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Exposure to bisphenol A among school children in eastern China: A multicenter cross-sectional study

Abstract

Bisphenol A (BPA) is one of the highest production and consumption volume chemicals in the world. Although exposure of children to BPA has been studied in Western countries, little is known about its level in China. In this study, total BPA was measured in the morning urine samples of 666 school children aged 9–12 years from three regions in eastern China in 2012. A rapid and sensitive ultraperformance liquid chromatography (UPLC) tandem mass spectrometry (MS/MS) method was used for the measurement and urinary concentrations of BPA were presented as unadjusted (ng/ml), creatinine-adjusted (μg/g creatinine) and specific gravity (SG)-adjusted (ng/ml) forms. BPA was detected in 98.9% of urine samples with their unadjusted concentrations ranging from 0.1 to 326.0 ng/ml (LOD=0.06 ng/ml), indicating that the exposure of BPA was common for school children living in eastern China. The geometric mean and median of BPA was 1.11 ng/ml (creatinine-adjusted: 2.32 μg/g creatinine; SG-adjusted: 1.17 ng/ml) and 1.00 ng/ml (creatinine-adjusted: 2.22 μg/g creatinine; SG-adjusted: 1.07 ng/ml), respectively. The highest urinary BPA level was found in the age group of 12 years with GM concentration of 1.55 ng/ml, and it decreased with decreasing age (11 years: 1.18 ng/ml; 10 years: 1.05 ng/ml; and 9 years: 0.99 ng/ml), but there was a lack of consistency for age associated with BPA levels in three study areas. The estimated daily intake of BPA (0.023 μg/kg bw/day) was much lower than the tolerable daily and reference dose of 50 μg/kg bw/day recommended by either the European Food Safety Authority or the US Environment Protection Agency. There was no significant difference in urinary BPA concentrations between children who were overweight or obese and those with normal weight (P=0.26), whereas BPA daily intake was unexpectedly higher among normal-weight children (P=0.003). Compared with creatinine correction, the correction method of specific gravity is preferred to evaluate BPA exposure for children.

INTRODUCTION

Bisphenol A (BPA) is primarily used in the production of polycarbonate (PC) plastics and epoxy resins that are widely found in various products of daily life such as reusable bottles, electronic equipment, medical devices (e.g., dental sealants) and plastic containers. To protect food and drinks from direct contact with metals, epoxy resins are also used in the internal coating of food and beverage cans. With an annual production of more than 3.5 million tons, BPA has been one of the highest volume chemicals produced worldwide.1 The total production capacity of BPA added up to 4.7 million tons in 2007, and 43.5% of the global output originally came from the Asian region.2 Over the past few years, the strongest growth of BPA market worldwide happened in China, and the volume of BPA consumption grew from 1.06 × 105 to 5.70 × 105 tons in mainland China during 2001–2007, with an estimate of demand for BPA (mainly polycarbonate and epoxy resins) of 2.25 × 106 tons in 2010.3

BPA is considered as a suspected environmental endocrine disruptor that has been shown to interfere with human reproductive or developmental system. Recently, it has been reported that BPA increases carcinogenic risk, the risks of cardiovascular diseases and diabetes in adults4, 5 and childhood obesity.6, 7 BPA has been detected in different types of media including soil, sediment, air, municipal waste and food.2 People can be exposed to BPA through a variety of sources.8 The major route of human exposure to BPA seems to be the dietary pathway.9, 10 Once ingested, BPA is efficiently absorbed (>95%) and is rapidly and mainly excreted in the urine as BPA conjugates. The urinary concentration of total (free plus conjugated) BPA has often been used to evaluate the exposure level of BPA from all sources.1 Studies of BPA metabolites in urine specimens from various regions such as the United States, Germany and Japan,11, 12, 13, 14 have indicated a widespread exposure of human to BPA, and most of these studies were conducted in developed countries and in adults. Other studies have detected a high level of urinary BPA in school children.11, 15, 16 Although the production and consumption of BPA is rapidly increasing in China, there is limited information on human exposure to BPA for Chinese population, especially for Chinese children. A recent study conducted in the southern China found that BPA was 100% detected in the urine of children aged 324 years, with a geometric mean (GM) concentration of urinary BPA being 3 μg/l (2.75 μg/g creatinine, LOD=0.9 ng/l).17 Another study on a Chinese population showed that urinary BPA level and detectable rate were higher in the younger than the older age groups.18 Young children may be more susceptible to BPA exposure in daily life because of using plastic bottles or drinking bottled beverages.

The objectives of the current study were to quantify the urinary BPA concentrations in spot morning voids in a cohort of Chinese children and to estimate their daily intake doses of BPA using urinary biomonitoring according to gender, age and body mass index (BMI). In addition, we compared the specific gravity (SG) and creatinine methods for adjusting urinary BPA concentrations and to determine the preferable one for correction. To our knowledge, it is the first multicenter study of children’s exposure to BPA in China.

MATERIALS AND METHODS

Study Population

This study population comprised subjects from three sites representing three important regions of Yangtze River Delta in China, Shanghai City, Jiangsu Province and Zhejiang Province, known as the regions to produce the largest volumes of BPA commercially in China because of their developed manufacturing.3 One primary school was randomly selected from local primary schools in each of the three sites, including Minhang District (Shanghai), Haimen City (Jiangsu Province) and Yuhuan County (Zhejiang Province) (Supplementary Figure S1 and Supplementary Files). In each selected school, children were randomly chosen from grades 3–5 on the basis of the annually regular physical examination. Those with liver, kidney or endocrine diseases were excluded. A total of 1050 students aged 9–12 years were recruited, and 968 students accepted to participate. The study was approved by the Ethical Review Board of Fudan University School of Public Health. Guardians provided a written informed consent before participating.

Overweight and obesity were defined according to the BMI criteria proposed by the Working Group on Obesity in China (WGOC) (Supplementary Table S1).19 Information on body weight and height was obtained from annual regular physical examinations.

Sample Collection

First morning urine was collected at home by participants themselves or with the aid of their guardians at the same day as annual regular physical examination. Spot urine samples were collected in 25 ml polypropylene tubes. All the participants were told to avoid contact of urine with plastic products in the process of urine collection to minimize the contamination of BPA. The samples were transported to laboratory as soon as possible, split into three aliquots with 5 ml polypropylene tubes and stored at −80 °C until analysis. All urine samples were collected during the period from March to May 2012.

Standard and Sample Analysis

BPA standard was purchased from Cambridge Isotope Laboratories (Cambridge, MA, USA). BPA-d16 was used as an internal standard and was obtained from Cambridge Isotope Laboratories. BPA in urine was analyzed using the method that has been previously published.20 Briefly, 20 μl of BPA-d16 (1.6 μg/ml) was spiked into 1 ml of the urine sample. Then, each sample was buffered with 200 μl of 1.0 M ammonium acetate buffer (pH 5.0), and 15 μl of β-glucuronidase from Helix pomatia (type H-2, Sigma-Aldrich) was added. The mixture was incubated overnight at 37 °C for deconjugation. Oasis MAX mixed-mode solid-phase extraction (SPE) cartridge (combining reversed-phase and anion-exchange mechanisms, 150 mg/6 ml; Waters, Milford, MA, USA) was preconditioned with 4 ml of methanol and 4 ml of pure water. BPA was eluted from the cartridge with 5 ml of methanol after 4 ml of 30% methanol solution and 4 ml of 30% methanol solution containing 1% formic acid were used to remove urine impurities of different pH. The eluates were concentrated to dryness under a gentle stream of nitrogen. The final mixture after derivatization by dansyl chloride was homogenized for analysis by ultraperformance liquid chromatography (UPLC) coupled with triple quadrupole mass spectrometry (MS/MS).

An Acquity UPLC system connected to a Xevo TQ-S triple quadrupole mass spectrometer with an electrospray ionization (ESI) source (Waters) was used for the measurement of BPA. Chromatographic separation was achieved using a C18 column (Acquity UPLC BEH C18, 100 mm × 2.1 mm × 1.7 μm). BPA was detected in positive ion mode with a mobile phase of methanol/water containing 10 mM ammonium formate, both at a flow rate of 0.3 ml/min. The mobile phase gradient was as follows: 0 min (20%), 3.0 min (50%), 6.0 min (80%), 9.0 min (95%), 11.0 min (100%), 11.5 min (20%) and 14 min (20%). Multiple-reaction monitoring (MRM) mode was used for the quantitative analysis of these compounds. MS/MS parameters were optimized by direct syringe infusion of BPA into the mass spectrometer. The method limit of detection (LOD) for BPA was 0.06 ng/ml.

Urinary SG and creatinine levels were detected for the correction of urinary dilution. SG was measured using a handheld refractometer (Atago PAL 10-S; Tokyo, Japan). All samples were sent to a local hospital to analyze the creatinine concentrations by an enzymatic method in which 1 ml urine was needed. The results were obtained using automatic biochemical analyzer (ARCHITECT C8000, Abbott Laboratories, IL, USA).

Quality Assurance/Quality Control

Three field blanks were taken in each individual sampling site in order to assess the possible contamination. For each batch of 90 samples analyzed, 4 reagent blanks and 4 urine samples spiked with BPA at three different spiking concentrations (5, 10 and 50 ng/ml) were processed to check the background values of our laboratory, and stability and accuracy of this monitoring method. New calibration standards were prepared at the beginning of every batch of samples analyzed, with concentrations ranging from 0.1 to 200 ng/ml (6 levels included). During instrumental analysis, as a check for the drift of chromatographic retention time, the change of instrumental sensitivity and cross-contamination between urine samples, a midpoint calibration standard was injected after every 10 samples. The LOD was calculated as a signal-to-noise ratio of 3, from the chromatograms of urine samples spiked with the lowest concentration of analyte tested.

The study samples were analyzed in 12 separate batches configured with 12 internal standard curves, including 48 reagent blanks and spiked urine samples. The correlation coefficient of calibration curves was 0.992. The BPA retention time variation was <2% and the cross-contamination between urine samples was not found. The average recovery and relative standard deviation (RSD) of BPA from spiked matrix were 95.6% and 4.0% at the spiked samples. To help reduce variability in BPA concentrations related to fluctuations in urine output, results were adjusted for both creatinine levels and SG.

We analyzed three standard samples with different creatinine levels per 100 urine samples, and the quality control chart is presented in Supplementary Figure S2.

Statistical Analysis

In the data analysis, descriptive statistics (25th and 75th percentiles, median, arithmetic mean (AM), GM and its 95% confidence interval) were calculated. BPA concentrations below the LOD were assigned a value of LOD divided by the square root of 2 or by 2 in the computation of GM and AM, respectively.21, 22 Besides the original unadjusted urinary BPA concentrations, we adjusted urinary BPA concentrations for both creatinine and SG. SG-adjusted urinary BPA concentrations were calculated by the formula Pc=P[(1.022-1)/(SG-1)], where Pc is the SG-adjusted BPA concentration (ng/ml), P is the measured unadjusted urinary BPA concentration, 1.022 is the sample population median SG value, and SG in the formula is the measured specific gravity for each urine sample.23

In order to make comparisons with other studies, we estimated daily intakes of BPA by calculating: daily intake (ng/day)=urinary BPA concentration (ng/ml) × urinary output (ml/day), and daily intake (ng/kg body weight/day)=urinary BPA concentration (ng/ml) × urinary output (ml/day)/body weight (kg).24 For practical reasons, no 24 h urine excretion rates were collected for the children. Therefore, generic values based on age and gender were used to describe urinary output.25, 26 We divided children into two age groups (≤11 and 12 years). The ICRP reference value for 15-year-old children was used for the 12-year age group (1200 ml/day) and the ICRP value for children aged 10 years was used for the ≤11-year age group (700 ml/day).

Given the large variations in BPA concentrations, a natural log-transformation was used. The data still failed to obey the normal distribution after transformation (P<0.001). Therefore, Kruskal–Wallis H-test was used to compare urinary BPA concentrations and estimated daily children’s intakes of BPA according to resident area and age. The χ2 test for trend was used to explore the age-related change of urinary BPA levels. Differences in urinary BPA levels and BPA daily intakes between different genders and BMI groups were tested using the Mann–Whitney U-test. Spearman’s rank correlation coefficient was used to examine the relationships between creatinine-adjusted and SG-adjusted values of BPA concentrations. Data analyses were performed using SPSS version 17.0 (SPSS, Chicago, IL, USA). Statistical significance was set at P<0.05, two tailed.

RESULTS AND DISCUSSION

Of the 968 subjects with urine samples, 165 were excluded from the analysis because of a lack of demographic information. When we adopted the guidelines of the US Department of Transportation to determine valid creatinine concentration of urine for correction (≥5 mg/dl),27 4 urine samples were too dilute to be included. None of the urinary creatinine concentrations were >300 mg/dl, considered too concentrated according to WHO.28 In our study, specific gravity that ranged from 1.010 to 1.030 was considered valid. Therefore, 133 urine samples were excluded. Finally, a total of 666 urine samples were analyzed. The demographic characteristics between the children included and excluded were similar (Supplementary Table S2).

Concentrations and Profiles

Of the 666 subjects, 346 (52%) were male and 320 (48%) were female. The age distribution is presented in Supplementary Table S3. BPA was detected in 98.9% of the samples with concentrations ranging from 0.1 to 326.0 ng/ml. Concentrations and profiles of BPA by study areas are shown in Table 1.

Table 1 Concentrations of urinary BPA (unadjusted (ng/ml), creatinine adjusted (μg/g) and SG adjusted (ng/ml)) in Chinese school children.

The GM and median concentrations of BPA for all subjects were 1.11 (95% confidence interval: 1.02–1.21 ng/ml) and 1.00 ng/ml, respectively. The medians of creatinine-adjusted and SG-adjusted urinary BPA concentrations were 2.22 μg/g and 1.07 ng/ml, respectively. In this study, significant differences in the concentrations of BPA were observed among three sites (P<0.001, Supplementary Table S4). The average level of BPA was the highest in Yuhuan (median 2.20 ng/ml), nearly 3 times higher compared with Haimen (0.80 ng/ml) and Minhang (0.70 ng/ml). No difference in the urinary BPA concentrations was found between the latter two sites (P=0.48). Yuhuan is located in an island in Zhejiang Province. Abundant natural resources and developed waterway transport provide some major advantages that allow Yuhuan to become one of the largest production bases in China, and this may cause comparatively serious BPA pollution. In addition, the local people have a greater chance of having access to the seafood polluted by the BPA and plenty of seafood packaging products like canned fish that may contain BPA.9 Therefore, these unique geographical environment and lifestyles could have a negative effect on the exposure of BPA to local people, especially children. No significant difference existed in urinary BPA concentrations between males and females for all subjects (P=0.26), which was similar to the results from several other studies.11, 13 Our study showed that children who were overweight or obese tended to have higher urinary BPA concentrations than normal-weight children, but the difference was not significant (P=0.26), consistent with the results reported in Canada.15 There is a possibility that overweight and obese children have a greater overall energy intake, and thus consume more canned food and drinks. They may also have higher urinary BPA concentrations, because BPA is stored and released from adipose tissue.6

Several studies have reported that urinary BPA concentrations in children were higher than those in adults,11, 13, 15 indicating that children may have a higher exposure risk. This is the first large-scale multisite study of this issue in China. We found highest urinary BPA concentrations in the age group of 12 years with a median concentration of 1.35 ng/ml, and it decreased with decreasing age (11 years: 1.10 ng/ml; 10 years: 1.00 ng/ml; and 9 years: 0.90 ng/ml; P=0.021; Supplementary Table S5). The SG-adjusted and creatinine-adjusted average urinary concentrations for the four age groups were 1.34, 1.12, 1.02 and 0.95 ng/ml, and 2.84, 2.28, 2.23 and 1.99 μg/g, respectively. However, there were variations among the sampling areas (Figure 1). There was an increase in concentrations of urinary BPA with increasing age in Haimen (P=0.015). However, an opposite direction was observed for children living in Yuhuan, namely a significant decrease in levels of urinary BPA with increasing age (P=0.025), and this was similar to the study results reported for Japanese school children.29 There was no obvious age-related change in the urinary BPA concentrations in the Minhang area (P=0.412). Several studies with wider age ranges reported a significant decrease in the urinary BPA levels with increasing age.11, 13, 24 The three different trends in individual areas in our study may be attributed to much narrower age group interval (1 year only), and therefore the age-related change of urinary BPA levels was less evident and more stochastic considering the varied local environmental conditions and lifestyles such as dietary habits. Whether or not the special profiles of BPA exposure among Chinese school children in eastern areas exist in other parts of China needs further studies.

Figure 1
figure1

Median concentrations (ng/ml; creatinine-adjusted in μg/g) of urinary BPA in different age and sex groups among three areas in China. The error line in each bar represents the 95% CI.

In order to make comparison with other studies, GM concentrations of urinary BPA were calculated. The 2003–2004 NHANES in the United States reported that the highest urinary BPA concentrations were detected in young children after adjusting for creatinine, followed by adolescents and adults. The creatinine-adjusted BPA concentration in children (6–11 years) was 2 times (4.3 μg/g) higher than in adults (2.4 μg/g).11 In another study from Canada, creatinine-adjusted urinary BPA concentration in children (6–11 years) was higher than those in other older age categories with a GM value of 2.00 μg/g creatinine.15 He et al.18 have reported that urinary BPA concentrations for Chinese adults over 20 years of age ranged from 0.26 (>50 years) to 1.06 ng/ml (31–40 years) in east and middle mainland China. The measured level of urinary BPA in children aged 9–12 years (1.11 ng/ml) in this study was also higher than that for adults from the same areas. High concentrations of BPA in children may be related to their high food consumption, relevant product usage and air inhalation rates in relation to their body weight and also different profiles of their absorption, distribution, metabolism and/or excretion of BPA.11 In the present study, the creatinine-adjusted level of urinary BPA for children was lower than that found for either children or adults in the US study11 but higher than that found in the Canadian study.15 In the GerES IV study, the unadjusted urinary BPA concentrations in children in the age category of 9–11 years (GM 2.22 ng/ml) and 12–14 years (2.42 ng/ml) were almost twice higher compared with the present study (1.11 ng/ml).13 In contrast, a pilot study in Egypt showed that both the unadjusted and SG-adjusted concentrations of BPA (0.84 and 1.00 ng/ml) in 57 girls aged 10–13 years were lower than those found in Chinese school children.30 These comparisons suggest that the average BPA exposure levels are higher in some major developed countries than those in developing countries, and this may be attributed to the differences in geography, race, economic condition, lifestyle and other sociodemographic factors such as production and use of BPA.

However, there is an increase in BPA exposure for Chinese people, and especially for children, because of dramatically increased production and consumption of BPA in China. A recent study conducted in southern China17 reported that the least square geometric mean (LSGM) concentration of urinary BPA for children aged 7–12 years (4.10 ng/ml) was close to that of children aged 6–11 years in the United States (4.50 ng/ml). The average urinary BPA level of Chinese children aged 13–17 years (3.71 ng/ml) was even higher than that of American children aged 12–19 years (3.00 ng/ml).11

In our study, although a spot urine sample was collected instead of 24-h urine, the large sample size may reduce the variation and provide sufficient statistical power to categorize the average population exposure level of BPA.31 Furthermore, we used a highly sensitive and selective MS/MS analytical method, and nearly 99% of our samples had detectable BPA levels that may provide a comprehensive evaluation. Comparisons of characteristics with several common detection methods are listed in Supplementary Table S6.32, 33, 34, 35, 36, 37, 38

Comparison of Specific Gravity and Creatinine Corrections for Adjusting Urinary BPA Concentrations

Urinary volume is influenced by various factors that raise the variation of urinary dilution, consequently, changing the concentrations of excreted substances.39 In this study, both creatinine and SG corrections that are considered as common correction methods were adopted to adjust the urinary BPA concentrations. Overall, the median of SG-adjusted urinary BPA concentrations (1.07 ng/ml) was similar to the unadjusted one (1.00 ng/ml), whereas the creatinine-adjusted median value (2.22 μg/g creatinine) was approximately twice as much as the unadjusted one (P<0.001). This may suggest that there existed a wide variation in the urinary concentrations of creatinine in children. The mean SG (1.022) and creatinine value (60.48 mg/dl) were both slightly higher in the high BMI (overweight and obesity) group than in the normal BMI group (1.021, 59.59 mg/dl), but the differences were non-significant (P=0.316 and P=0.645, respectively). Different age groups showed statistically significant difference either for SG (P=0.01) or creatinine (P=0.012; Supplementary Figures S3 and S4). Spearman’s rank correlation analysis was conducted between the natural log-transformation of SG-adjusted and creatinine-adjusted concentrations of urinary BPA (y=log(x+1)) (Supplementary Figure S5), and the correlation coefficient was 0.83 (P<0.001). In order to evaluate the effect of either creatinine or SG correction, we estimated the reduction in variance of BPA concentrations by using an index similar to the coefficient of variation (CV) (considering the skewed distribution): , where DV means degree of variation, X is the raw or adjusted BPA concentrations after creatinine or SG correction, M is the median concentration of the group and N is the individual sample size. The results are shown in Supplementary Figure S6. Unexpectedly, the DV of the total creatinine-adjusted BPA concentrations (278.7%) was even higher than that of the unadjusted concentrations (223.9%), but the DV for the SG-adjusted BPA concentrations (219.4%) was lower than the unadjusted concentrations. SG-adjusted BPA concentrations provided a more reasonable result by reducing urine dilution-related variance as compared with creatinine correction.

Besides, the mixed model to investigate the relative influence of the natural logarithm (In) of the creatinine concentrations and In of the SG as an independent variable to characterize the relationship between In of the urinary BPA and sex, age, BMI and area is provided below: Yij=β0+β1X1ij+β2X2ij+β3X3ij+β4X4ij+ai +ɛij, where Yij represents In of the urinary BPA concentration plus 1 (the jth children of the ith area) and X1ij, X2ij and X3ij represent the sex, age and BMI, respectively. X4ij represents In of the creatinine concentrations or In of the SG, and ai and ɛij represent the random effects of the area and an error term. The result is provided in Table 2. When used alone with creatinine or SG variables in the model, In of the SG was highly significant (P<0.001), whereas In of the creatinine concentrations seemed non-significant with the P-value of 0.14. The Akaike’s information criterion (AIC) was also provided for each model; a smaller AIC indicates a better model fit. The models that included In of the SG had the smaller AIC, indicating the better model fits (AIC=1200) compared with using In of the creatinine concentrations (AIC=1239). BMI may be another significant predictor of urinary BPA (P=0.043–0.046). The models demonstrated that normalization with SG provided a better model fit than normalization with creatinine concentration when monitoring urinary BPA levels in children.

Table 2 Mixed models for predicting urinary BPA concentrations with the comparison of using creatinine concentration and specific gravity (SG) as independent variable.ab

In summary, although creatinine correction was the most common method for adjusting variable dilution in adult urine samples, SG correction was more preferable for children based on the results of our study as well as other previous studies that reported creatinine not being a reliable correction measure for children.40, 41 Another study pointed out that specific gravity was affected more by the presence of heavy molecules and temperature, whereas creatinine excretion was influenced by time of day, age, sex, diet, BMI and activity level, resulting in inter- and intra-subject variations.23

Estimation of Human Exposure to BPA

Daily intake calculations based on biomonitoring data (e.g., urine or blood) reflect real exposure, for which all possible exposure sources are included.42 BPA levels in urine reflect exposure that occurred within 24 h of sampling.43 The urinary BPA concentration (μg/ml) was used in the estimation of amount excreted in 24 h based on the volume of urine output (ml).

The estimated daily intake (EDI) doses (expressed in μg/kg body weight/day) of BPA in Chinese primary school children are shown in Figure 2 and Table 3. The median EDI of total children was 0.023 μg/kg bw/day. The EDI of BPA for children in Yuhuan was the highest (0.051 μg/kg bw/day). The median EDI of BPA for children aged 12 years (0.044 μg/kg bw/day) was twice as great as that for the children aged 9–11 years (0.022 μg/kg bw/day). The European Commission estimated the daily intake of BPA to be 1.2 μg/kg bw/day for children between 4 and 6 years of age, and 0.4 μg/kg bw/day for adults living in the EU countries.44 The European Food Safety Authority45 and the US Environment Protection Agency46 established a value of 50 μg/kg bw/day as the tolerable daily intake (TDI) and reference dose (RfD), respectively. It was obvious that the average EDI of BPA in Chinese children was much lower than the value recommended. However, the EFSA or EPA criteria have been questioned as animal and epidemiological investigations showed harmful effects when exposure level was lower than the current reference value.47, 48

Figure 2
figure2

Profiles for the estimated daily intake (median) of BPA (expressed in μg/total body weight/day and μg/kg body weight/day). The error line in each bar represents the 95% CI.

Table 3 Estimated daily intakes of BPA based on urinary concentrations for Chinese children (expressed in μg/kg body weight/day).

The EDI values for BPA in other studies are summarized in Table 4. The EDI of BPA in Chinese children was lower than the values reported for the US children aged 6–19 years (0.048–0.071 μg/kg bw/day)11, 24 as well as for the German children aged 3–14 years (0.060 μg/kg bw/day).13 However, the EDI values of BPA in this study were similar to the values reported for the Canadian children (0.025 and 0.031 μg/kg bw/day for children aged 6–11 and 12–19 years, respectively).15

Table 4 Urinary BPA concentrations (ng/ml) and estimated daily intake (μg/day and μg/kg/day) of children and adolescents in current study and other studies.

We also calculated the EDI (expressed in μg/day) to evaluate the body burden of BPA for the target population (Figure 2 and Supplementary Table S7). There was almost no difference between males and females in terms of EDI of BPA, and the difference of EDI values of BPA was also not significant between children with normal BMI and those overweight or obese (Supplementary Table S8). When estimated on the basis of a calculation of μg/kg bw/day, EDI values of BPA were significantly higher in the normal-weight group than those in the overweight and obese groups (Supplementary Table S9). Higher BMI may lead to a lower intake estimate per unit of body mass because of body dilution.

Several studies have estimated that food contributes to >90% of the overall BPA exposure for all age groups, whereas other exposure pathways through inhalation, dental surgery and dermal absorption account for <5%.49, 50 A study of preschool children in the United States found that dietary ingestion of BPA accounted for >95% of the young children’s excreted amounts of urinary BPA with estimated median intake doses of 109 ng/kg/day.51 Their estimated median excreted amount of urinary BPA was 114 ng/kg/day. The highest estimated BPA dietary exposure was in infants because of their extensive usage of PC bottles.31 For young children, canned foods with PC coating, consumption of beverage lined with PC bottles, more food packaging and microwaved foodstuff while having meals may be the main oral intake sources probably.16 Toys containing BPA may be an additive pathway of exposure for young children.10

CONCLUSION

Widespread and continuous exposure to BPA has been a public health concern all over the world. So far, BPA can be found in urine in a majority of people monitored worldwide,31 of whom children are most vulnerable to the exposure of BPA. Very few studies have been conducted to explore exposure of children to BPA in China. To our knowledge, our study is the first multisite study to investigate the state and profiles of BPA exposure for primary school children in Yangtze River Delta of eastern China. BPA was detected in 98.9% of all samples, indicating the exposure of BPA was common for Chinese school children, but the average level was lower than those reported from the United States and Germany. There was a lack of consistency for age associated with BPA levels among school children. To evaluate the exposure to BPA for children through their urinary BPA concentrations, the correction method of specific gravity is preferred. BPA exposure from dietary pathway and other routines such as air or indoor dust is associated with childhood obesity, however, besides BPA intake amount, some other behaviors like the imbalance of nutrition may also result in high body weight that makes BPA exposure assessment more complex. The exposure is common in Chinese school children, but there is a lack of information concerning various exposure routes to BPA, for which further studies are urgently needed.

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Acknowledgements

This study was supported by the Natural Science Foundation of China (No. 81373089), 985 Innovation Platform Project for Superiority Subject of Ministry of Education of China (No. EZF201001), grants of the National Health Research Program from the State Ministry of Health of China (No. 201202012) and New Teacher Fund for Doctor Station, the Ministry of Education of China (No. 20120071120051).

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Correspondence to Ying Zhou.

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Wang, B., Wang, H., Zhou, W. et al. Exposure to bisphenol A among school children in eastern China: A multicenter cross-sectional study. J Expo Sci Environ Epidemiol 24, 657–664 (2014). https://doi.org/10.1038/jes.2014.36

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Keywords

  • BPA
  • urine
  • daily intake
  • China
  • children

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