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Urinary Concentrations of Bisphenols and their Association with Biomarkers of Oxidative Stress in People Living Near E-waste Recycling Facilities in China Tao Zhang, Jingchuan Xue, Chuanzi Gao, Rong-Liang Qiu, Yanxi Li, Xiao Li, Mingzhi Huang, and Kurunthachalam Kannan Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b00032 • Publication Date (Web): 14 Mar 2016 Downloaded from http://pubs.acs.org on March 15, 2016
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Environmental Science & Technology
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Urinary Concentrations of Bisphenols and their Association with Biomarkers of
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Oxidative Stress in People Living Near E-waste Recycling Facilities in China
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Tao Zhang1*, Jingchuan Xue2, Chuan-zi Gao1, Rong-liang Qiu1, Yan-xi Li1, Xiao Li1, Ming-zhi
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Huang3, Kurunthachalam Kannan2, 4*
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1
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Pollution Control and Remediation Technology, Sun Yat-sen University, Guangzhou 510275, PR China
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2
School of Environmental Science and Engineering, Guangdong Provincial Key Laboratory of Environmental
Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences,
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School of Public Health, State University of New York at Albany, Albany, NY 12201, USA
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3
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Geo-simulation, Sun Yat-sen University, Guangzhou 510275, PR China
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4
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Center, King Abdulaziz University, Jeddah, Saudi Arabia
Department of Water Resources and Environment, Guangdong Provincial Key Laboratory of Urbanization and
Biochemistry Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd Medical Research
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Corresponding author:
17 18 19 20 21 22 23 24 25 26 27 28 29 30 31
K. Kannan Wadsworth Center Empire State Plaza, PO Box 509 Albany, NY 12201-0509 Tel: +1-518-474-0015 Fax: +1-518-473-2895 E-mail:
[email protected] Tao Zhang School of Environmental Science and Engineering, Sun Yat-Sen University 135 Xingang West Street, Guangzhou, 510275, China Tel: 86-22-84113454 Email:
[email protected] Submission to: Environmental Science Technology
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Abstract
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In this study, concentrations of bisphenol A (BPA) and seven other bisphenols (BPs) were
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measured in urine samples collected from people living in and around e-waste dismantling facilities,
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and in matched reference population from rural and urban areas in China. BPA, bisphenol S (BPS),
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and bisphenol F (BPF) were frequently detected (detection frequencies: > 90%) in urine samples
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collected from individuals who living near e-waste facilities, with geometric mean (GM)
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concentrations of 2.99 (or 3.75), 0.361 (or 0.469) and 0.349 (or 0.435) ng/mL (or µg/g Cre),
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respectively; other five BPs were rarely found in urine samples, regardless of the sampling site. The
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urinary concentrations of BPA and BPF, but not BPS, were significantly higher in individuals from e-
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waste recycling locations than did individuals from rural reference location. Our findings indicated
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that e-waste dismantling activities contribute to human exposure to BPA and BPF. 8-hydroxy-2’-
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deoxyguanosine (8-OHdG) was measured in urine as a marker of oxidative stress. In the e-waste
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dismantling location, urinary 8-OHdG was significantly and positively correlated (p < 0.001) with
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urinary BPA and BPS, but not BPF; a similar correlation was also observed in reference sites. These
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findings suggested that BPA and BPS exposure are associated with elevated oxidative stress.
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Environmental Science & Technology
Introduction
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Along with the economic prosperity, ownership of electronic/electrical products (e-products) has
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been rapidly increasing around the world. However, rapid and continuing technological innovations
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lead to early obsolescence of e-products. The combination of increasing ownership and shortened
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lifespan eventually results in mounting piles of electronic waste (e-waste), which has emerged as a
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significant global problem in recent years.1 It was reported that approximately 40 million tons of e-
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wastes have been generated per year globally.2 At present, approximately 70% of the e-waste
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generated worldwide is processed in China every year (i.e., 28 million tons yr-1).3 E-waste contains
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toxic organic pollutants and metals; primitive recycling processes employed in several developing
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countries result in the release of these toxicants into the environment.4-7
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Bisphenol A (BPA; 2,2-bis(4-hydroxyphenyl)propane) is one of the highest production volume
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chemicals, which has been widely used in the manufacture of polycarbonate plastics and the resin
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lining of e-products.8,9 E-wastes contain approximately 30% plastics by weight, i.e., 12 million tons
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of plastic wastes are generated annually from e-products worldwide.2,10 Open burning of plastics
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contained in e-wastes can be a significant emission source of BPA into the atmospheric
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environment.4 Further, BPA can be emitted from the combustion of printed circuit boards in e-waste.5
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Bi et al found three orders of magnitude greater concentrations of BPA in dust collected from e-waste
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workshops (780 µg/g) than those in house dust (0.67 µg/g).11 With the increase in concern over BPA
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exposure, studies have shown that even at low doses BPA can affect human health.12-14 Low-dose
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BPA exerted c-Myc-dependent genotoxic and mitogenic effects on ERα-negative mammary cells,12
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and had real and measurable effects on brain development and behavior.13 For general adults,
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exposure to certain environmental BPA might induce oxidative stress.14 Despite these, little is known
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on human exposure to BPA in e-waste recycling sites.
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Because of the concern over the toxicity of BPA, manufacturers have begun replacing BPA
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from the products with alternative substances (i.e., other bisphenols or BPs).15-17 For example,
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bisphenol S (BPS; 4,4’-sulfonyldiphenol) has been used as an alternative to BPA in the production of
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baby bottles and thermal receipt papers; BPS, bisphenol F (BPF; 4,4’-dihydroxydiphenylmethane)
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and bisphenol AF [BPAF; 4,4’-(hexafluoroisopropylidene)diphenol] are used in the manufacture of
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certain plastics and epoxy resins.16,17 Studies have shown that BPA alternatives are widely found in
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thermal receipt papers, indoor dust, personal care products, and foodstuffs.18-22 It is worth to note that
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several alternatives of BPA may also be harmful to human health, and they have endocrine-disrupting
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effects.13,23 The potentials for human exposure to BPA and several other BPs (the molecular
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structures of BPs were shown in Table S1) are co-existing in e-waste dismantling sites.
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The mechanisms of toxicants-induced health effects are believed to involve oxidative stress.24
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Many in vitro and laboratory animal studies have shown that BPA can cause oxidative stress by the
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release of reactive oxygen species (ROS) and/or by the impairment of antioxidant defenses;25-28
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however, only few studies have examined the association between urinary BPA levels and oxidative
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stress.14,29,30 As one of the predominant forms of oxidative lesions in DNA, 8-hydroxy-2’-
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deoxyguanosine (8-OHdG) is a critical biomarker for oxidative DNA damage. In this study, we
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therefore investigated human exposure to BPs in e-waste dismantling locations and examined the
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association of BP exposures on oxidative stress by measuring eight BPs and 8-OHdG in urine
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samples collected from individuals living in one of the three largest e-waste recycling locations in
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China.
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Materials and Methods
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Study Areas and Sample Collection. First morning void urine samples were collected from
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local residents in an e-waste recycling region located in Longtang Town, Qingyuan City, China,
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during July to August 2014. Longtang Town comprises of 14 villages with a population of
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approximately 70,000 and an area of 153 km2. Two villages were selected in this study on the basis
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of the differences in the scale of e-waste recycling operations. Village#1 had a high density of e-
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waste workshops (> 50% of families had e-waste operations) that were involved in equipment
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dismantling and plastic recovery (i.e., stripping plastic materials from e-waste). Village#2 had a
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lesser density of e-waste recycling operations (approximately 20% of families had e-waste
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workshops). Villages #1 and #2 were assigned as high-density (HDED) and low-density e-waste
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dismantling (LDED) areas, respectively. In addition, village#3 that did not have any e-waste
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dismantling workshops, located 80 km northwest of Longtang, was chosen as a rural reference area.
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The population, automobile traffic, lifestyle, and socioeconomic status were very similar among these
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three villages. Guangzhou, the capital of Guangdong Province located 60 km southeast of Longtang,
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was selected as an urban reference area. The sampling locations are shown in Figure S1.
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This study was approved by the Institutional Review Board of Sun Yat-sen University, China.
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An informed consent was obtained from all subjects and self-administered questionnaire surveys
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were completed by each participant (or their guardian) and information regarding age, gender,
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occupational history, and place of residence were collected. The participants (total: n = 116; males: n
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= 66) in the e-waste recycling villages were between the ages of 0.4 and 87 years and were all born
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local. Overall, 51 of 116 participants were from the HDED area and 34% of them were non-adults (
LOQ) 100 GM 2.99 c
median min max
3.75 3.00 3.42 0.233 0.795 27.6 134
97
90
9
2
3
3
7
100
100
0.361
0.349
0.0278
0.0288
0.0290
0.0600
0.0174
4.31
8.00
0.469 0.364 0.500 < LOQ d < LOQ 1.38 2.48
0.435 0.365 0.432 < LOQ < LOQ 8.68 17.0
0.03 < LOQ 0.0325 < LOQ < LOQ 0.142 0.138
0.04 < LOQ 0.0327 < LOQ < LOQ 0.0582 0.165
0.04 < LOQ 0.0358 < LOQ < LOQ 0.0936 0.222
0.06 < LOQ 0.0600 < LOQ < LOQ 0.136 0.332
0.02 < LOQ 0.0224 < LOQ < LOQ 0.134 0.148
5.40 4.06 5.20 0.737 1.37 28.6 137
10.0 8.67 9.55 0.719 2.80 32.8 27.8
Rural reference area (n e = 22) 91 100 N (% > LOQ) GM 0.589 0.388 1.52 1.03 median 0.648 0.398 2.07 0.914 min < LOQ 0.192 0.194 0.477 max 4.12 1.07 4.10 2.12
0.0886 0.219 0.0500 0.125 < LOQ 0.0653 0.855 3.06
Urban reference area (n = 20) N (% > LOQ) 80 100 GM 0.952 0.652 1.78 1.51 median 1.42 0.835 1.76 1.68 min < LOQ 0.113 < LOQ 0.412 max 4.07 1.57 7.13 4.21
0.556 1.12 0.484 1.22 0.127 0.260 3.04 4.32
41
100
23 0.0329 0.0527 < LOQ 0.0612 < LOQ 0.0192 0.112 0.116 0 < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ
14 0.0274 0.0422 < LOQ 0.0490 < LOQ 0.0153 0.531 0.0924 0 < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ < LOQ
5 0.0441 0.0844 < LOQ 0.0979 < LOQ 0.0306 0.336 0.185 5 0.0207 0.0383 < LOQ < LOQ < LOQ < LOQ 0.0414 0.0899
9 0.0706 0.127 < LOQ 0.147 < LOQ 0.0460 0.703 0.277 15 0.0244 0.0469 < LOQ < LOQ < LOQ < LOQ 0.1020 0.261
a
14 0.0338 0.0527 < LOQ 0.0612 < LOQ 0.0192 0.550 0.116 20 0.0132 0.0259 < LOQ < LOQ < LOQ < LOQ 0.0736 0.193
100 1.59 3.63 1.46 3.66 0.64 1.56 5.48 9.89
100 6.84 19.8 8.55 22.6 0.0474 8.71 36.7 34.9
100 2.75 5.41 2.89 5.43 0.740 2.06 8.10 12.8
100 7.31 18.4 6.55 17.7 0.783 9.24 28.8 29.9
∑BPs: the sum concentrations of all target BPs. b the concentrations were calculated based on all participants from e-waste dismantling area with high-density and low-density workshops. c Italic: creatinine-adjusted concentration (µg/g Cre). d < LOQ: concentrations value lower than LOQ. e n: the number of samples.
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Table 2. Pearson Correlations among Urinary Concentrations a of Three Commonly Detectable BPs (BPA, BPS and BPF) in E-waste Recycling, Rural and Urban reference Areas in China. BPA
e-waste recycling area BPS BPF
BPA
1
BPS
r = 0.329 p < 0.001 r = 0.249 p < 0.01
BPF
BPA
1
BPS
r = 0.316 p < 0.01 r = 0.327 p < 0.001
BPF a
BPA
rural reference area BPS BPF
BPA
urban reference area BPS BPF
based on creatinine-unadjusted urinary concentrations 1 1 1 r = 0.048 p = 0.615
r = 0.071 p = 0.754 r = 0.202 p = 0.603
1
1 r = 0.008 p = 0.983
1
r = 0.041 p = 0.864 r = 0.272 p = 0.246
1 r = 0.270 p = 0.250
1
based on creatinine-adjusted urinary concentrations 1 1 1 r = 0.279 p = 0.101
1
r = 0.136 p = 0.726 r = 0.503 p = 0.168
1
r = 0.494 p = 0.176
1
we used log urinary concentrations for these estimations.
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r = 0.031 p = 0.906 r = 0.259 p = 0.316
1 r = 0.253 p = 0.327
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creatinine-adjusted
1.2 0.6 0.0
1.2 0.6
urban control (all)
rural control (all)
e-waste (NOP)
rural control (all)
urban control (all)
e-waste (NOP)
e-waste (OP)
e-waste (LDED)
e-waste (HDED)
0.0 e-waste (all)
urban control (all)
rural control (all)
e-waste (OP)
e-waste (NOP)
e-waste (LDED)
e-waste (all)
e-waste (HDED)
0.0
1.8
e-waste (OP)
2.5
1.8
e-waste (LDED)
5.0
(c) BPF
e-waste (HDED)
Concentrations (ng/mL or µg/g Cre)
Concentrations (ng/mL or µg/g Cre)
7.5
2.4
(b) BPS
e-waste (all)
2.4
(a) BPA
Concentrations (ng/mL or µg/g Cre)
unadjusted 10.0
Figure 1. Geometric mean concentrations of BPA (plot a), BPS (plot b) and BPF (plot c) in urine samples collected from reference areas and e-waste dismantling areas, as stratified by the number of e-waste workshops, occupational status, and place of residence. The abscissa of e-waste (all), rural (all) and urban (all) represent the data for all participants from e-waste dismantling, rural and urban reference areas respectively; e-waste (HDED) and e-waste (LDED) represent the data for participants from high-density and low-density e-waste dismantling workshop areas, respectively; e-waste (OP) and e-waste (NOP) represent the data for occupational exposure and non-occupational exposure participants, respectively, within the e-waste dismantling area.
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BPA
BPS
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BPF
e-waste area in China, 2014 rural area in China, 2014
human urine
urban area in China, 2014 U.S., 2014 U.S., 2013 U.S., 2011 U.S., 2010 U.S., 2009 U.S., 2007 U.S., 2001 U.S., 2000
exposure sources
indoor dust (home in China, 2010) indoor dust (e-waste site in Vietnam, 2012) foodstuff (China, 2012) foodstuff (U.S., 2008-2012) personal care products (China, 2012-2013) personal care products (U.S., 2012-2013) thermal paper (Danmark, 2014) household paper (Danmark, 2013) 0%
50%
100%
Figure 2. Composition profiles of several commonly detected bisphenols in human urine and exposure sources. Unadjusted urinary concentrations of BPs were used; profiles of BPs in urine samples from e-waste, rural and urban areas in China were generated in this study; profile of BPs in human urine from the U.S. was from another study;15 to analyze the exposure sources of BPs in this study, the composition profiles of BPs in each human exposure source were cited from several previous studies.18,20-22 The numbers in abscissa were the sampling dates.
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e-waste recycling area 0.5
1.0 0.5 0.0 -0.5 -1.0
1.5
r = 0.386 p < 0.001
0.0
Log urinary BPF
r = 0.413 p < 0.001
1.5
Log urinary BPS
Log urinary BPA
2.0
-0.5 -1.0 -1.5 -2.0
-0.5
0.0
0.5
1.0
1.5
0.5 0.0 -0.5 -1.0 -1.5
-0.5
2.0
r = 0.118 p = 0.208
1.0
Log urinary 8-OHdG
0.0
0.5
1.0
1.5
2.0
-0.5
Log urinary 8-OHdG
0.0
0.5
1.0
1.5
2.0
Log urinary 8-OHdG
control area 0.4
0.5 0.0 -0.5 -1.0
1.0
r = 0.479 p < 0.001
Log urinary BPF
r = 0.465 p < 0.01
Log urinary BPS
Log urinary BPA
1.0
0.0 -0.4 -0.8
-1.0
-0.4
0.2
0.8
1.4
Log urinary 8-OHdG
2.0
0.0 -0.5 -1.0 -1.5
-1.2
-1.5
r = 0.223 p = 0.155
0.5
-1.0
-0.4
0.2
0.8
1.4
2.0
Log urinary 8-OHdG
-1.0
-0.4
0.2
0.8
1.4
2.0
Log urinary 8-OHdG
Figure 3. Pearson correlations of urinary BPA, BPS and BPF concentrations with urinary 8-OHdG concentrations in individuals living in e-waste dismantling and reference areas, respectively. We used log urinary concentrations for these analyses. Reference area refers to combined data from rural and urban reference areas.
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TOC Art
BPS BPF BP
BPA AF
BP AP
BPZ BPZ
B BP
Human Exposure? & Oxidative Stress?
E-waste Recycling
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