Environ. Sci. Technol. 2010, 44, 3956–3962
Elevated Body Burdens of PBDEs, Dioxins, and PCBs on Thyroid Hormone Homeostasis at an Electronic Waste Recycling Site in China J I A N Q I N G Z H A N G , * ,† Y O U S H E N G J I A N G , † JIAN ZHOU,† BIN WU,† YIN LIANG,‡ ZHAOQIONG PENG,† DAOKUI FANG,† BIN LIU,† HAIYAN HUANG,† CAI HE,† CHUNLEI WANG,† AND FEINA LU† Shenzhen Center for Disease Control and Prevention, No. 21, 1st road Tianbei, Luohu district, Shenzhen, Guangdong, PR China 518020, and Luqiao Hospital of Traditional Chinese Medicine, No. 101, Donglu qiao road, Luqiao district, Taizhou, Zhejiang Province, PR China 318050
Received September 23, 2009. Revised manuscript received March 16, 2010. Accepted March 21, 2010.
A cross-sectional study of 25 sample sets (each set consisted of maternal serum and cord whole blood) from 50 pregnant women in zone A (n ) 25 from exposed group) and zone B (n ) 25 from reference group) was conducted to examine the association between thyroid hormone (TH) levels and PBDE, PCDD/ F, and PCB exposures. Thyroid hormones TT3, TT4, and TSH levels were measured in maternal serum at 16 weeks of gestation. The concentrations of PBDEs, PCDD/Fs, and PCBs were determined by isotope dilution HRGC/HRMS in cord blood samples. Body burdens of the three contaminants in cord blood in zone A (median: ∑ TEQ-PCDD/Fs 0.041, ∑ TEQ-PCBs 0.022 pg WHO-TEQ/g, ∑ PBDEs 23.4 pg/g whole weight, respectively) were significantly higher than those from the reference area (median: ∑ TEQ-PCDD/Fs 0.014, ∑ TEQ-PCBs 0.0041 pg WHOTEQ/g, ∑ PBDEs 16.15 pg/g, respectively) (p < 0.05). Levels of TT4 and TSH in serum in zone A were significantly lower than those in zone B (p < 0.05). A negative correlation was found between TT4 levels and body burdens of PCDD/Fs and PCBs. However, there was no significant association of concentration of PBDEs and levels of the three thyroid hormones. Our results suggest that electronic waste (e-waste) recycling contributes to high body burdens of PBDEs, PCDD/Fs, and PCBs and affects thyroid hormone homeostasis in humans. The potential health risk for neonates still needs further investigation.
Introduction Polybrominated diphenyl ethers (PBDEs), polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), and polychlorinated biphenyls (PCBs) are persistent halogenated chemicals and are ubiquitous in the environment. These three categories persistent organic pollutants (POPs) are lipophilic and can bioaccumulate in the human food chain * Corresponding author phone: +86 0755 25617553; fax: +86 0755 25531955; e-mail:
[email protected]. † Shenzhen Center for Disease Control and Prevention. ‡ Luqiao Hospital of Traditional Chinese Medicine. 3956
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and in humans (1). PCDD/Fs and PCBs are known persistent organic pollutants (POPs), and commercial mixtures of pentabromodiphenyl ether (Penta-BDE) and octabromodiphenyl ether (Octa-BDE) were recently included in the Stockholm Convention on Persistent Organic Pollutants at the fourth Conference of the Parties in May of 2009 (2). Although PCDD/F and PCB levels in the environment and in human tissues are decreasing, PBDE levels have increased substantially during the past two to three decades in the United States and Europe (3, 4). Disposal and dismantling of electronic waste (e-waste) can release persistent organic pollutants including PBDEs, PCDD/Fs, and PCBs into the environment (5). Concurrent exposure to PBDEs, PCDD/Fs, and PCBs was found in populations involved in uncontrolled e-waste recycling operations in a small town of southeastern China (6, 7). Therefore, hazardous POPs including PBDEs, PCDD/Fs, PCBs, and PAHs are released into the environment and might pose a threat to the health of local residents and workers (6-8). PBDEs, PCDD/Fs, and PCBs can disturb endocrine hormone homeostasis and affect thyroid hormone (THs) equilibrium, as has been observed in rats, seals, and fish (9-11). The effects of PBDEs, PCDD/Fs, and PCBs on thyroid hormone homeostasis have also been studied in humans. However, there are only relatively few reports, and the results are not consistent (12-16). There is a research gap related to thyroid effects of PBDEs, PCDD/Fs, and PCBs coexposure in humans. Prenatal PCB and PBDE exposures were found to be associated with reduced TT4 and FT4 in neonates (17), and PCBs could affect THs homeostasis in neonates even at low background levels in a Mexican-American population (18). A previous report which found higher neonatal bloodTSH after prenatal exposure to TCDD demonstrated that dioxins had a long-lasting effect on neonatal thyroid function (19). Moreover, decreased total T4 (TT4) and increased thyroid-stimulating hormone (TSH) in plasma were reported in animals exposed to PBDEs and PCBs (10, 20). Similarly, gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rats was found to affect thyroid function (21). The objective of our study is to explore the relationship between thyroid hormone levels and the body burdens of PBDEs, PCDD/Fs, and PCBs in humans living near an e-waste town.
Experimental Section Sampling Site Description. An e-waste recycling town in southeast China was chosen for sampling populations that are exposed to elevated levels of PBDEs, PCDD/Fs, and PCBs (zone A). This town has an area of 274 km2 and 420000 local residents. The reference area (zone B) is located 250 km away from the e-waste area with a population of 530000. The e-waste recycling activities in zone A have been carried out for more than 25 years. Uncontrolled disposal including open air burning, acid leaching, and physical dismantling has brought environmental POPs pollution that might threaten the health of local residents (8, 22). The body burdens from human milk, placenta, and hair of people from the e-waste processing site showed significantly higher levels of PCDD/ Fs than those from a reference site (8). The PCDD/Fs, PCBs, and PBDEs levels in various sample matrices in zone A and comparison with other locations in the world are presented in Table S1. Study Population. In total, 50 pregnant women were recruited from April 2007 to December 2007. The sampling criteria were that pregnant women had resided in the local 10.1021/es902883a
2010 American Chemical Society
Published on Web 04/21/2010
area for at least 5 years in both zone A and zone B groups. Twenty-five subjects were interviewed at the obstetric clinic of two central hospitals located in zone A and zone B, respectively, during the same period. Personal questionnaire data including age, inhabitation time in the local area, and medical history were collected (Table S2). The subjects were between 19 and 38 years of age and were pregnant for the first time with no known complications, infectious disease, cigarette smoking, or alcohol consumption. The subjects who had a heredity history of thyroid disease and current or past thyroid disease were excluded. Sample Collection. Collection of blood from the donors was divided into two stages. Serum was first drawn at 16 weeks of maternal gestation for determination of T3, T4, and TSH, and in the second stage, 30-50 g of umbilical cord blood was collected in glass bottles at the time of delivery; these samples were used for the analysis of PBDEs, PCDD/ Fs, and PCBs. Each blood sample was stored at -80 °C until shipment on dry ice to the laboratory. A trained nurse carefully assessed structural and functional information of the newborn babies. The Human Ethical Committee of Shenzhen Center for Disease Control & Prevention inspected, reviewed, and approved the study protocol. Each of the participants was provided informed consent document and wrote consent after receiving a detailed explanation of the study and its potential consequences. Laboratory Analysis. Concentrations of thyroid-stimulating hormone (TSH, thyrotropin), total thyroxine (T4), and total triiodothyronine (T3) were measured in the 50 maternal serum samples by radioimmunoassay methods. TT3, TT4, and TSH commercial kits were purchased from Diagnostic Products Corporation (Los Angeles, California, U.S.A.), and the three hormones were measured according to the protocol provided by the manufacturer. Intra-assay and inter-assay coefficient of variations (CVs) were 3.1% and 3.5% for T3, 4.2% and 4.5% for T4, and 5.6% and 6.3% for TSH, respectively. The concentrations of six PBDE congeners (BDE-28, -47, -99, -100, -153, -154), seven 2,3,7,8-substituted PCDDs and ten PCDFs, four nonortho PCBs (PCB-77, -81, -126, and -169), eight mono-ortho PCBs (PCB-105, -114, -118, -123, -156, -157, -167, -189) (combined together as dioxin-like PCBs), and six indicator PCBs (PCB-28, -52, -101, -138, -153, and -180) were determined in cord whole blood samples using isotope dilution HRGC/HRMS (high-resolution mass spectrometry, MAT95XL, Thermo Finnigan, Bremen, Germany) for identification and quantification. Detailed description of PCDD/Fs, PCBs, and PBDEs determination, quality assurance and quality control are described in the Supporting Information (SI) and elsewhere in other literature (23, 24). PCDD/F, PCB, and PBDE concentrations were reported as pg/g whole weight. Toxic equivalents (TEQs) were calculated using the toxicity equivalence factors (TEFs) recommended by the WHO (25) assuming that the nondetected values were equal to their limits of detection. Statistical Analysis. All statistical analysis was performed with SAS 9.1 (SAS Institute Inc., Cary, NC). Normality test (Shapiro-wilk test) was executed for all continuous variables. Those data that showed non-normal distribution were log transformed, after which the data can be approximated as normal distributed. The differences in pollutant level, thyroid hormones, maternal age, and birth weight of neonates from zone A and zone B were assessed by the Student t-test, and categorical variable (baby gender) was assessed by the chisquare test. For those parameters that did not show normal distribution even after transformation such as birth length and Apgar score, Wilcoxon nonparametric test was used for statistical analysis.
A multiple linear regression model was used to explore the relationship between factors (ΣTEQ-PCDD/Fs, ΣTEQPCB, ΣPBDE, maternal age) and thyroid hormone levels. As some factors were highly correlated, principal component analysis (PCA) was first carried out on transformed data, and then multiple regression was performed to elucidate the relationship between the principal component (PC, pollutants) and thyroid hormone levels. The level of significance was set at p < 0.05 (two tailed).
Results and Discussion Characteristics of the Participants. The characteristics of the 50 mothers from zone A and zone B are described in Table S2. The results showed that there was no significant difference between the two groups in terms of characteristics of the mothers and birth outcome of the neonates (see the SI). Body Burdens of Dioxins, PCBs, and PBDEs and the Levels of Thyroid Hormone in Mothers. Levels of ∑TEQPCDD/Fs, ∑TEQ-PCBs, and ∑PBDEs and thyroid hormone levels for zone A and zone B are presented in Table 1. The levels of ∑TEQ-PCDD/Fs, ∑TEQ-PCBs (DL-PCBs), and ∑PBDEs in whole blood in zone A were statistically higher than those in zone B (p < 0.05). The median value of ∑TEQ-PCDD/ Fs and ∑TEQ-PCBs (DL-PCBs) in zone A (∑TEQ-PCDD/Fs: median: 0.041 pg WHO-TEQ/g; ∑TEQ-PCBs: median: 0.022 pg WHO-TEQ/g) was nearly 3- and 5-fold higher than those in zone B (∑TEQ-PCDD/Fs: median: 0.014 pg WHO-TEQ/g; ∑TEQ-PCBs: median: 0.0041 pg WHO-TEQ/g) (p < 0.01). Additionally, median concentration of ∑TEQ-nonortho-PCBs was 0.013 and 0.0025 for zone A and zone B, and the median concentration of ∑TEQ-mono-ortho-PCBs was 0.0093 and 0.0016 pg WHO-TEQ/g for zone A and zone B (p < 0.0001), respectively. Moreover, median concentration of ∑ indicatorPCBs was 171.42 (range 43.22-1167.01) pg/g and 131.59 (range 3.81-321.76) pg/g in zone A and zone B (p < 0.05), respectively. The results showed that there were higher body burdens of PCDD/Fs and PCBs in zone A, which was consistent with previous results reported by Chan (8) on body loading of PCDD/Fs in placenta and hair, but different from Bi’s (6) report on PCBs in serum, which showed no difference between electronics dismantling workers at an e-waste site and fishing industry inhabitants 50 km away. In total, concentrations of tri- through hepta-BDE congeners ranged from 7.7 to 201.3 pg/g whole blood (median: 23.43 pg/ g) and 1.58 to 134.3 pg/g whole blood (median: 16.15 pg/g) in zone A and zone B, respectively. The ∑PBDE concentrations in zone A was significantly higher than that in zone B (p ) 0.01). These results were consistent with previous studies on electronics dismantling workers in China and Sweden (6, 26) and with a recent study with regards to significantly higher PBDE levels in umbilical cord blood samples from another e-waste recycling area of China (27). These reports together with the results of our study demonstrated that there were elevated exposures of PCDD/Fs, PCBs, and PBDEs in residents at the electronic waste recycling site. Levels of PCDD/Fs, PCBs, or PBDEs in human blood have been analyzed in numerous studies. Serum is the most frequently analyzed blood component (28), whereas only limited reports on PCDD/Fs, PCBs, or PBDEs concentrations have been reported in whole blood (24, 29). It is usually very difficult to analyze and normalize the lipid content in whole blood because the lipid content in umbilical cord blood can be considerably lower, and the absolute level in umbilical cord blood can be as low as 20% of the maternal blood lipid absolute concentration and thus might lead to a large error when presenting concentrations on a lipid basis (30, 31). No systematic studies have been conducted showing the affinity of the different congeners of the three persistent organic pollutants to certain components such as lipid, serum, or VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Concentration of PCDD/Fs, PCBs, and PBDEs in Cord Whole Blood and Thyroid Hormone Level in Vein Serum of Maternal for zone A and zone Ba compounds and hormones
zone A (n ) 25) median
minimum maximum
zone B (n ) 25) 95%CI
median
minimum maximum
95%CI
p-value
b,l
TEQ-PCDD/Fs 0.041 0.0017 0.172 0.0017-0.15 0.014 0.0012 0.049 0.0012-0.049 0.0028 TEQ-PCDDsc,l 0.015 0.0011 0.11 0.0011-0.11 0.0070 0.00083 0.017 0.00084-0.17 0.052 d,l TEQ-PCDFs 0.018 0.00062 0.062 0.00062-0.062 0.0071 0.00032 0.033 0.00032-0.033 0.0054 0.022 0.0034 0.055 0.0034-0.041 0.0041 0.00083 0.020 0.00083-0.020
