Tofu Consumption and Blood Lead Levels in Young Chinese Adults

Changzhong Chen1, Xiaobin Wang2, Dafang Chen3, Guang Li4, Alayne Ronnenberg5, Hirokatsu Watanabe6, Xinru Wang7, Louise Ryan1, David C. Christiani1 and Xiping Xu1,8

1 Department of Environmental Health, Harvard School of Public Health, Boston, MA.
2 Department of Pediatrics, Boston University School of Medicine and Boston Medical Center, Boston, MA.
3 Center for Ecogenetics, Beijing Medical University, Beijing, China.
4 Liaoning Provincial Anti-Epidemic Station, Shenyang, China.
5 Department of Population and International Health, Harvard School of Public Health, Boston, MA.
6 Department of Information Systems, University of Occupational and Environmental Health, Kitakyushu, Japan.
7 Nanjing Medical University, Nanjing, China.
8 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Tofu is a commonly consumed food in China. Tofu may interfere with lead absorption and retention because of its high calcium content. In this observational study, the authors examined whether dietary tofu intake was associated with blood lead levels among young adults in Shenyang, China. The analyses included 605 men and 550 women who completed baseline questionnaires and had blood lead measurements taken in 1996–1998 as part of a prospective cohort study on reproductive health. Mean blood lead levels were 13.2 µg/dl in men and 10.1 µg/dl in women. Blood lead levels were negatively associated with tofu intake in both genders. A linear trend test showed a 3.7% (0.5-µg/dl) decrease in blood lead level with each higher category of tofu intake (p = 0.003). The highest tofu intake group (>=750 g/week) had blood lead levels 11.3% lower (95% confidence interval: 4.1, 18.0) than those of the lowest tofu intake group (<250 g/week). In all regression models, data were adjusted for gender, age, height, body mass index, district, cigarette smoking, alcohol drinking, education, occupation, use of vitamin supplements, season, and dietary intake of meat, fish, vegetables, eggs, and milk. In conclusion, the authors found a significant inverse dose-response relation between tofu consumption and blood lead levels in this Chinese population.

adult; calcium; dietary; lead; linear models; soybeans

Abbreviations: BLL, blood lead level; CI, confidence interval


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Lead is a well-known environmental toxin that affects multiple organ systems in a dose-related fashion (1GoGo–3Go). More than 1 million workers in over 100 different occupations in the United States may be exposed to lead. Lead is also a widely prevalent hazard in China, where the consumption of lead was approximately 180,000 tons in 1975, ranking eighth in the world (4Go). Data from the World Health Organization's Global Monitoring System from 1981–1989 suggested that mean blood lead levels among urban Chinese were 5–13 µg/dl for men and 3–11 µg/dl for women, with the city of Shenyang being ranked as having the highest blood lead levels for both genders (5Go).

Gastrointestinal tract absorption is the major mechanism by which lead enters the human body (6Go). The role of nutritional status in altering susceptibility to lead toxicity has long been recognized (7Go). Mounting evidence suggests that nutritional factors—such as the protein and fat content of foods, as well as dietary intakes of calcium, iron, zinc, and vitamins D and C—influence lead absorption, mobilization, distribution, retention, and excretion (6GoGoGoGoGoGoGoGoGoGoGoGoGoGoGoGoGo–23Go). To date, however, most data have been derived from experimental studies of animals; epidemiologic data on the relation between dietary calcium intake and blood lead levels in humans are scanty, particularly for adults (12Go).

Tofu (soybean curd) is a commonly consumed food in China. Tofu is produced by exposing filtered soybean mash to calcium or magnesium salts, which precipitate the soy solids into a curd. Thus, tofu has a high content of calcium. A variety of metabolic studies have suggested that dietary calcium intake may influence lead absorption and retention among children (21Go) and adults (10Go, 18Go). We hypothesized that higher tofu intake might be associated with lower blood lead levels, particularly among populations with concurrent lead exposure.

In this study, we examined whether tofu consumption was associated with blood lead levels among young Chinese adults. Our analysis was based on blood lead measurements and epidemiologic data obtained from the baseline survey of a large prospective cohort study carried out in Shenyang, China. This population had relatively high lead exposure.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study population
From July 1996 to December 1998, we established a cohort of newlywed couples in two districts (Tiexi and Dadong) in Shenyang, China. The Tiexi district is a heavily industrialized area, whereas Dadong is a residential area. Couples were recruited at the time of marriage registration to participate in a comprehensive prospective study designed to investigate the effects of various environmental and occupational exposures on reproductive outcomes. Women who had been married previously or had a medically diagnosed gynecologic or endocrine disease were ineligible. A consent form was obtained from all participants. This study was approved by the institutional review board of the Harvard School of Public Health.

Baseline survey
Upon enrollment, a physical examination was performed, and height and weight were measured according to a standard protocol. A structured baseline questionnaire was administered by a trained interviewer to all couples at enrollment for collection of information on sociodemographic characteristics, occupational exposures, personal habits such as cigarette smoking and alcohol drinking, living environment, passive exposure to cigarette smoke, and diet. A 10-ml blood sample was collected via venipuncture in a heparinized, metal-free Vacutainer tube (Becton Dickinson, Franklin Lakes, New Jersey) for measurement of blood lead levels.

Dietary assessment
As part of the baseline questionnaire interview, information on dietary intake of tofu, meat, fish, eggs, milk, and vegetables and use of vitamin supplements was obtained. In Shenyang, tofu is consumed in either regular (85 percent) or dried (15 percent) form. Both forms of tofu are sold on the market in units of jin (1 jin = 500 g). The major difference between the two forms of tofu is that the water content of regular tofu is approximately double that of dried tofu. Conversely, the calcium content of dried tofu is approximately double that of regular tofu. Our field interviewers specifically asked the question, "Do you eat tofu frequently (count the yearly averaged weekly intake of regular and dried tofu)?" and provided as choices four categories of weekly intake: <0.5 jin (<250 g), 0.5–<1 jin (250–499 g), 1.0–<1.5 jin (500–749 g), and >=1.5 jin (>=750 g). Intake of dried tofu was converted into equivalent regular tofu intake for coding. All analyses were based on the equivalent regular tofu intake.

Information on intake of meat and fish was obtained in a similar manner. Daily vegetable intake was recorded in categories of <0.2 jin (100 g), 0.2–<0.5 jin (100–249 g), 0.5–<1.0 jin (250–499 g), and >=1.0 jin (>=500 g). Weekly egg intake was categorized as <=2, 3–6, or >=7. Weekly milk intake was ascertained as a specific amount (ml), and intake of vitamin supplements was categorized as use of vitamins A, B, C, and E. In this analysis, however, we collapsed vitamin supplement use into a simple yes/no variable, because fewer than 10 percent of the subjects took any type of vitamin supplement at all.

Sources of lead exposure
Residents of both districts had opportunities for exposure to lead-containing paint and gasoline; lead-based paints are still in use in China, and leaded gasoline was not banned until 1998. Additional sources of lead exposure in Tiexi included a metallurgic plant, a battery plant, and a paint plant.

Blood lead measurement
The first batch of blood samples was transported in heat-insulated boxes at -20°C to a laboratory in Kitakyushu, Japan, and samples were kept frozen until analyzed. The rest of the samples were analyzed at Nanjing Medical University in Nanjing, China, using the same method. The concentration of lead in whole blood was measured with a Perkin-Elmer 5100ZL atomic absorption spectrophotometer (Perkin-Elmer, Norwalk, Connecticut) (24Go).

Statistical analysis
The major question of interest was whether tofu intake would be associated with blood lead levels after data were controlled for intake of other nutrients (meat, fish, veg-etables, eggs, milk, and supplemental vitamins) and population characteristics (gender, age, education, district, occupation, season, cigarette smoking, alcohol drinking, height, and body mass index (weight (kg)/height (m)2)) that might affect blood lead levels (25Go, 26Go). All data were double-entered using Epi Info (version 6.0; Centers for Disease Control and Prevention, Atlanta, Georgia) and then exported to SAS (version 6.12; SAS Institute, Inc., Cary, North Carolina) for analysis.

We first examined the distribution of tofu intakes according to the population characteristics listed above. We performed a chi-squared test to examine differences in tofu intake among various levels of each variable. Because the distribution of values for blood lead level (BLL) was strongly skewed toward the upper end, we transformed blood lead levels to the loge scale for analysis. We then plotted the distribution of loge(BLL) against tofu intake by gender. By inverse transformation, we calculated geometric mean values (and 95 percent confidence intervals) stratified by the individual covariates. We performed a trend test to detect any dose-response trend between tofu intake levels and loge(BLL) within each stratum.

We applied a multiple linear regression model to estimate the independent association between tofu intake levels and loge(BLL), with adjustment for gender, age, education, occupation, cigarette smoking, alcohol drinking, district, season, height, and body mass index, along with use of vita-min supplements and dietary intake of meat, fish, vegetables, eggs, and milk. Adjusted mean values for loge(BLL) were calculated by applying LSMEAN in the PROC GLM procedure in SAS for each category of tofu intake, separately for men and women, and the values were then converted to the non-loge scale by inverse transformation. The parameter estimated from the linear regression model on loge(BLL) was used to calculate a percentage difference and 95 percent confidence interval as (1 - exp(ß ± 1.96 x standard error)) x 100 (where ß is the regression coefficient from the above model). We also calculated the absolute difference (and 95 percent confidence interval) by multiplying the percentage difference by the adjusted mean of the reference group. Finally, we applied multiple logistic regression to estimate the odds ratio (and 95 percent confidence interval) for having an elevated blood lead level, defined as >=25 mg/dl, for higher tofu intake groups compared with the reference group. All p values were two-sided.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A total of 1,155 subjects had complete epidemiologic questionnaires and blood lead measurements from the baseline survey. A total of 465 subjects (257 men and 208 women) were from Dadong (the residential district), and 690 subjects (348 men and 342 women) were from Tiexi (the industrial district). Table 1 shows the demographic characteristics of the study population for the total sample and by district. Subjects in the two districts were similar in terms of age, height, weight, body mass index, education, cigarette smoking, alcohol drinking, and meat, egg, tofu, and fish consumption. The prevalence of cigarette smoking and alcohol drinking was high among men in both areas (63 percent and 64 percent, respectively), whereas very few women were smokers or alcohol drinkers. The majority of subjects (90.8 percent; 1,049 of 1,155) reported no use of vitamin supplements, while 3.2 percent reported taking vitamin C and 2.3 percent reported taking multivitamins. Women tended to have a higher percentage of vitamin supplement use than men (11.1 percent vs 7.4 percent). Subjects from Tiexi (the industrial district) were more likely to be factory workers and they consumed more vegetables, but they were less likely to take vitamin supplements and consumed less milk.


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TABLE 1. Characteristics of the study population in a study of tofu intake and blood lead levels, by district, Shenyang, China, 1996–1998

 
Table 2 presents geometric mean values for blood lead levels across tofu consumption categories, stratified by gender, district, occupation, education, and vegetable intake. Mean blood lead levels were 11.4 µg/dl for men and 8.2 µg/dl for women in Dadong and 14.9 µg/dl for men and 11.4 µg/dl for women in Tiexi. Inverse relations between tofu intake and blood lead levels were noted for almost all strata. Linear trend tests gave statistically significant results for the total sample (p < 0.001) and for most of the strata.


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TABLE 2. Geometric mean values for blood lead levels (µg/dl) across categories of tofu intake, by gender, district, occupation, education, and vegetable consumption, Shenyang, China, 1996–1998

 
Table 3 shows associations between tofu consumption and blood lead levels obtained using linear regression models on loge(BLL), with adjustment for gender, age, height, body mass index, education, occupation, cigarette smoking, alcohol drinking, district, season, vitamin supplement use, and dietary intake of meat, fish, vegetables, eggs, and milk. Compared with the reference group, tofu intake of >=750 g/week was associated with an 11.3 percent (95 percent confidence interval (CI): 4.1, 18.0) or 1.4-µg/dl (95 percent CI: 0.5, 2.2) decrease in blood lead levels. A linear trend test showed a 3.7 percent (95 percent CI: 1.4, 6.0) or 0.5-µg/dl (95 percent CI: 0.2, 0.7) decrease in blood lead levels with each higher category of tofu intake (p = 0.003). Stratified analyses showed that the magnitude of the association between tofu consumption and blood lead levels was slightly greater for men than for women and was greater for the industrial district (Tiexi ) than for the residential district (Dadong). However, the differences in the regression coefficients were not statistically significant between men and women (p = 0.619) or between the industrial and residential districts (p = 0.208).


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TABLE 3. Adjusted* association between tofu intake (in categories) and blood lead levels in the total sample and in subgroups, Shenyang, China, 1996–1998

 
Fifty-three of the subjects (4.6 percent) had elevated blood lead levels, defined as >=25 µg/dl (table 4). Again, logistic regression analysis demonstrated an inverse relation between tofu intake and risk of elevated blood lead levels. Compared with the reference group, the odds ratio for the highest tofu intake group was 0.17 (95 percent CI: 0.05, 0.56); that is, there was an 83 percent reduction in the odds of elevated blood lead levels.


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TABLE 4. Adjusted* odds ratios for elevated blood lead levels (>=25 µg/dl) according to category of tofu intake, Shenyang, China, 1996–1998

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To our knowledge, few population-based studies to date have examined the relation between tofu consumption and blood lead levels. This study had several strengths: The epidemiologic and dietary data were obtained with a standard questionnaire by trained interviewers. The blood lead levels were measured by a credible laboratory according to a standard protocol. We considered and adjusted for a large number of potentially confounding factors. All of the women in this study were nulliparous and fell within a relatively narrow age range, which minimized the confounding effect of age and parity. Most importantly, the study results are robust and consistently demonstrate a dose-response relation between tofu intake and blood lead level defined both as a continuous variable and as a binary variable.

The biologic mechanism by which tofu consumption affects blood lead levels remains to be determined. Gastrointestinal tract absorption is the major mechanism by which lead enters the human body (6Go). The role of nutritional status in altering susceptibility to lead toxicity has long been recognized (7Go). Diets low in calcium (11Go, 20Go, 23Go) have been observed to increase lead uptake from food and to enhance accumulation of lead in the body. Higher milk intake during pregnancy is associated with lower maternal and umbilical cord lead levels in postpartum women (27Go). A cross-sectional study from Mexico (17Go) suggested that consumption of foods high in calcium protects against the accumulation of lead in bones. The biologic interactions between lead and calcium have been recognized for decades. Although these interactions are not well understood, they may involve the following mechanisms: Calcium may compete with lead for intestinal absorption (28Go), and calcium intake may affect osteoporosis, with concomitant lead mobilization from bone (26Go). In addition to calcium, phytic acid chelates metal cations, such as zinc, iron, and calcium (29GoGo–31Go), forming insoluble phytate salts and thus inhibiting mineral absorption. While it is possible that phytic acid inhibits lead absorption, few data on this subject are available. Because tofu has high content of both calcium and phytic acid (the storage form of phosphorus in seeds), it is biologically plausible that tofu may inhibit lead absorption and retention, thus reducing blood lead levels. Conceivably, such an effect should be more prominent in populations with higher concurrent exposure. Consistently, our data showed that the magnitude of association between tofu consumption and blood lead levels was greater for men and for subjects living in the industrial district, who had higher blood lead levels.

Several methodological limitations of our study must be noted. Because of its cross-sectional nature, the study could not define cumulative dietary intake of various nutrients and time-dependent environmental/occupational variables. The information on dietary intake was based on unvalidated self-reports, which were neither comprehensive nor precise. Nevertheless, blood lead levels were objective measurements, and neither the interviewers nor the study participants were aware of subjects' blood lead levels at the time of the survey. Studies have suggested that a number of other nutrients may interact with lead, including iron (8Go), vitamin D (9Go, 32Go), vitamin C (33Go, 34Go), and dietary protein and fat (13Go, 15Go). While our analysis adjusted for intake of meat, fish, eggs, vegetables, and milk, as well as vitamin supplement use, we did not have biochemical measurements of specific nutrients, nor did we have biochemical measurements of specific ingredients in tofu. Tofu is an inexpensive, widely available, and commonly consumed food in China. To our knowledge, tofu intakes are determined mainly by individuals' dietary preferences rather than by personal characteristics. We could not assess the potentially complex interactions of multiple nutrients with lead in this study. Since the study was based on newlywed couples, we are cautious about generalizing the findings to children or older adults. Further research is clearly needed to corroborate our results.

In summary, this large community-based study of young Chinese adults found a significant inverse dose-response relation between tofu intake and blood lead levels. The study findings, if confirmed, will have important implications. Additional research needed includes an intervention study to evaluate whether increasing tofu intake either produces a decrease in blood lead levels or prevents a rise in blood lead levels in response to increased lead exposure. Further elucidation of how tofu (particularly its specific ingredients) interacts with lead may provide additional insight into the biologic mechanisms of absorption, retention, mobilization, distribution, and elimination of lead in humans. From a public health perspective, although controlling environmental sources of lead exposure remains the principal means of preventing lead toxicity, appropriate dietary adjustments may serve as an important adjunct to these measures.


    ACKNOWLEDGMENTS
 
This study was supported in part by grants 1R01 ES08337 and 2 P42 ES-05947 from the US National Institute of Environmental Health Sciences (with funding provided by the US Environmental Protection Agency), grant 1R01 HD32505 from the US National Institute of Child Health and Human Development, and grant 20-FY98-0701 from the March of Dimes Birth Defects Foundation. Dr. Changzhong Chen was supported in part by Fogarty International Center Training Grant TW00828.


    NOTES
 
Correspondence to Dr. Xiping Xu, Department of Environmental Health, FXB101, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02115 (e-mail: xxu{at}hohp.harvard.edu).


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 MATERIALS AND METHODS
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 DISCUSSION
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Received for publication June 6, 2000. Accepted for publication November 15, 2000.





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