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Organochlorine pesticides and their metabolites in human breast milk from Shanghai, China

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Abstract

Organochlorine pesticides (OCPs) are persistent organic pollutants that could cause deleterious effects on human health. Breast milk represents a noninvasive specimen source to assess maternal and infant exposure to OCPs. This study recruited 142 pregnant mothers in 2011–2012 in Shanghai, China, and their breast milk samples were collected during lactation and analyzed for 27 OCP compounds. Detection rates were in a range of 65.5 to 100 %. In particular, metabolites of 2,2-bis(chlorophenyl)-1,1,1-trichloroethane (DDT) such as 2-chloro-1,1-bis(4-chlorophenyl)ethylene (DDMU), 2,2-bis(4-chlorophenyl)ethanol (DDOH), bis(4-chlorophenyl)ketone (DBP), and 4,4′-dichlorodiphenylmethane (DDM) were detected in most milk samples. DDTs, hexachlorobenzene (HCB), and hexachlorocyclohexane (HCH) were dominant OCPs with mean levels of 316, 49.8, and 41.5 ng/g lipid content, respectively, whereas levels of methoxychlor, ∑Drins, ∑Heptachlor, ∑Chlordane, and ∑Endosulfan were fairly low (0.87–5.6 ng/g lipid content). Milk concentrations of OCPs were weakly correlated with maternal age, body weight, and body mass indexes (BMIs). ∑OCPs in this study were much lower than those in human breast milk samples collected in 2002 and 2007. Consumption of higher amounts of fish was associated with higher milk levels of OCPs. Specific OCP patterns in breast milk samples from migrant mothers in Shanghai reflected features of OCP production, use, and exposure in their home provinces. The probabilistic exposure assessment model reveals that Shanghai infants were exposed to low levels of OCPs through breast milk consumption. However, infants as the vulnerable group might be subject to the potential additive and/or synergistic health effects from complex OCP exposure.

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References

  • Adekunte AO, Tiwari BK, O’Donnell CP (2010) Exposure assessment of dioxins and dioxin-like PCBs in pasteurised bovine milk using probabilistic modelling. Chemosphere 81:509–516

    Article  CAS  Google Scholar 

  • Al-Rahman SHA (2012) Persistent organochlorines in human breast milk from Al-Sharkia Governorate, Egypt. Int J Environ Anal Chem 92:1215–1225

  • Androutsopoulos VP, Hernandez AF, Liesivuori J, Tsatsakis AM (2013) A mechanistic overview of health associated effects of low levels of organochlorine and organophosphorous pesticides. Toxicol 307:89–94

    Article  CAS  Google Scholar 

  • Axmon A, Rignell-Hydbom A (2006) Estimations of past male and female serum concentrations of biomarkers of persistent organochlorine pollutants and their impact on fecundability estimates. Environ Res 101:387–394

    Article  CAS  Google Scholar 

  • Barber JL, Sweetman AJ, van Wijk D, Jones KC (2005) Hexachlorobenzene in the global environment: emissions, levels, distribution, trends and processes. Sci Total Environ 349:1–44

    Article  CAS  Google Scholar 

  • Barr DB, Weihe P, Davis MD, Needham LL, Grandjean P (2006) Serum polychlorinated biphenyl and organochlorine insecticide concentrations in a Faroese birth cohort. Chemosphere 62:1167–1182

    Article  CAS  Google Scholar 

  • Bennett WD, Zeman KL, Kim C (1996) Variability of fine particle deposition in healthy adults: effect of age and gender. Am J Resp Crit Care Med 153:1641–1647

    Article  CAS  Google Scholar 

  • Boada LD, Zumbado M, Henriquez-Hernandez LA, Almeida-Gonzalez M, Alvarez-Leon EE, Serra-Majem L, Luzardo OP (2012) Complex organochlorine pesticide mixtures as determinant factor for breast cancer risk: a population-based case-control study in the Canary Islands (Spain). Environ Health: A Glob Access Sci Sour 11:28

    Article  Google Scholar 

  • Carpenter DO (2013) Effects of persistent and bioactive organic pollutants on human health. Wiley Online Library http://onlinelibrary.wiley.com/book/10.1002/9781118679654

  • Chan JKY, Xing GH, Xu Y, Liang Y, Chen LX, Wu SC, Wong CKC, Leung CKM, Wong MH (2007) Body loadings and health risk assessment of polychlorinated dibenzo-p-dioxins and dibenzofurans at an intensive electronic waste recycling site in China. Environ Sci Technol 41:7668–7674

    Article  CAS  Google Scholar 

  • Chao HR, Wang SL, Lin TC, Chung XH (2006) Levels of organochlorine pesticides in human milk from central Taiwan. Chemosphere 62:1774–1785

    Article  CAS  Google Scholar 

  • Cioroiu M, Tarcau D, Mocanu R, Cucu-Man S, Nechita B, Luca M (2010) Organochlorine pesticides in colostrums in case of normal and preterm labor (IASI, Romania). Sci Total Environ 408:2639–2645

    Article  CAS  Google Scholar 

  • Cok I, Mazmanci B, Mazmanci MA, Turgut C, Henkelmann B, Schramm KW (2012) Analysis of human milk to assess exposure to PAHs, PCBs and organochlorine pesticides in the vicinity Mediterranean City Mersin, Turkey. Environ Int 40:63–69

    Article  CAS  Google Scholar 

  • Ennaceur S, Gandoura N, Driss MR (2008) Distribution of polychlorinated biphenyls and organochlorine pesticides in human breast milk from various locations in Tunisia: levels of contamination, influencing factors, and infant risk assessment. Environ Res 108:86–93

    Article  CAS  Google Scholar 

  • FAO/WHO (2009) Inventory of IPCS and other WHO pesticide evaluations and summary of toxicological evaluations performed by the Joint Meeting on Pesticide Residues (JMPR) through 2009. Available at: http://www.who.int/ipcs/publications/jmpr/pesticide_inventory_edition10.pdf

  • Faroon O, Harris MO (2002): Toxicological profile for DDT, DDE, and DDD. US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry

  • Fujii Y, Haraguchi K, Harada KH, Hitomi T, Inoue K, Itoh Y, Watanabe T, Takenaka K, Uehara S, Yang HR, Kim MY, Moon CS, Kim HS, Wang PY, Liu AP, Hung NN, Koizumi A (2011) Detection of dicofol and related pesticides in human breast milk from China, Korea and Japan. Chemosphere 82:25–31

    Article  CAS  Google Scholar 

  • Fujii Y, Ito Y, Harada KH, Hitomi T, Koizumi A, Haraguchi K (2012) Comparative survey of levels of chlorinated cyclodiene pesticides in breast milk from some cities of China, Korea and Japan. Chemosphere 89:452–457

    Article  CAS  Google Scholar 

  • GB 2763-2012 (2012) National Standard of the People’s Republic of China: national food safety standard. Maximum residue limits for pesticides in food. Available at: http://www.agrichina.org/admin/kindeditor-4.1.2/attached/file/20140107/20140107174206_4831.pdf (accessed 4/30/2014).

  • Glynn A, Lignell S, Darnerud PO, Aune M, Ankarberg EH, Bergdahl IA, Barregard L, Bensryd I (2011) Regional differences in levels of chlorinated and brominated pollutants in mother’s milk from primiparous women in Sweden. Environ Int 37:71–79

    Article  CAS  Google Scholar 

  • Guo Y, Yu HY, Zeng EY (2009) Occurrence, source diagnosis, and biological effect assessment of DDT and its metabolites in various environmental compartments of the Pearl River Delta, South China: a review. Environ Pollut 157:1753–1763

    Article  CAS  Google Scholar 

  • Haraguchi K et al (2009) Levels and regional trends of persistent organochlorines and polybrominated diphenyl ethers in Asian breast milk demonstrate POPs signatures unique to individual countries. Environ Int 35:1072–1079

    Article  CAS  Google Scholar 

  • Hassine SB, Ameur WB, Gandoura N, Driss MR (2012) Determination of chlorinated pesticides, polychlorinated biphenyls, and polybrominated diphenyl ethers in human milk from Bizerte (Tunisia) in 2010. Chemosphere 89:369–377

    Article  CAS  Google Scholar 

  • Health Canada (1996) Provisional tolerable dietary intake (PTDI). Values presently used by contaminants toxicology section. Food Directorate, Ottawa, Canada

  • Heusinkveld HJ, Westerink RHS (2012) Organochlorine insecticides lindane and dieldrin and their binary mixture disturb calcium homeostasis in dopaminergic PC12 cells. Environ Sci Technol 46:1842–1848

  • Hung H, Kallenborn R, Breivik K, Su YS, Brorstrom-Lunden E, Olafsdottir K, Thorlacius JM, Leppanen S, Bossi R, Skov H, Mano S, Patton GW, Stern G, Sverko E, Fellin P (2010) Atmospheric monitoring of organic pollutants in the Arctic under the Arctic Monitoring and Assessment Programme (AMAP): 1993-2006. Sci Total Environ 408:2854–2873

    Article  CAS  Google Scholar 

  • Jiang YF, Wang XT, Jia Y, Wang F, Wu MH, Sheng GY, Fu JM (2009) Occurrence, distribution and possible sources of organochlorine pesticides in agricultural soil of Shanghai, China. J Hazard Mater 170:989–997

    Article  CAS  Google Scholar 

  • Johnson-Restrepo B, Addink R, Wong C, Arcaro K, Kannan K (2007) Polybrominated diphenyl ethers and organochlorine pesticides in human breast milk from Massachusetts, USA. J Environ Monit 9:1205–1212

    Article  CAS  Google Scholar 

  • Kalantzi OI, Martin FL, Thomas GO, Alcock RE, Tang HR, Drury SC, Carmichael PL, Nicholson JK, Jones KC (2004) Different levels of polybrominated diphenyl ethers (PBDEs) and chlorinated compounds in breast milk from two UK regions. Environ Health Perspect 112:1085–1091

    Article  CAS  Google Scholar 

  • Kunisue T, Someya M, Kayama F, Jin Y, Tanabe S (2004) Persistent organochlorines in human breast milk collected from primiparae in Dalian and Shenyang, China. Environ Pollut 131:381–392

    Article  CAS  Google Scholar 

  • LaKind JS, Berlin CM, Sjodin A, Turner W, Wang RY, Needham LL, Paul IM, Stokes JL, Naiman DQ, Patterson DG (2009) Do human milk concentrations of persistent organic chemicals really decline during lactation? Chemical concentrations during lactation and milk/serum partitioning. Environ Health Perspect 117:1625–1631

    Article  CAS  Google Scholar 

  • Lee SA, Dai Q, Zheng W, Gao YT, Blair A, Tessari JD, Ji BT, Shu XO (2007) Association of serum concentration of organochlorine pesticides with dietary intake and other lifestyle factors among urban Chinese women. Environ Int 33:157–163

    Article  CAS  Google Scholar 

  • Lee S, Kim S, Lee HK, Lee IS, Park J, Kim HJ, Lee JJ, Choi G, Choi S, Kim S, Kim SY, Choi K, Kim S, Moon HB (2013) Contamination of polychlorinated biphenyls and organochlorine pesticides in breast milk in Korea: time-course variation, influencing factors, and exposure assessment. Chemosphere 93:1578–1585

    Article  CAS  Google Scholar 

  • Li Y, Guo C, Wang G, Yang Y, Zhu Y, Xu M, Yuan H, Zhang G, Gao S, Zhu X (2003) Dynamic study on the accumulative levels of benzene hexachloride (BHC) and dichloro-diphenyl-trichloroethane (DDT) in the mothers’ milk in Shanghai. J Environ Occup Med 20:181–185 (in Chinese)

    CAS  Google Scholar 

  • Li H, Ji CY, Zong XN, Zhang YQ (2009) Height and weight standardized growth charts for Chinese children and adolescents aged 0 to 18 years. Zhonghua Er Ke Za Zhi Chin J Pediatr 47:487–492 (in Chinese)

    Google Scholar 

  • Liu T, Chen ZL, Shen YF, Gan L, Cao L, Lv ZZ (2007) Monitoring bioaccumulation and toxic effects of hexachlorobenzene using the polyurethane foam unit method in the microbial communities of the Fuhe River, Wuhan. J Environ Sci-China 19:738–744

    Article  CAS  Google Scholar 

  • Lu D, Feng C, Lin Y, Wang D, Ip HSS, Qiu X, Wang G, She J (2014) Determination of organochlorines, polychlorinated biphenyls and polybrominated diphenyl ethers in human hair: estimation of external and internal exposure. Chemosphere 114:327–336

    Article  CAS  Google Scholar 

  • Mao HY, Liu B (2008) Synergistic microglial reactive oxygen species generation induced by pesticides lindane and dieldrin. Neuroreport 19:1317–1320

    Article  CAS  Google Scholar 

  • Mrema EJ, Rubino FM, Brambilla G, Moretto A, Tsatsakis AM, Colosio C (2013) Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicol 307:74–88

    Article  CAS  Google Scholar 

  • Nicolopoulou-Stamati P, Pitsos MA (2001) The impact of endocrine disrupters on the female reproductive system. Hum Reprod Update 7:323–330

    Article  CAS  Google Scholar 

  • Perera FP, Rauh V, Whyatt RM, Tang D, Tsai WY, Bernert JT, Tu YH, Andrews H, Barr DB, Camann DE, Diaz D, Dietrich J, Reyes A, Kinney PL (2005) A summary of recent findings on birth outcomes and developmental effects of prenatal ETS, PAH, and pesticide exposures. Neurotoxicol 26:573–587

    Article  CAS  Google Scholar 

  • Polder A, Thomsen C, Lindstrom G, Loken KB, Skaare JU (2008) Levels and temporal trends of chlorinated pesticides, polychlorinated biphenyls and brominated flame retardants in individual human breast milk samples from Northern and Southern Norway. Chemosphere 73:14–23

    Article  CAS  Google Scholar 

  • Polder A, Skaare JU, Skjerve E, Loken KB, Eggesbo M (2009) Levels of chlorinated pesticides and polychlorinated biphenyls in Norwegian breast milk (2002-2006), and factors that may predict the level of contamination. Sci Total Environ 407:4584–4590

    Article  CAS  Google Scholar 

  • Qiu XH, Zhu T, Yao B, Hu JX, Hu SW (2005) Contribution of dicofol to the current DDT pollution in China. Environ Sci Technol 39:4385–4390

    Article  CAS  Google Scholar 

  • Reed L, Büchner V, Tchounwou PB (2007) Environmental toxicology and health effects associated with hexachlorobenzene exposure. Rev Environ Health 22:213–244

    Article  CAS  Google Scholar 

  • Ribas-Fito NR, Grimalt JO, Marco E, Sala M, Mazon C, Sunyer J (2005) Breastfeeding and concentrations of HCB and p,p’-DDE at the age of 1 year. Environ Res 98:8–13

    Article  CAS  Google Scholar 

  • Schecter A, Colacino J, Haffner D, Patel K, Opel M, Papke O, Birnbaum L (2010) Perfluorinated compounds, polychlorinated biphenyls, and organochlorine pesticide contamination in composite food samples from Dallas, Texas, USA. Environ Health Perspect 118:796–802

    Article  CAS  Google Scholar 

  • Shen H, Maine KM, Andersson AM, Damgaard IN, Virtanen HE, Skakkebaek NE, Toppari J, Schramm KW (2008) Concentrations of persistent organochlorine compounds in human milk and placenta are higher in Denmark than in Finland. Hum Reprod 23:201–210

    Article  CAS  Google Scholar 

  • Sonawane BR (1995) Chemical contaminants in human milk: an overview. Environ Health Perspect 103:197–205

    Article  CAS  Google Scholar 

  • Stacey CI, Tatum T (1985) House treatment with organochlorine pesticides and their levels in human milk—Perth, Western Australia. Bull Environ Contam Toxicol 35:202–208

    Article  CAS  Google Scholar 

  • Stacey CI, Perriman WS, Whitney S (1985) Organochlorine pesticide residue levels in human milk: Western Australia, 1979–1980. Arch Environ Health 40:102–108

  • Stellman SD, Djordjevic MV, Britton JA, Muscat JE, Citron ML, Kemeny M, Busch E, Gong L (2000) Breast cancer risk in relation to adipose concentrations of organochlorine pesticides and polychlorinated biphenyls in Long Island, New York. Cancer Epidemiol Biomark 9:1241–1249

    CAS  Google Scholar 

  • Stuetz W, Prapamontol T, Erhardt JG, Classen HG (2001) Organochlorine pesticide residues in human milk of a Hmong hill tribe living in Northern Thailand. Sci Total Environ 273:53–60

    Article  CAS  Google Scholar 

  • Sun Z, Yang Z (2013) Evaluation of breast milk intake in exclusively breast-fed infants aged 0-6 months. Acta Nutrimenta Sin 35:134–141 (in Chinese)

    Google Scholar 

  • Sun SJ, Zhao JH, Koga M, Ma YX, Liu DW, Nakamura M, Liu HJ, Horiguchi H, Clark GC, Kayama F (2005) Persistent organic pollutants in human milk in women from urban and rural areas in Northern China. Environ Res 99:285–293

    Article  CAS  Google Scholar 

  • Tsydenova OV, Sudaryanto A, Kajiwara N, Kunisue T, Batoev VB, Tanabe S (2007) Organohalogen compounds in human breast milk from Republic of Buryatia, Russia. Environ Pollut 146:225–232

    Article  CAS  Google Scholar 

  • Van Oostdam J, Gilman A, Dewailly E, Usher P, Wheatley B, Kuhnlein H, Neve S, Walker J, Tracy B, Feeley M, Jerome V, Kwavnick B (1999) Human health implications of environmental contaminants in Arctic Canada: a review. Sci Total Environ 230:1–82

    Article  Google Scholar 

  • Wetterauer B, Ricking M, Otte JC, Hallare AV, Rastall A, Erdinger L, Schwarzbauer J, Braunbeck T, Hollert H (2012) Toxicity, dioxin-like activities, and endocrine effects of DDT metabolites-DDA, DDMU, DDMS, and DDCN. Environ Sci Pollut Res 19:403–415

    Article  CAS  Google Scholar 

  • WHO Expert Consultation (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363:157–164

    Article  Google Scholar 

  • Wong MH, Leung AOW, Chan JKY, Choi MPK (2005) A review on the usage of POP pesticides in China, with emphasis on DDT loadings in human milk. Chemosphere 60:740–752

    Article  CAS  Google Scholar 

  • Xia Chuanguo DZ (2001) Situations of termite harmfulness and chemical control in China. Pest Sci Adm S1:16–19 (in Chinese)

    Google Scholar 

  • Xing YN, Guo Y, Xie M, Shen RL, Zeng EY (2009) Detection of DDT and its metabolites in two estuaries of South China using a SPME-based device: first report of p,p’-DDMU in water column. Environ Pollut 157:1382–1387

    Article  CAS  Google Scholar 

  • Xu DD, Dan M, Song Y, Chai ZF, Zhuang GS (2005) Concentration characteristics of extractable organohalogens in PM2.5 and PM10 in Beijing, China. Atmos Environ 39:4119–4128

    Article  CAS  Google Scholar 

  • Yang YY, Li DL, Mu D (2008) Levels, seasonal variations and sources of organochlorine pesticides in ambient air of Guangzhou, China. Atmos Environ 42:677–687

    Article  CAS  Google Scholar 

  • Yearbooks CE (1990-2002) Editorial Committee on China Environmental Yearbooks, China Environmental Yearbooks, Beijing, China

  • Yu HY, Bao LJ, Liang Y, Zeng EY (2011) Field validation of anaerobic degradation pathways for dichlorodiphenyltrichloroethane (DDT) and 13 metabolites in marine sediment cores from China. Environ Sci Technol 45:5245–5252

    Article  CAS  Google Scholar 

  • Zala SM, Penn DJ (2004) Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664

    Article  Google Scholar 

  • Zhang LF, Dong L, Shi SX, Zhou L, Zhang T, Huang YR (2009) Organochlorine pesticides contamination in surface soils from two pesticide factories in Southeast China. Chemosphere 77:628–633

    Article  CAS  Google Scholar 

  • Zheng XY, Chen DZ, Liu XD, Zhou QF, Liu Y, Yang W, Jiang GB (2010) Spatial and seasonal variations of organochlorine compounds in air on an urban-rural transect across Tianjin, China. Chemosphere 78:92–98

    Article  CAS  Google Scholar 

  • Zhou PP, Wu YN, Yin SA, Li JG, Zhao Y, Zhang L, Chen HJ, Liu YP, Yang X, Li XW (2011) National survey of the levels of persistent organochlorine pesticides in the breast milk of mothers in China. Environ Pollut 159:524–531

    Article  CAS  Google Scholar 

  • Zhou J, Zeng XY, Zheng KW, Zhu XJ, Ma L, Xu Q, Zhang XL, Yu YX, Sheng GY, Fu JM (2012) Musks and organochlorine pesticides in breast milk from Shanghai, China: levels, temporal trends and exposure assessment. Ecotoxicol Environ Saf 84:325–333

    Article  CAS  Google Scholar 

  • Zietz BP, Hoopmann M, Funcke M, Huppmann R, Suchenwirth R, Gierden E (2008) Long-term biomonitoring of polychlorinated biphenyls and organochlorine pesticides in human milk from mothers living in Northern Germany. Int J Hyg Environ Health 211:624–638

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by the National Special Research Fund for Non-Profit Sector (Health) (No. 200902009, Health Administration of China) and Specific Research Project of Shanghai Municipality for public health. We thank the Gynaecology and Obstetrics Department of Pujiang Hospital, Shanghai for sampling breast milk and questionnaire survey as well as the mothers who collaborated with the study and donated breast milk samples. The views and opinions expressed in this article are those of the authors and do not necessarily reflect and are not subject to the official and government policy.

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Correspondence to Guoquan Wang or Zhijun Zhou.

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Dasheng Lu and Dongli Wang contributed equally to this work.

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Lu, D., Wang, D., Ni, R. et al. Organochlorine pesticides and their metabolites in human breast milk from Shanghai, China. Environ Sci Pollut Res 22, 9293–9306 (2015). https://doi.org/10.1007/s11356-015-4072-z

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