A national survey of polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBs) in Chinese mothers’ milk

Chemosphere 84 (2011) 625–633

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A national survey of polybrominated diphenyl ethers (PBDEs) and indicator polychlorinated biphenyls (PCBs) in Chinese mothers’ milk Lei Zhang a, Jingguang Li a,b,⇑, Yunfeng Zhao a, Xiaowei Li a, Xin Yang a, Sheng Wen a,c, Zongwei Cai b, Yongning Wu a a b c

Key Lab of Chemical Safety and Health, National Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, 29 Nanwei Road, Beijing 100050, China Department of Chemistry, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China Hubei Provincial Centre for Disease Control and Prevention, 6 Zhuodaoquanbei Road, Wuhan 430079, China

a r t i c l e

i n f o

Article history: Received 18 November 2010 Received in revised form 9 March 2011 Accepted 22 March 2011 Available online 19 April 2011 Keywords: Polybrominated diphenyl ethers Indicator polychlorinated biphenyls Human milk Body burden Risk assessment

a b s t r a c t Seven polybrominated diphenyl ethers (PBDEs) congeners (BDE-28, BDE-47, BDE-99, BDE-100, BDE-153, BDE-154 and BDE-183) and six indicator polychlorinated biphenyls (PCBs) congeners (CB-28, CB-52, CB101, CB-138, CB-153 and CB-180) were measured in 24 pooled human milk samples comprised of 1237 individual samples from 12 provinces in China. The samples were taken to estimate the background body burden of general population and assess nursing infant exposure via human milk in China. The median P P 1 lipid weight (lw), respectively. concentrations of 7PBDEs and 6PCBs were 1.49 and 10.50 ng g P BDE-28, BDE-47 and BDE-153 were predominant PBDE congeners accounting for nearly 70% of 7PBDEs. As for indicator PCBs, CB-153 was the most abundant congener, followed by CB-138. In our study, there was no significantly statistical relationship between concentrations of PBDEs in milk samples and materP P nal age as well as dietary habits. 7PBDEs did not correlate to 6PCBs in Chinese mothers’ milk. The human exposure to indicator PCBs in China was found to be significantly determined by maternal age, dietary habits and geographical factors. It is suggested that Chinese general population is probably exposed to PBDEs with multiple sources and pathways. The estimated daily intakes (EDI) of BDE-47, BDE-99 and BDE-153 for the Chinese nursing infant were much lower than corresponding threshold reference values suggested by USEPA. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) are persistent, lipophilic chemicals identified as global environmental and human contaminants. PBDEs are one class of brominated flame retardants (BFRs) widely used in electronic appliances, textiles, furnishings and various other consumer products. Due to persistence and bioavailability/biomagnification in combination with very large production and consumption, PBDEs have become ubiquitous in biological and environmental samples worldwide (Wang et al., 2007). The levels of PBDEs in human tissue increased exponentially from the 1970s, but appeared to have stabilized or decreased since the late 1990s or early 2000s (Meironyté et al., 1999; Akutsu et al., 2003; Thomsen et al., 2007; Fängström et al., 2008; Lignell et al., 2009). The commercial use and production of Penta- and Octa-BDE mixtures have been banned in the European Union and Japan since the late 1990s ⇑ Corresponding author at: Key Lab of Chemical Safety and Health, National Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, 29 Nanwei Road, Beijing 100050, China. Tel./fax: +86 010 83132933. E-mail address: [email protected] (J. Li). 0045-6535/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2011.03.041

(Akutsu et al., 2003; Wang et al., 2007). Similarly, the United States ceased the production of these BFRs in 2005 (Wang et al., 2007). Unlike PBDEs, the production and use of PCBs have been banned all over the world and levels of PCBs in human tissues have decreased rapidly since the 1970s (Jaraczewska et al., 2006; Raab et al., 2007; Bordajandi et al., 2008; Lignell et al., 2009). Human exposure to PCBs and dioxins mainly comes from food of animal origin (Liem et al., 2000). Although PBDEs could be bioaccumulated in the food chain, the prime exposure pathway for the general population is unclear. Diet intake has been suggested the most important pathway in Belgium (Roosens et al., 2010), but another study indicated that ingestion and dermal absorption of house dust is the largest contributor in the United States (Johnson-Restrepo and Kannan, 2009). Collectively, human milk has been estimated as the main exposure source of PBDEs for breastfeeding infants (Johnson-Restrepo and Kannan, 2009; Toms et al., 2009a; Roosens et al., 2010). The fetus and developing children are far more sensitive than the adults to the effects of many chemicals. Thus, the accumulation of organic contaminants in human milk has been a matter of growing concern in the world. In this study, a national survey of PBDEs and indicator PCBs levels in human milk was carried out for the first time to evaluate the

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background body burden of general population and breastfeeding infant exposure and investigate how levels of PBDEs in human milk vary with diet habits and geographical location in China.

2. Materials and methods 2.1. Samples collection and preparation The selection of volunteering mothers and collection of human milk samples followed the ‘Guideline for Developing a National Protocol’ of the Fourth WHO-Coordinated Survey of Human milk for Persistent Organic Pollutants in Cooperation with UNEP (WHO, 2007a; Li et al., 2009). All participants were told the objective of this study and signed the participant information and consent form. Donors were all primiparous mothers, willing to provide a minimum of 100 mL milk. These participants came from 12 provinces (shown in Fig.1). The population of these provinces accounts for about 50% of the total population of China. In each province, one urban site and two rural sites were selected. These regions were also sampling sites for the Chinese Total Dietary Study (TDS) in 2000. A total of 1237 human milk samples were obtained from August to November in 2007. An individual human milk sample was collected either using a pump or by hand directly expressing the milk into the pre-washed polypropylene jar, which was provided to the mothers by the study team, frozen immediately and kept at 20 °C in our laboratory until analysis. These samples were divided into 24 pools based on mother’s residence. For each province the urban individual human milk samples were pooled into one composite sample and rural samples were pooled into another composite sample. When the collection of a pool was com-

pleted the milk was thawed, homogenized by shaking, and 10 mL from each individual was pooled giving a composite milk sample from each region. The pooled samples were stored at 20 °C until analyzed. A questionnaire was applied to record the content of face-toface interview for each mother. The information included date of birth, place of birth, residence record, dietary habits (vegetarian/ omnivore), occupation and history of smoking. The average consumption of aquatic foods, meat, eggs and dairy products derived from the Chinese TDS in 2000 was applied to reflect general dietary habits of the mothers from every province. The consumption data was obtained from a 3-d household dietary survey in the same 12 provinces (Li et al., 2007).

2.2. Analytical methods Analysis of PBDEs and indicator PCBs were described elsewhere (Li et al., 2008, 2009), with slightly modification. Briefly, approximately 100 mL of pooled human milk sample was freeze-dried and spiked with 13C-labeled internal standards of PBDEs (13CBDE-28, -47, -99, -100, -153, -154 and -183) and 13C-labeled internal standards of indicator PCBs (13C-CB-28, -52, -101, -138, -153 and-180). The samples were Soxhlet-extracted with a mixture of 50% hexane/dichloromethane (1:1) for 24 h. Gravimetric lipid determination was performed after solvent evaporation. The lipid fraction was dissolved in hexane and removed by shaking with acid-modified silica gel at 60 °C. The hexane extracts were then concentrated prior to clean-up on a Power Prep instrument (Fluid Management System, Waltham, MA, USA) with multiple silica columns and alumina columns. Elution through the different columns

Fig. 1. Sampling provinces in China in 2007.

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was computer controlled. The fraction containing the PBDEs and indicator PCBs was collected. After concentrating this fraction to approximately 50 lL, the 13C-labeled injection standards (13C-CB70, -111 and -170) were added prior to instrument analysis. The identification and quantification was performed by high resolution gas chromatography – high resolution mass spectrometry (HRGC/HRMS, MAT95XP, ThermoFinnigan, Germany). DB-5MS capillary columns, 15 m  0.25 mm i.d. 0.1 lm and 60 m  0.25 mm i.d. 0.25 lm, were applied to analysis of PBDEs and indicator PCBs, respectively. 2.3. QA/QC In this study, one procedural blank were performed every eleven human milk samples. The amount of detected congeners should be more than three times of that in the procedural blank. The concentrations of the detected congeners have been corrected by subtracting the procedural blank level in this study. The recoveries of internal standard were all in the range of 40–110%. The laboratory performance was validated by successfully participating in inter-laboratory comparison studies of PBDEs and indicator PCBs in human milk organized by the Norwegian Institute of Public Health in 2006. Z-scores of sum PBDEs without BDE209 and sum indicator PCBs were 0.33 and 0.94, respectively. 2.4. Statistical analysis The values for most PBDE congeners (BDE-28, -47, -99, -100, 153 and -154) and indicator PCB congeners (CB-52, -101, -138 and -153) were normally distributed. The data of BDE-183 and CB-180 were log-transformed before performing statistical analysis. For these congeners, Independent-samples t-test was applied to determine differences of urban/rural areas and inland/coastal areas, respectively. Because of the unknown distribution of the data of CB-28, Wilcoxon rank-sum test was applied to determine the geographical differences. Spearman correlation analyses were used to investigate correlations between the concentrations of

PBDE congeners and indicator PCB congeners, maternal age, milk lipid content and dietary habits. All statistical analyses were performed with the SAS software package (version 8.2; SAS Institute Inc., Cary, NC). All p values are two-tailed, and a were set at a significance level of 0.05. 3. Results 3.1. Characteristics of the participants The participants were recruited in 24 regions from 12 provinces in China (Table 1). The mean age and lipid content of the pooled sample were 25.5 years and 3.8%, respectively. The donors were almost all omnivores, which was consistent with the Chinese TDS. According to the questionnaires, none of the mothers smoked and suffered from occupational exposure. 3.2. Concentrations and profiles of POPs in human milk The concentrations of selected PBDE congeners in the 24 pooled samples obtained from August to November in 2007 are presented in Table 2. All PBDE congeners were determined above limit of quantitation (LOQ) in all samples. The mean ± standard deviation P and median 7PBDEs concentrations were 1.58 ± 0.58 and 1 1.49 ng g lw, respectively. Across all regions the concentrations P of 7PBDEs varied by a factor of about three from a minimum of 0.85 ng g 1 lw detected in the urban area of Hebei and rural area of Ningxia to a maximum of 2.97 ng g 1 lw detected in the rural area of Guangxi. There was no significant difference found between the concentrations of PBDEs in human milk from distinct geographical locations (costal or inland, rural or urban). The congener profiles of PBDEs in all samples are shown in Fig. 2. BDE-28, BDE47 and BDE-153 were predominant congeners, and these three P congeners accounted for nearly 70% of 7PBDEs in most samples. Results of the determination of indicator PCBs in human milk pooled samples are shown in Table 3. All 6 selected indicator PCB congeners were measured in almost all samples. The concentraP tions of 6PCBs varied from 2.36 ng g 1 lw (rural area of Ningxia)

Table 1 Descriptive statistics of the participants. Regions

Number of participants

Age (years)

Milk lipid (%)

Average

Range

Urban area of Hebei Rural area of Hebei Urban area of Heilongjiang Rural area of Heilongjiang Urban area of Liaoning Rural area of Liaoning Urban area of Hean Rural area of Hean Urban area of Ningxia Rural area of Ningxia Urban area of Shanxi Rural area of Shanxi Urban area of Hubei Rural area of Hubei Urban area of Sichuan Rural area of Sichuan Urban area of Guangxi Rural area of Guangxi Urban area of Shanghai Rural area of Shanghai Urban area of Jiangxi Rural area of Jiangxi Urban area of Fujian Rural area of Fujian

40 60 50 52 50 60 50 60 50 60 50 40 50 60 30 55 50 60 50 60 50 60 50 40

27.7 24.9 25.8 24.7 26.4 26.8 27.6 23.8 25.2 21.5 26.9 25.5 25.7 24.6 24.2 24.7 28.1 25.2 27.1 26.7 23.9 24.3 26.0 24.5

21–35 19–35 21–30 20–34 20–31 20–36 21–35 20–30 20–36 18–29 21–35 19–34 19–30 20–30 20–29 20–30 23–34 18–37 23–35 21–35 18–33 18–30 21–29 18–29

3.0 2.6 3.5 3.5 3.3 4.0 2.8 5.0 4.5 4.2 3.9 4.0 3.0 4.9 2.7 4.4 5.0 5.1 3.5 3.4 4.1 3.0 3.9 3.8

Mean

–

25.5

–

3.8

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Table 2 Concentrations of PBDEs in breast milk samples (ng g

1

lipid weight).

Regions

BDE-28

BDE-47

BDE-99

BDE-100

BDE-153

BDE-154

BDE-183

P PBDEs

Urban area of Hebei Rural area of Hebei Urban area of Heilongjiang Rural area of Heilongjiang Urban area of Liaoning Rural area of Liaoning Urban area of Henan Rural area of Henan Urban area of Ningxia Rural area of Ningxia Urban area of Shanxi Rural area of Shanxi Urban area of Hubei Rural area of Hubei Urban area of Sichuan Rural area of Sichuan Urban area of Guangxi Rural area of Guangxi Urban area of Shanghai Rural area of Shanghai Urban area of Jiangxi Rural area of Jiangxi Urban area of Fujian Rural area of Fujian

0.16 0.41 0.21 0.28 0.37 0.50 0.26 0.15 0.31 0.22 0.40 0.36 0.27 0.29 0.24 0.16 0.41 0.49 0.21 0.38 0.25 0.30 0.16 0.15

0.33 0.62 0.21 0.29 0.37 0.61 0.35 0.25 0.31 0.32 0.38 0.65 0.35 0.51 0.46 0.23 0.68 0.73 0.36 0.41 0.49 0.38 0.41 0.52

0.09 0.13 0.05 0.07 0.09 0.11 0.08 0.05 0.04 0.10 0.06 0.12 0.09 0.07 0.14 0.06 0.13 0.11 0.09 0.06 0.08 0.06 0.07 0.07

0.10 0.07 0.06 0.04 0.08 0.13 0.05 0.04 0.03 0.02 0.08 0.13 0.08 0.13 0.07 0.04 0.14 0.21 0.13 0.08 0.13 0.09 0.08 0.13

0.10 0.46 0.25 0.38 0.45 0.99 0.36 0.28 0.14 0.14 0.39 0.48 0.52 0.46 0.69 0.57 0.94 1.14 0.55 0.37 0.54 0.45 0.52 0.66

0.03 0.03 0.01 0.02 0.03 0.06 0.02 0.01 0.01 0.01 0.02 0.02 0.03 0.05 0.04 0.05 0.04 0.06 0.04 0.03 0.04 0.03 0.03 0.08

0.04 0.11 0.09 0.04 0.11 0.19 0.09 0.08 0.03 0.04 0.07 0.09 0.15 0.38 0.48 0.18 0.14 0.22 0.07 0.15 0.49 0.14 0.31 0.30

0.85 1.83 0.89 1.12 1.51 2.59 1.21 0.86 0.87 0.85 1.39 1.85 1.49 1.89 2.13 1.30 2.48 2.97 1.45 1.49 2.01 1.44 1.58 1.91

Mean SD Median Min Max

0.29 0.11 0.28 0.15 0.50

0.43 0.15 0.38 0.21 0.73

0.08 0.03 0.08 0.04 0.14

0.09 0.04 0.08 0.02 0.21

0.49 0.26 0.46 0.10 1.14

0.03 0.02 0.03 0.01 0.08

0.17 0.13 0.12 0.03 0.49

1.58 0.58 1.49 0.85 2.97

to 28.75 ng g 1 lw (urban area of Shanghai) with a mean of 11.71 ng g 1 lw and a median of 10.50 ng g 1 lw. Moreover, the PCB levels in human milk from coastal area were significantly higher than that from inland areas (p < 0.01). CB-153 was the most predominant congener, followed by CB-138. There was no significant correlation between levels of PBDEs (individual congeners and the sum) in human milk samples and maternal age, fat content of human milk, dietary consumption using Spearman correlation tests (p > 0.05). However, maternal age, consumption of eggs and aquatic foods were all significantly P positive correlated to 6PCBs (p < 0.001), but fat content of human P milk was negatively associated with 6PCBs (p < 0.05). No significant correlation was found between concentrations of PBDEs and those of PCBs (p > 0.05). In our previous study, dioxin-like polychlorinated biphenyls (dl-PCBs) and PCDD/Fs were measured in P the same human milk samples (Li et al., 2009). 6PCBs was significantly correlated to TEQdl-PCBs and TEQPCDD/Fs (p < 0.01), and P 7PBDEs was correlated to TEQdl-PCBs (p < 0.01). 3.3. Infant exposure The calculation of daily intake of PBDEs, assuming that an average infant weighs 5 kg and consumes 700 mL human milk per day (Li et al., 2009), showed that the median infant’s estimated daily P P intake (EDI) of PBDEs and indicator PCBs via human milk in China was approximately 8.1 ng kg 1 body wt day 1 and 54.6 ng kg 1 body wt day 1, respectively. 4. Discussion 4.1. PBDEs in human milk To understand the magnitude of contamination by PBDEs, the results from this study are compared with those observed in other countries (Table 4). Global comparison indicated that the levels ob-

served in this study are only higher than that from Vietnam (Haraguchi et al., 2009), comparable to those from Czech Repulic (Kazda et al., 2004), Germany (Vieth et al., 2005), Poland (Jaraczewska et al., 2006), Indonesia (Sudaryanto et al., 2008a), Japan (Haraguchi et al., 2009) and Norway (Thomsen et al., 2010). The concentrations reported here are slightly lower than those from Sweden (Lind et al., 2003), the United Kingdom (Kalantzi et al., 2004), Denmark (Main et al., 2007), Finland (Main et al., 2007), Italy (Ingelido et al., 2007), Spain (Schuhmacher et al., 2007), Korea (Haraguchi et al., 2009) and France (Antignac et al., 2009), and much lower than that from Australia (Toms et al., 2007), Canada (She et al., 2007) and USA (Schecter et al., 2003, 2010; JohnsonRestrepo et al., 2007; She et al., 2007; Wu et al., 2007; Dunn et al., 2010). These results may reflect the amounts of usage and composition of commercial PBDEs mixtures in different countries (Zhu et al., 2009b). The amounts of these commercial mixtures demanded in North America were much higher than that in Europe and Asia. However, China is one of the major BFR-manufacturing countries (especially Deca-BDE) and significant countries of destination for electric waste (e-waste) from developed countries (Wang et al., 2007; Ni and Zeng, 2009). It has been estimated that about 261,000 tons of PBDEs were imported into Guangdong province in 2002 in scrap electronic devices (Martin et al., 2004). This estimate is about 3-fold higher than the global production of PBDEs in 1999. Moreover, significantly higher levels of PBDEs have been detected in human biological samples from production area and e-waste recycling sites (Jin et al., 2009; Wen et al., 2009; Wu et al., 2010). But the human exposure to PBDEs seems to be low in China, which may be due to the relatively less amount of usage of commercial PBDEs in the past. Owing to the wide use and large production, levels of PBDEs in human milk collected from developed countries increased rapidly during two decades from 1970s (Meironyté et al., 1999; Akutsu et al., 2003). The production and usage of low brominated BDEs (Penta- and Octa-BDE commercial mixtures) has been restricted and banned in Europe, USA and Japan. Time trend studies pointed

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Fig. 2. PBDE congener profiles in breast milk samples from China.

Table 3 Concentrations of indicator PCBs in breast milk samples (ng g Regions

CB-28

1

lipid weight). CB-101

CB-138

CB-153

CB-180

P

a

0.32 0.19 0.18 0.22 0.18 0.34 0.17 0.07 0.04 0.09 0.15 0.13 0.27 0.08 0.18 0.05 0.26 0.16 0.22 0.27 0.13 0.17 0.15 0.24

9.26 4.60 3.70 2.47 6.52 5.27 3.56 1.21 1.28 0.91 2.34 2.12 4.83 3.89 3.19 1.89 4.65 2.64 9.61 5.22 3.20 5.13 3.58 6.23

11.02 5.30 5.48 3.61 6.02 11.18 4.51 1.66 1.95 0.49 3.12 2.80 8.16 5.04 2.69 3.29 7.27 3.86 15.85 10.14 3.41 7.54 5.94 10.51

0.15 0.44 0.76 0.35 0.72 1.18 0.55 0.22 0.22 0.05 0.45 0.30 0.96 0.60 0.46 0.14 0.87 0.33 1.83 1.61 0.47 0.62 0.51 1.87

20.75 12.05 10.72 7.29 14.19 18.84 9.63 3.67 4.13 2.36 7.53 6.48 15.06 10.27 7.88 5.89 14.18 7.41 28.75 18.41 9.81 14.35 10.93 20.46

0.14 0.06 0.15 (0.0005)a 0.25

0.18 0.08 0.18 0.04 0.34

4.05 2.26 3.64 0.91 9.61

5.87 3.72 5.17 0.49 15.85

0.65 0.51 0.49 0.05 1.87

11.71 6.35 10.50 2.36 28.75

CB-52 a

Urban area of Hebei Rural area of Hebei Urban area of Heilongjiang Rural area of Heilongjiang Urban area of Liaoning Rural area of Liaoning Urban area of Henan Rural area of Henan Urban area of Ningxia Rural area of Ningxia Urban area of Shanxi Rural area of Shanxi Urban area of Hubei Rural area of Hubei Urban area of Sichuan Rural area of Sichuan Urban area of Guangxi Rural area of Guangxi Urban area of Shanghai Rural area of Shanghai Urban area of Jiangxi Rural area of Jiangxi Urban area of Fujian Rural area of Fujian

(0.0003) 1.30 0.49 0.50 0.57 0.70 0.68 0.42 0.58 0.65 1.31 0.98 0.67 0.57 1.14 0.44 0.99 0.33 1.02 0.92 2.49 0.77 0.62 1.41

Mean SD Median Min Max

0.81 0.49 0.68 (0.0003)a 2.49

(0.0005) 0.22 0.11 0.14 0.18 0.17 0.16 0.09 0.06 0.17 0.16 0.15 0.17 0.09 0.22 0.08 0.14 0.09 0.22 0.25 0.11 0.12 0.13 0.20

out that PBDE levels (the Sum of tri- to hexabrominated congeners) in human milk appeared to have stabilized or decreased in Europe and Japan since the late 1990s (Akutsu et al., 2003; Fängström et al., 2008; Lignell et al., 2009). A similar trend has been observed in serum samples from Norway (Thomsen et al., 2007). However, the concentrations of PBDEs in human milk from Texas have not significantly decreased following the discontinuation of the production of the Penta- and Octa- commercial mixtures (Schecter et al., 2003, 2010), which might due to limited numbers of milk samples. Unfortunately, there is no formal restriction or ban on commercial usage and production of PBDEs in China. It was re-

6PCBs

ported that Octa-BDE commercial mixture was still producing in China (Sudaryanto et al., 2008b). Hence, a long-term project for the trend study on PBDEs levels in human milk samples is necessary and worthy. In previous studies, levels of PBDEs were determined in human milk samples from some regions of China (showed in Fig. 3), including Beijing (Zhang et al., 2009), Tianjin (Zhu et al., 2009b), Nanjing, Zhoushan (Sudaryanto et al., 2008b), Guangdong (Bi et al., 2006) and Taiwan (Chao et al., 2007, 2010). The concentrations of PBDEs in this study were in line with those from Beijing, Tianjin, Southern Taiwan, Nanjing and Zhoushan, but lower than those from Guang-

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Table 4 P Comparison of concentrations of PBDEs in breast milk from different countries and regions (ng g

a b c d

Number of Type of donors samples

1

lipid weight).

BDE-28 BDE-47 BDE-99 BDE-100 BDE-153 BDE-154 BDE-183

P

Country/region

Sampling year

Sweden (Uppsala County)a Denmarka Finlanda Norwaya Germanya Francea United Kingdoma Poland (Wielkopolska)c Czech Republic (Olomouc)a Spain (Madrid)a Spain (Madrid)a Italy (Rome)a USA (Texas)a USA and Canada (Pacific Northwest)a USA (Massachusetts)a

1996–1999 93

Individuals NAc

1.78

0.43

0.27

0.50

0.06

NAc

3.15

Lind et al. (2003)

1997–2001 1997–2001 2003–2005 2001–2004 2004–2006 2001–2003 2004

36 32 393 89 77 54 22

Individuals Individuals Individuals Individuals Individuals Individuals Individuals

1.05 1.24 0.99 0.51 1.152 2.7 1.07

0.44 0.39 0.27 0.16 0.527 0.8 0.47

0.26 0.30 0.25 0.15 0.226 0.5 0.15

1.0 0.67 0.45 0.49 0.781 1.3 0.53

0.04 0.04 0.036 0.02 0.040 0.4 NDd

0.05 NDd 0.060 0.03 0.119 NAc 0.08

3.27 3.11 2.1 1.72 2.51 6.3 2.5

Main et al. (2007) Main et al. (2007) Thomsen et al. (2010) Vieth et al. (2005) Antignac et al. (2009) Kalantzi et al. (2004) Jaraczewska et al. (2006)

2003

103

Individuals 0.07

0.61

0.22

0.12

0.15

0.09

0.24

NAc

Kazda et al. (2004)

2003–2004 2003–2004 2000–2001 2002 2003

22 30 10 47 40

Individuals Individuals Pools Individuals Individuals

0.37 0.22 1.9 18.4 27.8

0.51 0.38 0.97 5.7 5.36

0.58 0.46 0.48 9.2 5.25

0.13 0.10 0.47 2.0 4.79

0.02 NDd 0.070 0.22 0.40

0.30 0.28 0.092 0.07 0.20

6.1 5.5 4.1 34.0 50.4

Gómara et al. (2007) Gómara et al. (2007) Ingelido et al. (2007) Schecter et al. (2003) She et al. (2007)

2004

38

Individuals 0.47

7.69

1.46

NDd

1.06

0.05

4.13

19.8

USA (the Greater Boston)a USA (New Hampshire)a USA (Texas)a Australiaa Japanb Vietnam (Hanoi)b Korea (Seoul)b Indonesiaa China

2004–2005 46

Individuals 0.9

13.9

2.4

2.4

3.0

0.2

0.1

0.10 0.12 0.093 0.03 0.089 0.2 0.07

0.01 NDd 0.082 1.2 1.72

PBDEs Reference

30.2

Johnson-Restrepo et al. (2007) Wu et al. (2007)

d

2005–2006 40

Individuals 1.5

13.4

2.0

2.5

4.9

0.1

ND

29.7

Dunn et al. (2010)

2007 2002–2003 2007–2008 2007 2007 2001–2003 2007

Individuals Pools Individuals Individuals Individuals Individuals Pools

14.9 5.59 0.64 0.19 2.0 0.30 0.38

3.0 1.84 0.12 0.02 0.33 0.15 0.08

2.8 1.25 0.11 0.02 0.28 0.11 0.08

6.6 1.02 0.39 0.14 0.86 0.22 0.46

0.3 0.14 0.16 0.005 0.13 0.03 0.03

0.3 0.11 NAc NAc NAc 0.09 0.12

27.8 11.0 1.5 0.42 3.7 1.5 1.49

Schecter et al. (2010) Toms et al. (2007) Haraguchi et al. (2009) Haraguchi et al. (2009) Haraguchi et al. (2009) Sudaryanto et al. (2008a) This study

29 157 60 20 20 30 1327

0.3 NAc 0.07 0.04 0.14 0.03 0.28

Median. Mean. NA: not available. ND: no detection.

Fig. 3. Levels of PBDEs in breast milk from some regions of China.

dong and Central Taiwan. Guangdong is the main recipient for ewaste in China. The pooled sample from Guangxi, which is located next to Guangdong, had higher levels of PBDEs in this study. In previous studies, BDE-47 was the most predominant congener in human milk and the concentration of BDE-47 was significantly higher than that of other congeners (tri- to heptabrominated congeners) (Akutsu et al., 2003; Lind et al., 2003; Schecter et al., 2003, 2010; Kalantzi et al., 2004; Kazda et al., 2004; Toms et al., 2009a; Thomsen et al., 2010). However, in this study the contribution of BDE-153 was greater or equal to that of BDE-47 in most pooled samples (Fig. 2), which was similar to profiles observed in human milk samples from the Faroe Islands

(Fängström et al., 2005), Germany (Vieth et al., 2005), Denmark (Main et al., 2007), Russia (Tsydenova et al., 2007) and Indonesia (Sudaryanto et al., 2008a). A recent Swedish study on time trends showed that patterns of PBDE congeners in human milk significantly changed and the contribution of BDE-153 increased (Lignell et al., 2009). These differences may be explained by different commercial PBDE mixtures used as exposure source and difference in persistence. BDE-47 dominates in some Penta-BDE mixtures, whereas BDE-153 is a significant component of some Octa-BDE mixtures (La Guardia et al., 2006). Moreover, the elimination half-live for BDE-153 was much longer than that for other congeners in human body (Vieth et al., 2005).

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Interestingly, BDE-28 was a major congener in human milk samples from China which is different from almost all other countries (listed in Table 4). BDE-28 is not typically among the most abundant congeners, although a high abundance of this congener was observed in human milk samples from Japan (Akutsu et al., 2003) and Spain (Bordajandi et al., 2008). The Japanese situation may be partly explained by the past use of peculiar Tetra- and Penta-BDE commercial products (Akutsu et al., 2003). However, there is no information on the use or production of these products in China. Meanwhile, BDE-183 was observed as a major congener in human milk samples from Hubei, Jiangxi, Sichuan and Fujian province, which was consistent with the production of commercial Octa-BDE products in China (Sudaryanto et al., 2008b). BDE-183 is a major congener found in commercial Octa-BDE products. However, surprisingly, a recent Chinese study showed that BDE-28, BDE-153 and BDE-183 were major components in human milk from mothers with high exposure in Deca-BDE production area (Jin et al., 2009), suggested that high Deca-BDE exposure might result in elevated levels of low brominated BDEs in humans. 4.2. Indicator PCBs in human milk Indicator PCBs analyzed in this study were much lower than that found in other studies (Kalantzi et al., 2004; Fängström et al., 2005; Jaraczewska et al., 2006; Ingelido et al., 2007; She et al., 2007; Polder et al., 2008; Raab et al., 2008). Comparing the congener profile in human milk in China and other countries, there were some similarities and differences. CB-153 and CB-138 were the most abundant congeners, which are similar to that found in other countries (Inoue et al., 2006; Jaraczewska et al., 2006; Ingelido et al., 2007; She et al., 2007; Bordajandi et al., 2008; Polder et al., 2008; Raab et al., 2008). However, the contribution of CB180 was higher in European countries than that in China, while the proportion of lower chlorinated PCB congeners (CB-28 and CB-52) was much higher in China. These findings in Chinese human milk samples are consistent with the results reported in Chinese adipose tissue samples (Wang et al., 2010). Nevertheless, these comparisons have to be made with caution because of the different sampling periods in these studies. Time trend studies show rapidly decreasing trends in most European countries after the bans on usage and production of PCBs in the 1970s (Jaraczewska et al., 2006; Raab et al., 2007; Bordajandi et al., 2008; Lignell et al., 2009). Moreover, the relative abundance of PCB congeners would vary along the breastfeeding period (González et al., 1995) and significant differences were found in the levels collected at various intervals (Jaraczewska et al., 2006). The observed relatively low levels of indicator PCBs in human milk in this study are probably due to the agricultural characteristics and limited industrial activities in China before the 1970s when the use and production of PCBs had been banned in the world. 4.3. Exposure factors and pathways As persistent lipophilic contaminants, indicator PCBs in Chinese human milk was significantly associated with maternal age in this study. This observation was consistent with previous studies (Polder et al., 2008; Raab et al., 2008; Sudaryanto et al., 2008a), indicating its bioaccumulation over years. However, unlike indicator PCBs, there was no correlation between levels of PBDEs and maternal age, which was consistent with that in various studies (Schecter et al., 2003; Kazda et al., 2004; Chao et al., 2007; Polder et al., 2008; Raab et al., 2008; Sudaryanto et al., 2008a,b; Wang et al., 2008; Lacorte and Ikonomou, 2009). But, some recent studies indicated significant associations between levels of PBDEs in human milk and maternal age (Haraguchi et al., 2009; Lignell et al.,

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2009; Thomsen et al., 2010; Dunn et al., 2010). The absence of age-dependence might be partly due to continuing exposure yet to reach steady state in human tissue (Chao et al., 2010). And certain potential confounders, such as parity/nursing history, education and diet habits, might conceal the age correlation (Thomsen et al., 2010). Furthermore, the application of pooled sample and the wide variation of mothers’ age might partly explain this lack of association in this study. Nevertheless, studies on levels of PBDEs in human serum samples did not show increasing trends among ages (Toms et al., 2008, 2009b). However, another American study showed that adults (>60 years) and older were twice as likely as adults 20–59 years old to have a serum BDE-47 concentration above the 95th percentile (Sjödin et al., 2008). For many persistent organic pollutants, e.g. PCBs and dioxins, 85–95% of the total exposure mainly comes from food of animal origin (Liem et al., 2000). In the present study, significantly positive correlations were found between levels of indicator PCBs in human milk and the consumption of eggs and aquatic foods. However, no statistical association was found between the concentrations of PBDEs in milk and dietary characteristics, which was consistent with previous studies (Lind et al., 2003; Ingelido et al., 2007; Sudaryanto et al., 2008a,b; Wang et al., 2008; Zhu et al., 2009a). But, a few studies have reported a strong positive relationship between PBDE concentrations in human milk and dietary intake of fish and shellfish (Ohta et al., 2002), dairy products and meat (Wu et al., 2007), food of animal origin (Li et al., 2008), postpartum saturated fat consumption (Dunn et al., 2010). This contradiction of association between PBDEs and dietary habits or food consumption might stem from distinct methodologies or strategies, such as food consumption data source. Food consumption data usually derive from food frequency questionnaires, 24-h dietary recalls and household dietary survey applied in this study, which usually have certain limitations (WHO, 2007b). And food consumption or dietary habits might be difficult to reflect variations of PBDE levels in food species and accurate dietary intake of PBDEs. Besides, the indoor environment would be another important source for human exposure (Allen et al., 2007). A recent assessment of human exposure to PBDEs indicated that ingestion and dermal absorption of house dust is the largest contributor in the United States (Johnson-Restrepo and Kannan, 2009). In previous studies, the significant correlations observed beP P tween PBDEs and PCBs in milk suggested similar human exposure via dietary intake in the United Kingdom (Kalantzi et al., 2004) and Japan (Inoue et al., 2006). However, no statistical relationship P P was found between PBDEs and PCBs in the present study. P 6PCBs was significantly correlated to the TEQ of PCDD/Fs and P dl-PCBs, and 7PBDEs was significantly correlated to the TEQ of dl-PCBs. All these results suggested different exposure pathways among these contaminants. Besides dietary intake, other exposure sources and pathways of PBDEs in humans might exist in China. Geographical factors (costal or inland, urban or rural) were major determinants of PCBs levels in human milk (Kalantzi et al., 2004; Sudaryanto et al., 2008a; Haraguchi et al., 2009). Similarly, in this study, PCB concentrations in human milk from coastal areas were higher than that from inland areas, probably due to the greater consumption of seafood in coastal areas. However, there was no difference between urban areas and rural areas, although the mean P concentrations of 6PCBs in urban samples were slightly higher than that in rural samples. The levels of PBDEs in urban human milk were higher than that in rural samples in certain provinces, including Henan, Sichuan and Jiangxi. In our previous study, significantly higher PBDE concentrations were observed in urban human milk samples from Beijing, probably due to more consumption of animal origin food in urban areas (Li et al., 2008). Another probable reason was greater amounts of application of PBDEs in more industrialized and urban-

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ized areas (Sudaryanto et al., 2008b). However, in our study, the rural mothers’ milk contained higher or comparable PBDE levels in most provinces, indicating relative higher levels of PBDE exposure in rural areas.

2007BAC27B02), the National Nature Science Foundation of China (Grant Nos. 20837003 and 20907048), the National High-Tech Research Program of China (Grant No. 2006AA06Z403) and the Yong Scientist Foundation of China CDC (Grant No. 2009A205).

4.4. Infant exposure risks

References

It has been estimated that human milk is the main exposure source of PBDEs for breastfeeding infants (Johnson-Restrepo and Kannan, 2009; Toms et al., 2009a). The accumulation of exogenous compounds in human milk poses the growing question on the adverse effects on nursing infants in the world, because the fetus and developing children are far more sensitive than adults. In China, the maximum EDI of BDE-47, BDE-99 and BDE-153 via human milk for nursing infants in China were several orders of magnitude lower than the corresponding threshold reference values suggested by USEPA (Johnson-Restrepo et al., 2007). Nevertheless, continued surveillance for PBDEs as well as other POPs in human milk is worthy and crucial for providing information on public health and temporal trends. Furthermore, formula feeding could lead to the ingestion of much lower amounts of PBDEs than breast milk feeding, but the undoubtedly immunological, nutritional and psychological benefits of maternal feeding outweigh the risks of contaminant transfer (Carrizo et al., 2007). Interestingly, a previous Australian study which investigated PBDEs in human serum samples from population of various age groups from newborn to adults has showed that the peak concentration of PBDEs was observed in serum samples from children at 2.6–3 years of age which was later than the period when breastfeeding is typically ceased (Toms et al., 2009b). 5. Conclusion This is the first national survey of PBDEs and indicator PCBs in human milk in China. By comparison with other studies in the world, the levels of PBDEs and indicator PCBs in Chinese mother’s milk are relatively low, implying low human exposure to these contaminants in China. BDE-28, BDE-47 and BDE-153 were major PBDE congeners in most pooled human milk samples, while BDE183 was detected at relatively high levels in certain samples. The most predominant congener of indicator PCB was CB-153, followed by CB-138 in almost all milk samples. The contributions of lower chlorinated PCBs were relatively higher compared to other studies. No significant correlation was found between levels of PBDEs and indicator PCBs. Concentrations of PBDEs in human milk were not significantly associated with maternal age, food consumption and geographical location (coastal or inland, rural or urban). However, the maternal age, dietary habits and geographical location (coastal or inland) were probable determinants of indicator PCB levels in human milk in China. Due to the lack of information on commercial PBDE mixtures used in China and habits of participants, it was difficult to identify the major exposure sources and pathways of PBDEs. However, the results of this study suggested that PBDE exposures to Chinese people are probably from multiple sources and various pathways, and geographical difference of PBDE exposure might exist. The estimated daily intakes of BDE-47, BDE-99 and BDE-153 for infants in China were several orders of magnitude lower than the corresponding threshold reference values suggested by USEPA. Acknowledgements We would like to express our gratitude to all participant mothers in this study. This study was supported by the National Science and Technology Support Program of China (Grant No.

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