Article pubs.acs.org/est
Concentrations and Profiles of Urinary Polycyclic Aromatic Hydrocarbon Metabolites (OH-PAHs) in Several Asian Countries Ying Guo,† Kurunthachalam Senthilkumar,‡ Husam Alomirah,§ Hyo-Bang Moon,∥ Tu Binh Minh,⊥ Mustafa Ali Mohd,# Haruhiko Nakata,¶ and Kurunthachalam Kannan*,†,$ †
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, Empire State Plaza, P.O. Box 509, Albany, New York 12201-0509, United States ‡ Department of Natural Sciences, Savannah State University, Savannah, Georgia 31404, United States § Biotechnology Department, Kuwait Institute for Scientific Research, P.O. Box 24885, 13109 Safat, Kuwait ∥ Department of Marine Science and Convergence Technology, College of Science and Technology, Hanyang University, Ansan 426-791, South Korea ⊥ UNIDO BAT/BEP Project Office, Pollution Control Department, Vietnam Environment Administration, Ba Dinh, Hanoi, Vietnam # Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia ¶ Graduate School of Science and Technology, Kumamoto University, 2-39-1 Kurokami, Kumamoto 860-8555, Japan $ International Joint Research Center for Persistent Toxic Substances, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China S Supporting Information *
ABSTRACT: Concentrations of 12 hydroxylated polycyclic aromatic hydrocarbons (OH-PAHs) were determined in 306 urine samples collected from seven Asian countries (China, India, Japan, Korea, Kuwait, Malaysia, and Vietnam) by highperformance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). The total concentrations of OH-PAHs found in the seven Asian countries were in the following increasing order: Malaysia (median: 2260 pg/mL) < Japan (4030 pg/ mL) < China (5770 pg/mL) < India (6750 pg/mL) < Vietnam (8560 pg/mL) < Korea (9340 pg/mL) < Kuwait (10 170 pg/mL). The measured urinary concentrations of 1-hydroxypyrene (1-PYR) in samples from Malaysia, Korea, and Japan (∼ 100 pg/mL) were similar to those reported for North America and Western Europe. The concentrations of 1-PYR in urine samples from China, India, and Vietnam were 4−10 times higher than those reported for other countries, thus far. Among the 12 OH-PAH compounds analyzed, hydroxynaphthalene (NAP: sum of 1-hydroxynaphthalene and 2-hydroxynaphthalene) was the dominant compound (accounting for 60−90% of total OH-PAHs), followed by hydroxyphenanthrene (PHEN: sum of 2-hydroxyphenanthrene, 3-hydroxyphenanthrene, 4-hydroxyphenanthrene, and 9-hydroxyphenanthrene [3−16%]), 2-hydroxyfluorene (3−20%), and 1-PYR (2−8%). The total daily intakes (DIs) of PAHs were estimated based on the urinary concentrations of their metabolites. The DIs of naphthalene were found to be higher for populations in Korea, Kuwait, and Vietnam (> 10 μg/day) than those of the other countries studied (∼ 5 μg/day). The DIs of phenanthrene and pyrene (> 10 μg/day) in the populations of China, India, and Vietnam were higher than those estimated for the populations in the other countries studied (∼ 5 μg/day).
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INTRODUCTION
Human exposure to PAHs can occur through inhalation of air or cigarette smoke, ingestion of food, and dermal absorption of soil or dust particles. The half-life of PAHs in the human body is on the order of a few hours, e.g., the half-life of 1hydroxypyrene (1-PYR), a metabolite of pyrene, is 6−35 h.3 The low molecular weight OH-PAHs, which consist of 2−3 benzene rings, are excreted mainly into urine as conjugated
Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants in the environment. PAHs are carcinogenic, and their exposures have been associated with cancers in humans. Exposure to PAHs has been shown to disrupt seminal DNA and affect male fertility.1 Data from the 2001−2004 National Health and Nutrition Examination Survey (NHANES) of the Centers for Disease Control and Prevention (CDC) in the U.S. indicated that several hydroxy-PAHs (OHPAHs) were significantly associated with self-reported cardiovascular diseases in humans.2 © 2013 American Chemical Society
Received: Revised: Accepted: Published: 2932
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species,4 while the high molecular weight PAHs (≥4 benzene rings) are excreted primarily in the feces. Thus, urinary levels of OH-PAHs, particularly 1-PYR,5,6 have been used as biomarkers of human exposure to PAHs. The CDC has been determining the levels of OH-PAHs in urine samples collected from a representative U.S. population.4,7,8 Biomonitoring studies that involve measurements of OH-PAHs in urine from populations have been conducted in Korea9 and Germany.10,11 A few studies also have reported the exposure of children to PAHs, using 1-PYR as a biomarker of exposure.12−15 The results from biomonitoring studies have shown associations between urinary OH-PAH concentrations and poor semen quality,16 altered thyroid hormone homeostasis,17 and development of cancers18 in humans. Despite the ubiquitous occurrence of and exposure of people to PAHs, very few studies have reported urinary OH-PAH concentrations in populations in Asian countries. A few studies have reported OH-PAH concentrations in urine from China,1,13,17,19−21 Japan,22,23 and Korea.9,24−26 Most of these studies analyzed a single OH-PAH biomarker, 1-PYR, in urine. The exposure patterns of PAHs can vary depending on environmental, dietary, and demographic features. It is important to measure the profiles of a wide range of OHPAHs if we are to assess cumulative exposures and the risks from exposure to PAHs. For instance, 2-hydroxyfluorene (2FLUO) was reported to be negatively associated with thyroid hormone levels,17 and 2-hydroxynaphthalene (2-NAP) was reported to be associated with smoking history.27 Thus, simultaneous measurement of several OH-PAHs is crucial for the assessment of exposure doses, sources of exposures, and association of exposures to health outcomes or health risks. In the present study, we measured 12 OH-PAHs in 306 urine samples collected from the general population of seven Asian countries: China (n = 84), India (n = 38), Japan (n = 34), Korea (n = 60), Kuwait (n = 38), Malaysia (n = 29), and Vietnam (n = 23), with the aims of investigating geographic distribution of concentrations and profiles of urinary OH-PAHs and daily exposure doses to PAHs, which are important for establishing the baseline levels needed for determining future trends in exposures.
as described earlier.28 The urine samples were thawed at room temperature and diluted with 2 mL of Milli-Q water and then extracted with 5 mL of organic solvent twice (80% pentane/ 20% toluene, v:v) by shaking in a reciprocating orbital shaker for 30 min. The combined extracts were washed with 1 mL of AgNO3 solution (1 M), concentrated to near dryness, and dissolved into 0.4 mL of methanol for instrumental analysis. All of the sample preparation steps were performed in a dark room to avoid possible photodegradation of target analytes. A total of 12 OH-PAHs, 1-hydroxynaphthalene (1-NAP), 2-NAP, 2FLUO, 2-hydroxyphenanthrene (2-PHEN), 3-hydroxyphenanthrene (3-PHEN), 4-hydroxyphenanthrene (4-PHEN), 9hydroxyphenanthrene (9-PHEN), 1-PYR, 1-hydroxychrysene (1-CHRY), 6-hydroxychrysene (6-CHRY), 3-hydroxybenzo[c]phenanthrene (3-BCP), and 1-hydroxybenz[a]anthacene (1BAA), were analyzed in this study. Seven isotopically labeled OH-PAHs were used as internal standards: d7-1-NAP, d7-2NAP, 13C6-1-PYR, 13C6-3-PHEN, 13C6-3-BCP, 13C6-1-BAA, and 13 C6-6-CHRY. The standards (purity ≥98%) were purchased from MRI (Kansas City, MO), CDN Isotopes (Pointe-Claire, Quebec, Canada), and Cambridge Isotope Laboratories, Inc. (Andover, MA). 13C6-6-CHRY and 13C6-3-PHEN were used for the quantification of the two metabolites of chrysene and four metabolites of phenanthrene and 2-FLUO. An ABSciex 5500 triple quadrupole mass spectrometer (ESIMS-MS; Applied Biosystems, Foster City, CA), equipped with an Agilent 1100 Series HPLC system (Agilent Technologies, Inc., Santa Clara, CA), was used for analysis. Chromatographic separation was achieved using an Agilent Eclipse Plus C18 column (100 mm × 4.6 mm, 3.5 μm). The mobile phases were methanol (A) and methanol−water solution (2:3, v:v) (B) pumped at a flow rate of 350 μL/min. The mobile phase gradient maintained was as follows: 0.0−2.0 min, 95% B; 5.0− 15 min, 45% B; 16.0−19.0 min, 20% B; 25.0−32.0 min, 95% B. Target compounds were determined by multiple-reaction monitoring (MRM) in the negative ionization mode. The limit of quantification (LOQ) was 40 pg/mL for 1-NAP and 2NAP and 10 pg/mL for all other target compounds. Details of sample preparation and instrumental analysis are presented in the SI. Quality Assurance and Quality Control (QA/QC). For each batch of 30 samples analyzed, a method blank, a spiked blank, and a pair of matrix-spiked sample/duplicate were processed. The results of the QA/QC analyses are shown in SI Table S2. On the basis of the isotope-diluted method, the corrected recoveries of target analytes spiked into sample matrices and passed through the entire analytical procedure were between 85% and 137%. Procedural blanks contained, on average in pg/mL, ∼20 NAP, ∼10 PHEN, and ∼70 1-PYR. The reported concentrations in samples were subtracted from blank values for NAP, PHEN, and PYR. In this study, the sum concentrations of all 12 target analytes, sum of 1-NAP and 2NAP, sum of 1-CHRY and 6-CHRY, and sum of 2-PHEN, 3PHEN, 4-PHEN, and 9-PHEN are denoted as Σ12OH-PAHs, NAP, CHRY, and PHEN, respectively. Samples were categorized into three groups on the basis of age as 40 yrs. The reported concentrations were not creatinine adjusted, although results for urinary creatinine levels are available. As reported in our previous studies,29 the creatinine concentrations in urine from Asian countries were all within the normal range of values, and creatinine adjustment did not alter the conclusions. Our primary goal was to establish the baseline levels on the occurrence and profiles of OH-PAHs
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MATERIAL AND METHODS Sample Collection. Urine samples (1−10 mL) were collected from the general populations in seven Asian countries. Samples from China (number of samples for females/males: 40/44), India (21/17), Japan (7/27), Kuwait (15/23), Malaysia (19/10), and Vietnam (13/10) were collected from May to July 2010 and in May 2012. Urine samples from Korea (n = 60, ages not known) were collected during 2006−2007 (Table S1, Supporting Information (SI)). The samples from China, India, Japan, Korea, Kuwait, Malaysia, and Vietnam originated from the cities of Guangzhou/Shanghai/Harbin, Mettupalayam/ Chennai, Ehime/Kumamoto, Seoul/Busan/Yeosu, Al-Asma/ Al-Jahra governorates, Kuala Lumpur, and Hanoi, respectively (Figure S1). The average age of donors for the seven countries ranged from 30 to 51 years. Spot urine samples were collected in 50-mL polypropylene tubes from healthy volunteers with no occupational exposures. Institutional Review Board approvals were obtained from the New York State Department of Health (NYSDOH) for the analysis of urine samples. Sample Preparation and Analysis. Concentrations of OH-PAHs in urine (0.5−2.0 mL) were determined after enzymatic deconjugation, followed by liquid−liquid extraction, 2933
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except for China and Korea. The concentrations of Σ12OHPAHs increased with age for both males and females from China and were higher in males than in females from Korea (p < 0.05). It should be noted, however, that this interpretation is tempered by the small sample size available for each country. Geographical Distribution of OH-PAH Profiles. Among the 12 metabolites analyzed, 1-NAP, 2-NAP, 2-FLUO, 2PHEN, 3-PHEN, 9-PHEN, and 1-PYR were frequently detected in urine samples (detection rate: >95%). 4-PHEN was found in 79% of samples, but other target compounds were seldom detected (3−14%). These results were similar to the U.S. NHAHES findings, which indicated that the major OHPAHs found in human urine were metabolites of naphthalene, fluorene, phenanthrene, and pyrene, while other target compounds were below the limit of detection (LOD).4 In each of the Asian countries studied, concentrations of NAP were the highest (median values ranged between 2050 and 9180 pg/mL), followed, in decreasing order, by PHEN (138−1040 pg/mL), 2-FLUO (112−893 pg/mL), and 1-PYR (65−463 pg/mL) (Figure 2). NAP accounted for 60% of the
in urine from the general populations in Asian countries because such information was not available prior to this study. Data were analyzed using SPSS, Version 17.0. Comparisons among samples were conducted using ANOVA or nonparametric statistical tests (Kruskal−Wallis H or Mann− Whitney U). Statistical significance was set at p < 0.05.
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RESULTS AND DISCUSSION OH-PAHs. The concentrations of Σ12OH-PAHs (sum of 12 OH-PAHs) in urine samples ranged from 136 to 236 000 pg/ mL (n = 306) in the seven Asian countries studied, with an overall median value of 5920 pg/mL (Figure 1). Concen-
Figure 1. Concentrations of Σ12OH-PAHs (concentrations of sum of 12 hydroxy PAHs) in urine samples collected from seven Asian countries (ng/mL). The horizontal lines represent the 10th, 50th, and 90th percentiles, and the boxes represent the 25th and 75th percentiles. Outliers are shown as individual points.
trations of Σ12OH-PAHs varied significantly among the seven Asian countries (p < 0.05). The lowest concentrations of Σ12OH-PAHs were found in urine samples from Malaysia (median: 2260 pg/mL), and the highest concentrations were found in samples from Kuwait (10 170 pg/mL). No significant differences in urinary Σ12OH-PAH concentrations were found among samples from China (5770 pg/mL), India (6750 pg/ mL), Vietnam (8560 pg/mL), and Korea (9340 pg/mL) (p > 0.05). A study indicated that the concentrations of PAHs in the atmosphere of Asian countries during 2001 to 2009 were, in decreasing order, China and India > Korea > Malaysia and Vietnam > Japan. 30 The geographic pattern of PAH concentrations in the atmosphere of several Asian countries is consistent with the concentrations of OH-PAHs measured in urine from these countries. The concentrations of Σ12OHPAHs in urine from Malaysia and Japan were comparable to those reported for Germany (mean: 3220 pg/mL).31 The measured concentrations of Σ12OH-PAHs in urine from China and India were similar to those reported for the U.S. population in 2001−2002 (geometric mean: 5610).4 The concentrations of Σ12OH-PAHs determined in urine in our study were 1−2 orders of magnitude lower than those reported for occupationally exposed populations, such as coke oven workers in Poland (median: 155 000 pg/mL),32 and smokers in Germany (mean: 15 000 pg/mL).31 In general, no significant difference in Σ 12OH-PAH concentrations was found for samples from various age groups or between females and males from any individual country,
Figure 2. Distribution of profiles of individual OH-PAHs in urine samples from seven Asian countries (ng/mL). The bars represent the mean values and the error bars represent standard deviation.
total Σ12OH-PAH concentrations in China and India to 90% in Korea. 2-FLUO and PHEN accounted for 3% of the total Σ12OH-PAH concentrations in Korea to 20% in China. 1-PYR accounted for 2% (Korea) to 8% (Japan) of the total Σ12OHPAH concentrations. Other target compounds accounted for 10 μg/day) than those estimated for the other countries (∼ 5 μg/day). The total DIs of naphthalene, pyrene, fluorene, and phenanthrene ranged from 8.7 μg/day (Malaysia) to 39.5 μg/day (India). The total DIs of PAHs estimated for Malaysia, Japan, and Korea (∼ 10 μg/day) in our study were similar to those estimated from dietary exposure studies in Western Europe (1.6−8.42 μg/day).38 It should be noted that several uncertainties exist in our exposure calculations, although the crude estimates derived from this study can help in understanding potential risks from exposures and can guide the design of future exposure and risk assessment studies. The Reference Doses (RfDs) of the U.S. EPA derived from chronic oral exposure for naphthalene, fluorene and pyrene were 20, 40 and 30 μg/kg-day, respectively.39,40 However, as shown in Figure 4, even the total daily intakes of PAHs were generally less than 50 μg/day (60%−90% of samples for each
from China, India, and Vietnam were 4−10 times higher than those reported for other countries thus far (Figure 3). The top three rapidly growing economies in Asia, China, India, and Vietnam, occupied the three highest urinary concentrations for 1-PYR, which suggests that pyrene exposure can be associated with rapid urban and industrial development. Concentrations of CHRY, 3-BCP, and 1-BAA in urine from Asian countries were generally below the LOD. As noted, PAHs with high molecular weight are excreted primarily in the feces,4 and, therefore, urine may not be the suitable matrix for the assessment of exposure to high molecular weight PAHs. Human Exposure to PAHs. A recent study reported that 6.8% of pyrene, 60% of fluorene, and 11% of phenanthrene exposed through diet were excreted via urine within 24 h of exposure.37 The major sources of human exposure to PAHs are still not clear. Inhalation may be a dominant source of exposure for some low molecular weight PAHs, such as naphthalene. The data from urinary biomonitoring studies can be used in the assessment of total daily exposure to certain environmental chemicals, including PAHs. For the estimation of human exposure to PAHs, we assumed that 100% of the daily dose of PAHs was through diet. The daily intakes (DIs) of naphthalene, pyrene, fluorene, and phenanthrene by the populations in Asian countries were estimated by the following equation: DI = CV ×
naphthalene
M1 1 × M2 f
where DI is the total daily intake of PAHs (μg/day), C is the urinary OH-PAH concentration (μg/L), V is the human daily excretion volume of urine (L/day) (assumed a volume of 2.0 L), M1 and M2 are the respective molecular weights of parent PAH and its metabolite (g/mol), and f is the ratio of OH-PAH
Figure 4. Frequency distribution of daily intakes (DIs, μg/day) of PAHs in seven Asian countries, estimated from urinary concentrations of hydroxy PAHs. 2936
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country), with a maximum value of ~ 300 μg/day. The results indicate that the estimated exposure doses for all PAHs compounds from our study were far below their RfDs of the U.S. EPA. In summary, this study establishes baseline concentrations of several OH-PAHs in urine from seven Asian countries. This study also shows that the occurrence and profiles of OH-PAHs in Asian countries vary, and this is the first study to document elevated levels of OH-PAHs in urine from several Asian countries. Our results indicate that people in China, India, and Vietnam are exposed to great concentrations of PAHs. Studies have shown that the concentrations of OH-PAHs in urine are influenced by people’s lifestyle,41 environmental factors,13 and sampling time.3,42 Therefore, the results, determined from the small sample size available from each country, should be interpreted with caution. Further studies are needed to describe the sources, pathways, and health effects from exposure to PAHs in Asian populations.
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(5) Bouchard, M.; Viau, C. Urinary 1-hydroxypyrene as a biomarker of exposure to polycyclic aromatic hydrocarbons: Biological monitoring strategies and methodology for determining biological exposure indices for various work environments. Biomarkers 1999, 4, 159−187. (6) Hemat, H.; Wittsiepe, J.; Wilhelm, M.; Miller, J.; Goen, T. High levels of 1-hydroxypyrene and hydroxyphenanthrenes in urine of children and adults from Afghanistan. J. Exposure Sci. Environ. Epidemiol. 2012, 22, 46−51. (7) Grainger, J.; Huang, W.; Patterson, D. G., Jr; Turner, W. E.; Pirkle, J.; Caudill, S. P.; Wang, R. Y.; Needham, L. L.; Sampson, E. J. Reference range levels of polycyclic aromatic hydrocarbons in the US population by measurement of urinary monohydroxy metabolites. Environ. Res. 2006, 100, 394−423. (8) U.S. CDC. Fourth National Report on Human Exposure to Environmental Chemicals. Http://www.cdc.gov/exposurePort/pdf/ FourthReport_UpdatedTable_Sep2012.pdf (accessed 2012, December). (9) Sul, D.; Ahn, R.; Im, H.; Oh, E.; Kim, J. H.; Kim, J. G.; Kim, P.; Kim, H. A.; Park, W. Y.; Son, B. S.; Shin, D.; Shim, A. S.; Yang, W.; Yu, S. D.; Lee, K. H.; Lee, K. J.; Lee, S. D.; Lee, J. W.; Lee, C. K.; Jang, B. K.; Choi, K.; Han, D. H.; Hwang, M. Y.; Lee, J. H. Korea National Survey for Environmental Pollutants in the human body 2008: 1hydroxypyrene, 2-naphthol, and cotinine in urine of the Korean population. Environ. Res. 2012, 118, 25−30. (10) Becker, K.; Schulz, C.; Kaus, S.; Seiwert, M.; Seifert, B. German Environmental Survey 1998 (GerES III): Environmental pollutants in the urine of the German population. Int. J. Hyg. Environ. Health 2003, 206, 15−24. (11) Wilhelm, M.; Hardt, J.; Schulz, C.; Angerer, J. New reference value and the background exposure for the PAH metabolites 1hydroxypyrene and 1- and 2-naphthol in urine of the general population in Germany: Basis for validation of human biomonitoring data in environmental medicine. Int. J. Hyg. Environ. Health 2008, 211, 447−453. (12) Kuo, C. T.; Chen, H. W.; Chen, J. L. Determination of 1hydroxypyrene in children urine using column-switching liquid chromatography and fluorescence detection. J. Chromatogr., B 2004, 805, 187−193. (13) Fan, R.; Wang, D.; Mao, C.; Ou, S.; Lian, Z.; Huang, S.; Lin, Q.; Ding, R.; She, J. Preliminary study of children’s exposure to PAHs and its association with 8-hydroxy-2′-deoxyguanosine in Guangzhou, China. Environ. Int. 2012, 42, 53−58. (14) Mucha, A. P.; Hryhorczuk, D.; Serdyuk, A.; Nakonechny, J.; Zvinchuk, A.; Erdal, S.; Caudill, M.; Scheff, P.; Lukyanova, E.; Shrkiryak-Nyzhnyk, Z.; Chislovska, N. Urinary 1-hydroxypyrene as a biomarker of PAH exposure in 3-year-old Ukrainian children. Environ. Health Perspect. 2006, 114, 603−609. (15) Hansen, A. M.; Raaschou-Nielsen, O.; Knudsen, L. E. Urinary 1hydroxypyrene in children living in city and rural residences in Denmark. Sci. Total Environ. 2006, 363, 70−77. (16) Xia, Y.; Zhu, P.; Han, Y.; Lu, C.; Wang, S.; Gu, A.; Fu, G.; Zhao, R.; Song, L.; Wang, X. Urinary metabolites of polycyclic aromatic hydrocarbons in relation to idiopathic male infertility. Hum. Reprod. 2009, 24, 1067−1074. (17) Zhu, P.; Bian, Z.; Xia, Y.; Han, Y.; Qiao, S.; Zhao, R.; Jin, N.; Wang, S.; Peng, Y.; Wang, X. Relationship between urinary metabolites of polycyclic aromatic hydrocarbons and thyroid hormone levels in Chinese non-occupational exposure adult males. Chemosphere 2009, 77, 883−888. (18) Mumford, J. L.; Li, X.; Hu, F.; Lu, X. B.; Chuang, J. C. Human exposure and dosimetry of polycyclic aromatic hydrocarbons in urine from Xuan Wei, China with high lung cancer mortality associated with exposure to unvented coal smoke. Carcinogenesis 1995, 16, 3031− 3036. (19) Huang, W.; Smith, T. J.; Ngo, L.; Wang, T.; Chen, H.; Wu, F.; Herrick, R. F.; Christiani, D. C.; Ding, H. Characterizing and biological monitoring of polycyclic aromatic hydrocarbons in exposures to diesel exhaust. Environ. Sci. Technol. 2007, 41, 2711−2716.
ASSOCIATED CONTENT
S Supporting Information *
Method of sample preparation and instrumental analysis, additional tables containing detailed information about samples, QA/QC results, figures of sampling sites, and contributions of individual compounds to total PAHs. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*Phone: 1-518-474-0015; fax: 1-518-473-2895; e-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank all the donors for kindly providing the samples. We thank Madam Suad Al-Hooti (Biotechnology Department, KISR) for providing the Kuwaiti urine samples, Dr. Nguyen Hung Minh (VEA) and Dr. Vu Duc Loi (VAST) for collection of samples in Hanoi, and Mr. V. Prabhu for samples from Chennai, India. This research (analytical method development) was supported by a biomonitoring grant (1U38EH000464-04) from the Centers for Disease Control and Prevention (CDC), Atlanta, GA.
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REFERENCES
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Environmental Science & Technology
Article
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