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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
Article in Environmental Science & Technology · March 2016
Impact Factor: 5.33 · DOI: 10.1021/acs.est.6b00032
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Available from: Jingchuan Xue Retrieved on: 12 April 2016
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,
‡Chuan-zi Gao,
†Rong-liang Qiu,
†Yan-xi Li,
†Xiao Li,
†Ming-zhi Huang,
§and Kurunthachalam Kannan*
,‡,∥†School of Environmental Science and Engineering, Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Sun Yat-sen University, Guangzhou 510275, People’s Republic of China
‡Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Albany, New York 12201, United States
§Department of Water Resources and Environment, Guangdong Provincial Key Laboratory of Urbanization and Geo-simulation, Sun Yat-sen University, Guangzhou 510275, Peopl’s Republic of China
∥Biochemistry Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah 22252, Saudi Arabia
*S Supporting Information
ABSTRACT: In this study, concentrations of bisphenol A (BPA) and seven other bisphenols (BPs) were measured in urine samples collected from people living in and around e-waste dismantling facilities, and in matched reference population from rural and urban areas in China. BPA, bisphenol S (BPS), and bisphenol F (BPF) were frequently detected (detection frequencies: > 90%) in urine samples collected from individuals who live near e-waste facilities, with geometric mean (GM) concentrations of 2.99 (or 3.75), 0.361 (or 0.469), and 0.349 (or 0.435) ng/
mL (or μg/g Cre), respectively; the other five BPs were rarely found in urine samples, regardless of the sampling location. The urinary concentrations of BPA and BPF, but not BPS, were significantly higher in individuals from e-waste recycling locations than did individuals from a rural reference location. Our findings indicated that e-waste dismantling activities contribute to human exposure to BPA and BPF. 8-Hydroxy-2′-deoxyguanosine (8-OHdG) was measured in urine
as a marker of oxidative stress. In the e-waste dismantling location, urinary 8-OHdG was significantly and positively correlated (p
< 0.001) with urinary BPA and BPS, but not BPF; a similar correlation was also observed in reference sites. Thesefindings suggest that BPA and BPS exposures are associated with elevated oxidative stress.
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INTRODUCTIONAlong with the economic prosperity, ownership of electronic/
electrical products (e-products) has been rapidly increasing around the world. However, rapid and continuing technological innovations lead to early obsolescence of e-products. The combination of increasing ownership and shortened lifespan eventually results in mounting piles of electronic waste (e- waste), which has emerged as a significant global problem in recent years.1 It was reported that approximately 40 million tons of e-wastes have been generated per year globally.2 At present, approximately 70% of the e-waste generated worldwide is processed in China every year (i.e., 28 million tons yr−1).3E- waste contains toxic organic pollutants and metals; primitive recycling processes employed in several developing countries result in the release of toxicants into the environment.4−7
Bisphenol A (BPA; 2,2-bis(4-hydroxyphenyl)propane) is one of the highest production volume chemicals, which has been widely used in the manufacture of polycarbonate plastics and
the resin lining of e-products.8,9E-wastes contain approximately 30% plastics by weight, i.e., 12 million tons of plastic wastes are generated annually from e-products worldwide.2,10 Open burning of plastics contained in e-wastes can be a significant emission source of BPA into the atmospheric environment.4 Further, BPA can be emitted from the combustion of printed circuit boards in e-waste.5Bi et al. found 3 orders of magnitude greater concentrations of BPA in dust collected from e-waste workshops (780μg/g) than those in house dust (0.67μg/g).11 Studies have shown that even low doses of BPA can affect human health.12−14 Low-dose BPA exerted c-Myc-dependent genotoxic and mitogenic effects on ERα-negative mammary cells12 and had real and measurable effects on brain
Received: January 4, 2016 Revised: March 4, 2016 Accepted: March 14, 2016
pubs.acs.org/est
© XXXX American Chemical Society A DOI:10.1021/acs.est.6b00032
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development and behavior.13 For general adults, exposure to certain environmental BPA might induce oxidative stress.14 Despite these, little is known on human exposure to BPA in e- waste recycling sites.
Because of the concern over the toxicity of BPA, manufacturers have begun replacing BPA from the products with alternative substances (i.e., other bisphenols or BPs).15−17 For example, bisphenol S (BPS; 4,4′-sulfonyldiphenol) has been used as an alternative to BPA in the production of baby bottles and thermal receipt papers; BPS, bisphenol F (BPF;
4,4′-dihydroxydiphenylmethane) and bisphenol AF [BPAF;
4,4′-(hexafluoroisopropylidene)diphenol] are used in the manufacture of certain plastics and epoxy resins.16,17 Studies have shown that BPA alternatives are widely found in thermal receipt papers, indoor dust, personal care products, and foodstuffs.18−22 It is noteworthy that several alternatives of BPA may also be harmful to human health, and they have endocrine-disrupting effects.13,23 The potential for human coexposure to BPA and several other BPs (the molecular structures of BPs were shown in Table S1 of the Supporting Information, SI) exists in e-waste dismantling sites.
The mechanisms of toxicant-induced health effects are believed to involve oxidative stress.24 Many in vitro and laboratory animal studies have shown that BPA can cause oxidative stress by the release of reactive oxygen species (ROS) and/or by the impairment of antioxidant defenses;25−28 however, only a few studies have examined the association between urinary BPA levels and oxidative stress.14,29,30As one of the predominant forms of oxidative lesions in DNA, 8- hydroxy-2′-deoxyguanosine (8-OHdG) is a critical biomarker for oxidative DNA damage. In this study, we therefore investigated human exposure to BPs in e-waste dismantling locations and examined the association of BP exposures on oxidative stress by measuring eight BPs and 8-OHdG in urine samples collected from individuals living in one of the three largest e-waste recycling locations in China.
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MATERIALS AND METHODSStudy Areas and Sample Collection.First morning void urine samples were collected from local residents in an e-waste recycling region located in Longtang Town, Qingyuan City, China, during July to August 2014. Longtang Town comprises 14 villages with a population of approximately 70 000 and an area of 153 km2. Two villages were selected in this study on the basis of the differences in the scale of e-waste recycling operations. Village#1 had a high density of e-waste workshops (>50% of families had e-waste operations) that were involved in equipment dismantling and plastic recovery (i.e., stripping plastic materials from e-waste). Village #2 had a lesser density of e-waste recycling operations (approximately 20% of families had e-waste workshops). Villages #1 and #2 were assigned as high-density (HDED) and low-density e-waste dismantling (LDED) areas, respectively. In addition, village#3 did not have any e-waste dismantling workshops, located 80 km northwest of Longtang, was chosen as a rural reference area. The population, automobile traffic, lifestyle, and socioeconomic status were very similar among these three villages. Guangzhou, the capital of Guangdong Province located 60 km southeast of Longtang, was selected as an urban reference area. The sampling locations are shown inFigure S1.
This study was approved by the Institutional Review Board of Sun Yat-sen University, China. An informed consent was obtained from all subjects and self-administered questionnaire
surveys were completed by each participant (or their guardian) and information regarding age, gender, occupational history, and place of residence were collected. The participants (total:n
= 116; males: n = 66) in the e-waste recycling villages were between the ages of 0.4 and 87 years and were all born local.
Overall, 51 of 116 participants were from the HDED area and 34% of them were nonadults (<18 years). The numbers of donors from the rural and urban reference sites were 22 (males:
n = 11) and 20 (males: n = 9), respectively. Additional information regarding the donors is provided inTable S2. All collected urine samples were stored in polypropylene (PP) tubes at −20°C before analysis.
Bisphenols Extraction and Analysis.Urine samples were extracted and analyzed for BPA, BPS, BPF, bisphenol B [BPB;
2,2-bis(4-hydroxyphenyl)butane], bisphenol Z [BPZ; 4,4′- cyclohexylidenebisphenol; 98%], bisphenol AP [BPAP; 4,4′- (1-phenylethylidene)bisphenol; 99%] and BPAF by following the method described elsewhere,31 with some modifications.
Briefly, an aliquot (0.5 mL) of urine was spiked with 50μL of
13C12−BPA (0.1 ng/μL) prior to extraction. The samples were buffered with 0.3 mL of 1.0 M ammonium acetate that contained 22 units ofβ-glucuronidase (prepared by spiking 50 μL of β-glucuronidase into 100 mL of 1.0 M ammonium acetate solution) and digested at 37°C for 12 h. Thereafter, the samples were extracted twice with 3 mL each ethyl acetate (2× 3 mL). For each successive extraction, the mixture was shaken vigorously for 40 min and then centrifuged at 4500×g for 10 min. The supernatants were combined and washed with 1.0 mL of Milli-Q water. After centrifugation at 4500×gfor 10 min, the supernatant was transferred into a 15 mL glass tube and concentrated to near-dryness under a gentle nitrogen stream.
The extract was reconstituted with 0.5 mL of methanol and vortex mixed for analysis.
An Applied Biosystems API 5500 electrospray triple quadrupole mass spectrometer (ESI−MS/MS; Applied Bio- systems, Foster City, CA, U.S.A.) equipped with Waters Acquity UPLC system (Waters, Milford, MA, U.S.A.) was used for identification and quantification of BPs. Ten microliters of extracts were injected onto a Thermo Betasil C18 chromato- graphic column (100×2.1 mm2, 5μm) serially connected with a guard column (Betasil C18, 20 ×2.1 mm2, 5μm; Thermo Electron). The mobile phase comprised methanol (A) and Milli-Q water/methanol (90%/10%, % v/v; B) at aflow rate of 200μL/min, and the gradient was as follows: 0−4 min, 15% A;
4−6 min, 15−55% A; 6−7.5 min, 55−85% A; 7.5−9.5 min, 85% A; 9.5−10 min, 85−95% A; 10−14 min, 95% A; 14−15 min, 95−15% A; and 15−22 min, 15%. The negative ion multiple reaction monitoring (MRM) mode was used, and the MRM transitions monitored are shown in Table S1. The electrospray ionization voltage was set at−4.5 kV. The collision and curtain gas (nitrogen)flow rates were set at 7 and 20 psi, respectively, and the source heater was set at 600 °C. The nebulizer gas (ion source gas 1) and the heater gas (ion source gas 2) were set at 45 and 60 psi, respectively. The data acquisition was performed at a scan speed of 80 ms and a resolving power of 0.70 full width at half-maximum.
8-Hydroxy-2′-deoxyguanosine Analysis. The urinary levels of 8-OHdG were measured using the method described previously.32In brief, 0.1 mL of urine was diluted 5-fold with Milli-Q water, and 20 ng of labeled internal standard (15N5-8- OHdG) was added and analyzed by MRM in the positive ionization mode by UPLC−MS/MS.
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Table1.Concentrations(ng/mL;μg/gCre)ofEightBisphenolsandtheBiomarkerofOxidativeStressinUrineSamplesfromE-WasteDismantlingandReferenceAreasin China bisphenolsoxidativestress BPABPSBPFBPBBPZBPPBPAPBPAF∑BPsa8-OHdG E-wastedismantlingareab(n=116) N(%>LOQ)100979092337100100 GM2.990.3610.3490.02780.02880.02900.06000.01744.318.00 3.75c 0.4690.4350.030.040.040.060.025.4010.0 median3.000.3640.365<LOQ<LOQ<LOQ<LOQ<LOQ4.068.67 3.420.5000.4320.03250.03270.03580.06000.02245.209.55 min0.233<LOQd<LOQ<LOQ<LOQ<LOQ<LOQ<LOQ0.7370.719 0.795<LOQ<LOQ<LOQ<LOQ<LOQ<LOQ<LOQ1.372.80 max27.61.388.680.1420.05820.09360.1360.13428.632.8 1342.4817.00.1380.1650.2220.3320.14813727.8 ruralreferencearea(ne =22) N(%>LOQ)911004123145914100100 GM0.5890.3880.08860.03290.02740.04410.07060.03381.596.84 1.521.030.2190.05270.04220.08440.1270.05273.6319.8 median0.6480.3980.0500<LOQ<LOQ<LOQ<LOQ<LOQ1.468.55 2.070.9140.1250.06120.04900.09790.1470.06123.6622.6 min<LOQ0.192<LOQ<LOQ<LOQ<LOQ<LOQ<LOQ0.640.0474 0.1940.4770.06530.01920.01530.03060.04600.01921.568.71 max4.121.070.8550.1120.5310.3360.7030.5505.4836.7 4.102.123.060.1160.09240.1850.2770.1169.8934.9 urbanreferencearea(n=20) N(%>LOQ)801001000051520100100 GM0.9520.6520.556<LOQ<LOQ0.02070.02440.01322.757.31 1.781.511.12<LOQ<LOQ0.03830.04690.02595.4118.4 median1.420.8350.484<LOQ<LOQ<LOQ<LOQ<LOQ2.896.55 1.761.681.22<LOQ<LOQ<LOQ<LOQ<LOQ5.4317.7 min<LOQ0.1130.127<LOQ<LOQ<LOQ<LOQ<LOQ0.7400.783 <LOQ0.4120.260<LOQ<LOQ<LOQ<LOQ<LOQ2.069.24 max4.071.573.04<LOQ<LOQ0.04140.10200.07368.1028.8 7.134.214.32<LOQ<LOQ0.08990.2610.19312.829.9 a ∑BPs:thesumconcentrationsofalltargetBPs.b Theconcentrationswerecalculatedbasedonallparticipantsfrome-wastedismantlingareawithhigh-densityandlow-densityworkshops.c Italic: creatinine-adjustedconcentration(μg/gCre).d <LOQ:concentrationsvaluelowerthanLOQ.e n:thenumberofsamples.
DOI:10.1021/acs.est.6b00032 Environ. Sci. Technol.XXXX, XXX, XXX−XXX C
Creatinine Analysis. Creatinine was analyzed by UPLC− MS/MS after diluting urine samples (5 μL) to approximately 320-fold and adding 800 ng of creatinine-d3(80μL, 10 ng/μL).
Quality Assurance and Quality Control. Blank- and matrix-spike recoveries of individual BPs through the analytical procedure were determined by spiking (10 ng each) 8 BPs into Milli-Q water and randomly selected urine samples, respec- tively. Mean recoveries of BPs spiked into Milli-Q water (n= 8) ranged from 85±10% (BPF) to 98±13% (BPS), and those spiked into urine samples (n = 8) ranged from 84 ± 12%
(BPB) to 102 ±17% (BPA). 13C12−BPA was spiked into all samples (5.0 ng each) prior to extraction, and the recoveries of
13C12−BPA was 95% ± 15%. The reported concentrations of BPs in samples were not corrected for the recoveries of internal standards. Methanol was injected after every batch of 10 samples as a check for memory effects. Ten procedure blanks, consisting of Milli-Q water, were prepared in the same way as real samples to monitor for contamination in reagents and glassware. All instrumental blanks and procedure blanks were free of detectable concentrations of the target BPs analyzed, except for BPA, which was found in procedure blanks at 0.08± 0.06 ng/mL. The reported concentrations of BPA in samples were blank-corrected.
A 10-point calibration standard was prepared in methanol at concentrations that ranged from 0.01 to 50 ng/mL and was injected before every 20 samples. The regression coefficient of the calibration curve was >99%. The limits of quantitation (LOQs) were determined based on the lowest point in the calibration standard, the volume of urine taken for analysis and the concentration factor. The LOQ was 0.05 ng/mL for BPA, BPB and BPAF; 0.08 ng/mL for BPZ and BPP; and 0.12 ng/
mL for BPF, BPS, and BPAP.
Statistical Analysis. Data analysis was performed with SPSS Version 19.0. Urinary concentrations of BPs were tested for normality using the Kolmogorov−Smirnov test. Differences between groups were analyzed by one-way ANOVA when the two sets of data were distributed normally; otherwise, Mann− Whitney U-test was used. Log-transformation urinary concen- trations were used for correlation analyses. Pearson correlation
coefficients were used for the analysis of relationship between two sets of data with normal distribution; otherwise, the Spearman’s rank correlation coefficient was used. A value ofp<
0.05 denoted significance.
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RESULTS AND DISCUSSIONConcentrations (total) of 8 BPs in urine samples collected from donors from e-waste recycling villages, and two reference sites are shown in Table 1 [geometric mean (GM), median, minimum and maximum]. Values below the LOQ were assigned a value equal to half of their corresponding LOQs.
Urinary Concentrations of BPA. In the e-waste recycling sites, urinary concentrations of BPA ranged from 0.233 to 27.6 ng/mL [or 0.795 to 134 μg/g creatinine (Cre)], with a GM value of 2.99 ng/mL (or 3.75μg/g Cre) (Table 1). The urinary concentrations of BPA varied by the sampling sites, the highest GM urinary concentration of BPA was obtained in e-waste dismantling site, followed by (in decreasing order) urban reference area (GM: 0.952 ng/mL) and rural reference area (0.589 ng/mL) (Table 1 and Figure 1). No significant difference was found in the concentrations of urinary BPA between the urban and rural reference areas (p = 0.337).
However, the concentrations of BPA in donors from e-waste dismantling villages were significantly (p < 0.01) higher than those in the two reference areas (Table 1). Meanwhile, occupationally exposed e-waste workers (GM: 5.58 ng/mL) had significantly higher (p < 0.05) BPA concentrations than nonoccupationally exposed donors (2.77 ng/mL) living in the e-waste recycling sites (Figure 1); and urinary BPA concentrations in donors from HDED area (4.06 ng/mL or 4.73μg/g Cre) were significantly (p< 0.05) higher than those in donors from LDED area (2.36 ng/mL or 2.94μg/g Cre). E- waste typically contains 30% plastic and epoxy resin based materials by weight,10 and BPA is widely used in the manufacture of plastics and epoxy resins.16In China, most e- waste recycling operations are primitive, e.g., plastic scraps that cannot be sorted visually are burned.6 Significant positive correlation was observed between atmospheric aerosol levels of BPA and 1,3,5-triphenylbenzene, a tracer for plastic burning, 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 nonoccupational exposure participants, respectively, within the e-waste dismantling area.
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indicating that open burning of plastics should be a significant emission source of atmospheric BPA.4In addition, BPA can be emitted by the incineration of printed circuit boards of obsolete computers and other electronics.5The elevated concentrations of BPA in e-waste workers found in this study are consistent with the presence of BPA in e-waste.
Human exposure to BPA is widespread.15,33−42Nevertheless, this is the first study to document elevated urinary levels of BPA (and other BPs as described below) in e-waste site residents. When the data were compared with the reported urinary BPA concentrations in the general population in China, the GM concentrations of BPA (nonoccupational residents only) in e-waste recycling area (GM: 2.77 ng/mL or 3.36μg/g Cre; Figure 1) were much higher than those reported for Shanghai (0.45−0.87 ng/mL), Tianjin (1.01 ng/mL), and Harbin (1.17 ng/mL);33−37but comparable to that reported for Guangzhou (3.00 ng/mL).37 It is noteworthy that all participants recruited in that earlier study from Guangzhou were aged from 3 to 24 years.37The GM urinary concentration of BPA were 3.54 ng/mL for subjects 3 to 24 years old in e- waste site, which was higher than that earlier reported for Guangzhou.37 In comparison with the contemporaneous studies from other countries, our data (GM: 2.77 ng/mL or 3.36μg/g Cre;Figure 1) were higher than those reported for the general population from the U.S. (0.36 ng/mL), Mexico (0.70 ng/mL), Turkey (0.74μg/g Cre), Egypt (0.80 ng/mL), Canada (1.16 ng/mL), Spain (2.00 μg/g Cre), and several Asian countries (0.84−2.00 ng/mL).15,36,38−42
We also compared urinary BPA concentrations reported for occupationally exposed individuals.43 The urinary BPA concentrations in workers (GM: 55.7 ng/mL or 32.0 μg/g Cre) from BPA production facilities were much higher than those in e-waste workers (5.58 ng/mL or 7.57μg/g Cre;Figure 1).43Although dust ingestion and dermal absorption are minor contributors (<10% of total exposure) to the daily exposure to BPA by the general population,20,44these exposure pathways can be a dominant source for occupational exposures in e-waste workshops and production facilities of BPA-containing materials, as high concentrations of BPA in indoor dust (a marker of indoor contamination) were found in e-waste workshops (780 μg/g) and BPA production facilities (4660 μg/g);11,44these concentrations are 3 to 4 orders of magnitude greater than those reported in house dust (0.67 μg/g).20 Therefore, the high urinary BPA concentrations found in
workers from BPA (or epoxy resin) production facilities in comparison with those of e-waste workers can be explained by the indoor contamination levels. The measured BPA concentrations in e-waste workers were higher than the concentrations reported for workers who are in frequent contact with thermal paper receipts (1.02 ng/mL or 1.32μg/g Cre).45
Urinary Concentrations of Other Bisphenols.BPF and BPS were also detected frequently (>90%) in urine samples collected from the e-waste recycling sites, at GM concentrations of 0.349 ng/mL (or 0.435 μg/g Cre) and 0.361 ng/mL (or 0.469μg/g Cre), respectively (Table 1). Donors living in the e- waste recycling villages had significantly higher (p < 0.01) urinary BPF concentrations than those (GM: 0.09 ng/mL) from the rural reference area (Table 1). Furthermore, urinary BPF concentrations in donors from the HDED area (0.663 ng/
mL) were significantly higher (p < 0.001) than those in the LDED area (0.212 ng/mL) (Figure 1). These results further suggest that e-waste dismantling activities can contribute to human exposure to BPF. In contrast to that observed for BPA and BPF, no significant difference (p > 0.05) in urinary BPS concentrations was found between e-waste workers (0.361 ng/
mL) and rural reference (0.388 ng/mL) population; likewise, no difference in urinary BPS concentrations was observed (p>
0.05) between the HDED and LDED areas (Figure 1).
Interestingly, the highest urinary concentrations of BPF and BPS were found in the urban reference area, with GM values of 0.556 and 0.652 ng/mL, respectively (Table 1). BPF is used in plastics and epoxy resins, whereas BPS is primarily used in thermal receipt papers.16,17 The difference in the sources of exposures contributes to the observed difference in the concentrations of the three BPs between e-waste workers and reference populations. BPF has also been used in coatings for various applications such as lacquers, varnishes, liners, and food packaging.46 BPF and BPS have been reported to occur in foodstuffs, personal care products, and paper products.18−22 People living in urban areas are in more frequent contact with BPF- or BPS-containing products than those living in rural areas, which can lead to higher urinary BPS and BPF concentrations in urban dwellers.
Data on human exposure to BPF and BPS are scarce.15,47−49 Our data on BPF concentrations in nonoccupationally exposed individuals (GM: 0.392 ng/mL) from e-waste dismantling areas are similar to that reported for the general U.S. population in Table 2. Pearson Correlations among Urinary Concentrationsaof Three Commonly Detectable BPs (BPA, BPS, and BPF) in E- Waste Recycling, Rural, and Urban Reference Areas in China
e-waste recycling area rural reference area urban reference area
BPA BPS BPF BPA BPS BPF BPA BPS BPF
based on creatinine-unadjusted urinary concentrations
BPA 1 1 1
BPS r= 0.329 1 r= 0.071 1 r= 0.041 1
p< 0.001 p= 0.754 p= 0.864
BPF r= 0.249 r= 0.048 1 r= 0.202 r= 0.008 1 r= 0.272 r= 0.270 1
p< 0.01 p= 0.615 p= 0.603 p= 0.983 p= 0.246 p= 0.250
based on creatinine-adjusted urinary concentrations
BPA 1 1 1
BPS r= 0.316 1 r= 0.136 1 r= 0.031 1
p< 0.01 p= 0.726 p= 0.906
BPF r= 0.327 r= 0.279 1 r= 0.503 r= 0.494 1 r= 0.259 r= 0.253 1
p< 0.001 p= 0.101 p= 0.168 p= 0.176 p= 0.316 p= 0.327
aWe used log urinary concentrations for these estimations.
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2014 (0.41 ng/mL), but slightly higher than those found in nonoccupationally exposed individuals living near a BPA substitutes manufacturing plant in southern China (0.23 ng/
mL).47Urinary BPS concentrations found in e-waste workers and in rural and urban reference population (Table 1) were greater than the concentrations reported in the U.S. (0.25 to 0.30 ng/mL) and several Asian countries (0.03 to 0.17 ng/mL), but less than the concentrations reported in Japan (1.18 ng/
mL).15,48,49
Despite the fact that BPAF was detected in foodstuffs and personal care products from China,21,22 BPAF was found in only a few urine samples analyzed (detection frequencies: 7− 20%) and at low concentrations (GM: 0.0132 to 0.0338μg/L) (Table 1). Thisfinding is consistent with that reported in the U.S.15 No significant difference in urinary concentrations of BPAF was found among e-waste workers and rural/urban reference populations, which indicated that e-waste dismantling is not a source of BPAF exposure in humans. BPB, BPZ, BPP, and BPAP were detected less frequently (detection frequencies:
0−23%) with GM concentrations ranging from < LOQ to 0.07 ng/mL (Table 1). Therefore, the results for these BPs are not discussed further.
Correlations, Profiles, and Sources Analysis. Correla- tions among the urinary concentrations of three commonly detectable BPs (i.e., BPA, BPS, and BPF) were examined using Pearson correlation analysis (Table 2). In the e-waste dismantling area, weak but significant correlations were found between BPA and BPS (based on creatinine-unadjusted levels:r
= 0.329, p < 0.001; based on creatinine-adjusted levels: r = 0.316, p< 0.01), and between BPA and BPF (r= 0.249,p<
0.01;r= 0.327,p< 0.001) concentrations, which indicated the existence of multiple sources for BPA, BPF and BPS. As described above, the differences in the sources of exposure to BPA, BPF, and BPS can explain the observed correlations. A recent study from China reported that BPF and BPS collectively accounted for 71% of Σ3BPs (Σ3BPs is the sum concentrations of BPA, BPS, and BPF) in personal care products (Figure 2). High proportion of BPS (26%) and BPF (33%) to Σ3BPs was reported in sewage sludge from China, which indicated high usage of BPF and BPS in this country.
Of the three commonly detected BPs (Figure 2), BPA was the predominant compound, accounting for 81% of theΣ3BPs in the e-waste recycling area, followed, in decreasing order, by BPS (10%) and BPF (9%). The percent contributions of BPA to the Σ3BPs in human urine samples from reference areas (44%−55%) were much less than those observed in the e-waste dismantling area. This pattern found in the e-waste site was different from that reported in the U.S. in 2014 (BPA vs BPS vs BPF = 35% vs 25% vs 40%; Figure 2), but was in line with those observed in the U.S. between 2000 and 2011 (Figure 2).15 Interestingly, the compositions of BPs in urine samples from rural (55% vs 36% vs 8%; Figure 2) and urban (44% vs 30% vs 26%; Figure 2) reference areas were similar to those found in the U.S. in 2014 (Figure 2).15 In the U.S., approximately 50−80% of the e-waste is shipped to destinations such as China.50As reported previously, the average lifespan of a new computer is approximately 2 years, and for other e- products is slightly longer (3 to 8 years).51Thus, the e-products dismantled in China in 2014 (sampling time of this study) might have been used in the U.S. approximately 5 years ago.
Further studies are needed to clarify the effects of international e-waste trade on composition profiles of urinary BPs in e-waste dismantling area.
A downward trend in urinary BPA concentrations and a slight upward trend in urinary BPS and BPF concentrations were found during 2010−2014 in the U.S.15 Wells et al. and Lakind et al. also found a decreasing trend in urinary BPA concentrations in the U.S.52,53Although the temporal trends of BPs in human urine were not reported in China, we previously measured BPA and BPS in urine samples collected from the general population in China in 2010.36,48 The ratio of GM urinary BPA to BPS concentrations in China in 2010 (BPA/
BPS ratio: 4.88) was much higher than that found in subjects living in the urban (1.46) and rural (1.51) reference areas in 2014 (as observed in this study),36,48 which indicated that alternatives of BPA are more and more used in China.
However, it is noteworthy that the profiles of urinary BPs found in e-waste recycling site could not reflect the change of BPs- related industry due to e-waste dismantling.
Associations between Bisphenols Exposure and Oxidative Stress.8-OHdG is a marker for oxidative damage to DNA and is a marker for oxidative stress. In this study, 8- OHdG was found in human urine and its concentrations ranged from 0.719 to 32.8 (GM: 8.00), from 0.0474 to 36.7 (6.84), and from 0.783 to 28.8 (7.31) ng/mL, respectively, in e- waste recycling, rural reference and urban reference areas (Table 1). Urinary 8-OHdG concentrations did not vary by the occupational status of donors (occupational vs nonoccupational exposure), place of residence (e-waste vs reference area), and the scale of e-waste operations (HDED vs LDED) (data not shown).
To explore the association between BPs concentrations and oxidative stress, we examined the relationships between urinary concentrations of BPs and 8-OHdG in e-waste dismantling and 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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reference areas, respectively. In the e-waste dismantling area, urinary 8-OHdG concentration was significantly positively correlated with urinary BPA (r= 0.413,p< 0.001) and BPS (r
= 0.386,p < 0.001) concentrations, respectively; however, no significant relationship was found between urinary 8-OHdG and BPF (r = 0.118, p = 0.208) (Figure 3) concentrations.
Interestingly, similar patterns were also observed in reference areas (Figure 3), regardless of exposure levels.
Our results are in line with those reported previously by Hong et al. and Yang et al.,14,29and suggest that exposure to BPA is positively associated with oxidative stress. Hong et al.
studied a large population of Korean adults (n = 960, mean urinary BPA level: 2.74 ng/mL), and showed a positive association (p < 0.01) between urinary BPA and 8-OHdG concentrations.14Yang et al. studied a general adults population (n = 485, GM urinary BPA level: 0.53−0.61 μg/g Cre) and found an association between urinary BPA and 8-OHdG concentrations.29In laboratory animal studies, the underlying mechanism of BPA-induced oxidative stress has been ex- plored.54−56It was suggested that BPA caused tissue injury in the liver, kidney, brain, and other organs by the formation of ROS which can lead to significant oxidative damage54−56 and revealed that low doses of BPA can generate ROS by decreasing the activities of antioxidant enzymes and increasing lipid peroxidation.55
To our knowledge, this is the first study to examine the associations between the marker of oxidative stress and urinary BPS and BPF levels in humans living in polluted sites, although few in vitro studies have discussed the possible effects of BPS and BPF on human health.23,57Michałowicz et al. examined the effects of BPA, BPF, BPS, and BPAF on human peripheral blood mononuclear cells and found that these BPs were capable of inducing oxidative stress.57 Furthermore, Rochester and
Bolden reviewed current literature on BPs, and suggested that BPS and BPF are as hormonally active as BPA.23Urinary BPS concentrations were significantly correlated with 8-OHdG in this study (Figure 3).
However, it is noteworthy that many pollutants other than BPs released from e-waste dismantling can also contribute to elevated oxidative stress. Wen et al. suggested that there was an increased cancer risk from oxidative stress as indicated by elevated 8-OHdG concentrations in the e-waste dismantling workers exposed to high levels of polychlorinated dibenzo-p- dioxins and dibenzofurans (PCDD/Fs), poly brominated diphenyl ethers (PBDEs), and polychlorinated biphenyls (PCBs).58 Further, Ni et al. found that exposures to heavy metals were associated with increased oxidative DNA damage in neonates living in e-waste site.59Therefore, coexposure to other oxidative stress promoters (e.g., PBDEs, heavy metals) from e-waste dismantling should be considered for studying associations which affect biomarkers such as 8-OHdG.
In summary, this study provides novel information on the effects of e-waste dismantling activities on human exposure to BPs. E-waste dismantling increases human exposure to BPA and BPF in residents living in the e-waste recycling areas.
Significant positive correlations between urinary concentrations of 8-OHdG and BPA/BPS, but not for BPF, in both e-waste dismantling and reference areas were found. The findings of this study suggest that BPA and BPS exposure are associated with oxidative stress.
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ASSOCIATED CONTENT*S Supporting Information
The Supporting Information is available free of charge on the ACS Publications websiteat DOI:10.1021/acs.est.6b00032.
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.
DOI:10.1021/acs.est.6b00032 Environ. Sci. Technol.XXXX, XXX, XXX−XXX G
Chemicals and reagents; Table S1, tandem MS parameters for the analysis of bisphenols; Table S2, detailed information of subjects recruited in this study;
and Figure S1, sampling locations of samples collected from e-waste dismantling and two reference areas in Guangdong Province, China (PDF)
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AUTHOR INFORMATION Corresponding Authors*Tel: 86-22-84113454; e-mail: [email protected] (T.Z.).
*Tel: +1-518-474-0015; fax: +1-518-473-2895; e-mail:
[email protected] (K.K.).
Notes
The authors declare no competingfinancial interest.
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ACKNOWLEDGMENTSThe Natural Science Foundation of China (No. 21207071 and No. 41225004) and Fundamental Research Funds for the Central Universities are acknowledged for their partial research support. A part of this study (analysis was performed at Wadsworth Center) was funded by a grant (1U38EH000464- 01) from the US CDC (Atlanta, GA) to Wadsworth Center, New York State Department of Health. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the CDC. We gratefully acknowledge the donors who contributed the urine samples for this study.
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