Abstract
The present study biomonitored the placental polychlorinated biphenyl (PCB) concentrations in women from Punjab Province, Pakistan, that provides the pioneer data for occurrence and body burden of PCBs in placental tissues from South Asian women. The ∑34PCB concentrations in placental tissues were ranged from 20.2 to 115.98 ng/g lipid weight (lip. wt.), with predominance of tetra-PCB (54.67%). The levels of ∑8DL-PCBs and ∑6-indicator PCBs were ranged from 2.03 to 27.64 ng/g (lip. wt.) and 1.71 to 30.8 ng/g (lip. wt.), respectively. The WHO-TEQ2005 values for DL-PCBs were ranged from 1.18 × 10−5 to 0.067 ng/g (lip. wt.), with highest value evaluated for CB-126. The estimated daily intake (EDI) for DL-PCBs was ranged from 9.27 × 10−8 to 5.25 × 10−4 pg WHO-TEQ/kg body weight (bw), which was within the tolerable daily intake (TDI) values established by international organizations. The spatial distribution patterns of Σ34PCB concentrations from study area have shown relative higher concentrations in samples from urban and industrial cities than rural areas, and industrial and urban releases along with e-waste handling were recognized as vital PCB sources in the environment. In order to ascertain the transplacental transfer of PCBs, the fetal growth parameters were correlated with the ∑34PCB concentrations in placental tissues. The relationship between ∑34PCB concentrations in placental tissues and infant’s anthropometric measures through multiple linear regression showed a negative correlation of infant’s body weight (R2 = 0.0728), crown to heel length (R2 = 0.068), head circumference (R2 = 0.0342), chest circumference (R2 = 0.0001), and mid arm circumference (R2 = 0.0096) that noticeably highlights the inhibited fetal anthropometric development associated with maternal PCB bioaccumulation. Hence, an immediate elimination of ongoing PCB addition in the studied area has been emphasized and further investigations are suggested to appropriately manage the public and neonatal health risks in the region.
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References
Agency for Toxic Substances and Disease Registry (ASTDR) (2014) Case studies in environmental medicine, polychlorinated biphenyls (PCBs) toxicity. Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services, pp 1–90
Ali N, Eqani SAMAS, Malik RN, Neels H, Covaci A (2013) Organohalogenated contaminants (OHCs) in human serum of mothers and children from Pakistan with urban and rural residential settings. Sci Total Environ 461-462:655–662
Ali N, Mehdi T, Malik RN, Eqani SAMAS, Kamal A, Dirtu AC, Neels H, Covaci A (2014) Levels and profile of several classes of organic contaminants in matched indoor dust and serum samples from occupational settings of Pakistan. Environ Pollut 193:269–276
Al-Saleh I, Al-Doush I, Alsabbaheen A, Mohamed GED, Rabbah A (2012) Levels of DDT and its metabolites in placenta, maternal and cord blood and their potential influence on neonatal anthropometric measures. Sci Total Environ 416:62–74
Aziz F, Syed JH, Malik RN, Katsoyiannis A, Mahmood A, Li J, Zhang G, Jones KC (2014) Occurrence of polycyclic aromatic hydrocarbons in the Soan River, Pakistan: insights into distribution, composition, sources and ecological risk assessment. Ecotoxicol Environ Saf 109:77–84
Baqar M, Arslan M, Sadef Y, Mahmood A, Qadir A, Ahmad SR (2017a) Persistent organic pollutants: potential threat to ecological integrities in term of geno-toxicity and oxidative stress. Hum Ecol Risk Assess 23:1249–1271
Baqar M, Mahmood A, Sadef Y, Mahmood A, Ahmad SR, Li J, Zhang G (2017b) Occurrence, ecological risk assessment and spatio-temporal variation of polychlorinated biphenyls (PCBs) in water and sediments along River Ravi and its northern tributaries, Pakistan. Environ Sci Pollut Res 24:27913–27930. https://doi.org/10.1007/s11356-017-0182-0
Bergonzi R, Specchia C, Dinolfo M, Tomasi C, De Palma G, Frusca T, Apostoli P (2009) Distribution of persistent organochlorine pollutants in maternal and foetal tissues: data from an Italian polluted urban area. Chemosphere 76:747–754
Breivik K, Sweetman A, Pacyna JM, Jones KC (2002) Towards a global historical emission inventory for selected PCB congeners—a mass balance approach: 1. Global production and consumption. Sci Total Environ 290:181–198
Chakraborty P, Zhang G, Li J, Selvaraj S, Breivik K, Jones KC (2016) Soil concentrations, occurrence, sources and estimation of air-soil exchange of polychlorinated biphenyls in Indian cities. Sci Total Environ 562:928–934
Cheema, K., and Badshah, S. (2013) Cement industry, Alternate Fuel and Environmental Benefits. Paper presented at the International Journal of Engineering Research and Technology
Chi KH, Chang MB, Kao SJ (2007) Historical trends of PCDD/Fs and dioxin-like PCBs in sediments buried in a reservoir in Northern Taiwan. Chemosphere 68:1733–1740
Chovancová J, Čonka K, Fabišiková A, Sejáková ZS, Dömötörová M, Drobná B, Wimmerová S (2012) PCDD/PCDF, DL-PCB and PBDE serum levels of Slovak general population. Chemosphere 88:1383–1389
Covaci A, Voorspoels S (2005) Optimization of the determination of polybrominateddiphenyl ethers in human serum using solid-phase extraction and gas chromatography-electron capture negative ionization mass spectrometry. J Chromatogr B 827(2):216–223
Covaci A, Hura C, Schepens P (2001) Selected persistent organochlorine pollutants in Romania. Sci Total Environ 280:143–152
Covaci A, Jorens P, Jacquemyn Y, Schepens P (2002) Distribution of PCBs and organochlorine pesticides in umbilical cord and maternal serum. Sci Total Environ 298(1–3):45–53
Dewan P, Jain V, Gupta P, Banerjee BD (2013) Organochlorine pesticide residues in maternal blood, cord blood, placenta, and breastmilk and their relation to birth size. Chemosphere 90:1704–1710
Diamond ML, Melymuk L, Csiszar SA, Robson M (2010) Estimation of PCB stocks, emissions, and urban fate: will our policies reduce concentrations and exposure. Environ Sci Technol 44:2777–2783
Eqani SAMAS, Malik RN, Katsoyiannis A, Zhang G, Chakraborty P, Mohammad A, Jones KC (2012a) Distribution and risk assessment of organochlorine contaminants in surface water from River Chenab, Pakistan. J Environ Monit 14:1645–1654
Eqani SAMAS, Malik RN, Zhang G, Mohammad A, Chakraborty P (2012b) Polychlorinated biphenyls (PCBs) in the sediments of the River Chenab, Pakistan. Chem Ecol 28:327–339
Eqani SAMAS, Malik RN, Zhang G, Cincinelli A, Rasheed A, Qadir A, Bokhari H, Mohammad A, Jones KC, Katsoyiannis A (2013) Uptake of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) by river water fish: the case of River Chenab. Sci Total Environ 450–451:83–91
European Commission. (2001) Scientific committee on food. Opinion of the scientific committee on food on the risk assessment of dioxins and dioxin-like PCBs in food. Update based on new scientific information available since the adoption of the SCF opinion of 22nd November 2000. CS/CNTM/DIOXIN/20 final, Adopted on 30 May 2001
Farooq S, Eqani SAMAS, Malik RN, Katsoyiannis A, Zhang G, Zhang Y, Li J, Xiang L, Jones KC, Shinwari ZK (2011) Occurrence, finger printing and ecological risk assessment of polycyclic aromatic hydrocarbons (PAHs) in the Chenab River, Pakistan. J Environ Monit 13:3207–3215
Fernandez MF, Parera J, Arrebola JP, Marina LS, Vrijheid M, Llop S, Abalos M, Tardon A, Castaño A, Abad E, Olea N (2012) Levels of polychlorinated dibenzo-p-dioxins, dibenzofurans and dioxin-like polychlorinated biphenyls in placentas from the Spanish INMA birth cohort study. Sci Total Environ 441:49–56
Fiedler H, Abad E, van Bavel B, de Boer J, Bogdal C, Malisch R (2013) The need for capacity building and first results for the Stockholm Convention Global Monitoring Plan. Trends Anal Chem 46:72–84
Gasic B, MacLeod M, Klanova J, Scheringer M, Ilic P, Lammel G, Pajovic A, Breivik K, Holoubek I, Hungerbühler K (2010) Quantification of sources of PCBs to the atmosphere in urban areas: a comparison of cities in North America, Western Europe and former Yugoslavia. Environ Pollut 158:3230–3235
Gómara B, Athanasiadou M, Quintanilla-López JE, González MJ, Bergman A (2012) Polychlorinated biphenyls and their hydroxylated metabolites in placenta from Madrid mothers. Environ Sci Pollut Res 19:139–147
Govarts E, Nieuwenhuijsen M, Schoeters G, Ballester F, Bloemen K, De Boer M, Chevrier C, Eggesbø M, Guxens M, Krämer U (2012) Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): a meta-analysis within 12 European birth cohorts. Environ Health Perspect 120:162–170
Hites RA (2004) Polybrominateddiphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science & Technology 38:945–956
International Agency for Research on Cancer (IARC) (2016). IARC monographs on the evaluation of carcinogenic risks to humans; polychlorinated biphenyls and polybrominated biphenyls, Volume 107 (2016). International Agency for Research on Cancer, Lyon
Iqbal M, Breivik K, Syed JH, Malik RN, Li J, Zhang G, Jones KC (2015) Emerging issue of e-waste in Pakistan: a review of status, research needs and data gaps. Environ Pollut 207:308–318
Japanese Environmental Health Committee of the Central Environment Council (1999). Report on Tolerable Daily Intake (TDI) of Dioxins and Related Compounds (Japan). Available at: https://www.env.go.jp/en/chemi/dioxins/tdi_report.pdf (Accessed on 03-06-2017)
Jin R, Zhan J, Liu G, Zhao Y, Zheng M, Yang L, Wang M (2017) Profiles of polychlorinated biphenyls (PCBs) in cement kilns co-processing solid waste. Chemosphere 174:165–172
Kim KS, Lee SC, Kim KH, Shim WJ, Hong SH, Choi KH, Yoon JH, Kim JG (2009) Survey on organochlorine pesticides, PCDD/Fs, dioxin-like PCBs and HCB in sediments from the Han River, Korea. Chemosphere 75:580–587
Kim SK, Yoon J (2014) Chronological trends of emission, environmental level and human exposure of POPs over the last 10 years (1999–2010) in Korea: implication to science and policy. Sci Total Environ 470–471:1346–1361
Kiviranta, H. (2005). Exposure and human PCDD/F and PCB body burden in Finland. Department of Environmental Health, National Public Health Institute, Kuopio, Finland. Available at: https://core.ac.uk/download/pdf/15167498.pdf (Accessed on 21-07-2017)
Kodavanti, P.R.S., Valdez, J., Yang, J.H., Curras-Collazo, M., and Loganathan, B.G. (2017). Chapter 39—polychlorinated biphenyls, polybrominated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans A2-Gupta, Ramesh C reproductive and developmental toxicology (second edition) (pp. 711–743): Academic Press
Laroo CA, Schenk CR, Sanchez LJ, McDonald J, Smith PL (2012) Emissions of PCDD/Fs, PCBs, and PAHs from legacy on-road heavy-duty diesel engines. Chemosphere 89:1287–1294
Leino O, Kiviranta H, Karjalainen AK, Kronberg-Kippilä C, Sinkko H, Larsen EH, Virtanen S, Tuomisto JT (2013) Pollutant concentrations in placenta. Food Chem Toxicol 54:59–69
Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C, Verreault J, Vijayan MM, Gabrielsen GW (2010) Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 408:2995–3043
Li J, Zhang G, Guo L, Xu W, Li X, Lee CS, Ding A, Wang T (2007) Organochlorine pesticides in the atmosphere of Guangzhou and Hong Kong: regional sources and long-range atmospheric transport. Atmos Environ 41:3889–3903
Lopez-Espinosa MJ, Granada A, Carreno J, Salvatierra M, Olea-Serrano F, Olea N (2007) Organochlorine pesticides in placentas from southern Spain and some related factors. Placenta 28:631–638
Ma J, Qiu X, Ren A, Jin L, Zhu T (2012) Using placenta to evaluate the polychlorinated biphenyls (PCBs) and polybrominateddiphenyl ethers (PBDEs) exposure of fetus in a region with high prevalence of neural tube defects. Ecotoxicol Environ Saf 86:141–146
Mahmood A, Malik RN, Li J, Zhang G (2014a) Levels, distribution profile, and risk assessment of polychlorinated biphenyls (PCBs) in water and sediment from two tributaries of the River Chenab, Pakistan. Environ Sci Pollut Res 21:7847–7855
Mahmood A, Syed JH, Malik RN, Zheng Q, Cheng Z, Li J, Zhang G (2014b) Polychlorinated biphenyls (PCBs) in air, soil, and cereal crops along the two tributaries of River Chenab, Pakistan: concentrations, distribution, and screening level risk assessment. Sci Total Environ 481:596–604
Malik RN, Mehboob F, Ali U, Katsoyiannis A, Schuster JK, Moeckel C, Jones KC (2014) Organo-halogenated contaminants (OHCs) in the sediments from the Soan River, Pakistan: OHCs (adsorbed TOC) burial flux, status and risk assessment. Sci Total Environ 481:343–351
Mumtaz, M., Mehmood, A., Qadir, A., Mahmood, A., Malik, R.N., Sabir, A.M., Li, J., and Zhang, G. (2016). Polychlorinated biphenyl (PCBs) in rice grains and straw; risk surveillance, congener specific analysis, distribution and source apportionment from selected districts of Punjab Province, Pakistan. Science of the Total Environment, 543, Part A, 620–627
Myllynen P, Pasanen M, Pelkonen O (2005) Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26:361–371
Nanes JA, Xia Y, Dassanayake RMAPS, Jones RM, Li A, Stodgell CJ, Walker C, Szabo S, Leuthner S, Durkin MS, Moye J, Miller RK (2014) Selected persistent organic pollutants in human placental tissue from the United States. Chemosphere 106:20–27
Needham, L.L., Grandjean, P., Heinzow, B., Jørgensen, P.J., Nielsen, F., Patterson, D.G. Jr, Sjödin, A., Turner, W.E., and Weihe, P. (2011). Partition of environmental chemicals between maternal and fetal blood and tissues. Environmental Science Technology, 45, 1121–1126
Porpora MG, Lucchini R, Abballe A, Ingelido AM, Valentini S, Fuggetta E, Cardi V, Ticino A, Marra V, Fulgenzi AR (2013) Placental transfer of persistent organic pollutants: a preliminary study on mother-newborn pairs. Int J Environ Res Public Health 10:699–711
Richards G, Agranovski IE (2017) Dioxin-like PCB emissions from cement kilns during the use of alternative fuels. J Hazard Mater 323:698–709
Sagiv KS, Tolbert PE, Altshul LM, Korrick SA (2007) Organochlorine exposures during pregnancy and infant size at birth. Epidemiology 18:120–129
Suzuki G, Nakano M, Nakano S (2005) Distribution of PCDDs/PCDFs and Co-PCBs in human maternal blood, cord blood, placenta, milk, and adipose tissue: dioxins showing high toxic equivalency factor accumulate in the placenta. Biosci Biotechnol Biochem 69:1836–1847
Syed JH, Malik RN, Li J, Zhang G, Jones KC (2013) Levels, distribution and air–soil exchange fluxes of polychlorinated biphenyls (PCBs) in the environment of Punjab Province, Pakistan. Ecotoxicol Environ Saf 97:189–195
Syed JH, Malik RN, Li J, Chaemfa C, Zhang G, Jones KC (2014) Status, distribution and ecological risk of organochlorines (OCs) in the surface sediments from the Ravi River, Pakistan. Sci Total Environ 472:204–211
Tan J, Loganath A, Chong YS, Obbard JP (2009) Exposure to persistent organic pollutants in utero and related maternal characteristics on birth outcomes: a multivariate data analysis approach. Chemosphere 74:428–433
Thomas GO, Wilkinson M, Hodson S, Jones KC (2006) Organohalogen Chemicals in Human Blood from the United Kingdom. Environ Pollut 141:30–41
Toan VD, Quy NP (2015) Residues of polychlorinated biphenyls (PCBs) in sediment from CauBay River and their impacts on agricultural soil, human health risk in KieuKy Area, Vietnam. Bull Environ Contam Toxicol 95:177–182
Tsukimori K, Morokuma S, Hori T, Takahashi K, Hirata T, Otera Y, Fukushima K, Kawamoto T, Wake N (2013) Characterization of placental transfer of polychlorinated dibenzo-p-dioxins, dibenzofurans and polychlorinated biphenyls in normal pregnancy. J Obstet Gynaecol Res 39:83–90
Ullah R, Malik RN, Muhammad A, Ahad K, Tariq M, Asghar R, Qadir A (2016) Higher concentrations and ecological risks of selected persistent organic pollutants in Macrobrachium Lamarrei from the streams of Sialkot, Pakistan. J Agric Sci Technol 6:27–34
United States Environmental Protection Agency (USEPA). (2000). Exposure and human health reassessment of 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Draft final. National Center for environmental assessment, U.S. Environmental Protection Agency, Washington, DC
United Nations Environmental Programme (UNEP) (2001) Final act of the conference of plenipotentiaries on the Stockholm convention on persistent organic pollutant. United Nations Environment Program, Geneva http://www.pops.int/default.htm
Vafeiadi M, Vrijheid M, Fthenou E, Chalkiadaki G, Rantakokko P, Kiviranta H, Kyrtopoulos SA, Chatzi L, Kogevinas M (2014) Persistent organic pollutants exposure during pregnancy, maternal gestational weight gain, and birth outcomes in the mother–child cohort in Crete, Greece (RHEA study). Environ Int 64:116–123
Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walker N, Peterson RE (2006) The 2005 World Health Organization reevaluation of human and mammaliantoxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241
Van Leeuwen FX, Feeley M, Schrenk D, Larsen JC, Farland W, Younes M (2000) Dioxins: WHO’s tolerable daily intake (TDI) revisited. Chemosphere 40:1095–1101
Vizcaino E, Grimalt JO, Fernández-Somoano A, Tardon A (2014) Transport of persistent organic pollutants across the human placenta. Environ Int 65:107–115
Wang SL, Chang YC, Chao HR, Li CM, Li LA, Lin LY, Päpke O (2006) Body burdens of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls and their relations to estrogen metabolism in pregnant women. Environ Health Perspect 114:740–745
Wang SL, Lin CY, Leon Guo Y, Lin LY, Chou WL, Chang LW (2004) Infant exposure to polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs)—correlation between prenatal and postnatal exposure. Chemosphere 54:1459–1473
WHO/FAO. 2001. Joint FAO/WHO Expert Committee on Food Additives. Fifty-seventh meeting. Rome, 5–14 June, 2001
World Health Organization (WHO) (1998) Assessment of the health risk of dioxins: reevaluation of the tolerable daily intake TDI. World Health Organization, Geneva, pp 25–29
Wu K, Xu X, Liu J, Guo Y, Huo X (2011) In utero exposure to polychlorinated biphenyls and reduced neonatal physiological development from Guiyu, China. Ecotoxicol Environ Saf 74:2141–2147
Yasmeen H, Qadir A, Mumtaz M, Eqani SAMAS, Syed JH, Mahmood A, Jamil N, Nazar F, Ali H, Ahmad MS, Tanveer ZI, Ahmad MS (2017) Risk profile and health vulnerability of female workers who pick cotton by organanochlorine pesticides from southern Punjab, Pakistan. Environ Toxicol Chem 36:1193–1201
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We express our sincere gratitude to the State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, China for providing support for laboratory analysis.
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Naqvi, A., Qadir, A., Mahmood, A. et al. Quantification of polychlorinated biphenyl contamination using human placenta as biomarker from Punjab Province, Pakistan. Environ Sci Pollut Res 25, 14551–14562 (2018). https://doi.org/10.1007/s11356-018-1535-z
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DOI: https://doi.org/10.1007/s11356-018-1535-z