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Articles

Validity and Reproducibility of a Self-Administered Food-Frequency Questionnaire to Assess Isoflavone Intake in a Japanese Population in Comparison with Dietary Records and Blood and Urine Isoflavones¹

Seiichiro Yamamoto², Tomotaka Sobue, Satoshi Sasaki, Minatsu Kobayashi, Yusuke Arai^*, Mariko Uehara^*, Herman Adlercreutz, Shaw Watanabe^*, Tosei Takahashi^*, Yoji Iitoi^*, Yasuhiko Iwase^*, Masayuki Akabane^* and Shoichiro Tsugane

National Cancer Center Research Institute, Tokyo and Kashiwa, Japan; ^* Tokyo University of Agriculture, Tokyo, Japan; and Institute for Preventive Medicine, Nutrition and Cancer, Folkhälsan Research Center and Division of Clinical Chemistry, PB60, 14 University of Helsinki, Finland

²To whom correspondence should be addressed. E-mail: siyamamo{at}ncc.go.jp.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Valid food-frequency questionnaires (FFQ) need to be developed to assess isoflavone intake in investigations of its possible association with the lower incidence of breast and prostate cancer in Asian countries. We investigated the validity and reproducibility of isoflavone (daidzein and genistein) intakes from self-administered semiquantitative FFQ used in the JPHC Study (Japan Public Health Center-based Prospective Study on Cancer and Cardiovascular Diseases). We also investigated the number of food items that would be sufficient to ensure validity and reproducibility. We collected FFQ, dietary records (DR), blood and urine samples from 215 subjects among JPHC Study participants, estimated isoflavone intakes from FFQ and DR, and measured serum isoflavone concentration and urine isoflavone excretion. For daidzein, mean intakes estimated from FFQ and DR, serum concentration and urine excretion were 18.3 mg/d, 14.5 mg/d, 119.9 nmol/L and 17.0 µmol/d and for genistein, 31.4 mg/d, 23.4 mg/d, 475.3 nmol/L and 14.2 µmol/d, respectively. Results were similar when analyzed by sex. Spearman correlation coefficients for daidzein of energy-adjusted intakes from FFQ with those from DR, serum concentration and creatinine-adjusted urinary excretion were 0.64, 0.31 and 0.43, respectively. Correlations between two FFQ estimates with a 1-y interval were 0.76. Results were similar for genistein. The shorter version of the FFQ with three items (natto, miso and tofu for miso soup) showed a similar correlation. The original FFQ and the shorter versions have sufficient validity and reproducibility to be used in epidemiologic studies.

KEY WORDS: • Isoflavone • validity • semiquantitative food-frequency questionnaire • dietary record • biomarker • JPHC Study

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Asian countries such as Japan have lower incidences of breast and prostate cancer than Western countries. A major reason for the disparity may be the difference in diets, including differences in soybean intake. Soybeans are a major source of isoflavones, one group of phytoestrogens. Many experimental studies have shown anticarcinogenic effects of soy or genistein on hormone-related cancers, which may be related to their estrogenic, antiestrogenic or other effects (1 –3) . In addition, their anticarcinogenic effects on other cancers such as colon and liver cancer have also been demonstrated in experimental studies. Other possible mechanisms by which soybean isoflavones may be anticarcinogenic include inhibition of protein tyrosine kinases and other enzyme activities, stimulation of sex hormone–binding globulin production, antioxidant effects and inhibition of angiogenesis (1 ,2 ,4) . Contrary to the results from experimental studies, epidemiologic studies have not provided sufficient evidence of an association between isoflavone intake and cancer (5) . Studies to investigate such an association should be conducted in Asian countries because isoflavone intakes vary more widely than in Western countries. Unfortunately, however, an association between isoflavone intake and cancer has not been reported from Asian countries. One reason is that no validated tools exist that can be used in epidemiologic studies to estimate isoflavone intake.

In this study, we developed estimation methods of isoflavone intake using a semiquantitative food-frequency questionnaire (FFQ)³ and evaluated its validity and reproducibility. This FFQ was originally developed and used in the 5-y follow-up survey of the Japan Public Health Center-based Prospective Study on Cancer and Cardiovascular Diseases (JPHC Study), which is an ongoing large-scale cohort study, including 140,000 Japanese subjects (6 ,7) . The present study was conducted as a part of validation studies for the FFQ of the JPHC Study Cohort I (8 ,9) . Estimated isoflavone intakes from FFQ were compared with those from dietary records (DR), serum isoflavone levels and urinary isoflavone excretion to investigate their validity. Reproducibility of the FFQ estimates was also investigated by comparing two FFQ estimates. The association between the biomarkers and DR estimates was also studied. In addition, we investigated how many food items are sufficient to ensure validity and reproducibility.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Study subjects were a subsample of the participants in the JPHC Study Cohort I. A total of 247 subjects [122 men and 125 women, 56 from the Ninohe public health center (PHC) area in Iwate Prefecture, 71 from the Yokote PHC area in Akita Prefecture, 60 from the Saku PHC area in Nagano Prefecture and 60 from the Ishikawa PHC area in Okinawa Prefecture] volunteered initially. The subjects provided 7-d DR four times (a total of 28 d) in different seasons of the year, i.e., winter (February-March), spring (May-June), summer (August-September) and autumn (November-December) in 1994. In the Ishikawa PHC, with its subtropical climate, 7-d diet records were collected only twice (winter and summer, 1994), because seasonal variations are expected to be small. Mean ages were 55.6 y for men and 55.3 y for women. Mean height, weight and body mass index were 164.5 cm, 65.8 kg and 24.3 kg/m², respectively, for men and 151.1 cm, 53.3 kg , 23.9 kg/m², respectively, for women. The mean intakes of energy, protein, total fat and carbohydrate were 9816.9 kJ/d, 92.9 g/d, 59.2 g/d, 316.8 g/d, respectively, for men and 7612.8 kJ/d, 76.2 g/d, 52.9 g/d, 256.9 g/d, respectively, for women. These figures were close to those reported in the National Nutritional Survey among similar age groups in the same year for both sexes (10) .

We collected semiweighed (weighed or portion size) DR over seven consecutive days. Research dietitians instructed the subjects to record all foods and beverages prepared and consumed in a specially designed booklet. The participants were asked to provide detailed descriptions of each food, including the method of preparation and recipes whenever possible. The dietitians checked the records at each subject’s home, work place or community center during the survey and reviewed them in a standardized way after completion. The mean daily consumptions of energy and three major nutrients were calculated from the records using the Standard Food Composition Table published by the Science and Technology Agency of Japan in 1982 (11) .

Urine samples (24-h) were collected voluntarily on any day during a 7-d DR in spring and autumn (urine samples were not collected from the subjects in the Ishikawa PHC area). A simple portable device (Urine Mate P, Sumitomo Bakelite, Tokyo) was used for the collection. After measurement of the total urine volume, samples were stored frozen at -80°C until analysis.

Three months after the subjects completed the dietary records (February 1995 in three PHC areas and February 1996 in the Ishikawa PHC area), they were requested to fill in the FFQ to evaluate its validity. The isoflavone intake estimated by FFQ was compared with that estimated by DR or by results obtained from the biological specimens. Subjects were also asked to fill in the FFQ 1 y later (February 1996) in three PHC areas and 1 y before in the Ishikawa PHC area to evaluate the reproducibility of the FFQ. For the estimation of isoflavone intakes from the FFQ, the same composition table was used as for the estimation from DR. The results for daidzein and genistein, the main soy isoflavones, are presented.

In this observational study, study participation and all of the data collection were on a voluntary basis. Oral informed consent was obtained from all of the subjects.

Estimation of isoflavone intake from DR and FFQ.

Subjects with complete dietary records (i.e., 28 d for the Ninohe, Yokote and Saku areas and 14 d for the Ishikawa area) and the first FFQ were used for the analysis (total 215, including 102 men and 113 women). The isoflavone intakes were estimated using the specially developed food composition table for isoflavones in Japanese foods (12 ,13) . DR estimates were calculated as the mean intakes over 14 d (Ishikawa) or 28 d (other three areas). FFQ estimates were calculated using the following eight items in the FFQ: miso (fermented soybean paste) soup, tofu for miso soup, tofu for other dishes, yushi-tofu, freeze-dried tofu, deep-fried tofu, natto (fermented soybeans) and soymilk. For miso soup, the questions on frequency of intakes ranged from almost none to 1–3 d/mo, 1–2 d/wk, 3–4 d/wk, 5–6 d/wk and daily. The questions on number of bowls consumed ranged from 1, 2, 3, 4, 5, 6, 7–9 to 10 per day. The relative salt content, which corresponds to the relative miso content, was classified as less salty, medium and salty. For other items, except soymilk, the frequency and relative portion sizes were requested. The categories of frequency ranged from none to 1–3 times/mo, 1–2 times/wk, 3–4 times/wk, 5–6 times/wk, once/d, 2–3 times/d, 4–6 times/d and 7 times/d. The portion sizes were set as follows: 20 g (tofu for miso soup), 75 g (tofu for other dishes), 150 g (yushi-tofu), 60 g (freeze-dried tofu), 2 g (deep-fried tofu) and 50 g (natto). The categories of relative portion size ranged from small (50% smaller) to medium, and large (50% larger). Because only frequency (same categories as others) was asked for soymilk, 200 mL was used as the portion size. Isoflavone intake was estimated by the frequency, portion size, relative portion size and isoflavone content in the food composition tables. The relative salt (miso) content (0.75 for less salty, 1 for normal and 1.3 for salty) was also used for the calculation of isoflavone intake from miso soup.

From the subjects with complete dietary records a second FFQ was obtained and analyzed for 93 men and 109 women to investigate FFQ reproducibility.

The validity and reproducibility of the "hypothetical" shorter versions of the original FFQ (i.e., 8 items) were investigated to assess isoflavone intake. The hypothetical shorter versions were constructed as follows: combinations of 2–7 food items from the original FFQ, and 8 single food items, each of which was included in the original FFQ.

Analysis of serum isoflavones.

Serum taken in the winter session was used for the study. Among the subjects with complete dietary records, serum was obtained and analyzed for 93 men and 109 women. A sensitive and convenient time-resolved fluoroimmunoassay (TR-FIA) method was used for analysis of serum isoflavones (14) at Helsinki University.

For the recovery calculation, 20 µL of ³H-estradiol glucuronide was added to tubes containing 200 µL of serum. After mixing and equilibrating for 30 min at room temperature, 200 µL of 0.1 mol/L acetate buffer (pH 5.0) containing 200 U/L glucuronidase and 2000 U/L sulfatase was added to the tubes. After mixing using a Vortex mixer and incubation overnight at 37°C, 2.0 mL of diethyl ether was added, and the phytoestrogens were extracted after equilibrating the phases with a Vortex mixer. The water phase was frozen in a solid carbon dioxide/ethanol mixture, and the ether phase was transferred into disposable glass tubes. After thawing, the water phase was reextracted with the same amount of ether, and the ether phases were combined and evaporated completely in a 45°C water bath. Then 200 µL of 50 mmol/L Tris-HCl buffer containing 5 g/L bovine serum albumin (pH 7.8) (assay buffer) was added to the tubes containing the dry residues; after thorough mixing, 20 µL (in duplicate) of the solution was taken for TR-FIA of each compound. This volume corresponds to 20 µL of the original serum sample. The samples giving a value outside the range of the standard curve were diluted with assay buffer. Another 20 µL of the solution was taken for liquid scintillation counting for determination of recovery. On the basis of these results, the final values were corrected for losses during hydrolysis and extraction.

Standard or hydrolyzed and extracted serum (20 µL) was pipetted into prewashed goat anti rabbit immunoglobulin G microtitration wells. To each well was added 100 µL of a polyclonal antiserum (dilution of 1:40,000 for daidzein and 1:50,000 for genistein) in assay buffer and 100 µL of europium-labeled daidzein or genistein (dilution 1:40,000 and 1:400,000 for daidzein and genistein, respectively). After incubation and shaking the strips slowly on a DELFIA plate shaker (Wallac, Turku, Finland) at room temperature for 90 min, the strips were washed with a DELFIA plate washer (using the no. 29 T3 program). Enhancement solution (200 µL) was added to each well, and the strips were shaken slowly for an additional 5 min. The enhanced fluorescence was measured in a VICTOR 1420 multilabel counter (Wallac, Turku, Finland). Complete validation of the method has been published (14) .

Calculation of the serum isoflavone concentration was done according to the formula: serum isoflavone (nmol/L) = concentration (read) x 1/recovery x dilution factor (nmol/L).

Analysis of urinary isoflavones.

The 24-h urine samples taken in the spring session were used for the study. Among the subjects with complete dietary records, urine samples were obtained and analyzed for 33 men and 60 women. Creatinine and isoflavones were measured in the urine samples. Creatinine was analyzed by Jaffe’s procedure. The urinary isoflavones and metabolites were analyzed at Tokyo University of Agriculture using the extraction method of Adlercreutz et al. (15) combined with the modified HPLC method described by Gamache et al. (16) . For the recovery calculation, 20 µL of ³H-estradiol glucuronide was added to the tubes containing 1 mL of urine. After mixing and equilibrating for 30 min at room temperature, 0.5 mL enzyme solution [0.5 mL Helix pomatia juice (Type HP-2S, Sigma, St. Louis, MO) in 10 mL of 0.2 mol/L acetate buffer (pH 4.0) containing 0.15 g ascorbic acid] was added to the tubes. After mixing, the sample was hydrolyzed overnight at 37°C and then extracted twice with 5 mL diethyl ether, and the ether fraction was evaporated to dryness under a flow of nitrogen gas. The residue was dissolved in 0.2 mL methanol, and a 20-µL sample was injected onto a HPLC column with diode-array UV detection, scanning from 250 to 400 nm (Beckman Coulter K.K., Tokyo, Japan). Another 20 µL of the solution was taken for liquid scintillation counting for a determination of recovery. Peaks were detected at 254 nm for daidzein and genistein and at 280 nm for equol and O-DMA. The HPLC column was ODS-80Ts-Qa (150 x 4.6 mm i.d., 5-µm particle size; Tosoh, Tokyo, Japan) with a guard column (TSKguardgel ODS-80Ts, 1.5x3.2 mm i.d., 5-µm particle size; Tosoh), and temperature was kept at 25°C using a column oven. HPLC analysis was carried out by linear gradient, from 1.5:0.5:8.0 [methanol/acetonitrile/0.2 mol/L acetate buffer (pH 4.0), v/v/v] to 6.0:3.0:1.0 for 45 min, returning to its initial condition for 5 min. The flow rate was 1.0 mL/min.

Quantification was done by measuring peak areas based on calibration plots of the peak area of standards at various concentrations (from 4 to 160 µmol/L) and corrected for losses during hydrolysis and extraction based on the recovery data. All solvents and chemicals were of HPLC grade or analytical grade.

Intra- and interassay CV for the present method were assessed by repeated measurement of isoflavones in three urine samples with different concentrations. Both intra- and interassay CV were <10% in the three different concentrations.

Calculation of urine isoflavones was done according to the formula: urine isoflavones (µmol/d) = concentration (µmol/L) x1/recoveryx urine volume (L/d).

Statistical analysis.

Mean, standard deviation and quartiles of the distribution were calculated to compare the distribution of FFQ estimates, DR estimates, serum levels and urine excretions. To check the normality of the distribution, skewness and kurtosis were calculated. To compare the means, t test was used. The contribution of food items to DR estimates and FFQ estimates was also examined. To investigate the validity of the intake estimates from FFQ, correlation coefficients among FFQ estimates, DR estimates, serum levels and urine excretion were calculated. Correlation coefficients with energy-adjustment (intake estimates) and creatinine-adjustment (urine excretion) were also calculated. Energy and creatinine were adjusted by residual methods. Seasonal variation in DR estimates and their correlation with other estimates were also investigated. Reproducibility of FFQ estimates was evaluated by correlation coefficients between two FFQ estimates. All of the correlation coefficients are shown with their 95% confidence interval to evaluate the accuracy of the estimates. Validity and reproducibility of the shorter versions of the original FFQ were also investigated by the analysis described above. All analyses were conducted by sex, but results were pooled when there were no gender differences. Statistical analysis were conducted using SAS Software version 6.12 (SAS Institute, Cary, NC).

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The distribution of FFQ estimates, DR estimates, serum levels and urine excretion of isoflavones are shown in Table 1 . Skewness and kurtosis showed different patterns among the estimates. Only DR estimates showed approximate normality. Estimated mean intakes were higher as assessed by FFQ than by DR (P < 0.001). Variations in intake were greater in FFQ estimates than in DR estimates in terms of standard deviations, interquartile ranges and skewness.

The contribution of food items to DR and FFQ estimates are shown in Table 2 . Food items appearing in the DR, originally categorized by the items in the standard food composition table (14) , were categorized into the same items in the FFQ. Only four items (tofu for miso soup, other tofu, miso and natto) contributed >80% of total isoflavone intake in both the DR and FFQ estimates, although natto’s contribution was higher in the FFQ estimate.

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

In epidemiologic studies, biochemical indicators of dietary intake have great intuitive appeal as the gold standard with which to assess the validity of a dietary questionnaire. The fundamental advantage of using a biochemical indicator is that measurement errors should be essentially uncorrelated with errors in any dietary questionnaire. Furthermore, biochemical indicators are unlikely to be influenced by dietary intake alone because individuals generally differ to some degree in their absorption and metabolism in addition to the variations of the diurnal or menstrual cycles. Thus, the capacity to demonstrate a correlation between the questionnaire assessment of intake and the biochemical indicator provides almost unquestionable qualitative documentation of validity. Our correlation coefficients between the FFQ and serum level/urinary excretion were 0.3, even for the shorter version. These are comparable to those for the well-established questionnaire used to assess other nutrients (17) .

According to the above-mentioned criteria, our FFQ has sufficient validity and reproducibility to estimate isoflavone intake to be used in epidemiologic studies. The shorter version of FFQ with at least three items (natto, miso, tofu for miso soup) has sufficient validity and reproducibility and the one-item FFQ such as natto and miso may be sufficient. Our correlations among FFQ, DR and urine excretion were similar to those in Japanese in the United States assessed using the Block FFQ, which was modified for Japanese by the addition of 58 items (18) .

These isoflavone intakes, blood concentrations and urine excretions were comparable to those cited in other reports of Japanese subjects and higher than those for Western populations. Daidzein intake estimates of our subjects were 7 times higher than those of Chinese in Singapore, and 700 times higher than for U.S. Caucasians (13 ,18 –21) . A similar, although less striking discrepancy was observed for biomarkers. Blood daidzein concentrations in our subjects were 15 times higher than those in Finnish omnivorous subjects and 3 times higher than those in Finnish vegetarians (14 ,22 –24) . Urine daidzein excretion in our subjects was 50 times higher than those in Finnish omnivorous subjects and 3 times higher than those in American macrobiotics (22 ,25 –28) .

Correlation coefficients of energy/creatinine-adjusted intake were higher than those of nonadjusted intakes among FFQ vs. DR and FFQ vs. urine. These three estimates (FFQ, DR and urine) have the dimension of 1/d and are influenced by body size. Energy/creatinine adjustment can reduce the influence of body size, resulting in a possible increase in the correlation between adjusted estimates. In contrast, not only did correlation coefficients with serum levels not increase after energy/creatinine adjustment, some of them actually decreased after the adjustment. Such decreases may be due to errors in energy intake estimates.

FFQ estimates tended to be larger than the DR estimates although the correlation was high. This overestimation was largely due to the overestimation of isoflavone intake from natto (Table 2) . Although the contribution of natto was 16.5% in DR daidzein estimates, the corresponding figure was 33.9% in FFQ estimates. Because correlations between natto and other estimates were high (Table 5) , the natto portion size used may have been inappropriate. Although the natto portion size was shown as 50 g in the FFQ, 20 g may be a more appropriate amount to prevent overestimation of FFQ estimates.

Our study subjects were a subsample of the JPHC Study, which took place in a Japanese population. However, the subjects were not necessarily representative of all of the JPHC Study subjects because they were volunteers and possibly more health conscious than other subjects. This might suggest that the correlations of FFQ estimates and others observed in this study were slightly higher than in the general population.

Another limitation of the study was that a single urine and blood sample was used, although we collected two urine and blood samples for each subject. This may lead to the low correlation between FFQ and DR intake estimates and biomarkers because the single measurement has larger measurement error than the means over repeated samples. However, correlations between FFQ and DR intake estimates and single biomarker measurements were sufficiently high to be used in epidemiologic studies.

FFQ estimates correlated consistently with four season-specific DR estimates. Serum levels also correlated consistently with four season-specific DR estimates although correlations were lower than with FFQ estimates. Urine isoflavones in samples collected in the spring session had a higher association with DR estimates in the spring session compared with FFQ estimates and serum levels, but the lowest association with the DR estimates in other seasons. This suggests, in terms of estimating intakes, that FFQ are the most appropriate measure for long-term isoflavone intake, serum levels are the second best, and that urine excretion levels, although not appropriate for long-term may be the most appropriate measure for estimating short-term intakes. In experimental studies, the peak concentrations of daidzein and genistein in human plasma are generally seen 4–8 h after the ingestion of glycosides (29 –32) . Most of the daidzein and genistein in urine reaches a peak after 8–12 h and is excreted within 48 h after ingestion (30 –33) . There is little difference in the apparent peak time of isoflavones in biological fluids among races, although differences are observed in absolute levels due to interindividual variations in bioavailability (30 ,31 ,34 ,35) .

The correlations between the intake estimates and biomarkers observed for daidzein were similar to those for genistein. This is due in part to the fact that the ratio of genistein to daidzein in food composition tables did not vary greatly (one- to twofold with few exceptions) among food items.

This study showed the high validity and reproducibility of a FFQ to assess isoflavone intake in a Japanese population using 8 items. This suggests two possibilities. Isoflavone intake can be estimated by a simpler FFQ with fewer items in an Asian population. This means that it may be possible to investigate the association between isoflavone intake and cancer in cohort studies, even if the study has been conducted in the past without validation of isoflavone intake. Another possibility is to obtain improved intake estimates by changing the portion size such as we did with natto in our FFQ. This may lead to the development of estimation methods by FFQ that can circumvent the risk of overestimation. In that case, recommended intakes of isoflavones can be proposed using FFQ data if isoflavone intake proves to be effective in preventing cancer.

	ACKNOWLEDGMENTS

 
The authors wish to express their appreciation to the local staff in each study area, especially to the following dietitians for their painstaking efforts to conduct the dietary survey: Yuko Hatakeyama, Mayumi Morimoto, Masako Makino, Manami Nishizawa, Misako Tawada, Noriko Kamiunten and Satoko Takamori. We are also grateful to Walter Willett and Kazuko Yoshizawa at the Department of Nutrition, Harvard School of Public Health, for their helpful comments in designing the study.

	FOOTNOTES

 
¹ Supported by Grants-in-aid for Cancer Research, by the second Term Comprehensive Ten-Year Strategy for Cancer Control and by Research on Environmental Health from the Ministry of Health, Labour and Welfare of Japan and for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan.

³ Abbreviations used: DR, dietary record; FFQ, food-frequency questionnaire; JPHC Study, Japan Public Health Center-Based Prospective Study on Cancer and Cardiovascular Diseases; PHC, public health center; TR-FIA, time-resolved fluoroimmunoassay.

Manuscript received March 29, 2001. Initial review completed May 22, 2001. Revision accepted July 10, 2001.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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