4 weeks) ? Washout (2 weeks) chromatography using the method described by Sinclair ? Meat Diet (4 weeks) et al (1987): C12:0, C14:0, C14:1, C15:0, C16:0, C16:1, Figure 1 Study design. C17:1, C18:0, C18:1, C18:2n6, C18:3n6, C18:3n3, C20:0,
European Journal of Clinical Nutrition Soy vs meat and lipoprotein concentrations E Ashton and M Ball 16 C20:1, C20:2, C20:3n6, C20:4n6, C20:3n3, C22:0, C22:1, Table 2 Dietary intake of subjects (n 42)
C20:5n3, C22:2, C22:4, C24:0, C24:1, C22:5n3, and a a a C22:6n3. Nutrient Habitual diet Lean meat diet Tofu diet Urinary concentrations of genistein were measured after Energy (MJ) 10.2Æ 2.5 9.6Æ 1.9 9.5Æ 2.0* iso¯avonoids were deconjugated using glucuronidase Protein (%E) 16.5Æ 2.4 17.2Æ 2.3 16.9Æ 1.9 (Sigma Chemical Company, St Louis, USA) and extracted Carbohydrate (%) 43.2Æ 6.4 43.7Æ 5.3 44.0Æ 5.0 Total fat (%) 33.0Æ 5.6 32.4Æ 5.2 32.0Æ 5.3 with diethyl ether (BDH Chemicals, Melbourne, Australia), Saturated fat (%) 13.3Æ 2.7 12.9Æ 3.0 12.4Æ 2.8* by reverse-phase HPLC (Shimadzu system LC10A) accord- MUFA (%) 11.7Æ 2.8 11.9Æ 2.4 11.5Æ 2.5 ing to the method of Eldridge (1982). PUFA (%) 4.7Æ 1.5 4.8Æ 1.3 5.2Æ 1.3* PUFA:SAFA ratio 0.37Æ 0.15 0.39Æ 0.14 0.44Æ 0.16* Alcohol (%) 5.5Æ 5.7 4.9Æ 5.2 5.4Æ 5.7 Statistical analyses Fibre (g) 28.0Æ 10.2 28.0Æ 9.3 26.6Æ 7.5 Statistical analysis was performed using Statistical Cholesterol (mg) 278.2Æ 98.2 253.2Æ 72.7 189.5Æ 105.6b* Packages for Social Scientists (SPSS version 8.0.0, 1997, Chicago, IL). Wilcoxon signed rank test was used to aValues are mean Æ s.d. bP < 0.05 based on paired t-test between lean meat diet and tofu diet. compare serum TG between the two diets. A general *P < 0.05 based on paired t-test between habitual diet and tofu diet. linear model (GLM) was used to investigate the overall %E percentage of total energy intake. effect of the two diets on TC, LDL-C, HDL-C and LDL:HDL ratio taking into consideration the carry over effects and order effects. This is achieved by treating both time and diet as ®xed factors and identi®cation number as a random factor, and the GLM identi®es any interaction of SAFA (P 0.031) and dietary cholesterol (P 0.001) and the order the diets on the results (Fleiss, 1986). The signi®cantly lower in PUFA and PUFA : SAFA ratio relationship between urinary excretion of genistein and (P 0.012 and 0.003, respectively) compared with the lipoproteins was determined by Spearman's correlation. tofu diet. Pearson's correlation was used to identify any relationship Mean (s.d.) urine excretion of genistein per mmol crea- between the initial concentrations and change in concentra- tinine was signi®cantly higher on the tofu diet (P < 0.001, tions of TC, LDL-C and HDL-C. Spearman's correlation being 202 ng=mmol (196) on the tofu diet and 12 ng=mmol was used to identify any relationship between initial TG (11) on the meat diet, respectively. There was no signi®cant levels and the change in concentrations after the diets. correlation between the change in urinary genistein excre- tion and change in lipoprotein concentrations. Prior to starting the study, on their habitual diet, the Results subjects' TC, LDL-C and TG were signi®cantly higher than The mean (s.d.) BMI of subjects prior to commencing the after the tofu diet (P 0.001, P 0.026, and P 0.001, study was 26.2 kg=m2 (3.3). The mean weight of the respectively). HDL-C was signi®cantly lower on the habi- subjects did not change signi®cantly between diet periods. tual diet compared to the lean meat diet (P 0.006), and Lipoprotein concentrations of subjects prior to commen- the LDL:HDL ratio was signi®cantly higher (P 0.01), but cing the diet and after the two diets are given in Table 1. the results were not signi®cantly different from the tofu Subjects had initial TC concentrations between 4 and diet. TC, TG and HDL-C were signi®cantly lower on the 7.5 mmol=l. The mean dietary intakes for the 42 subjects tofu diet compared with the meat diet (Table 2). LDL-C prior to starting the diet and on the two diets are given in and LDL:HDL ratio were not signi®cantly different Table 2. There was no signi®cant difference between the between the two diets. There was no signi®cant carry lean meat and the tofu diet in dietary energy, protein, total over or order effect on the parameters measured according fat, SAFA, MUFA, PUFA, PUFA : SAFA ratio, carbo- to the GLM. There was a signi®cant relationship between hydrate, alcohol or ®bre when expressed as percentage of the initial concentration of HDL-C and the change in HDL- energy or expressed as grams of each nutrient. Dietary C on the two diets (r 0.482, P 0.001). There was no cholesterol was signi®cantly lower on the tofu diet. The signi®cant correlation between the initial concentration of habitual diet was not signi®cantly different to the lean meat TC, LDL-C and TG and their change on the two diets. diet in any of the nutrients analysed. On the other hand, the Subjects with initial TC of > 6.5 mmol=l did not have a habitual diet was signi®cantly higher in energy (P 0.009), greater change than those with TC < 6.5 mmol=l.
Table 1 Serum lipoprotein concentrations (n 42)
Mean difference between Lipoprotein Baselinea Lean meat dieta Tofu dieta meat and tofu diet 95% CIb
Total Cholesterol (mmol=l) 5.79Æ 0.97 5.65Æ 0.93 5.42Æ 1.02c* 0.23 0.02,0.43 LDL-C (mmol=l) 3.68Æ 0.86 3.56Æ 0.90 3.48Æ 0.92* 0.09 7 0.10,0.27 HDL-C (mmol=l) 1.25Æ 0.35 1.32Æ 0.34** 1.24Æ 0.27c 0.08 0.02,0.14 LDL : HDL ratio 3.16Æ 1.08 2.89Æ 1.07** 2.99Æ 1.14 7 0.11 7 0.32,0.11 Triglycerides (mmol=l) 1.96Æ 1.33 1.77Æ 0.95 1.62Æ 0.99***d 0.15 7 0.02,0.31
aValues are mean Æ s.d. bCI con®dence intervals of mean differences between meat and tofu diets. cP < 0.05 for difference between lean meat diet and tofu diet based on paired t-test. dP < 0.05 for difference between lean meat diet and tofu diet based on Wilcoxon signed rank test. *P < 0.05 for difference between baseline and tofu diet based on paired t-test. **P < 0.05 for difference between baseline and lean meat diet based on paired t-test. ***P < 0.05 for difference between baseline and tofu diet based on Wilcoxon signed rank test.
European Journal of Clinical Nutrition Soy vs meat and lipoprotein concentrations E Ashton and M Ball 17 Serum cholesteryl ester fatty acids were not signi®cantly further reason for the difference may thus be the different different between the diets except for linoleic acid protein in the diet the soy was compared against. (C18:2n6), which was signi®cantly higher on the tofu diet Hypercholesterolaemic subjects did not show a greater (P 0.03). response to the soy than those with normocholesterolaemia, and in contrast to the meta-analysis we did not ®nd a correlation with initial TC, LDL-C or TG levels and changes on the two diets (Anderson et al, 1995). The Discussion correlation between the initial HDL-C concentrations and Most investigations into the effect of soy, in both animals the change after the two diets indicated that subjects do and humans, have used soy in the form of textured vary in their response. vegetable protein, soy isolates or soy milk and compared In contrast to other studies which found that soy had it with casein in milk. In our study, meat was used as the little effect or a small positive effect on HDL-C our study major animal protein because it contributes a large percen- revealed the mean HDL-C was 6% lower on the soy diet tage of energy in the typical Western diet and can easily be compared with the meat diet, and the LDL:HDL ratio was replaced. Tofu was chosen to replace meat because it is a not signi®cantly different. The change appeared to be due regular constituent of the Asian diet, unlike isolated and to an increase of HDL-C on meat compared with the textured soy protein, it is readily available, can replace subjects' habitual diet (P 0.006). HDL-C levels then meat in both Asian and Western style recipes, and is high in returned to similar levels to those on habitual diet when phytoestrogens (Dwyer et al, 1994). on the soy diet. A rise in HDL-C may be due to the beef Assessment of subjects' food records and urinary iso- proteins, an effect which does not occur with casein. An ¯avone concentrations indicated that subjects complied increase in HDL-C was attributed to beef protein in the well with the prescribed diets. The macronutrient intake study conducted by Wiebe et al (1984) where they com- was not signi®cantly different except for the protein source pared the effect of beef protein vs a plant protein. The and dietary cholesterol. The latter was signi®cantly lower authors speculated that the cause might have been the lower on the tofu diet, but it is doubtful that a mean difference of carbohydrate content (9%) compared with the plant protein 90 mg=d in the context of a low-fat diet (total fat < 33% of diet. As the meat diet in the current study was less than 1% energy) and a low dietary cholesterol diet ( < 300 mg=d) lower in carbohydrate than the soy diet, it suggests an had an impact on our ®ndings. Using the equation derived in¯uence on HDL-C through some other mechanism. by Howell et al (1997), from a meta-analysis of dietary An explanation for the other differences between this intervention studies, this difference in dietary cholesterol study and others could also be the difference in animal would only possibly cause a 0.05 mmol=l difference in TC. protein source used for comparison rather than the effect of Serum cholesteryl ester fatty acids were analysed in a the soy. Casein has been reported as hypercholesterolaemic subgroup to provide an independent assessment of the compared with plant protein (Carroll et al, 1978; Forsythe, difference in fat between the two diets. Results revealed 1995; Carroll & Kurowska, 1995). Most studies discuss linoleic acid was 8.5% higher on the tofu diet, although results as a decrease in LDL-C on plant protein diet dietary records indicated similar intake, and may indicate a compared with the animal protein (usually casein) diet. small difference in intake in the few days prior to blood HDL-C is described in the same manner, but the indepen- sampling. This small difference may have contributed to dent effect of casein on LDL-C and HDL-C is not reported decreasing cholesterol on the tofu diet, if it replaced SAFA, (Carroll et al, 1978; Forsythe, 1995; Carroll & Kurowska, but would not explain the total change. Urinary excretion of 1995). In addition, our study controlled fat intake carefully, genistein con®rmed that subjects consumed quantities of whereas other studies where fat was considered `similar' iso¯avones that exceed that of the Japanese population have differed by up to 10%. A lower SAFA intake on the (Adlercreutz et al, 1991). soy diet of only 5 ± 10% could augment any LDL-C low- Studies have fairly consistently shown that soy protein ering. compared to milk protein decreases TC, LDL-C and TG The 290 g of tofu consumed supplied 80 mg=d of iso- concentrations without signi®cantly affecting HDL-C con- ¯avones (Reinli & Block, 1996) 50 mg=d higher than the centrations. These changes would be expected to reduce the average intake of people consuming a traditional Japanese risk of CHD (Kannel, 1995). In agreement with most diet (Messina, 1995). Iso¯avones are phytochemicals that studies, our results indicated that the soy decreased TC have been suggested as the component of soy that may and TG concentrations, but the mean LDL-C was only 2% decrease lipoproteins; however studies of the effect of lower on the tofu diet. Anderson's meta-analysis (Anderson iso¯avones are inconsistent (Baum et al, 1998; Craig, et al, 1995) found a mean decrease in LDL-C of 1997; Gooderham et al, 1996). Some studies have found 0.56 mmol=l or 12.9% on the soy diet. It is proposed that no effects of isolated genistein on lipoprotein levels (Hodg- our study did not achieve the signi®cant reduction in LDL- son et al, 1998; Nestel et al, 1997), and it is not possible to C found in many studies in the meta-analysis (Anderson et assess any effect of phytochemicals in studies in the meta- al, 1995), because of the smaller amount of soy protein analysis (Anderson et al, 1995) as the measurement tech- consumed. Studies using isolated soy and textured soy nology has only recently become available. However it is protein have been able to supply large amounts of soy likely that the iso¯avone content of most of the diets is low protein per day, the average being 47 g=d compared with 35 (Sirtori, et al, 1997) due to processing, and that they are not g=d on the current study. This is because isolated soy the major effector of any lipoprotein changes. protein is 90% protein and soy concentrates are 70% soy Several other possible mechanisms of action of the soy protein whereas tofu is 8.3% protein, and there is a limit on on lipoproteins have been speculated including the different the amount of tofu it is practical to consume. However, a amino acid concentrations (Forsythe, 1995; Carroll & third of studies in the meta-analysis also had 30 g soy Kurowska, 1995; Potter, 1995; Horigome & Cho, 1992; protein per day and some showed an effect on LDL-C and a Sanchez & Hubbard, 1991), hormonal and endocrine in¯u-
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