Polybrominated Diphenyl Ethers (PBDEs) in Paired Human Hair and

Dec 9, 2013 - ... were different from those in dust collected in the houses of residents ...... Patterson , D. G. , Jr. Serum levels of polybroninated...
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Polybrominated Diphenyl Ethers (PBDEs) in Paired Human Hair and Serum from e‑Waste Recycling Workers: Source Apportionment of Hair PBDEs and Relationship between Hair and Serum Jing Zheng,†,§ Ke-Hui Chen,‡ Xiao-Jun Luo,*,‡ Xiao Yan,§ Chun-Tao He,§ Yun-Jiang Yu,† Guo-Cheng Hu,† Xiao-Wu Peng,† Ming-Zhong Ren,† Zhong-Yi Yang,*,§ and Bi-Xian Mai‡ †

Center for Environmental Health Research, South China Institute of Environmental Sciences, Ministry of Environmental Protection, Guangzhou, 510655 Guangdong, People’s Republic of China ‡ State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640 Guangdong, People’s Republic of China § State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275 Guangdong, People’s Republic of China ABSTRACT: Human hair has been widely used as a bioindicator for human persistent organic pollutants (POPs) exposure, but studies on the sources of hair POPs and the relationship between hair and body burden are limited. This study analyzed the possible source apportionment of hair PBDEs and examined the relationship between PBDE concentrations in paired hair and serum from e-waste recycling workers. Using the ratio of BDE 99/47 and BDE 209/207 as indices, we calculated that only 15% of the highly brominated congeners (nona- and deca-BDE congeners) comes from exogenous (external) exposure for both female and male hair, but an average of 64% and 55% of the lower-brominated congeners (tetra- to penta-BDE congeners) come from exogenous exposure for female and male hair, respectively. The higher contribution of exogenous exposure for lessbrominated congeners could be related to their relatively lower log KOW and higher volatility than higher-brominated congeners, which make them more readily to evaporate from dust and then to be adsorbed on hair. Higher hair PBDE levels and higher exogenous exposure of less-brominated congeners in females than in males can be attributed to a longer exogenous exposure time for females than males. Significant positive relationships were found in trito hepta-BDE congeners (BDE 28, 47, 66, 85, 100, 153, 154, and 183) (R = 0.36−0.55, p < 0.05) between hair and serum, but this relationship was not found for octa- to deca-BDE. Difference in the half-lives between highly brominated congeners and lessbrominated congeners could be a reason. This result also implied that we should treat the results of correlation analyses between hair and other organs cautiously.

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INTRODUCTION Polybrominated diphenyl ethers (PBDEs) have been used extensively in plastics, electronic equipment, textiles, and other materials as a flame retardant for more than 40 years. The three major commercial PBDE mixtures are penta-, octa-, and decaBDE. There is increasing regulation and an accompanying phasing-out of the production and commercial use of PBDE technical mixtures due to their potential toxicity to the environment and human health.1 PBDEs can enter the environment during the processes of production, application, disposal, and recycling,2,3 and their levels in the environment have generally been increasing since the 1970s.4 Scientific studies have found that PBDEs are present in human serum, blood, milk in females, and adipose tissues of almost all individuals.5,6 Monitoring of PBDEs in humans has become essential for exposure and risk assessment. Blood is a common biological specimen tested for PBDE biomarkers.7−9 However, as an © 2013 American Chemical Society

invasive matrix, there are limits and regulations to the amount of blood that can be collected.10 Hair, on the other hand, has been identified as a potential noninvasive matrix to assess the level of human exposure to POPs.11 There are several advantages to using hair for human biomonitoring, such as low cost and convenient sample collection, transportation, and storage. Several studies have demonstrated hair to be a good indicator for exposure to heavy metals, drugs, and organic pollutants in humans.10,12 However, several limitations prevent the wide application of hair as a matrix for biomonitoring.13 One of the primary limitations is the difficulty in distinguishing between exogenous (external) and endogenous (internal) contamination. In a recent study, however, we found that the Received: Revised: Accepted: Published: 791

October 4, 2013 December 4, 2013 December 9, 2013 December 9, 2013 dx.doi.org/10.1021/es4044402 | Environ. Sci. Technol. 2014, 48, 791−796

Environmental Science & Technology

Article

shaking incubator (1 h, 40 °C) twice to efficiently remove external contamination (e.g., fine soil particles, dust), as validated by SEM images in our previous study.17 After rinsing with Milli-Q water, hair samples were then freeze-dried and cut into small pieces (2−3 mm). Sample Preparation and Analysis. Details of the extraction and cleanup for hair samples have been reported in Zheng et al.,14,18 and those for serum samples have been provided in Yan et al.19 The methods are briefly described below. Before extraction, each sample was spiked with surrogate standards (BDE 77, BDE 181, and 13C-BDE 209). Hair samples were incubated with hydrochloric acid (4 M) and a hexane/ dichloromethane mixture (4:1, v/v). Analytes in the residual liquid were extracted by liquid−liquid extraction. Each extract was purified with a multilayer silica/alumina column. Serum samples were denatured using hydrochloric acid (6 M) and 2propanol and were extracted with a mixture of hexane/methyltert-butyl ether (MTBE) (1:1, v/v). Lipids were removed by concentrated sulfuric acid. The combined extracts were then further purified by a multilayer silica/alumina column. The total lipid content was calculated from the total triglyceride and cholesterol values measured in the serum.20 Before injection, 10 μL of an internal standard (BDE 118 and BDE 128) (2 ppm) was added to each sample, and each sample was finally condensed to 100 μL. PBDEs were analyzed by a Shimadzu 2010 gas chromatograph coupled with a mass spectrometer (GC-MS) with electron capture negative ionization (ECNI) in the selected ion monitoring mode. Octa- through deca-BDEs were separated by a DB-5HT (15 m × 0.25 mm × 0.1 μm) capillary column. A DB-XLB (30 m × 0.25 mm × 0.25 μm) capillary column was used for the determination of tetra- through hepta-BDE congeners. Samples (1 μL) were manually injected in splitless mode. Quality Assurance and Quality Control. Instrumental QC included regular injection of solvent blanks and standard solutions. For method QC, a full suite of quality control was assessed using surrogate standards, procedural blanks, spiked blanks, and spiked matrices. The recoveries of surrogate standards BDE 77, BDE 181, and 13C-BDE 209 were in the range of 85%−125%, 72%−113%, and 52%−126% in hair samples and 67%−118%, 71%−110%, and 65%−142% in serum samples, respectively. The final results were not recovery-corrected. Only trace amounts ( 0.05), for which the weak correlation of highly brominated PBDEs between hair and serum may be primarily responsible (Table 2). Moderate positive correlations were commonly found in tri- to heptaBDEs, including BDE 28, BDE 47, BDE 66, BDE 85, BDE 100, BDE 153, BDE 154, and BDE 183 (R = 0.36−0.55, p < 0.05), with the exception of BDE 99 (R = 0.29, p > 0.05) (Table 2). The levels of octa- to deca-BDEs, however, did not correlate or weakly correlated between hair and serum (R = 0.10−0.36, p > 0.05). This result contradicted the source apportionment determined above. It is very difficult to provide a convincing explanation for this observation. The relatively short biological half-lives of highly brominated congeners compared to lessbrominated congeners in humans could be a cause. For

and 62% of the total PBDEs, respectively. This result has rarely been reported in serum samples from nonoccupational exposure people but was consistent with studies investigating the occupational PBDE exposure populations in electronic recycling facilities in Europe or China.21,22 The difference in PBDE profiles between hair and serum may indicate that not all hair PBDE is derived from endogenous exposure by serum. In a previous study, the congener profile of hair samples was also found to be different from that of dust collected in e-waste recycling workshops and residents’ houses.14 The contribution of BDE 209 was higher in dust than in hair samples, while the combined contributions of all nona-BDE congeners were lower in dust samples than in hair samples. Meanwhile, the contribution of BDE 99 in hair samples was lower than that of BDE 47, while the opposite was observed in the dust samples in the previous study. These findings suggest that exogenous exposure by dust was not the major source for hair PBDEs. Obviously, both exogenous and endogenous exposure contributed to hair PBDEs. To gain insight into the relative contribution of exogenous and endogenous exposure to hair PBDEs, we compared the PBDE congener profiles in hair samples (acceptors), in serum samples (internal sources), and in dust samples (external sources). The dust samples, both from workshops and residences, were collected from the same e-waste recycling areas as the serum and hair samples studied in this study. Detailed information and PBDE concentrations of the dust samples have been reported in our previous study.14 Considering the living environment of e-waste recycling workers, the dust samples from both workshops and residences were combined as representative of external sources for hair PBDEs. As shown in Figure 2, most of the individual BDE

Figure 2. PBDE congener profiles in hair, serum, and dust samples from e-waste recycling areas.

congener proportions relative to total PBDEs in hair samples fell between those in serum and in dust. For example, the percentage of BDE 209 to total PBDEs in hair was higher by 7% than that in serum and lower by 43% than that in dust, while the abundance of nona-BDE (including 206, 207, and 208) was lower by 8% and higher by 13% than those in serum and in dust, respectively. As observed in Figure 1, the difference in PBDE congener profiles between hair and serum samples mainly lies in the contribution of BDE 99, BDE 197, and BDE 207. It is believed that this difference can be attributed to in vivo metabolism of 794

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moderate positive correlation in PBDE levels between hair and serum was found for tri- to hepta-BDEs. However, such correlations were not found for octa- to deca- BDE congeners. This result suggested that a good correlation between hair and other tissues cannot definitively show that endogenous exposure is the main source of hair PBDEs. These findings are important in the study of hair as a bioindicator for human PBDE exposure.

Table 2. Spearman Correlation Coefficients for PBDE Concentrations in Serum and Hair Samples n BDE 28 BDE 47 BDE 66 BDE 85 BDE 99 BDE 100 BDE 153 BDE 154 BDE 183

n

R

P

32

0.4306

R

0.0139

P BDE 196

26

0.3611

0.0699

32

0.4684

0.0069

BDE 197

32

0.1912

0.2944

32

0.4729

0.0063

BDE 202

29

0.0959

0.6207

32

0.5454

0.0012

BDE 203

32

0.3443

0.0536

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AUTHOR INFORMATION

Corresponding Authors

30

0.2937

0.1152

BDE 206

32

0.1616

0.3768

30

0.485

0.0066

BDE 207

32

0.1096

0.5503

32

0.3574

0.0446

BDE 208

32

0.1995

0.2737

*Phone: +86-20-85290146. Fax: +86-20-85290706. E-mail: [email protected]. *Phone: +86-20-84112008. Fax: +86-20-84112008. E-mail: [email protected].

26

0.5273

0.0056

BDE 209

32

0.1213

0.5083

Notes

32

0.3972

0.0244

total PBDEs

32

0.1633

0.3718

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Nature Science Foundation of China (No. 21307037, 41230639, 41273118, 21177119) and Nature Science Foundation of Guangdong Province (No. S2013040011752)

example, the half-life of BDE 209 is estimated to be approximately 15 days, while BDE 183 has a half-life of 94 days (95% CI 68−120 days).28 The half-life of BDE 153 is in the range of 2 years.29 As a bioindicator, hair reflected a relatively longer period of exposure than serum due to its lower growth rate. The short half-lives of highly brominated congeners in serum meant that the highly brominated congeners in serum did not match those in hair, which resulted in a weak correlation between hair and serum. A lack of correlation between the levels of BDE 99 in hair and serum was found in the present study. Similar results have been reported in the hair and internal tissues of hedgehogs. D’Havé et al. (2005) suggested that this may be explained by the differential accumulation of this congener in hair and internal tissues. In our opinion, the in vivo metabolism, such as the debromination of BDE 99 to BDE 47, could also contribute to this observation. Few studies have reported a correlation between PBDEs in human hair and serum or other tissues. Only one such study has been conducted on endogenous samples, by D’Havé et al. (2005), in which the relationships between hair PBDE content and that of other tissues such as liver, kidney, and muscle were investigated. Similar to the present study, significant correlations between hair and other tissues were found for congeners of BDE 28, 47, 99, 100, 153, 154, and 183. No octato deca-congeners were detected in the study of D’Havé et al. (2005). Based on the observed correlation between hair and other tissues, the author concluded that hair can be considered as a suitable indicator of PBDE exposure in terrestrial mammals and can be used in nondestructive monitoring schemes. However, our result indicated that one should be more wary of this deduction when considerations of human exposure in which indoor dust exposure plays an important role, especially for occupation population. It should be kept in mind that different tissues or organs exhibit characteristic bioaccumulation of chemicals due to the differences in components and organ functions. This study is the first attempt to provide empirical evidence of the source apportionment of human hair PBDEs. The endogenous pathway is the major source of highly brominated BDE congeners, while the exogenous pathway predominates for less-brominated BDEs. Furthermore, we showed for the first time the association between human hair and the serum concentration of PBDEs in e-waste recycling workers. A

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