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Research Communication

Neither Background Diet Nor Type of Soy Food Affects Short-Term Isoflavone Bioavailability in Women^{1 ,2}

Food Science and Human Nutrition, Iowa State University, Ames, IA 50011

³To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
To characterize bioavailability of soybean isoflavones, proposed anticarcinogenic food components, eight women, ages 20–41 y, were fed 0.9 mg isoflavones/kg body wt from soymilk at 0730, 1230 and 1730 h for 1 d. Subjects consumed three background diets in random order: a diet prepared for them (basic foods diet) or a self-selected diet at the specified times, or a self-selected diet eaten ad libitum. In a second study, women were fed single isoflavone doses of 0.8–1.4 mg/kg in breakfast casseroles containing tofu, tempeh, cooked soybeans or texturized vegetable protein. Both studies were conducted in randomized, cross-over designs. Plasma, urine and fecal isoflavones were measured by reverse-phase HPLC. After consumption of background diets, 48-h urinary recovery of daidzein (D) was 26–27%, and of genistein (G), 18–20% of the dose given with each diet. At 24 h after consumption of different background diets, plasma D and G concentrations were similar (1.4 ± 0.7 mmol/L) and were not affected by diet selection. Urinary recoveries of D over 24 h from the various soy foods were 38–51%, and of G, 9–16% of the dose given. In both studies, urinary recovery of D was significantly greater than that of G. Only a few percentage of the total isoflavone dose was recovered in feces, probably due to bacterial breakdown of these compounds. Therefore, isoflavone bioavailability may not be affected by choice of background diet or food source of isoflavones.

KEY WORDS: • isoflavones • bioavailability • diet selection • soybean foods • humans

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Isoflavones are abundant in soybean foods (0.2–1.5 mg/g) (Wang and Murphy 1994 ). The three isoflavones, daidzein (D)⁴ , genistein (G) and glycitein, are found in four chemical forms (aglycone, glucoside, acetylglucoside and malonylglucoside) (Kudou et al. 1991 ). Glycitein is weakly estrogenic (Song et al. 1999 ), as are G and D (Farmakalidis and Murphy 1985 ). Estrogen-like activity is one of many proposed anticarcinogenic mechanisms of these compounds (Messina and Barnes 1991 ). Dietary intake of soybean isoflavones was associated with lower breast and prostatic cancer incidence in Eastern Asia (Adlercreutz et al. 1995 ). An isoflavone extract providing 240 mg total isoflavones/kg diet significantly suppressed rat hepatocarcinogenesis initiated by diethylnitrosamine and promoted by phenobarbital (Lee et al. 1995 ). Rats consuming a soy-based diet develop fewer mammary tumors following administration of the carcinogens N-methylnitrosourea and 7,12-dimethylbenz[a]-anthracene than rats fed isonitrogenous and isocaloric diets without soy (Barnes et al. 1990 ). G inhibited the growth of estrogen receptor-negative or -positive human breast cancer cell lines [50% inhibitory concentration (IC₅₀) = 24–44 mmol/L; Peterson and Barnes 1991] and inhibited activation of tyrosine kinases (IC₅₀ = 3–100 mmol/L; Akiyama et al. 1987 ). D and G (IC₅₀ of 8 and 2.2 mmol/L, respectively) inhibited production of inositol phosphates, key intracellular signals of proliferation stimulated by AlF₄ in 3T3 cells (Higashi and Ogawara 1992 ). These findings suggest that isoflavones in soybean foods might play a role in human cancer protection.

Characterization of isoflavone bioavailability in humans is needed to assess the role of these compounds in cancer risk reduction. Previous human feeding studies showed that absorption of isoflavones from soymilk in a controlled liquid diet was dose-dependent (Xu et al. 1994 , 1995 ). But, people eat a variety of soybean foods and background diets. Fermentation increases the isoflavone aglycone content of soy foods, and processing alters the type of isoflavone glycoside. Therefore, soy food type might alter human isoflavone bioavailability. These studies address this hypothesis. Furthermore, it is of practical concern in studying the biological effects of these compounds to determine if carefully defined diets limit interindividual variability in isoflavone bioavailability compared with diets consumed ad libitum.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Subjects and protocol.

The procedures for this feeding study were approved by the Human Subjects Committee of Iowa State University (ISU). Written informed consent of subjects was obtained. All subjects were omnivorous and in good health, based on medical histories and physical examinations performed by Student Health Center physicians at ISU. Subjects did not take any medications including antibiotics during the feeding studies.

Expt. 1.

Eight women between 20 and 41 y of age, with body weight of 58.4 ± 10.5 kg and body mass index of 21.4 ± 2.2 kg/m² (means ± SD), were fed three servings of isoflavones per day (0.9 mg/kg body weight in each meal) from soymilk powder (Now Foods, Glendale Heights, IL) reconstituted with distilled water. The three doses of soymilk were served at 0730, 1230 and 1730 h, with each day of dosing separated by a 1-wk washout period. Subjects were asked not to consume anything for 10 h before soymilk dosing. Different background diets were consumed in a randomized cross-over design. A basic-foods diet was consumed at 0730, 1230 and 1730 h, with the soymilk doses. This diet consisted of a toasted plain bagel, 14 g grape jelly, and 250 mL orange juice at 0730 h; two slices white bread, 28 g Swiss cheese (Kraft^TM, Glenview, IL), mustard, one medium apple, 15 regular potato chips (28 g, Pringle’s^TM, Procter & Gamble, Cincinnati, OH) and 250 mL water at 1230 h; two slices white bread, 14 g Colby Jack cheese (Kraft^TM), mustard, 15 tortilla chips (12 g; Tostitos^TM, Frito-Lay, Plano, TX), 254 mL orange juice at 1730 h, 22 honey-flavored Teddy Grahams^TM (28 g; Nabisco, Parsippanny, NJ) and a medium apple at 1930 h. Subjects eating the basic foods diet were instructed not to eat anything other than what was given on the feeding day. When the subjects ate a self-selected diet, they chose their own foods but consumed them at the same time as the soymilk doses. When the subjects ate ad libitum, they chose their own foods and meal times, but soymilk was consumed at the same times as with the other feeding regimens. Subjects consuming self-selected and ad libitum diets were instructed to completely record their food and beverage intakes during each feeding day. Dietary data were analyzed by Nutritionist IV version 2.0 (N-Squared Computing, Salem, OR).

Expt. 2.

The subjects were 10 women between 20 and 35 y of age, with body weight of 59.6 ± 6.0 kg and body mass index of 21.6 ± 1.2 kg/m². Subjects were fed four types of soybean foods: tofu, texturized vegetable protein (TVP), tempeh or cooked soybeans. Subjects were instructed not to eat anything other than what was given on the feeding day. Soy foods were given at breakfast in a baked casserole consisting of the soy food (~30 g TVP, 100 g tempeh or cooked soy beans or 300 g tofu, providing approximately equal amounts of isoflavones from each food) mixed with one large egg, 40 g sharp cheddar cheese (Kraft^TM) and 70 g salsa (Pace^TM Thick & Chunky, San Antonio, TX), one slice white bread, one cup orange juice, and 250 mL water at 0730 h and other meals exactly as for the basic foods diet in expt. 1. The controlled diet was designed to meet subjects’ average energy requirement according to the Recommended Dietary Allowances tables (Food and Nutrition Board 1989 ). Feeding days were separated by 1-wk washout periods. Isoflavone dose ranged from 0.8–1.4 mg/kg body weight based on HPLC analysis of the soybean foods ingested. Data from some subjects fed tempeh and tofu (six at the first feeding and five at the second feeding) were not used because packages of those commercial soy foods were mixed in unknown amounts and the ingested isoflavone dose could not be determined.

In both studies, during the washout periods subjects were asked not to eat any foods from a list of items which may contain isoflavones. No adverse effects such as diarrhea were reported after soy food dosing.

Biological sample collection.

In both experiments, 5 mL venous blood samples wase collected in heparinized vacuum containers by medical technologists under stringent aseptic conditions at the ISU Student Health Center. Blood samples were collected within 1 h before dosing (time "0") and at 6.5 and 24 h after dosing. Samples were centrifuged within 1 h after collection at 3000 x g for 20 min at 4°C (Model 4D; International Equipment, Needham Heights, MA), and plasma was stored at -20°C. In expt. 1, a urine sample was collected from each subject in the morning, before dosing (time "0"), and then urine was pooled in four 12-h increments over the first 48 h after dosing. The first urination of d 3 after dosing was also collected. In expt. 2, urine was collected at time "0" and for only 24 h and the first urination of d 2 after dosing, and also pooled in 12-h increments. Urine volume was recorded and 50 mL aliquots of each sample stored at -20°C. In both experiments, capsules containing 1 g carmine red (Pharmaceutical Service, University of Iowa, Iowa City, IA) were given at breakfast. One fecal sample from each subject was collected before feeding (time "0") and feces collected until the dye marker was completely excreted. Feces were freeze-dried (VirTis lyophilizer, Gardiner, NY). After recording the dry weights of samples, feces were ground to a fine powder in a coffee mill (Braun Company, Lynnfield, MA). Each dry fecal sample (10 g) was stored in a -20°C freezer until analysis.

Soy milk powder and soy foods analysis.

The concentrations of total isoflavones in soymilk powder and four soy foods were measured as isoflavone aglycones after hydrolysis in 1 mol/L HCl at 98°C (Wang et al. 1990 ). HPLC analysis was as described by Wang and Murphy (1994) . Samples were analyzed in triplicate.

Biological sample analysis.

Sample preparation for plasma and urine isoflavone analysis was performed according to the methods described by Lundh et al. (1988) . Plasma and urine samples were treated with glucuronidase/sulfatase (Sigma Chemicals Company, St. Louis, MO) to produce isoflavone aglycones. Fecal samples were prepared as described (Xu et al. 1994 ). Chromatographic analysis of plasma, urine and fecal samples was as described by Xu et al. (1994) . Samples were injected with a Spectra-Physics Autosampler Model 8780XR (Spectra-Physics, Fremont, CA). Isoflavones were separated over a 3.9 mm i.d. x 30 cm length µ-Bondapak C18 reverse-phase column (Waters-Millipore, Bedford, MA) with gradient elution at ambient temperature. A Beckman (Fullerton, CA) HPLC system including two Model 110B pumps, one Model 420 Microprocessor solvent flow controller, with a Model 163 variable wavelength detector set at 254 nm connected with a Model 427 integrator was used.

Daidzein (4',7-dihydroxyisoflavone) was obtained from Life Science Group, ICN Pharmaceuticals,, Plainview, NY; G (4',5,7-trihydroxyisoflavone) from Calbiochem Corporation, La Jolla, CA and equol (4',7-isoflavandiol) was a generous gift from Dr. H. Adlercreutz (Department of Clinical Chemistry, University of Helsinki, Finland). Recovery was measured by spiking plasma, urine and fecal samples randomly with D, G or equol (100 µL, 1.5 mg/L).

Statistical methods.

ANOVA (General Linear Model) was performed with the Statistical Analysis System (SAS Institute, Cary, NC) version 6.06 on the Iowa State University mainframe computer to evaluate nutrient composition of subjects’ diets and isoflavone bioavailability. Values are means ± SD. A P-value of 0.05 or less was considered to be significant. Subjects and feeding times were treated as blocks. Percentage recovery of isoflavone from urine and feces and plasma isoflavone concentrations over time were compared among treatments and between G and D. If the effect from any factor other than type of isoflavone was significant, Tukey’s test was used for comparison of means within the factor.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Isoflavone concentration in soymilk powder was 1.25 ± 0.08 mg/g. G and D were 56.0 and 44.0%, respectively, of the molar total of the two isoflavones. Soy food isoflavone concentrations were: tofu, 0.46 ± 0.09 mg/g (57:43, G/D); tempeh, 0.64 ± 0.02 mg/g (60:40, G/D); TVP, 0.42 ± 0.01 mg/g (54:46, G/D); and cooked soybean, 0.58 ± 0.02 mg/g (54:46, G/D). D, G and equol recoveries from spiked samples of urine, plasma and feces were 80–92, 64–78 and 57–72%, respectively.

Expt. 1.

Intakes of energy (8,530 ± 130 kJ/d), carbohydrate (322 ± 5 g/d) and dietary fiber (12 ± 2 g/g, soluble + insoluble) did not differ significantly among the three background diets (data not shown). Intakes of fat, protein and cholesterol from self-selected, and ad libitum diets were significantly greater than those from the basic foods diet (P < 0.05) (Table 1 ). After consuming basic, self-selected and ad libitum diets, urinary isoflavone recovery as a percentage of intake did not differ significantly with diet selection (P > 0.1), and averaged 27 ± 9% for D and 19 ± 8% for G (Table 2 ). Urinary recovery of D was greater than that of G (P < 0.05) for all diets. Total fecal excretion of isoflavones was 4% of the ingested amount, and not different among background diets. No equol was found in any sample although the recovery of equol was between 62 and 74% in all spiked samples.

Plasma isoflavone concentration of D or G was significantly increased to an average of 2.5 ± 0.9 µmol/L at 6.5 h after dosing compared with time "0" and did not differ with background diet (data not shown). At 24 h postdosing, plasma D or G averaged 1.4 ± 0.9 µmol/L. The plasma concentrations of D and G did not differ at either time after dosing and did not differ with background diet.

Expt. 2.

Protein intake when subjects consumed TVP was significantly greater than from the other three soy foods, 118 ± 15 g/d for TVP vs. an average of 75–79 ± 2 g/d for the three groups fed the other foods. During feeding of the four soybean foods, 21–34% of the ingested total isoflavone dose was excreted. Urinary recoveries of D and G over 24 h after soy dosing did not differ with soy food type (cooked soybean, TVP, tofu and tempeh) (P > 0.1) and averaged overall about 45% for D and about 14% for G (Table 3 ). Urinary recovery of D was about 2.5 times greater than that of G for all types of soy foods tested (P < 0.01). Total fecal excretion of isoflavones was 1% of the ingested amount.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

On average, cooked soybean, TVP and soy milk powder contain > 95% of total isoflavones as glucosides, whereas tofu contains about 20% of its isoflavones as aglycones, and in tempeh, 40% of isoflavones are aglycones (Wang and Murphy 1994 ). Glucosides of isoflavones may be poorly hydrolyzed by mammalian intestinal digestive enzymes. Glucosides are more hydrophilic than their aglycones, and their greater molecular weight should also limit their absorption (Brown 1988 ). Urinary isoflavones in both studies were 20–35% of ingested doses (Tables 2 , 3) , which were much greater than the percentage of aglycones in total isoflavones of cooked soybean, TVP or soy milk powder. It seems likely that hydrolysis of isoflavone glucosides to their aglycones by ß-glucosidases of gut microflora or foods is needed for soy isoflavone absorption (Xu et al. 1995 ).

Although the four soy foods studied contain various amounts of isoflavone glucosides and aglycones, urinary recovery of either D or G was not significantly different among four soy food treatments (Table 3) . These data suggest that difference in type of soy food does not affect isoflavone absorption and bioavailability, and gut bacterial ß-glucosidases may have similar efficiency of hydrolysis for the various isoflavone glucosides. Similarly, almond ß-glucosidases can hydrolyze the ß-glucosidic bond between the carbohydrate moiety and the isoflavone nucleus regardless of the difference in carbohydrate group (Farmakalidis and Murphy 1985 ). The ß-glucosidases in the human gut may act similarly to almond ß-glucosidase.

Four soybean foods provided similar human bioavailability of isoflavones. Although tempeh may have had somewhat lesser bioavailability than did tofu, soy beans or TVP, in terms of total isoflavones recovered from the dose given, the small number of subjects did not permit the detection of any significant difference among the soy foods studied. There is such great interindividual variability in isoflavone bioavailability (Tables 2 and 3) that such differences might not be easy to detect. The average recovery of isoflavones (% of dose excreted) from the four soy foods tested was about 30% (Table 3) . After feeding single meals (0.9 mg isoflavones/kg body weight) of tofu and TVP to women, total isoflavone recovery was the same with either soy food, ~37% of the dose given (Tew et al. 1996 ). Recovery of isoflavones after soy milk feeding was about 26% (Table 2) . In previous studies, recovery of isoflavones from soy milk was 17% (Xu et al. 1994 ) at each of three single doses (0.7–2.0 mg isoflavones/kg body weight) fed to women, and 14 or 34% in women fed three soy milk-containing meals during 1 d (Xu et al. 1995 ). The difference in isoflavone recovery between the two subgroups of women studied was that women who excreted 10-fold greater amounts of fecal isoflavones excreted more than twofold more urinary isoflavones. It seems that interindividual variation in isoflavone recovery may play a more important role than soy food form in determining human isoflavone bioavailability, but additional studies are needed.

Seemingly, it is only the total amount of isoflavones from the food, rather than the form of food that matters. The ratio of glycone/aglycone forms of isoflavones depends upon the processing of the different soy food forms, but this ratio may not be important to isoflavone bioavailability. A study comparing tofu and TVP (tofu usually contains a two-fivefold greater ratio of glycones to aglycones than does TVP) also showed no difference in isoflavone bioavailability according to soy food, but only according to the amount of each isoflavone in the food (Tew et al. 1996 ). But, a study comparing urinary excretion of isoflavones from tempeh vs. soybean pieces (the tempeh contained a 20-fold greater ratio of aglycones/glycones than did the soy beans) fed as part of all meals over 9 d to 17 men found 70% greater recovery of D when tempeh was fed than after feeding soy bean pieces. G was also recovered to a significantly greater extent after tempeh feeding than after consumption of soy bean pieces (Hutchins et al. 1995 ). In this study, the recovery data represent daily recoveries, rather than recovery of a single dose. The recovery of multiple doses fed during a day seems to be prolonged to about 48 h compared with 24 h for a single dose (see Xu et al. 1995 vs. Xu et al. 1994 ), but total recovery was comparable (14% when three doses of soy milk were given (Xu et al. 1995 ) vs. 17% when one soy milk dose was given (Xu et al. 1994 ). Therefore, study design probably does not account for the difference between the findings of Hutchins et al. (1995) and the present study. It is possible that the gender difference between the two studies accounts for the different results, but a gender difference in gut microfloral ability to metabolize glycosides seems unlikely.

Further studies to clarify longer-term influences on isoflavone bioavailability would be desirable, but short-term studies suggest, in general, that choice of background diet or soy food form would not be crucial determinants of the biological effects of soy isoflavones.

	FOOTNOTES

 
¹ Presented in part at Experimental Biology, April 13, 1995, Atlanta, GA [Xu, X., Wang, H.-J., Murphy, P. A. & Hendrich, S. (1995) Type of soy food does not affect bioavailability of a single dose of soy isoflavones in women. FASEB J. 9: A457.].

² Journal paper No. J-17673 of the Iowa Agriculture and Home Economics Experiment Station, Ames, IA. Project No. 3075, supported by Hatch Act and State of Iowa funds, National Institutes of Health grant CA 56308–02, and the Center for Designing Foods to Improve Nutrition, Iowa State University.

⁴ Abbreviations used: D, daidzein; G, genistein; IC₅₀, concentration causing 50% inhibition of action; ISU, Iowa State University; TVP, texturized vegetable protein.

Manuscript received July 23, 1999. Revision accepted December 6, 1999.

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