Polybrominated Diphenyl Ethers (PBDEs) in Aborted Human

Article pubs.acs.org/est

Polybrominated Diphenyl Ethers (PBDEs) in Aborted Human Fetuses and Placental Transfer during the First Trimester of Pregnancy Yaxian Zhao,† Xianli Ruan,‡,§ Yuanyuan Li,† Minchan Yan,§ and Zhanfen Qin*,† †

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China ‡ Taizhou Hospital, Taizhou 318000, People’s Republic of China § Tongde Hospital of Zhejiang Province, Hangzhou 310012, People’s Republic of China S Supporting Information *

ABSTRACT: Data on early human fetal exposure to polybrominated diphenyl ethers (PBDEs) is limited. However, early pregnancy, in particular the first trimester, is critical for fetal development. We investigated exposure to PBDEs and placental transfer during early pregnancy by analyzing PBDEs in paired aborted fetuses (n = 65), placentas (n = 65), and maternal blood samples (n = 31) at 10−13 weeks gestation, which were collected in a hospital near electronic wastes (ewastes) recycling sites in Taizhou, China. Mean total PBDE (∑PBDE) concentrations were 4.46, 7.90, and 15.7 ng/g of lipid weight (lw) in the fetuses, placentas, and blood, respectively. The three matrices had roughly similar PBDE congener profiles, dominated by BDE-209, BDE-197, BDE153, BDE-47, and BDE-28. Significant correlations were found between ∑PBDE concentrations in the paired matrices. Comparing the concentration ratios between the paired samples, we observed significantly higher fetus/blood and fetus/placenta ratios for BDE-28, BDE-99, and BDE-47 than for BDE-197, BDE-209, and BDE-153, while opposite results were found in placenta/blood ratios. Our results indicate that PBDEs can enter the fetus during the first trimester and low-brominated congeners cross the placenta more easily than high-brominated congeners, which tend to remain in the placenta. This phenomenon is consistent with findings at the end of pregnancy.

■

al.21 reported a relationship between elevated cord blood PBDE concentrations and depressed indicators of neurodevelopment. Because the developing fetus might be more sensitive to the effects of chemicals than adults, it is important to understand the extent and effect of prenatal exposure to potentially toxic chemicals. Schecter et al.7 reported, for the first time, the presence of PBDEs in 11 human fetal (second and third trimesters) livers from the U.S. A Canadian group 8,9 investigated PBDE concentrations in placentas as well as fetal livers at early to midgestation collected in Montreal. These studies promoted our understanding of early human fetal exposure to PBDEs. However, data on early fetal exposure to PBDEs have still been limited because of the difficulty of collecting fetal samples. In particular, the placental transfer of PBDEs at early stages of pregnancy has been unclear because of the lack of data on paired maternal blood samples. Because of relatively less use of PBDEs in China, the PBDE levels in human samples from the general population are much

INTRODUCTION Polybrominated diphenyl ethers (PBDEs) have been widely used as flame retardants and have become ubiquitous pollutants in the environment. 1−3 Because of their potential to bioaccumulate, PBDEs have been found in various biotic samples worldwide.4,5 High PBDE concentrations have also been reported in human tissues, such as blood, adipose tissue, placenta, and semen.6−10 There is an increasing amount of data showing that PBDEs have a range of adverse effects, including thyroid hormone disruption, permanent learning and memory impairment, behavioral changes, hearing deficits, delayed puberty onset, decreased sperm count, and fetal malformations in laboratory animals.11−14 It is believed that exposure to PBDEs in utero or during infancy could lead to more significant harm than exposure during adulthood and at much lower concentrations.15−17 Previous reports have demonstrated the existence of PBDEs in human cord blood, showing that PBDEs can cross the blood−placenta barrier into the fetus.18,19 Several epidemiologic studies have suggested that exposure to PBDEs might have adverse effects on fetal development. Wu et al.20 found higher PBDE concentrations in newborn infants with adverse birth outcomes than in healthy newborn infants. Herbstman et © XXXX American Chemical Society

Received: December 30, 2012 Revised: April 18, 2013 Accepted: April 26, 2013

A

dx.doi.org/10.1021/es305349x | Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Environmental Science & Technology

Article

lower than those in the North American population and comparable to those in other Asian countries.5,22−25 However, primitive recycling of electronic wastes (e-wastes) containing PBDEs at the end of the 20th century and in the early 2000s in some areas, such as Taizhou and Guiyu, in China, resulted in heavy PBDE pollution. Very high PBDE levels were found in residents in e-waste recycling sites.26,27 To investigate fetal exposure to PBDEs and placental transfer during early stages of pregnancy, in this study, we measured PBDEs in aborted fetal and placental tissue and maternal blood collected in Wenling Women’s and Children’s Hospital, in Taizhou, China, where we expected to collect some samples from residents in the surrounding area of e-waste recycling sites.

Table 1. Sample Population Characteristics (n = 65) characteristic maternal age (years) 30 gestational week 10 11 12 13 fetus weight (g) 3.0 maternal occupation farmer non-farmer maternal smoking smoking none/passive smoker e-waste recycling site near home/work (≤3 km) yes no

■

MATERIALS AND METHODS Chemicals. A total of nine PBDE congeners (BDE-28, BDE-47, BDE-99, BDE-100, BDE-153, BDE-154, BDE-183, BDE-197, and BDE-209), from tri- to deca-BDE, were analyzed. These were the most abundant congeners in technical mixtures (penta-, octa-, and deca-BDE) and environmental matrices. BDE-71 was added as a recovery standard for the trito octa-BDEs, and 13C-labeled BDE-209 was used as an internal standard for BDE-209. All PBDE standards were purchased from Cambridge Isotope Laboratories (Andover, MA). All solvents and other materials were high-performance liquid chromatography (HPLC)-grade or better. Sample Collection and Storage. Between October 2009 and May 2011, we collected aborted human fetuses and placentas (villous region) (10−13 weeks gestation) and maternal whole blood samples from healthy pregnant women who chose a surgical abortion because of an unwanted pregnancy, in Wenling Women’s and Children’s Hospital, in Wenling, Taizhou, Zhejiang Province, China. Wenling Women’s and Children’s Hospital is one of the closest hospitals to the e-waste recycling centralized area in Wenling (approximately 13−16 km), but few pregnant women in this hospital are from the e-waste recycling centralized area because they generally go to community health service centers near their homes for an abortion. In this hospital, we expected to collect some samples from residents in the surrounding area of e-waste recycling sites. Prior to collecting samples, we submitted an application form of the collection and use of the fetal tissues to the Ethics Committee of this hospital. The Ethics Committee signed the ethical approval for the collection and use of the fetal tissues after a check. All of the participants agreed to participate in the investigation and signed an informed consent form. The participants also answered a short questionnaire about their personal, lifestyle, and pregnant characteristics. The questionnaire included whether there were e-waste recycling sites within 3 km away from her home or work: if so, we defined her as the residents in e-waste recycling sites; if not, she was regarded as the residents in the surrounding area of e-waste recycling sites. The fetuses and placentas were cleaned to remove blood and other connective tissues with distilled water after collecting. Maternal blood samples were collected before abortion. Samples were frozen at −20 °C in acetone-washed glass vials, stored in the dark in portable freezers, and shipped on dry ice to the laboratory for PBDE analysis. We obtained 65 paired aborted fetuses and placentas and 31 maternal blood samples. Table 1 shows the characteristics of these participants, who were the residents in the surrounding area of e-waste recycling sites.

n (%) 3 (4.6) 48 (73.8) 14 (21.6) 7 27 25 6

(10.8) (41.5) (38.5) (9.2)

18 24 14 9

(27.7) (36.9) (21.5) (13.9)

40 (61.5) 25 (38.5) 2 (3.1) 63 (96.9) 0 (0) 65 (100)

Sample Analysis. Blood samples were extracted following the method by Hovander et al.28 Briefly, approximately 5 mL of accurately weighed whole blood was poured into a screw-top centrifuge tube and spiked with 2 ng of BDE-71 and 20 ng of 13 C-BDE-209. Hydrochloric acid (6 M) and isopropanol were added to the sample, which was then rigorously mixed. Subsequently, we extracted each sample twice with methyltert-butyl ether/hexane (1:1, vol/vol). The combined organic phases were washed with aqueous potassium chloride (1 wt %/vol) and then evaporated to dryness for the gravimetric determination of the extracted lipid content. The concentrated extract was cleaned by passing it through a chromatography column (30 cm × 10 mm inner diameter) containing 8 g of sulfuric acid silica (30% acid by weight) and 2 g of anhydrous sodium sulfate on top and eluted with 100 mL of hexane. After elution, the extract was adjusted to the volume appropriate for gas chromatography−mass spectroscopy (GC−MS) analysis. Before extraction, the fetal and placental samples were freezedried using a lyophilizer. The freeze-dried samples were stored in tightly closed amber glass bottles and kept in a desiccator at −20 °C. All of the solid samples were analyzed using the method described by Dassanayake et al.,29 with some modifications. Briefly, after adding 2 ng of BDE-71 and 20 ng of 13C-BDE-209, the sample was thoroughly ground with anhydrous sodium sulfate using a glass pestle for approximately 5 min to produce a fine powder. Then, the sample was extracted with 30 mL of hexane/dichloromethane (1:1, vol/ vol) by ultrasonication for 4 min and centrifuged, and the solvent was removed. The extraction procedure was repeated twice. Lipid measurement and cleanup procedures for the fetal and placental samples were similar to those used for blood samples. Instrumental Parameters. PBDE analyses were completed by an Agilent 6890N/5973 GC−MS system (Agilent Technologies, Inc., Santa Clara, CA) operated in negative chemical ionization (NCI) mode and using selected ion B



Article

Table 2. PBDE Concentrations (ng/g of Lipida) in Aborted Fetuses (n = 65), Placentas (n = 65), and Maternal Blood (n = 31) PBDE, tissue BDE-28 fetus placenta blood BDE-47 fetus placenta blood BDE-99 fetus placenta blood BDE-100 fetus placenta blood BDE-153 fetus placenta blood BDE-154 fetus placenta blood BDE-183 fetus placenta blood BDE-197 fetus placenta blood BDE-209 fetus placenta blood ∑PBDEs fetus placenta blood

detectionb (%)

mean ± SD

minimum

25th percentile

median

75th percentile

maximum

100 100 100

0.38 ± 0.20 0.44 ± 0.22 1.15 ± 0.44

0.06 0.07 0.51

0.25 0.29 0.88

0.33 0.38 1.07

0.50 0.52 1.38

1.17 1.17 2.61

100 100 100

0.62 ± 0.36 0.73 ± 0.35 2.24 ± 0.71

0.17 0.25 1.43

0.37 0.53 1.73

0.55 0.65 2.00

0.74 0.82 2.73

1.85 1.69 4.48

98 100 100

0.20 ± 0.13 0.25 ± 0.20 0.71 ± 0.38

NDc 0.03 0.26

0.12 0.13 0.43

0.19 0.18 0.63

0.25 0.26 0.85

0.87 0.89 2.07

75 95 94

0.07 ± 0.07 0.15 ± 0.13 0.20 ± 0.17

ND ND ND

ND 0.07 0.08

0.07 0.12 0.16

0.12 0.19 0.26

0.46 0.73 0.76

100 100 100

0.62 ± 0.62 1.30 ± 0.75 3.06 ± 0.99

0.06 0.12 1.77

0.24 0.84 2.38

0.43 1.15 2.92

0.80 1.61 3.52

3.71 4.12 5.30

71 86 68

0.05 ± 0.05 0.10 ± 0.14 0.22 ± 0.15

ND ND ND

ND 0.04 0.11

0.04 0.07 0.22

0.06 0.11 0.30

0.34 1.03 0.61

86 100 97

0.20 ± 0.20 0.42 ± 0.41 0.41 ± 0.43

ND 0.07 ND

0.07 0.19 0.11

0.14 0.26 0.25

0.26 0.50 0.56

0.81 2.39 1.70

100 100 100

0.77 ± 0.66 1.59 ± 0.93 2.64 ± 0.91

0.15 0.59 1.07

0.38 1.08 1.92

0.59 1.45 2.69

0.94 1.84 2.94

4.59 6.38 5.01

100 100 100

1.55 ± 0.99 2.93 ± 1.46 5.05 ± 1.25

0.46 1.33 2.87

0.89 2.10 4.05

1.21 2.64 5.06

2.01 3.18 5.57

6.68 8.84 7.96

100 100 100

4.46 ± 2.88 7.90 ± 3.82 15.7 ± 4.51

1.08 3.37 10.3

2.71 6.06 12.2

3.68 7.00 14.8

5.46 8.47 17.7

19.9 26.7 28.2

a Mean lipid percentages of the fetuses, placentas, and blood were 1.07, 1.38, and 0.55%, respectively. bDetection rate is shown as a percentage (fetus and placenta, n = 65; blood, n = 31). cND = not detected.

monitoring (SIM). A 1 μL sample was injected in pulse splitless mode onto a Rtx-1614 fused silica capillary column (15 m × 0.25 mm inner diameter, 0.10 μm film thickness; Restek Corporation, Bellefonte, PA) with helium as a carrier gas at a constant flow rate of 1 mL/min. The ion source and transfer line temperatures were set to 150 and 280 °C, respectively. The GC oven temperature program was carried out as follows: isothermal at 100 °C, held for 2 min, increased to 250 °C at 25 °C/min, then to 260 °C at 1.5 °C/min, then to 325 °C at 25 °C/min, and held for 15 min. The ion fragments m/z 79 and 81 were monitored for the tri- to octa-BDE congeners, with m/z 488.7 and 486.7 for BDE-209 and m/z 492.7 and 494.7 for 13CBDE-209. Quality Assurance and Quality Control (QA/AC). The analytes were protected from light degradation throughout the extraction, cleanup, and analysis procedures by wrapping the containers with aluminum foil or using amber glassware. The

identification of the PBDE congeners was based on their retention times and the ratios of the monitored ions relative to the original congener standards. The accuracy of the whole method was checked using the fetal bovine serum samples and human full-term placenta samples (donated by one pregnant women living in Beijing, China) spiked with PBDE analytes, and the average recoveries of the PBDE congeners were 83− 105%. The recovery of the analytical method was monitored using BDE-71 and 13C-BDE-209. Recoveries [mean ± standard deviation (SD)] of BDE-71 and 13C-BDE-209 averaged 80 ± 6% and 64 ± 9% in blood, 86 ± 6% and 70 ± 10% in the fetuses, and 92 ± 11% and 68 ± 5% in the placentas, respectively. Results were corrected according to the recovery of the surrogate standard in each sample. The limits of detection (LODs), defined as 3 times the noise level, were in the range of 0.05−0.14 ng/g of lipid weight (lw) in blood samples, 0.007−0.18 ng/g of lw in the fetuses, and 0.007−0.22 C



Article

Kendall’s τ test revealed that there was not a significant correlation (p = 0.09) between the ∑PBDE concentration in the fetuses and gestational age (10−13 weeks). Similarly, the ∑PBDE concentration in the placentas did not correlate with gestational age (p = 0.67). A significant correlation was found between the ∑PBDE concentration in the 31 paired fetuses and maternal blood samples (p = 0.04). These results suggest that in utero exposure to PBDEs can be indicated by maternal blood PBDE concentrations. There were also significant correlations between the ∑PBDE concentrations in the 31 paired placenta and blood samples (p = 0.001) and between the 65 paired fetuses and placentas (p = 0.000). To characterize transplacental transfer of PBDEs, we calculated the concentration ratios between the fetus and blood samples (F/B) for the ∑PBDEs and each predominant congener, as shown in Figure 2. The higher the F/B ratio, the higher the relative amount transported across the placenta. The ∑PBDE F/B ratios in the 31 paired fetus and blood samples ranged from 0.15 to 0.33, with a mean of 0.23. Using the Kruskal−Wallis H test, we found no significant differences in the F/B ratios for BDE-28, BDE-99, and BDE-47. The F/B ratios for BDE-153, BDE-197, and BDE-209 were also similar to each other. The F/B ratios for BDE-28, BDE-99, and BDE47 were significantly higher than the ratios for BDE-153, BDE197, and BDE-209 (p < 0.05). These results suggest that the low-brominated congeners (BDE-28, BDE-99, and BDE-47) might be transferred to the fetus more easily than the highbrominated congeners (BDE-153, BDE-197, and BDE-209). We calculated the concentration ratios between the placenta and blood (P/B) and between the fetus and placenta (F/P) for the ∑PBDEs and each predominant congener to characterize the extent of PBDE retention in the placenta (Figure 2). The lower the P/B ratio and the higher the F/P ratio, the lower the relative amount of PBDEs was retained in the placenta. The ∑PBDE P/B ratios in the 31 paired placenta and blood samples ranged from 0.29 to 0.48, with a mean of 0.44. The ∑PBDE F/P ratios in the 65 paired fetuses and placentas ranged from 0.46 to 0.89, with a mean of 0.56. As shown in Figure 2, the P/B ratios for BDE-28, BDE-99, and BDE-47 were similar to each other but were significantly lower than those for BDE-153, BDE-197, and BDE-209 (p < 0.05). The F/ P ratios for BDE-28, BDE-99, and BDE-47 were similar to each other but were significantly higher than those for BDE-153, BDE-197, and BDE-209 (p < 0.05). These results suggest that the low-brominated congeners (BDE-28, BDE-99, and BDE47) might cross the placenta into the fetus more easily than high-brominated congeners (BDE-153, BDE-197, and BDE209), which tend to remain in the placenta more than the lowbrominated congeners.

ng/g of lw in the placentas. Concentrations below the LOD were regarded as zero when calculating the sum of the PBDE concentrations. Procedural blanks were analyzed with each extraction batch. All operational blanks were 5 might be limited or slow, while chemicals with log KOW values between −0.9 and 5 might easily cross the placental membrane.42 Therefore, the placental transfer of PBDEs should be limited because their log KOW values are higher than 5. However, previous data have shown that PBDE concentrations in cord blood were comparable to or slightly higher than concentrations in maternal blood, suggesting relatively free transfer of PBDEs from the maternal blood across the placenta.43,44 Moreover, several authors have noticed that low-brominated congeners made higher contribution to the ∑PBDE concentrations in cord blood than in maternal blood or that F/M ratios for low-brominated congeners were higher than F/M ratios for high-brominated congeners.37,38 These data suggest that there is less transport of the highly brominated PBDEs. Frederiksen et al.37 discussed in detail a decreasing trend in the placental transport of PBDE congeners with an increasing degree of bromination in paired maternal and umbilical blood. In agreement with these findings at the end of pregnancy, we also found that F/B ratios for the lowbrominated congeners were significantly higher than those for the high-brominated congeners. In addition, the P/B ratios for BDE-28, BDE-99, and BDE-47 were significantly lower than the ratios for BDE-153, BDE-197, and BDE-209, whereas the F/P ratios for BDE-28, BDE-99, and BDE-47 were significantly higher than the ratios for BDE-153, BDE-197, and BDE-209. Our results suggest that low-brominated congeners might more easily cross the placenta into the fetus, whereas highbrominated congeners tend to remain in the placenta. In other words, the placental barrier might partly prevent highbrominated congeners entering the fetus, even in the early stages of pregnancy. It is noted that tissue-specific differences in bioaccumulation and metabolism of PBDEs were neglected when the placental transport of PBDEs was discussed on the basis of apparent PBDE concentrations and congener patterns in paired fetuses, placentas, and maternal blood. To confirm our suggestion about the placental transport of PBDEs from this investigation, further experimental studies using in vitro or ex vivo early

■

ASSOCIATED CONTENT

S Supporting Information *

PBDE concentrations on a wet weight basis (Table S1). This material is available free of charge via the Internet at http:// pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*Telephone: 86-10-62946097. Fax: 86-10-62923563. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS We are grateful to reviewers and editors for reviewing the manuscript and their helpful comments. We acknowledge the Wenling Women’s and Children’s Hospital staff and participants. This work was supported by grants from the Hi-Tech Research and Development Program of China (863 Plan) (2010AA065105), the Public Welfare Research Project for Environmental Protection (201109048 and 201110250), and the National Natural Science Foundation of China (21077125). F



■

Article

(17) Talsness, C. E.; Kuriyama, S. N.; Sterner-Kock, A.; Schnitker, P.; Grande, S. W.; Shakibaei, M.; Andrade, A.; Grote, K.; Chahoud, I. In utero and lactational exposures to low doses of polybrominated diphenyl ether-47 alter the reproductive system and thyroid gland of female rat offspring. Environ. Health Perspect. 2008, 116 (3), 308−314. (18) Gómara, B.; Herrero, L.; Ramos, J. J.; Mateo, J. R.; Fernández, M. A.; García, J. F; González, M. J. Distribution of polybrominated diphenyl ethers in human umbilical cord serum, paternal serum, maternal serum, placentas, and breast milk from Madrid population, Spain. Environ. Sci. Technol. 2007, 41 (20), 6961−6968. (19) Herbstman, J. B.; Sjödin, A.; Apelberg, B. J.; Witter, F. R.; Patterson, D. G.; Halden, R. U.; Jones, R. S.; Park, A.; Zhang, Y.; Heidler, J.; Needham, L. L.; Goldman, L. R. Determinants of prenatal exposure to polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in an urban population. Environ. Health Perspect. 2007, 115 (12), 1794−1800. (20) Wu, K.; Xu, X.; Liu, J.; Guo, Y.; Li, Y.; Huo, X. Polybrominated diphenyl ethers in umbilical cord blood and relevant factors in neonates from Guiyu, China. Environ. Sci. Technol. 2010, 44 (2), 813− 819. (21) Herbstman, J. B.; Sjödin, A.; Kurzon, M.; Lederman, S. A.; Jones, R. S.; Rauh, V.; Needham, L. L.; Tang, D.; Niedzwiecki, M.; Wang, R. Y.; Perera, F. Prenatal exposure to PBDEs and neurodevelopment. Environ. Health Perspect. 2010, 118 (5), 712−719. (22) Bi, X. H.; Qu, W. Y.; Sheng, G. Y.; Zhang, W. B.; Mai, B. X.; Chen, D.; Yu, L.; Fu, J. Polybrominated diphenyl ethers in south China maternal and fetal blood and breast milk. Environ. Pollut. 2006, 144 (3), 1024−1030. (23) Wang, Y. W.; Jiang, G. B.; Lam, P. K.; Li, A. Polybrominated diphenyl ether in the east Asian environment: A critical review. Environ. Int. 2007, 33 (7), 963−973. (24) Zhu, L. G.; Ma, B. L.; Hites, R. A. Brominated flame retardants in serum from the general population in northern China. Environ. Sci. Technol. 2009, 43 (18), 6963−6968. (25) Zhang, L.; Li, J. G.; Zhao, Y. F.; Li, X. W.; Yang, X.; Wen, S.; Cai, Z. W.; Wu, Y. Q. A national survey of polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBs) in Chinese mothers’ milk. Chemosphere 2011, 84 (5), 625−633. (26) Qu, W. Y.; Bi, X. H.; Sheng, G. Y.; Lu, S. Y.; Fu, H.; Yuan, J.; Li, L. P. Exposure to polybrominated diphenyl ethers among workers at an electronic waste dismantling region in Guangdong, China. Environ. Int. 2007, 33 (8), 1029−1034. (27) Zhao, X. R.; Qin, Z. F.; Yang, Z. Z.; Zhao, Q.; Zhao, Y. X.; Qin, X. F.; Zhang, Y. C.; Ruan, X. L.; Zhang, Y. F.; Xu, X. B. Dual body burdens of polychlorinated biphenyls and polybrominated diphenyl ethers among local residents in an e-waste recycling region in southeast China. Chemosphere 2010, 78 (6), 659−666. (28) Hovander, L.; Athanasiadou, M.; Asplund, L.; Jensen, S.; Wehler, E. K. Extraction and cleanup methods for analysis of phenolic and neutral organohalogens in plasma. J. Anal. Toxicol. 2000, 24 (8), 696−703. (29) Dassanayake, R. M.; Wei, H.; Chen, R. C.; Li, A. Optimization of the matrix solid phase dispersion extraction procedure for the analysis of polybrominated diphenyl ethers in human placenta. Anal. Chem. 2009, 81 (23), 9795−9801. (30) Mazdai, A.; Dodder, N. G.; Abernathy, M. P.; Hites, R. A.; Bigsby, R. M. Polybrominated diphenyl ethers in maternal and fetal blood samples. Environ. Health Perspect. 2003, 111 (9), 1249−1252. (31) Sjödin, A.; Jones, R. S.; Focant, J.-F.; Lapeza, C.; Wang, R. Y.; McGahee, E. E. Retrospective time-trend study of polybrominated diphenyl ether and polybrominated and polychlorinated biphenyl levels in human serum from the United States. Environ. Sci. Technol. 2004, 112 (6), 654−658. (32) Qin, Y. Y.; Leung, C. K.; Lin, C.; Leung, A. O.; Wang, H. S.; Giesy, J. P.; Wong, M. H. Halogenated POPs and PAHs in blood plasma of Hong Kong residents. Environ. Sci. Technol. 2011, 45 (4), 1630−1637. (33) Zhao, Y. X.; Qin, X. F.; Li, Y.; Liu, P. Y.; Tian, M.; Yan, S. S.; Qin, Z. F.; Xu, X. B.; Yang, Y. J. Diffusion of polybrominated diphenyl

REFERENCES

(1) Alaee, M.; Arias, P.; Sjödin, A.; Bergman, A. An overview of commercially used brominated flame retardants, their applications, their use patterns in different ountries/regions and possible modes of release. Environ. Int. 2003, 29 (6), 683−689. (2) Darnerud, P. O.; Eriksen, G. S.; Jóhannesson, T.; Larsen, P. B.; Viluksela, M. Polybrominated diphenyl ethers: Occurrence, dietary exposure, and toxicology. Environ. Health Perspect. 2001, 109 (Supplement 1), 49−68. (3) Hale, R. C.; Alaee, M.; Manchester-Neesvig, J. B.; Stapleton, H. M.; Ikonomou, M. G. Polybrominated diphenyl ether flame retardants in the North American environment. Environ. Int. 2003, 29 (6), 771− 779. (4) Gebbink, W. A.; Sonne, C.; Dietz, R.; Kirkegaard, M.; Born, E. W.; Muir, D. C.; Letcher, R. J. Target tissue selectivity and burdens of diverse classes of brominated and chlorinated contaminants in polar bears (Ursus maritimus) from east Greenland. Environ. Sci. Technol. 2008, 42 (3), 752−759. (5) Hites, R. A. Polybrominated diphenyl ethers in the environment and in people: A meta-analysis of concentrations. Environ. Sci. Technol. 2004, 38 (4), 945−956. (6) Antignac, J. P.; Cariou, R.; Zalko, D.; Berrebi, A.; Cravedi, J. P.; Maume, D.; Marchand, P.; Monteau, F.; Riu, A.; Andre, F.; Le Bizec, B. Exposure assessment of French women and their newborn to brominated flame retardants: Determination of tri- to decapolybromodiphenylethers (PBDE) in maternal adipose tissue, serum, breast milk and cord serum. Environ. Pollut. 2009, 157 (1), 164−173. (7) Schecter, A.; Johnson-Welch, S.; Tung, K. C.; Harris, T. R.; Päpke, O.; Rosen, R. Polybrominated diphenyl ether (PBDE) levels in livers of U.S. human fetuses and newborns. J. Toxicol. Environ. Health, Part A 2007, 70 (1), 1−6. (8) Doucet, J.; Tague, B.; Arnold, D. L.; Cooke, G. M.; Hayward, S.; Goodyer, C. G. Persistent organic pollutant residues in human fetal liver and placenta from Greater Montreal, Quebec: A longitudinal study from 1998 through 2006. Environ. Health Perspect. 2009, 117 (4), 605−610. (9) Rawn, D.; Gaertner, D.; Sun, W.; Casey, V.; Curran, I.; Cooker, G.; Goodyer, C. Polybrominated diphenyl ethers (PBDEs) in Canadian human fetal liver and placental tissues. Organohalogen Compd. 2011, 73, 563−566. (10) Liu, P. Y.; Zhao, Y. X.; Zhu, Y. Y.; Qin, Z. F.; Ruan, X. L.; Zhang, Y. C.; Chen, B. J.; Li, Y.; Yan, S. S.; Qin, X. F.; Fu, S.; Xu, X. B. Determination of polybrominated diphenyl ethers in human semen. Environ. Int. 2012, 42, 132−137. (11) Branchi, I.; Capone, F.; Alleva, E.; Costa, L. G. Polybrominated diphenyl ethers: Neurobehavioral effects following developmental exposure. Neurotoxicology 2003, 24 (3), 449−462. (12) Stoker, T. E.; Cooper, R. L.; Lambright, C. S.; Wilson, V. S.; Furr, J.; Gray, L. E. In vivo and in vitro anti-androgenic effects of DE71, a commercial polybrominated diphenyl ether (PBDE) mixture. Toxicol. Appl. Pharmacol. 2005, 207 (1), 78−88. (13) Viberg, H.; Johansson, N.; Fredriksson, A.; Eriksson, J.; Marsh, G.; Eriksson, P. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicol. Sci. 2006, 92 (1), 211−218. (14) Zhou, T.; Taylor, M. M.; DeVito, M. J.; Crofton, K. M. Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol. Sci. 2002, 66 (1), 105−116. (15) Blake, C. A.; McCoy, G. L.; Hui, Y. Y.; LaVoie, H. A. Perinatal exposure to low-dose DE-71 increases serum thyroid hormones and gonadal osteopontin gene expression. Exp. Biol. Med. 2011, 236 (4), 445−455. (16) Bondy, G. S.; Gaertner, D.; Cherry, W.; MacLellan, E.; Coady, L.; Arnold, D. L; Doucet, J.; Rowsell, P. R. Brominated diphenyl ether (BDE) levels in liver, adipose, and milk from adult and juvenile rats exposed by gavage to the DE-71 technical mixture. Environ. Toxicol. 2011, 26 (6), 677−690. G



Article

ether (PBDE) from an e-waste recycling area to the surrounding regions in southeast China. Chemosphere 2009, 76 (11), 1470−1476. (34) Johnson-Restrepo, B.; Kannan, K.; Rapaport, D. P.; Rodan, B. D. Polybrominated diphenyl ethers and polychlorinated biphenyls in human adipose tissue from New York. Environ. Sci. Technol. 2005, 39 (14), 5177−5182. (35) Kunisue, T.; Takayanagi, N.; Isobe, T.; Takahashi, S.; Nose, M.; Yamada, T.; Komori, H.; Arita, N.; Ueda, N.; Tanabe, S. Polybrominated diphenyl ethers and persistent organochlorines in Japanese human adipose tissues. Environ. Int. 2007, 33 (8), 1048− 1056. (36) Foster, W. G.; Gregorovich, S.; Morrison, K. M.; Atkinson, S. A.; Kubwabo, C.; Stewart, B.; Teo, K. Human maternal and umbilical cord blood concentrations of polybrominated diphenyl ethers. Chemosphere 2011, 84 (10), 1301−1309. (37) Frederiksen, M.; Thomsen, C.; Frøshaug, M.; Vorkamp, K.; Thomsen, M.; Becher, G.; Knudsen, L. E. Polybrominated diphenyl ethers in paired samples of maternal and umbilical cord blood plasma and associations with house dust in a Danish cohort. Int. J. Hyg. Environ. Health 2010, 213 (4), 233−242. (38) Kawashiro, Y.; Fukata, H.; Omori-Inoue, M.; Kubonoya, K.; Jotaki, T.; Takigami, H.; Sakai, S.; Mori, C. Perinatal exposure to brominated flame retardants and polychlorinated biphenyls in Japan. Endocr. J. 2008, 55 (6), 1071−1084. (39) Vizcaino, E.; Grimalt, J. O.; Lopez-Espinosa, M. J.; Llop, S.; Rebagliato, M.; Ballester, F. Polybromodiphenyl ethers in mothers and their newborns from a non-occupationally exposed population (Valencia, Spain). Environ. Int. 2011, 37 (1), 152−157. (40) Takasuga, T.; Senthilkumar, K.; Takemori, H.; Ohi, E.; Tsuji, H.; Nagayama, J. Impact of fermented brown rice with Aspergillus oryzae (FEBRA) intake and concentrations of polybrominated diphenylethers (PBDEs) in blood of humans from Japan. Chemosphere 2004, 57 (8), 795−811. (41) Frederiksen, M.; Thomsen, M.; Vorkamp, K.; Knudsen, L. E. Patterns and concentration levels of polybrominated diphenyl ethers (PBDEs) in placental tissue of women in Denmark. Chemosphere 2009, 76 (11), 1464−1469. (42) Takahashi, O.; Oishi, S. Disposition of orally administered 2,2bis(4-hydroxyphenyl)propane (bisphenol A) in pregnant rats and the placental transfer to fetuses. Environ. Health Perspect. 2000, 108 (10), 931. (43) Kim, T. H.; Bang, D. Y.; Lim, H. J.; Jin Won, A.; Ahn, M. Y.; Patra, N.; Chung, K. K.; Kwack, S. J.; Park, K. L.; Han, S. Y. Comparisons of polybrominated diphenyl ethers levels in paired South Korean cord blood, maternal blood, and breast milk samples. Chemosphere 2012, 87 (1), 97−104. (44) Kang, C. S.; Lee, J. H.; Kim, S. K.; Lee, K. T.; Lee, J. S.; Park, P. S.; Yun, S. H.; Kannan, K.; Yoo, Y. W.; Ha, J. Y.; Lee, S. W. Polybrominated diphenyl ethers and synthetic musks in umbilical cord serum, maternal serum, and breast milk from Seoul, South Korea. Chemosphere 2010, 80 (2), 116−122. (45) Frederiksen, M.; Vorkamp, K.; Mathiesen, L.; Mose, T.; Knudsen, L. E. Research placental transfer of the polybrominated diphenyl ethers BDE-47, BDE-99 and BDE-209 in a human placenta perfusion system: an experimental study. Environ. Health 2010, 9, 32. (46) Costa, L. G.; Giordano, G. Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 2007, 28 (6), 1047−1067. (47) Williams, A. L.; DeSesso, J. M. The potential of selected brominated flame retardants to affect neurological development. J. Toxicol. Environ. Health, Part B 2010, 13 (5), 411−448. (48) Ta, T. A.; Koenig, C. M.; Golub, M. S.; Pessah, I. N.; Qi, L.; Aronov, P. A.; Berman, R. F. Bioaccumulation and behavioral effects of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicol. Teratol. 2011, 33 (3), 393−404.

H


Polybrominated Diphenyl Ethers (PBDEs) in Aborted Human

Recommend Documents