Article pubs.acs.org/est
Placental Transfer of Dechlorane Plus in Mother−Infant Pairs in an E‑Waste Recycling Area (Wenling, China) Yu-Jie Ben,† Xing-Hong Li,†,* You-Lin Yang,‡ Long Li,† Mei-Yun Zheng,‡ Wen-yue Wang,† and Xiao-Bai Xu† †
State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center of Eco-Environmental Sciences, Chinese Academy of Sciences, P.O. Box 2871, 18 Shuangqing Road, Haidian District, Beijing 100085, China ‡ First Hospital of Wenling, Taizhou 317004, Zhejiang Province, China S Supporting Information *
ABSTRACT: It has been reported that breastfeeding can expose newborns to dechlorane plus (DP), but transplacental transfer of DP has not been documented. We measured DP and its dechlorinated analogs in matched maternal blood− placenta−cord blood samples from 72 residents of the e-waste recycling area of Wenling, China. DP was detected in cord sera, indicating the occurrence of prenatal DP exposure and the transfer of DP across the placenta. The concentration ratio in the cord serum and maternal serum was estimated to be 0.45 for syn-DP and 0.35 for anti-DP, indicating the placenta partially limited DP transfer with a greater extent for anti-DP. The DP concentrations in the maternal serum, placenta, and cord serum strongly correlated, indicating that DP could transfer between the tissues. The DP concentrations in the matched samples could be predicted from each other. The anti-DP/ total DP concentration ratios in the placentas and cord sera were significantly different from those in the maternal sera, suggesting that DP stereoselectively bioaccumulates in human tissues. When the congener concentrations of polybrominated diphenyl ethers (PBDEs) were used as control variables, DP and total triiodothyronine concentrations were associated in the sera from mothers who had lived in Wenling for over 20 years.
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INTRODUCTION Dechlorane plus (DP) has been widely used as a flame retardant in electrical wire and cable coatings, computer and television connectors, and plastic roofing materials for almost 50 years.1 DP is now viewed as a global contaminant because of its persistence, potential for long-range atmospheric transport, and potential to bioaccumulate.1−3 Although the toxicological significance of DP has not been clarified, its continued widespread use and its bioaccumulation potential in wildlife and humans1−4 makes investigating its environmental behavior and toxicology important. Exposure to environmental pollutants during critical periods of development (the fetal and newborn periods) is of particular concern because of the potential influence pollutants may have on the growth, reproduction, and development of both wildlife and humans.5−8 Newborns will have been exposed to toxicants that could cross the placenta and will be further exposed through breastfeeding. DP and its analogs have recently been detected in human breast milk,9,10 indicating that newborns will be exposed to DP postnatally. Although DP and its dechlorinated analogs have been found in bird eggs and the transfer of DP from mother to offspring has been studied in wildlife,4,11,12 information on prenatal exposure to DP and its related compounds in humans is not available. © 2013 American Chemical Society
It would be beneficial to obtain a comprehensive understanding of human exposure to DP early in life. We measured DP and its dechlorinated analogs in matched maternal blood, cord blood, and placenta samples from women living in the ewaste recycling area of Wenling City, Taizhou, China. Our objective was to assess prenatal exposure to DP and its analogs and to examine the extent of transplacental transfer and possible adverse health effects. Furthermore, the stereoselective bioaccumulation of DP in three human compartments, possible sources of the monodechlorinated analog of DP (anti-[DP1Cl]), were also examined.
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EXPERIMENTAL SECTION Sample Collection. Samples were collected between July 2010 and July 2011. Seventy-two matched maternal blood, placenta, and cord blood samples were collected from mothers in the Wenling, Taizhou region, China. The Taizhou region in Zhejiang Province is one of two of largest e-waste recycling regions in China, while Wenling, with an approximate rural Received: Revised: Accepted: Published: 5187
June 24, 2013 November 16, 2013 November 21, 2013 November 21, 2013 dx.doi.org/10.1021/es404106b | Environ. Sci. Technol. 2014, 48, 5187−5193
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Article
delivery. The placenta samples were washed with 0.9% normal saline to remove blood and then homogenized and freeze-dried. All of the samples were kept at −20 °C until they were analyzed. Six field blanks (empty hexane-rinsed glass bottles) were collected at the same time as the tissue samples, and six operational field blanks (hexane-rinsed glass bottles filled with 30 mL distilled water at the sampling sites) were also collected. The samples were stored in glass vials with Teflon-lined screw caps from Agilent Technologies (Santa Clara, CA, U.S.A.). No target analytes (anti-[DP-2Cl], anti-[DP-1Cl], anti-DP, and synDP) were found during prescreening. Laboratory Analysis. Concentrations of syn-DP, anti-DP, anti-[DP-2Cl], anti-[DP-1Cl], and BDE congeners (including BDE-28, BDE-47, BDE-99, and BDE-153) were determined in maternal serum, cord serum, and placenta samples using an Agilent 6890/5973 GC/MSD system (Agilent Technologies) in negative chemical ionization mode. A detailed description of the analytical procedure has been published previously.9 The serum samples were extracted and cleaned following the procedure described by Ben et al.,9 except that 10.0 mL of each cord serum sample was analyzed. Placental tissue (2.0 g dry weight) was ground with anhydrous sodium sulfate and fortified with the internal standards (13C10-syn-DP, 13C10-antiDP, and BDE-77) and then ultrasonically extracted with 20 mL of a 1:1 (v:v) mixture of methyl tert-butyl ether and hexane. The sample was separated by centrifugation, the supernatant removed, and the extraction process repeated two more times. The combined extracts were concentrated by rotary evaporation, and the lipid content was determined gravimetrically. The extract was then transferred to a chromatography column (30 cm long, 10 mm id) containing 8 g of silica treated with concentrated sulfuric acid (30% acid by weight) covered with 2.5 g of anhydrous sodium sulfate, which was eluted with 50 mL of a 1:1 (v:v) mixture of hexane and dichloromethane. The eluent was concentrated to 50 μL for further analysis, and 13 C12PCB-208 (Cambridge Isotope Laboratories) was added as an injection internal standard. The recoveries of the internal standards that were spiked into the serum samples before extraction were 60−103% for 13C10syn-DP (Cambridge Isotope Laboratories Inc., Andover, MA, U.S.A.), 73−100% for 13C10-anti-DP (Cambridge Isotope Laboratories), and 75−110% for BDE-77. For the placenta analyses, recoveries were 70−109% for 13C10-syn-DP, 66−104% for 13C10-anti-DP, and 72−107% for BDE-77. Fetal bovine serum and olive oil (0.1 g) were used to represent the method blank of serum and placenta, respectively. Seven replicates of method blank spiked with the mixture of target analytes were processed through the entire extraction procedure and analyzed. The method detection limits (MDLs) were defined as the mean plus three standard deviations of values associated with the analysis. On the basis of the cord serum volume (10.0 mL), dry weight of the placenta samples (2.0 g), average lipid concentration (2.3 g L−1 for cord serum and 6.24% for dried placenta), and injection volume (20 μL for cord serum and 50 μL for placenta), MDLs for anti-[DP-2Cl], anti-[DP-1Cl], synDP, and anti-DP in cord serum were 59.5, 63.9, 124, and 131 pg g−1 lipid weight (lw), respectively. That was 26.5, 28.8, 56.6, and 60.1 pg g−1 lw for placenta, respectively. Lipids were determined in the placenta samples using the gravimetric method on the extracts, and a colorimetric method based on the sulfo−phospho−vanillin reaction was used to determine the lipids in the serum samples.13,14 Thyroid hormone levels, including thyroid stimulating hormone
population of 1.2 million and urban population of 0.2 million, was one of two major cities executing the e-waste recycling activities in Taizhou region. A detailed description of the sampling area has been published previously.9 The donors were screened according to their residential location and residential history. All donors are required to be residing in a rural area. The R20 group (n = 48) contained donors who had lived in Wenling for more than 20 years and were living or had recently lived in villages where e-waste recycling activities were undertaken but did not directly participate in e-waste recycling activities. The R3 group (n = 24) contained donors who had lived in Wenling for less than 3 years, had not previously lived in villages where e-waste recycling activities were undertaken, and did not participate in e-waste recycling activities. The study participants gave their informed consent, and each completed a questionnaire on their personal information, including their age at delivery, height, prepregnancy body weight, parity, education level, occupation, neonate body weight and length, Apgar score, gestational weeks, and how long they had lived in the area (Table 1). Maternal blood (approximately 20 mL) and umbilical cord blood (30−40 mL) samples were each collected at delivery and centrifuged to separate the sera, which was transferred into hexane-rinsed glass vials. To ensure the representativeness of the placental sample, a 4−5 cm section of placental tissue was collected from near the umbilical cord connection point after Table 1. General Characteristics of Study Participants (n = 72) residential time, in years (mean ± SD) maternal age at delivery, in years (mean ± SD) maternal prepregnancy BMIb,c (kg/m2) (mean ± SD) maternal parityd (mean ± SD) primipara multipara maternal education levelf [n (%)] ≤ 9 years >9 years maternal occupationf [n (%)] housewife employee neonate gender [n (%)] male female neonate Apgar score (mean ± SD) neonate gestational weeks (mean ± SD) neonate body weight, g (mean ± SD) neonate body length, cm (mean ± SD)
R20 (n = 48)
R3 (n = 24)
p-value
24.0 ± 3.0
1.0 ± 1.0
0.05). Prenatal Exposure of DP and Its Dechlorinated Analogs. Syn-DP and anti-DP were detected in all of the maternal sera, cord sera, and placentas, and anti-[DP-2Cl] was not detected in any of the samples. Several possible monodechlorinated analogs of DPs were found in the human samples (Figure SI-1, Supporting Information), but these peaks could not be quantified due to the absence of authentic standards, only except for anti-[DP-1Cl]. The concentrations of DP (syn-DP and anti-DP) and monodechlorinated analogs (anti-[DP-1Cl]) found in the three sample types on a lipid weight basis are presented in Table 2. Of the maternal sera, placenta, and cord sera, anti-[DP-1Cl] was detected in 81%, 69%, and 36% in the R20 group and 71%, 29%, and 4% in the R3 group, respectively. The DP concentrations in most of the cord sera samples were 1.35−4.76 ng g−1 lw (first to third quartiles) with a small number of samples having close to 100 ng g−1 lw, indicating that individual fetuses had widely different DP body burdens. A similar skewed DP concentration distribution was found in the placentas and maternal sera.
(TSH), total triiodothyronine (TT3), total thyroxine (TT4), free triiodothyronine (FT3), and free thyroxine (FT4), were determined in the serum samples using a chemiluminescent microparticle immunoassay at a local hospital. Data Analysis. All statistical analyses were performed using SPSS 13.0 software (SPSS Inc., Chicago, IL, U.S.A.). and leastsquares linear regressions were fitted using OriginPro8 SR0 software (www.OriginLab.com). The Kolmogorov−Smirnov test was used to test continuous variables for the normal distribution. The Pearson χ2 test and independent samples ttest (Mann−Whitney test) were used to test for differences related to demographic differences, THs, DP isomers, and monodechlorinated analog levels between the R20 and R3 groups. Analysis of the potential relationship in DP concentrations and THs expression was conducted using a partial correlations method. The paired-sample t-test was used to explore the differences in the fanti found in the three tissues analyzed. The Wilcoxon t-test was used for examining the difference of anti-[DP-1Cl]/anti-DP ratios in the maternal serum and placenta. A p-value 0.05), so the ratios for the two groups were combined for further data set analysis. For the total DPs, the F/M ratios in most of the samples were in the range of 0.20−0.59 (first to third quartiles), and the median of the F/M ratios was calculated as 0.38. These values showed the capacity of DP in crossing the placenta. Meanwhile, the F/M ratios were 0.7, p < 0.001 for each). Because there were significant associations based on lipid-adjusted DP concentrations, we linearly fitted (using the least-squares) the relative DP distributions in the maternal sera, cord sera, and placentas. The fitted equation model was expressed as log(y) = n log(x) + log(b)
(1)
where x was the DP concentration in the maternal serum, y was the DP concentration in the cord serum or placental tissue, and n and b are constant. Predicted equation, correlation coefficients, and p-values of the log-transformed lipid-adjusted DP concentrations for the maternal sera, cord sera, and placentas are shown in Table 3, and the plots are displayed in Figure SI-2 of the Supporting Information. Using these equations, we could use a DP concentration in a maternal serum sample to estimate the concentration in the placenta or cord serum, and to assess prenatal exposure. Furthermore, with a different expression, the fitted equation in the current study can be transferred as y = bxn with 0 < n < 1, implying the partitioning relationship for DP between the tissues may follow a power function. The function curve is upward and convex, meaning that y increases as x increases; however, the rate of changes decreases. This may help us better understand the pharmacokinetics of DP in the human body. In a previous study,9 we reported that DP concentrations in the breast milk could be predicted well based on DP concentration in the maternal serum using a simple linear structural relationship model. These relationships of DP concentrations were found among maternal serum−placenta− cord serum or between maternal serum−breast milk, indicating the dual pathways of prenatal and postnatal DP exposure in the early development stage of the life. Stereoselective Bioaccumulation of DP Isomers. Different physical−chemical properties of two stereoisomers of DP, syn- and anti-, may be subject to the variations in the bioaccumulation behavior in a human body.22 However, to date, information regarding the possible stereoselective bioaccumulation of DP in a human body is limited. The antiDP fractional abundance ( fanti), defined as the ratio of the antiDP concentration to the total DP concentration, was generally used to examine the possible stereoselective enrichment of DP isomers in a human body.1,3 The fanti values found in the maternal sera, placentas, and cord sera are shown in Table 2 and had normal distributions in both the R20 and the R3 groups. We combined the fanti values for the R20 and R3 groups and used the paired-sample t-test to explore the differences in the fanti values found in the three tissues analyzed. The fanti value was slightly higher but significant in the placentas compared to the maternal sera or cord sera (p < 0.05). The fanti value was also higher but significant in the maternal sera compared to the cord sera (p < 0.001). The significant difference of the fanti value in three compartments confirmed the occurrence of stereo5191
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No epidemiological studies of the potential health effects of DP on humans have yet been reported. We found a marginal difference of the TSH levels in maternal serum between the R20 (median 1.76 μIU mL−1) and R3 (median 2.25 μIU mL−1) groups (p = 0.046) (Table SI-1, Supporting Information), and DP concentrations were relatively higher in the R20 group than those in the R3 group (Table 2), implying the likelihood of a DP effect on the TSH concentration. However, Pearson correlation analyses showed an insignificant association between DP isomers and THs concentrations (log-transformation for both) in maternal sera of the R20 group (p > 0.05, n = 44). For the R3 group, the relationship between DP isomers and THs was not discussed due to small paired sample sizes (n = 22). Some BDE congeners have been shown to affect human thyroid hormone levels31−35 and have been found at relatively high concentrations in human tissues from Taizhou residents.36,37 Hence, we wish to separate and remove the influence of PBDEs in order to detect the possible relationship between DP and THs. In the present study, the BDE congeners in maternal serum samples were detected to be BDE-28, BDE-47, BDE-99, and BDE-153 in the R20 group with the detection frequency of 98%, 98%, 92%, and 100%, respectively. The median concentration was 0.64, 1.45, 0.54, and 6.09 ng g−1 lw, respectively. To subtract the effect of the PBDEs on thyroid hormone levels, the association between DP and thyroid hormones was adjusted based on the log-transformed four BDE congeners (including BDE-28, BDE-47, BDE-99, and BDE153) concentration. Then, the DP concentrations were positively associated with TT3 concentrations (after the logtransformation of both) (r = 0.37 and p = 0.020 for syn-DP, r = 0.360 and p = 0.024 for anti-DP). The association between DP contamination and TT3 levels suggested that DP may have some effects on thyroid hormone. In conclusion, DP and anti-[DP-1Cl] were detected in placenta and umbilical cord serum samples, indicating that they could translocate from maternal to fetal tissues. Maternal sera contained the highest DP concentrations and DP could be transferred across the placenta into the cord sera with partial restriction from the placenta. DP concentrations in each of three tissues could be predicted from the other tissue concentrations using fitted equation. Stereoselective bioaccumulation occurred in the course of the DP passage from the maternal blood to the cord blood. Although the association between DP concentrations and infant growth indices were not recorded, the correlation between DP and TT3 concentrations in maternal sera suggests that further research efforts are required into the toxicology of DP and the risks involved in human exposure to DP.
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Article
AUTHOR INFORMATION
Corresponding Author
*Tel: +86 10 62919177. Fax: +86 10 62923563. E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We gratefully acknowledge the contribution from the volunteer donors and their families in this study. We also thank the medical staffs who have provided their invaluable help during the sampling. Furthermore, the contribution from Professor Sijin Liu for his critical advice on data-set analysis and manuscript editing is greatly appreciated. This work was funded by the National Natural Science Foundation of China (21177152 and 20877092)and the Chinese Academy of Sciences (YSW2013B01).
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REFERENCES
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ASSOCIATED CONTENT
S Supporting Information *
Statistical description on thyroid hormone concentrations in maternal sera is presented in Table SI-1. Figures include an extracted ion chromatogram (m/z 617.7) of the maternal serum samples by GC/ECNI-LRMS and six fitted linear diagrams of DP concentration among maternal serum, placenta, and cord serum concentration. This material is available free of charge via the Internet at http://pubs.acs.org. 5192
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