Polychlorinated Biphenyls (PCBs) in Human Hair and Serum from E

Subscriber access provided by UNIV OF CALIFORNIA SAN DIEGO LIBRARIES

Article

Polychlorinated biphenyls (PCBs) in Human Hair and Serum from E-Waste Recycling Workers in Southern China: Concentrations, Chiral Signatures, Correlations, and Source Identification Jing Zheng, Lehuan Yu, She-Jun Chen, Guocheng Hu, Kehui Chen, Xiao Yan, Xiaojun Luo, Sukun Zhang, Yunjiang Yu, Zhongyi Yang, and Bi Xian Mai Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b04955 • Publication Date (Web): 12 Jan 2016 Downloaded from http://pubs.acs.org on January 12, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 26

Environmental Science & Technology

1

Polychlorinated biphenyls (PCBs) in Human Hair and Serum from

2

E-Waste Recycling Workers in Southern China: Concentrations, Chiral

3

Signatures, Correlations, and Source Identification

4

Jing Zheng, † Le-Huan Yu, †,‡ She-Jun Chen, *,‡ Guo-Cheng Hu,† Ke-Hui Chen, ‡,§ Xiao

5

Yan, ǁ Xiao-Jun Luo, ‡ Sukun Zhang, † Yun-Jiang Yu, *,† Zhong-Yi Yang,ǁ Bi-Xian Mai, ‡

6

†

7

Sciences, Ministry of Environmental Protection, Guangzhou 510655, China

8

‡

9

Environmental Protection and Resources Utilization, Guangzhou Institute of

Center for Environmental Health Research, South China Institute of Environmental

State Key Laboratory of Organic Geochemistry and Guangdong Key Laboratory of

10

Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China

11

§

12

ǁ

13

Guangzhou 510275, China

14 15

TOC Art

University of Chinese Academy of Sciences, Beijing 100049, China

State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yat-Sen University,

16

1

ACS Paragon Plus Environment


17

ABSTRACT

18

Hair is increasingly used as a biomarker for human exposure to persistent organic

19

pollutants (POPs). However, the internal and external sources of hair POPs remain a

20

controversial issue. This study analyzed polychlorinated biphenyls (PCBs) in human hair

21

and serum from electronic waste recycling workers. The median concentrations were 894

22

ng/g and 2868 ng/g lipid in hair and serum, respectively. The PCB concentrations in male

23

and female serum were similar, while concentrations in male hair were significantly

24

lower than in female hair. Significant correlations between the hair and serum PCB levels

25

and congener profiles suggest that air is the predominant PCB source in hair and that hair

26

and blood PCB levels are largely dependent on recent accumulation. The PCB95, 132,

27

and 183 chiral signatures in serum were significantly nonracemic, with mean enantiomer

28

fractions (EFs) of 0.440−0.693. Nevertheless, the hair EFs were essentially racemic

29

(mean EFs = 0.495−0.503). Source apportionment using the Chemical Mass Balance

30

model also indicated primary external PCB sources in human hair from the study area.

31

Air, blood, and indoor dust are responsible for, on average, 64.2%, 27.2%, and 8.79% of

32

the hair PCBs, respectively. This study evidenced that hair is a reliable matrix for

33

monitoring human POP exposure.

2


Page 2 of 26

Page 3 of 26

34


INTRODUCTION

35

Although blood, breast milk, and adipose have been extensively used for monitoring

36

human exposure to a variety of environmental contaminants, there are increasing studies

37

using hair as an additional biomarker for exposure to persistent organic pollutants

38

(POPs).1-5 Compared to other matrices, hair is easily and noninvasively collected,

39

low-cost, and easily transported and stored for analysis. In addition, hair analysis can

40

reveal both short and long-term exposure.6, 7

41

Each hair follicle root is surrounded by numerous capillary blood vessels that supply

42

substances to the hair.8 Some studies have suggested that hair serves as an indicator of

43

POP levels of endogenous tissues.7 Poon et al. reported significant correlations (r =

44

0.345−0.566) between human hair and serum polybrominated diphenyl ether (PBDE)

45

concentrations.9 Hair is enriched with lipids (3.5−4%) and has a tendency to absorb

46

lipophilic organic contaminants from external origins (e.g., from ambient air or dust).

47

Neuber et al. (1999) used preschool children’s hair as a passive sampler to monitor indoor

48

pesticide

49

concentrations in indoor dust and human hair have been recently observed.11 Altshul et al.

50

observed a strong p,p´-DDE correlation, moderate PCB congener correlations, and no

51

correlations for other organochlorines between hair and blood samples. They suggest that

52

organochlorines may originate from different sources.12 These inconsistent observations

53

highlight the importance of identifying internal and external sources of contaminants and

54

the correlations between hair and endogenous tissues.

contamination.10

In

addition,

positive

relationships

between

PBDE

55

Polychlorinated biphenyls (PCBs) are a well-known class of man-made organic

56

chemicals, which were formerly used in a variety of industrial and commercial

3



57

applications. They have received significant interest due to their persistent,

58

bioaccumulative, and toxic properties.13 In contrast to the decline of PCB levels in

59

developed countries after their restrictions in the 1970s, high levels have been reported at

60

electrical and electronic waste (e-waste) recycling sites in many developing countries.14

61

Continuous long-term exposure monitoring efforts are necessary to protect populations

62

living near e-waste sites, especially vulnerable populations, such as developing fetuses

63

and young children.15

64

Of the 209 PCB congeners, 19 congeners with three or four ortho-chlorine substituents

65

are chiral. The chirality of a compound can only be modified by biological transformation

66

processes (not by physical and chemical processes), such as enantioselective

67

biodegradation, metabolism, or binding to structure-sensitive biological receptors.16

68

Chiral PCBs undergo enantiomeric enrichment in mammals due to cytochrome P-450

69

enzyme metabolism.17 Metabolism is unlikely to occur in hair shafts consisting of

70

keratinized cells, which are cemented by the cell-membrane complex.8 Thus, PCB chiral

71

signatures may be capable of distinguishing between the external and internal sources of

72

these compounds in hair. We discussed this feasibility in a previous study via comparing

73

the PCB chiral signatures in hair and indoor dust.18

74

In the present study, concentrations and profiles PCBs were investigated in matched

75

hair and serum samples of e waste recycling workers in an e-waste area of southern

76

China, where high levels of PCBs in the environment have been reported.19 The

77

objectives of this study are to determine the internal and external sources of PCBs in

78

human hair and explore the PCB associations between hair and blood, which are

79

important for understanding the feasibility of using human hair as a POP exposure

4


Page 4 of 26

Page 5 of 26


80

biomarker. Certain atropisomeric PCB chiral signatures were also determined in hair and

81

serum to provide support for source identification in hair. Furthermore, we aim to conduct

82

source apportionment of PCBs in the hair by coupling PCB data of environmental

83

matrices from the study area. To date, only a few studies have described the correlation

84

between POP levels in human hair and internal tissues.9, 12, 20 To our knowledge, this is

85

the first report on the enantioselectivity of PCBs in human serum.

86 87

MATERIALS AND METHODS

88

Sample Collection. A total of 34 matched hair and serum samples were obtained from

89

e-waste recycling workers (19 males and 15 females) in a rural e-waste area in southern

90

China. The study area has been described in detail in another study.21 This research was

91

launched with authorization of the Ethics Committee in the School of Life Science, Sun

92

Yat-sen University. Samples were collected at a local hospital by medical professionals.

93

All participants provided full consent after being informed of the study's objectives in

94

July 2011. The participants were asked to fill out a questionnaire, which asked for their

95

age, gender, weight, height, and occupational history. Venous blood samples (8−10 mL)

96

were collected from each subject in anticoagulant-free tubes. They were centrifuged for 5

97

min at 3,000 rpm within 3 h of collection to isolate the serum. Hair was sampled by a

98

barber in a way similar to routine haircuts using clean stainless-steel scissors. Distal hair

99

of approximately 5 and 10 cm from the posterior vertex was cut for most male and female

100

participants, respectively.

101

Sample preparation and analysis. The hair and serum sample preparation procedures

102

and instrumental analysis have been described in a previous study.22 In brief, serum

5



Page 6 of 26

103

samples were denatured using hydrochloric acid (6 M) and 2-propanol. They were then

104

extracted using a hexane/methyl-tert-butylether (MTBE) (1:1, v/v) mixture after it was

105

spiked with surrogate standards (PCB65 and 204). Lipids were removed from the extracts

106

using concentrated sulfuric acid. Hair samples were rinsed with Milli-Q water in a

107

shaking incubator (1 h, 40 °C, twice) to remove possible dust or dirt adhering to the hair

108

surface, which was also recommended by a recent study.23 They were then freeze-dried,

109

cut into small pieces (2−3 mm), and homogenized. Hair was incubated overnight (12 h)

110

in hydrochloric acid (4 M) and a hexane/dichloromethane mixture (4:1, v/v). PCBs in the

111

incubation

112

hexane/dichloromethane mixture (4:1, v/v), which was repeated three times. The

113

combined extracts were purified on a silica/alumina column and condensed, after which

114

internal standards (PCB 24, 82, and 198) were added.

medium

were

extracted

via

liquid-liquid

extraction

with

a

115

PCBs were analyzed by an Agilent 6890 gas chromatograph equipped with a 5975B

116

mass spectrometer in electron impact ionization (EI) mode (GC-EI-MS). A DB-5ms

117

capillary column (60 m × 0.25 mm i.d., 0.25 µm film thickness) was used to separate the

118

PCB congeners. Enantiomer analysis was conducted using the Agilent GC-EI-MS. The

119

atropisomeric PCB 132 and 183 enantiomers were separated on a BGB-172 (30 m × 0.25

120

mm i.d., 0.18 µm film thickness) capillary column, while PCB 95 was separated on a

121

Chirasil-Dex (25 m × 0.25 mm i.d., 0.25 µm film thickness) column. Further instrumental

122

analysis information is provided in the Supporting Information (SI).

123

Quality Control. The PCB 65 and 204 surrogate standard recoveries ranged from 65

124

to 98% and from 72 to 118% in the serum samples, and 60−121% and 58−115% in the

125

hair samples, respectively. The final results were not recovery corrected. Serum (Milli-Q

6


Page 7 of 26


126

water) and hair sample (hydrochloric acid and a hexane/dichloromethane mixture)

127

procedural blanks were run with each sample batch. Only trace amounts (< 5% of the

128

concentrations found in the corresponding field-sample extracts) were detected in the

129

blanks, and the mean blank amounts were subtracted from the sample extracts. The mean

130

PCB congener recoveries of 21 individuals ranged from 51% to 103% for spiked blanks

131

and from 53% to 107% for spiked matrices, respectively.

132

Enantiomer Fraction (EF) Determination. The EF is defined as the peak area of the

133

first-eluted enantiomer divided by the total areas of both enantiomers, which were

134

calculated for each peak pair with a signal-to-noise ratio exceeding 10:1. The chiral

135

analysis was validated using a daily checking standard (an Aroclor mixture), and the

136

mean EFs were 0.498 ± 0.007 (n = 10). A conservative EF precision value of 0.032 (95%

137

confidence interval) was used for statistically comparing the sample and standard EFs.24

138

Data Analysis. The statistical analysis, including t-test, Pearson Product-Moment

139

Correlation, Spearman Rank Order Correlation, and linear regression, was performed

140

using SigmaPlot 12.5 (Systat Software, Inc., CA). The Chemical Mass Balance (CMB)

141

model was used for source apportionment of PCBs and PBDEs in the hair. It was

142

performed using CMB software (CMB8.2), which was developed by the United States

143

Environmental Protection Agency (US EPA). Additional model application details are

144

provided in the SI.

145 146

RESULTS AND DISCUSSION

147

Concentrations and Compositions. The hair and serum PCB concentrations,

148

including PCB28, 52, 66, 74, 95, 99, 101, 105, 118, 128, 138, 153, 164, 170/190, 177,

7



149

180, 187, and 209, which were detected in over 60% of the samples, are summarized in

150

Table 1. The individual PCB concentrations and associated information are given in SI

151

Table S1. The total PCB concentrations in the hair ranged from 161 to 3514 ng/g, with a

152

median of 894 ng/g. The serum PCB concentrations were between 256 and 11 200 ng/g

153

lipid, with a median of 2868 ng/g lipid. The maximum hair and serum concentrations

154

were both identified in a 50 year-old woman. The lipid-normalized hair concentrations

155

(4015−87 859 ng/g lipid, estimated using a hair lipid content of 4%) were 8 times higher

156

than the serum levels. These results are similar to those from a previous study, where

157

average human hair PCB levels were 6 times higher than serum levels.12

158

The male and female participants were 22−55 and 30−59 years old, with average ages

159

of 41 and 44 years, respectively. The male and female serum PCB concentrations were

160

quite similar (Table 1). Similar results have also been reported for human serums from

161

other locations.25, 26 This result suggests similar PCB sources and exposure routes for

162

residents living in this e-waste area. However, the male hair PCB concentrations (with a

163

median value of 611 ng/g) were significantly lower than those of females (1781 ng/g) (p

164

= 0.002). This is likely because the longer female hair encompasses a longer PCB

165

accumulation time than the shorter male hair (either from the ambient environment or

166

internal tissues), although information on the hair length for the individual participants

167

was not available. A recent study found significant PBDE concentration increases in hair

168

shafts from the proximal (root end) to distal segments.27 Hair washing frequency can also

169

affect the levels of hair contaminants as suggested in a previous study,12 however related

170

information was not obtained in the present study.

171

The hair and serum PCB congener profiles, which are compared with ambient air and

8


Page 8 of 26

Page 9 of 26


172

indoor dust (in homes or e-waste workshops) profiles from the study area,19,

28

173

depicted in Figure 1. Blood, air, and dust may represent typical internal and external hair

174

contaminants. The hair PCB congener profile closely resembled those in the air of this

175

area, with the exception of higher contributions of PCB28 and 52 in the air because of

176

their higher vapor pressures, suggesting air is the major PCB source in hair. The profile of

177

highly chlorinated PCBs in serum was similar to that in indoor dust. This indicated that

178

dust ingestion or inhalation plays an important role in the presence of PCBs in the

179

e-waste recycling workers’ blood.

are

180

In both the hair and serum in the present study, lower chlorinated congeners had

181

significant proportions compared to the PCB patterns typically found in human tissues

182

(serum, milk, and adipose), in which PCB 153 was frequently the predominant

183

congener.29-31 PCB153 in serum is thought to be an indicator of dietary PCB intake.32 The

184

congener patterns, as well as the high PCB levels in the air in this area (7825-76 330

185

pg/m3),19 further support the importance of air and indoor dust for exposure of the

186

e-waste recycling workers to PCBs. Similar congener profile was also found in human

187

serum from an e-waste recycling site in North Vietnam.33

188

There were no significant differences in both the hair and serum PCB profiles between

189

the male and female participants (SI Figure S1), indicating common exposure sources.

190

Marek et al. recently found that children are enriched in lower-molecular weight PCBs

191

compared to their mothers because of their different exposure sources (indoor air versus

192

diet).32 Nevertheless, there were appreciable differences between the hair and serum PCB

193

profiles. These differences are likely due to metabolism, because highly chlorinated PCBs

194

are generally more resistant to metabolism than lower chlorinated congeners. For instance,

9



195

easily metabolized congeners PCB52 and 101 displayed substantially lower percentages

196

in the serum than in the hair.

197

Correlations. Significant correlations existed among the PCB congeners in the hair

198

and serum, except for PCB209 and 95 in serum (SI Table S2). Potentially different

199

PCB209 and 95 biological activities may lead to weak or moderate correlations with

200

other congeners. The hair PCB levels exhibited no significant correlations with the age

201

for male, female, and all participants, with the exception of PCB209 in male hair

202

(positive correlation, r = 0.576, p = 0.010). Likewise, significant correlations were not

203

found between the serum PCB levels and age.

204

Statistically significant correlations (r = 0.403−0.605, p = 0.001−0.030) were identified

205

between the hair PCB levels and occupational exposure duration (years of e-waste

206

recycling experience; 1−11 years for the males and 4−11 for the females) for 14 highly

207

chlorinated congeners (from penta- to deca-CBs). In addition, these correlations were

208

observed for more PCB congeners in male hair than in female hair (Table 2). This result

209

is unexpected, because scalp hair grows at an average rate of approximately 1 cm/month.

210

Thus, hair contaminants are a result of recent (from a few months to a few years)

211

accumulation.6,

212

occupational exposure durations for an air exposure source. The lack of association for

213

lower chlorinated PCBs supports this hypothesis.

34

A weak association is expected between the hair PCBs and

214

The significant correlations between highly chlorinated PCBs and the exposure

215

duration suggest the existence of additional exposure sources for the hair. In addition to

216

incorporation from blood, substances can be incorporated from deep skin compartments

217

during hair shaft formation (although with some time delay) and via diffusion from

10


Page 10 of 26

Page 11 of 26


218

sebum secretions.8 It is likely that PCBs, especially the more persistent congeners, in

219

these storage compartments reflect the cumulative human body exposure, which explains

220

the significant correlation with the occupational exposure duration. However, this

221

potential source was only responsible for a small portion of the hair PCBs, as estimated

222

by the coefficients of determination (r2, 0.16−0.37) from the linear regression between

223

the highly chlorinated PCB hair levels and the occupational exposure duration, roughly

224

accounting for 16−37%. The serum PCB levels also exhibited significant correlations

225

with the occupational exposure duration for the more persistent congeners (PCB128, 138,

226

164, 177, and 180), but the correlations were weak for male and female participants,

227

separately (Table 1). Current PCB exposure and metabolism in the human body may

228

influence these correlations.

229

We found significant correlations between most hair and serum PCB concentrations,

230

with no gender difference observed (Table 3). Interestingly, the correlations are stronger

231

for lower chlorinated congeners than for highly chlorinated congeners. The hair and

232

serum congener profiles indicated that air is the predominant hair PCB source, while air

233

and indoor dust are the major sources of PCBs (lower and highly chlorinated PCBs,

234

respectively) in the blood. Thus, the hair-serum correlations confirm these results. The

235

correlations also clearly suggest that the hair and blood PCB levels are largely dependent

236

on recent accumulation in the study area, as less chlorinated PCBs are readily subject to

237

metabolism in humans compared to highly chlorinated congeners, with reported half-lives

238

ranging from a few months to a few decades.35 However, lower chlorinated PCB95 is an

239

exception and displayed no correlation between the hair and serum, which may suggest

240

that it is associated with different biological activities.

11



241

Altshul et al. examined the relationship between PCB and pesticide levels in hair and

242

blood samples from 10 subjects.12 They found strong correlations for p,p´-DDE (the most

243

stable metabolite of p,p´-DDT), moderate correlations for the more persistent PCB

244

congeners, but weak or no correlations for other organochlorine compounds. Nakao et al.

245

also found good correlations for the more persistent congeners of polychlorinated

246

dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), whereas weak or no correlations for

247

other PCDD/Fs between hair and blood samples from six donors.36 These observations

248

for average people are inconsistent with our results for occupationally exposed people,

249

with lower chlorinated PCBs (the less persistent congeners) exhibiting stronger

250

correlations. This indicated that the relationships between hair and blood organochlorine

251

compound concentrations may vary based on the exposure scenario.

252

Chiral signatures. Three chiral PCB congeners (PCB95, 132, and 183) were

253

determined in the hair and blood (Figure 2). The hair PCB chiral signatures were

254

essentially racemic or near-racemic, with mean EFs of 0.495 ± 0.010, 0.503 ± 0.010, and

255

0.498 ± 0.017 for PCB95, 132, and 183, respectively. In contrast, the blood chiral PCBs

256

displayed significantly nonracemic residues, and the enantiomeric shifts of PCB95 (EFs =

257

0.693 ± 0.172) were more pronounced than PCB132 (0.554 ± 0.058) and PCB183 (0.440

258

± 0.027). This observation is consistent with the finding that PCBs become more

259

susceptible to cytochrome P450 metabolism as the number of meta−para hydrogen atoms

260

increases.37 We measured the air EFs of PCBs in this e-waste area in a previous study,

261

finding that the chiral PCBs were racemic, with EFs of 0.499 ± 0.004, 0.484 ± 0.022, and

262

0.494 ± 0.020 for PCB95, 132, and 183, respectively.19 This finding further suggests that

263

external sources (e.g., air) are the primary PCB sources identified in human hair samples

12


Page 12 of 26

Page 13 of 26


264

from this area, while internal sources (e.g., blood) contribute to a small percentage of the

265

PCBs in human hair.

266

To our knowledge, no studies exist regarding enantiomeric PCB compositions in

267

human blood. Chu et al. determined PCB EFs in human tissues (muscle, kidney, brain,

268

and liver) from Belgium. PCB atropisomers in liver, the main organ for xenobiotic

269

metabolism, were much more nonracemic (PCB95 EFs = 0.510−0.748, PCB132 EFs =

270

0.324−0.492) than those in other tissues (EFs = 0.505−0.569 and 0.487−0.522,

271

respectively).38 Nonracemic signatures in breast milk have been reported in Switzerland

272

(PCB95 EFs=0.64−0.76, PCB132 EFs = 0.67−0.82) and Spain (PCB95 EFs = 0.515 ±

273

0.043, PCB132 EFs = 0.422 ± 0.040, and PCB183 EFs = 0.348 ± 0.045).39,

274

difference in enantioselectivity for these three congeners in human tissues suggests varied

275

PCB enantioselective elimination mechanisms in the human body, which are still poorly

276

understood.17

40

The

277

Implications for Organohalogen Compounds in Hair. Evidence from both the PCB

278

congener profiles and chiral signatures showed that air was the primary source of PCBs

279

in the hair. Thus, we explored the relationships between the partition of PCB

280

concentration in the hair of all participants and air (KHA) and the octanol-air partition

281

coefficient (KOA) of PCBs, which has been demonstrated to be a good predictor of

282

organohalogen compound partitioning between plants and the air.41 Air samples were

283

obtained during every month in 2007−2008 (not simultaneously collected with the hair).19

284

Thus, we calculate KHA values for each month (based on average concentrations) and

285

conducted a linear regression analysis for log KHA and log KOA (Table S3). A prevalent

286

linear relationship exists for most cases, indicating that KOA is a key factor controlling the

13



287

air to hair transfer of these compounds. The relationships are more pronounced for female

288

participants than for males, likely because female hair possesses a longer exposure time

289

to the air on average. According to the air-plant partition theory,41 a linear relationship

290

implies that a partitioning equilibrium is likely approached between the hair and air.

291

PBDEs were also measured in these samples and the log KHA−log KOA relationship was

292

examined for lower brominated congeners that are present in the gaseous phase.22 The

293

relationships are less significant for PBDEs than PCBs (data not shown). A non-linear

294

relationship typically exists between log KHA and log KOA if PCB and PBDE data are

295

simultaneously fit (Figure S2). This result suggests different PBDE (with increased KOA)

296

and PCB sources in the hair.

297

The results of this study highlight the importance of source apportionment of the

298

organohalogen compounds in hair. CMB was applied to apportion the major sources of

299

PCBs and PBDEs in the hair, respectively. Air, blood, and indoor dust sources were

300

involved in the source apportionment for PCBs in hair. The results showed that air

301

contributed 35.8−94.4% (on average 64.2 ± 17.2%) of the PCBs in the hair, while blood

302

and dust accounted for 5.57−64.2% (27.2 ± 15.1%) and 0−43.5% (8.79 ± 12.4%),

303

respectively (SI Table S4). It is evident that external sources (air and dust) dominate

304

PCBs in human hair in this area. Both the high air PCB levels in this e-waste area and the

305

human scalp hair lipid richness favor air to hair PCB accumulation. In a similar study, the

306

authors implied significant endogenous origins for most PCBs in human hair samples

307

from average people.12 These findings suggest that contributions of PCBs from internal or

308

external sources to hair vary depending on the surroundings of a given person. In addition,

309

a significant positive correlation between hair and blood likely exists for both exposure

14


Page 14 of 26

Page 15 of 26


310

scenarios, indicating that hair is a reliable matrix for monitoring human exposure to PCBs.

311

However, despite this significant correlation, it is still important that the primary PCB

312

exposure pathways and related environmental matrix levels (especially in the air and diet)

313

should be noted before using hair as a biomarker.

314

Source apportionment PBDEs was conducted for lower and highly brominated BDEs,

315

respectively. Because highly brominated congeners are barely present in the gaseous

316

phase, only blood and indoor dust sources were included in the source apportionment.

317

Results suggest that blood and dust are responsible for, on average, 47.9 ± 23.5% and

318

40.0 ± 23.3% of the lower brominated BDEs (tri- through hexa-BDEs) in hair,

319

respectively, which are significantly higher than air (12.2 ± 11.7%) (SI Table S4).

320

External sources (52% in total) remain dominant, which is similar to the rough estimate

321

(55−64%) from our previous study.22 The blood and dust contributions for highly

322

brominated BDEs (hepta- though deca-BDEs) were 54.6 ± 26.8% and 45.4 ± 26.8%,

323

respectively. This differs from the previous estimate (15% from external exposure).

324

Note that the source apportionment of hair contaminants may encompass relatively

325

large uncertainties compared to air quality applications, especially for highly brominated

326

BDEs, because of chemical bio-transformation in the human body (i.e., change of the

327

source profile abundances). For instance, BDE209 and 183 in human serum possess

328

estimated half-lives of 15 and 94 days, while the half-lives of PCBs and some lower

329

brominated BDE are estimated from a few months to decades.35, 42, 43 As a result, it is

330

possible that the internal contributions to POPs in the hair may be underestimated.

331

In conclusion, hair can serve as a reliable biomarker for monitoring human exposure to

332

POPs in both general and occupationally exposed settings. Additional studies of

15



333

contamination settings will help to further understand the link between hair and body

334

exposure. Although PCB chiral signatures are a useful tool for understanding external and

335

internal sources in hair, they are not necessarily suitable for other POPs, which may have

336

different sources.

337

ASSOCIATED CONTENT

338

The Supporting Information is available free of charge on the ACS Publications website

339

at DOI:

340

Further details of the instrumental analysis of atropisomeric PCBs and the CMB model.

341

Tables S1−4 giving detailed results for concentrations, correlation analysis, congener,

342

KHA−KOA linear regression analysis, and source apportionment. Figures S1−2 depicting

343

the gender-specific PCB profiles and KHA−KOA linear regression.

344

AUTHOR INFORMATION

345

Corresponding Authors

346

*Phone: +86-20-85291509; fax: +86-20-85290706; e-mail: [email protected].

347

* Phone: +86-20-29119807; fax: +86-20-29119627; e-mail: [email protected].

348

Notes

349

The authors declare no competing financial interest.

350

ACKNOWLEDGMENTS

351

This study was financially supported by the Strategic Priority Research Program of the

352

Chinese Academy of Sciences (No. XDB14020301), the National Science Foundation of

353

China (No. 21307037, 41422305, U1401233) and Guangdong Natural Science

354

Foundation (S2011010006081). The authors also acknowledge the US EPA for providing

355

the CMB8.2 model free of charge.

16


Page 16 of 26

Page 17 of 26


356

REFERNCES

357 358 359 360

(1) Zota, A. R.; Linderholm, L.; Park, J. S.; Petreas, M.; Guo, T.; Priyalsky, M. L.; Zoeller, R. T.; Woodruff, T. J., Temporal comparison of PBDEs, OH-PBDEs, PCBs, and OH-PCBs in the serum of second trimester pregnant women recruited from San Francisco General Hospital, California. Environ. Sci. Technol. 2013, 47, 11776-11784.

361 362 363 364

(2) Park, J. S.; She, J. W.; Holden, A.; Sharp, M.; Gephartg, R.; Souders-Mason, G.; Zhang, V.; Chow, J.; Leslie, B.; Hooper, K., High postnatal exposures to polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) via breast milk in California: Does BDE-209 transfer to breast milk? Environ. Sci. Technol. 2011, 45, 4579-4585.

365 366

(3) Harkins, D. K.; Susten, A. S., Hair analysis: Exploring the state of the science. Environ. Health Perspect. 2003, 111, 576-578.

367 368

(4) Covaci, A.; Hura, C.; Gheorghe, A.; Neels, H.; Dirtu, A. C., Organochlorine contaminants in hair of adolescents from Iassy, Romania. Chemosphere 2008, 72, 16-20.

369 370

(5) Esteban, M.; Castano, A., Non-invasive matrices in human biomonitoring: A review. Environ. Intern. 2009, 35, 438-449.

371 372 373

(6) Gill, U.; Covaci, A.; Ryan, J. J.; Emond, A., Determination of persistent organohalogenated pollutants in human hair reference material (BCR 397): An interlaboratory study. Anal. Bioanal. Chem. 2004, 380, 924-929.

374 375 376

(7) D'Have, H.; Covaci, A.; Scheirs, J.; Schepens, P.; Verhagen, R.; De Coen, W., Hair as an indicator of endogenous tissue levels of brominated flame retardants in mammals. Environ. Sci. Technol. 2005, 39, 6016-6020.

377 378

(8) Pragst, F.; Balikova, M. A., State of the art in hair analysis for detection of drug and alcohol abuse. Clin. Chim. Acta 2006, 370, 17-49.

379 380 381

(9) Poon, S.; Wade, M. G.; Aleksa, K.; Rawn, D. F. K.; Carnevale, A.; Gaertner, D. W.; Sadler, A.; Breton, F.; Koren, G.; Ernest, S. R.; Lalancette, C.; Robaire, B.; Hales, B. F.; Goodyer, C. G., Hair as a biomarker of systemic exposure to polybrominated diphenyl ethers. Environ. Sci. Technol. 2014, 48, 14650-14658.

382 383

(10) Neuber, K.; Merkel, G.; Randow, F. F. E., Indoor air pollution by lindane and DDT indicated by head hair samples of children. Toxicol. Lett. 1999, 107, 189-192.

384 385

(11) Kang, Y.; Wang, H. S.; Cheung, K. C.; Wong, M. H., Polybrominated diphenyl ethers (PBDEs) in indoor dust and human hair. Atmos. Environ. 2011, 45, 2386-2393.

386 387

(12) Altshul, L.; Covaci, A.; Hauser, R., The relationship between levels of PCBs and pesticides in human hair and blood: Preliminary results. Environ. Health Perspect. 2004, 112, 1193-1199.

388 389 390

(13) Diamond, M. L.; Melymuk, L.; Csiszar, S. A.; Robson, M., Estimation of PCB stocks, emissions, and urban fate: Will our policies reduce concentrations and exposure? Environ. Sci. Technol. 2010, 44, 2777-2783.

17



391 392 393

(14) Breivik, K.; Gioia, R.; Chakraborty, P.; Zhang, G.; Jones, K. C., Are reductions in industrial organic contaminants emissions in rich countries achieved partly by export of toxic wastes? Environ. Sci. Technol. 2011, 45, 9154-9160.

394 395 396

(15) Xing, G. H.; Chan, J. K. Y.; Leung, A. O. W.; Wu, S. C.; Wong, M. H., Environmental impact and human exposure to PCBs in Guiyu, an electronic waste recycling site in China. Environ. Intern. 2009, 35, 76-82.

397 398 399

(16) Lehmler, H. J.; Harrad, S. J.; Huhnerfuss, H.; Kania-Korwel, I.; Lee, C. M.; Lu, Z.; Wong, C. S., Chiral polychlorinated biphenyl transport, metabolism, and distribution: A review. Environ. Sci. Technol. 2010, 44, 2757-2766.

400 401 402

(17) Warner, N. A.; Martin, J. W.; Wong, C. S., Chiral polychlorinated biphenyls are biotransformed enantioselectively by mammalian cytochrome P-450 isozymes to form hydroxylated metabolites. Environ. Sci. Technol. 2009, 43, 114-121.

403 404 405

(18) Zheng, J.; Yan, X.; Chen, S. J.; Peng, X. W.; Hu, G. C.; Chen, K. H.; Luo, X. J.; Mai, B. X.; Yang, Z. Y., Polychlorinated biphenyls in human hair at an e-waste site in China: Composition profiles and chiral signatures in comparison to dust. Environ. Intern. 2013, 54, 128-133.

406 407 408

(19) Chen, S. J.; Tian, M.; Zheng, J.; Z.C., Z.; Luo, Y.; Luo, X. J.; Mai, B. X., Elevated levels of polychlorinated biphenyls (PCBs) in plants, air, and soils at an e-waste site in southern China and enantioselective biotransformation of chiral PCBs in plants. Environ. Sci. Technol. 2014, 48, 3847-3855.

409 410 411

(20) Zhang, H. D.; Wang, P.; Li, Y. M.; Shang, H. T.; Wang, Y. W.; Wang, T.; Zhang, Q. H.; Jiang, G. B., Assessment on the occupational exposure of manufacturing workers to Dechlorane Plus through blood and hair analysis. Environ. Sci. Technol. 2013, 47, 10567-10573.

412 413 414

(21) Tian, M.; Chen, S. J.; Wang, J.; Shi, T.; Luo, X. J.; Mai, B. X., Atmospheric deposition of halogenated flame retardants at urban, e-waste, and rural locations in southern China. Environ. Sci. Technol. 2011, 45, 4696-4701.

415 416 417 418

(22) Zheng, J.; Chen, K. H.; Luo, X. J.; Yan, X.; He, C. T.; Yu, Y. J.; Hu, G. C.; Peng, X. W.; Ren, M. Z.; Yang, Z. Y.; Mai, B. X., 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. Environ. Sci. Technol. 2014, 48, 791-796.

419 420 421

(23) Kucharska, A.; Covaci, A.; Vanermen, G.; Voorspoels, S., Non-invasive biomonitoring for PFRs and PSDEs: New insights in analysis of human hair externally exposed to selected flame retardants. Sci. Total Environ. 2015, 505, 1062-1071.

422 423 424

(24) Wong, C. S.; Mabury, S. A.; Whittle, D. M.; Backus, S. M.; Teixeira, C.; DeVault, D. S.; Bronte, C. R.; Muir, D. C. G., Organochlorine compounds in Lake Superior: Chiral polychlorinated biphenyls and biotransformation in the aquatic food web. Environ. Sci. Technol. 2004, 38, 84-92.

425 426 427

(25) Hovander, L.; Linderholm, L.; Athanasiadou, M.; Athanassiadis, I.; Bignert, A.; Fangstrom, B.; Kocan, A.; Petrik, J.; Trnovec, T.; Bergman, A., Levels of PCBs and their metabolites in the serum of residents of a highly contaminated area in eastern Slovakia. Environ. Sci. Technol. 2006, 40, 3696-3703.

18


Page 18 of 26

Page 19 of 26


428 429 430

(26) Wang, Y.; Xu, M.; Jin, J.; He, S. J.; Li, M. Y.; Sun, Y. M., Concentrations and relationships between classes of persistent halogenated organic compounds in pooled human serum samples and air from Laizhou Bay, China. Sci. Total Environ. 2014, 482, 276-282.

431 432

(27) Carnevale, A.; Aleksa, K.; Goodyer, C. G.; Koren, G., Investigating the use of hair to assess polybrominated diphenyl ether exposure retrospectively. Ther. Drug Monit. 2014, 36, 244-251.

433 434 435

(28) Zhu, Z. C.; Chen, S. J.; Ding, N.; Wang, J.; J., L. X.; B.X., M., Polychlorinated biphenyls in house dust at an e-waste site and urban site in the Pearl River Delta, southern China: Sources and human exposure and health risk. Environ. Sci. 2014, 35, 3066-3072 (in Chinese).

436 437 438

(29) Covaci, A.; Voorspoels, S.; Roosens, L.; Jacobs, W.; Blust, R.; Neels, H., Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in human liver and adipose tissue samples from Belgium. Chemosphere 2008, 73, 170-175.

439 440 441

(30) Hagmar, L.; Wallin, E.; Vessby, B.; Jonsson, B. A. G.; Bergman, A.; Rylander, L., Intra-individual variations and time trends 1991-2001 in human serum levels of PCB, DDE and hexachlorobenzene. Chemosphere 2006, 64, 1507-1513.

442 443

(31) Ryan, J. J.; Rawn, D. F. K., Polychlorinated dioxins, furans (PCDD/Fs), and polychlorinated biphenyls (PCBs) and their trends in Canadian human milk from 1992 to 2005. Chemosphere 2014, 102, 76-86.

444 445

(32) Marek, R. F.; Thorne, P. S.; Wang, K.; DeWall, J.; Hornbuckle, K. C., PCBs and OH-PCBs in serum from children and mothers in urban and rural US communities. Environ. Sci. Technol. 2013, 47, 3353-3361.

446 447 448

(33) Eguchi, A.; Nomiyama, K.; Tue, N. M.; Trang, P. T. K.; Viet, P. H.; Takahashi, S.; Tanabe, S., Residue profiles of organohalogen compounds in human serum from e-waste recycling sites in North Vietnam: Association with thyroid hormone levels. Environ. Res. 2015, 137, 440-449.

449 450 451

(34) Drooger, J. C.; Jager, A.; Lam, M. H.; den Boer, M. D.; Sleijfer, S.; Mathijssen, R. H. J.; de Bruijn, P., Development and validation of an UPLC-MS/MS method for the quantification of tamoxifen and its main metabolites in human scalp hair. J Pharmaceut Biomed 2015, 114, 416-425.

452 453 454

(35) Milbrath, M. O.; Wenger, Y.; Chang, C. W.; Emond, C.; Garabrant, D.; Gillespie, B. W.; Jolliet, O., Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ. Health Perspect. 2009, 117, 417-425.

455 456 457

(36) Nakao, T.; Aozasa, O.; Ohta, S.; Miyata, H., Assessment of human exposure to PCDDs, PCDFs and Co-PCBs using hair as a human pollution indicator sample 1: development of analytical method for human hair and evaluation for exposure assessment. Chemosphere 2002, 48, 885-896.

458 459 460

(37) Mcfarland, V. A.; Clarke, J. U., Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: Considerations for a congener-specific analysis. Environ. Health Perspect. 1989, 81, 225-239.

461 462

(38) Chu, S. G.; Covaci, A.; Schepens, P., Levels and chiral signatures of persistent organochlorine pollutants in human tissues from Belgium. Environ. Res. 2003, 93, 167-176.

19



463 464 465

(39) Bucheli, T. D.; Brandli, R. C., Two-dimensional gas chromatography coupled to triple quadrupole mass spectrometry for the unambiguous determination of atropisomeric polychlorinated biphenyls in environmental samples. J. Chromatogr. A 2006, 1110, 156-164.

466 467

(40) Bordajandi, L. R.; Abad, E.; Gonzalez, M. J., Occurrence of PCBs, PCDD/Fs, PBDEs and DDTs in Spanish breast milk: Enantiomeric fraction of chiral PCBs. Chemosphere 2008, 70, 567-575.

468 469

(41) McLachlan, M. S., Framework for the interpretation of measurements of SOCs in plants. Environ. Sci. Technol. 1999, 33, 1799-1804.

470 471 472

(42) Thuresson, K.; Hoglund, P.; Hagmar, L.; Sjodin, A.; Bergman, A.; Jakobsson, K., Apparent half-lives of hepta- to decabrominated diphenyl ethers in human serum as determined in occupationally exposed workers. Environ. Health Perspect. 2006, 114, 176-181.

473 474 475

(43) Sjödin, A.; Hagmar, L.; Klasson-Wehler, E.; Kronholm-Diab, K.; Jakobsson, E.; Bergman, A., Flame retardant exposure: polybrominated diphenyl ethers in blood from Swedish workers. Environ. Health Perspect. 1999, 107, 643-648.

20


Page 20 of 26

Page 21 of 26

476


Figure Captions

477 478

Figure 1. PCB congener profiles in hair and serum from e-waste recycling workers, air,

479

and indoor dust in the e-waste area of southern China. Hair and serum PCB congener

480

profiles from e-waste recycling workers, air, and indoor dust in the e-waste area of

481

southern China. Air and indoor dust data are taken from previous studies.21,28

482 483

Figure 2. Enantiomer Fractions (EFs) of PCBs in hair and serum from e-waste recycling

484

workers and air in southern China. Air data are taken from a previous study.21

21



485 Table 1. PCB Concentrations in Hair (ng/g) and Serum (ng/g lipid) from E-Waste Recycling Workers in Southern China Male hair Female hair Male serum Female serum Median Mean Range Median Mean Range Median Mean Range Median Mean Range PCB28 129 147 32.4-300 346 281 72.1-479 176 240 n.d.a-724 537 494 n.d.-1445 PCB52 49.9 65.5 8.83-168 192 162 36.4-288 n.d. n.d. PCB66 42.9 46.8 12.0-107 117 103 17.9-190 160 162 n.d.-406 273 262 n.d.-506 PCB74 27.4 29.5 7.58-64.6 70.8 61.8 11.8-114 286 330 n.d.-799 317 367 n.d.-983 PCB95 50.1 64.1 13.1-160 189 167 29.5-294 141 137 23.6-299 97.0 127 36.7-299 PCB99 31.4 31.9 7.42-111 73.8 73.7 11.5-184 223 271 n.d.-904 159 272 n.d.-943 PCB101 73.2 83.4 17.0-274 239 220 30.8-481 35.9 64.2 n.d.-261 40.1 90.4 n.d.-331 PCB105 23.0 38.2 6.14-191 85.4 100 13.4-315 125 209 n.d.-928 206 279 n.d.-1241 561 797 49.5-2850 PCB118 48.4 75.9 12.8-349 174 206 26.1-582 384 579 29.3-2353 PCB128 8.40 11.6 1.92-58.9 32.3 36.7 4.05-110 57.6 59.4 n.d.-163 58.5 71.0 n.d.-250 PCB138 20.4 27.5 5.59-125 77.7 82.5 12.0-228 301 356 n.d.-957 276 378 n.d.-1216 PCB153 28.1 33.6 8.65-146 98.7 101 14.9-255 341 404 n.d.-997 289 428 n.d.-1153 PCB164 8.48 10.2 1.91-43.2 31.0 32.2 5.06-78.5 90.2 116 n.d.-283 47.3 95.1 n.d.-345 PCB170/190 3.09 4.15 0.64-13.1 12.8 13.6 3.09-33.6 78.9 90.8 12.6-210 49.1 92.3 18.7-238 PCB177 1.88 2.30 0.47-6.68 6.42 6.01 1.25-11.3 15.7 21.6 n.d.-75.5 13.7 22.3 n.d.-66.2 PCB180 5.87 6.23 1.88-14.3 15.8 17.1 4.86-35.9 105 133 n.d.-376 71.0 122 n.d.-336 PCB187 3.18 3.67 1.02-8.54 8.99 9.14 2.65-17.1 51.8 54.4 n.d.-164 42.6 47.6 n.d.-120 PCB209 0.27 0.27 n.d.-1.46 1.55 2.02 n.d.-6.28 34.1 33.2 n.d.-81.8 38.6 35.8 n.d.-71.21 Total 611 682 161-2020 1781 1675 314-3514 2851 3263 315-8976 2888 3980 256-11200 a Not detectable. 486 487

22


Page 22 of 26

Page 23 of 26


488

Table 2. Spearman Rank Order Correlations of PCB Concentration (ng/g) and Occupational Exposure Duration (yr) for Male (n = 17), Female (n = 12), and All Participants (n = 29)

PCB28

Male

Hair Female

All

Male

Serum Female

All

0.062

-0.028

0.193

0.153

0.394

0.329

a

PCB52 0.281 0.110 0.305 PCB66 0.216 0.274 0.311 0.201 0.155 0.242 PCB74 0.176 0.338 0.289 0.272 0.432 0.346 b PCB95 0.229 0.210 0.318 -0.288 0.244 -0.008 PCB99 0.354 0.295 0.403b 0.400 0.435 0.389b PCB101 0.341 0.352 0.417b -0.007 0.329 0.211 b c PCB105 0.525 0.323 0.517 0.172 0.374 0.255 PCB118 0.471b 0.338 0.475c 0.156 0.324 0.279 b c PCB128 0.400 0.579 0.505 0.412 0.361 0.397b PCB138 0.502b 0.419 0.530c 0.259 0.482b 0.375b b c PCB153 0.540 0.387 0.545 0.224 0.462 0.344 b c PCB164 0.582 0.458 0.551 0.462 0.406 0.382b PCB170+190 0.588b 0.679b 0.605c 0.213 0.445 0.357 b b PCB177 0.580 0.558 0.572c 0.367 0.582b 0.467b PCB180 0.564b 0.615b 0.562c 0.291 0.525b 0.421b b c PCB187 0.513 0.444 0.530 0.057 0.444 0.265 b c PCB209 0.526 0.483 0.482 0.286 0.011 0.114 Total 0.328 0.288 0.393b 0.238 0.471b 0.358 a Correlation analysis was not performed because PCB52 was not detectable in serum. b Correlations are significant at p < 0.05. cCorrelations are significant at p < 0.01. 489 490

23



Page 24 of 26

491

Table 3. Pearson Product-Moment Correlations of PCB concentrations between Hair and Blood Male PCB28 PCB66 PCB74 PCB95 PCB99 PCB101 PCB105 PCB118 PCB128 PCB138 PCB153 PCB164 PCB170/190 PCB177 PCB180 PCB187 PCB209

r 0.600 0.742 0.754 0.416 0.742 0.816 0.810 0.828 0.404 0.722 0.679 0.652 0.537 0.366 0.376 0.462 0.254

p 0.006

Polychlorinated Biphenyls (PCBs) in Human Hair and Serum from E

Recommend Documents