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Persistent Organic Pollutants Residues in Human Breast Milk from Bathinda and Ludhiana Districts of Punjab, India

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Abstract

In the present study, persistent organic pollutants (POPs), including six congeners of polychlorinated biphenyls (PCBs) and organochlorine pesticides, were estimated in human breast milk samples collected from two districts of Punjab (India). The mean concentrations of POP residues were recorded higher in Bathinda district (PCBs: 33.7; DDTs: 519.2; HCHs: 46.6 ng g−1 lipid wt.) than Ludhiana (PCBs: 24.2; DDTs; 415.3; HCHs; 35.5 ng g−1 lipid wt.). Levels of PCBs and DDTs were observed higher in primiparas, whereas HCHs residues were seen more in multiparas. Risk analysis to POPs exposure through breast milk reflected that the daily intake for some infants was close to or above the tolerable daily intake limit for detrimental effects, which may raise a health concern. Comparative evaluation of present data indicated that DDT and HCHs residue levels in human breast milk from Punjab, India were among the lowest values reported for developing countries. The first-order kinetic reaction at a steady-state condition used to estimate the half-life of DDT and HCH suggested that DDT levels have declined from 18,211 to 490 ng g−1 lipid wt. with a half-life (Tdec1/2) of 3.25 years over a span of 15 years. Similarly, HCH levels have decreased from 8609 to 46.6 ng g−1 in this duration with Tdec1/2 of 2.25 years. Because some infants are still at risk, continuous monitoring of POPs in human milk is needed for surveillance and interpretation of time trends and for linkage to strict enforcement of agricultural regulations.

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References

  • Agency for Toxic Substances and Disease Registry (ATSDR) (2000) Toxicological profile for Polychlorinated Biphenyls (PCBs). U.S. Department of Health and Human Services, Public Health Service, Atlanta. https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=142&tid=26. Assessed 1 Aug 2017

  • Albers JMC, Kreis IA, Liem AKD, van Zoonen P (1996) Factors that influence the level of contamination of human milk with poly-chlorinated organic compounds. Arch Environ Contam Toxicol 30:285–291. https://doi.org/10.1007/bf00215810

    Article  CAS  Google Scholar 

  • AOAC (1999) Guidelines for single-laboratory validation of analytical methods for trace level concentrations of organic chemicals. http://www.iaea.org/trc/pest-qa Assessed 3 Aug 2017

  • Aronson KJ, Miller AB, Woolcott CG, Sterns EE, McCready DR, Lickley LA, Fish EB, Hiraki GY, Holloway C, Ross T, Hanna WM, SenGupta SK, Weber JP (2000) Breast adipose tissue concentrations of polychlorinated biphenyls and other organochlorines and breast cancer risk. Cancer Epidemiol Prev Biomar 9:55–63

    CAS  Google Scholar 

  • Aulakh RS, Gill JPS, Bedi JS, Sharma JK, Joia BS, Ockerman HW (2006) Organochlorine pesticide residues in poultry feed, chicken muscle and eggs at a poultry farm in Punjab, India. J Sci Food Agric 86:741–744. https://doi.org/10.1002/jsfa.2407

    Article  CAS  Google Scholar 

  • Ayotte P, Muckle G, Jacobson JL, Jacobson SW, Dewailly E, Inuit Cohort S (2003) Assessment of pre- and postnatal exposure to polychlorinated biphenyls: lessons from the Inuit Cohort Study. Environ Health Perspect 111:1253–1258

    Article  CAS  Google Scholar 

  • Battu RS, Singh B, Kang BK (2004) Contamination of liquid milk and butter with pesticide residues in the Ludhiana district of Punjab state, India. Ecotoxicol Environ Saf 59:324–331. https://doi.org/10.1016/j.ecoenv.2003.08.017

    Article  CAS  Google Scholar 

  • Beard J, Marshall S, Jong K, Newton R, Triplett-McBride T, Humphries B, Bronks R (2000) 1,1,1-trichloro-2,2-bis (p-chlorophenyl)-ethane (DDT) and reduced bone mineral density. Arch Environ Health 55:177–180

    Article  CAS  Google Scholar 

  • Bedi JS, Gill JPS, Aulakh RS, Joia BS, Sharma JK (2004) Contamination levels of DDT and HCH residues in different goat tissues. Indian J Ani Sci 74:11–13

    Google Scholar 

  • Bedi JS, Gill JPS, Aulakh RS, Kaur P, Sharma A, Pooni PA (2013) Pesticide residues in human breast milk: risk assessment for infants from Punjab, India. Sci Total Environ 463:720–726. https://doi.org/10.1016/j.scitotenv.2013.06.066

    Article  CAS  Google Scholar 

  • Bedi JS, Gill JPS, Aulakh RS, Kaur P (2015) Pesticide residues in bovine milk in Punjab, India: spatial variation and risk assessment to human health. Arch Environ Contam Toxicol 69:230–240. https://doi.org/10.1007/s00244-015-0163-6

    Article  CAS  Google Scholar 

  • Bentzen TW, Follmann EH, Amstrup SC, York GS, Wooller MJ, Muir DCG, O’Hara TM (2008) Dietary biomagnification of organochlorine contaminants in Alaskan polar bears. Can J Zoo 86:177–191. https://doi.org/10.1139/z07-124

    Article  CAS  Google Scholar 

  • Bhushan C, Bhardwaj A, Misra SS (2013) State of pesticide regulations in India. Centre for Science and Environment, New Delhi. http://cseindia.org/content/pesticide-regulations. Assessed 3 Aug 2017

  • Burke ER, Holden AJ, Shaw IC (2003) A method to determine residue levels of persistent organochlorine pesticides in human milk from Indonesian women. Chemosphere 50:529–535. https://doi.org/10.1016/S0045-6535(02)00492-7

    Article  CAS  Google Scholar 

  • Casals-Casas C, Desvergne B (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73:135–162. https://doi.org/10.1146/annurev-physiol-012110-142200

    Article  CAS  Google Scholar 

  • Cheema HK, Kang BK, Singh B (2004) Monitoring of HCH residues in bovine milk in Punjab, India. Indian J Environ Toxicol 14:54–58

    Google Scholar 

  • CIBRC (2009) Central Insecticide Board and Registration Committee) major uses of pesticides. Registered under the Insecticides Act, 1968 Department of Agriculture and operation, Committee Ministry of Agriculture, Government of India. http://cibrc.nic.in/. Accessed 2 Aug 2017

  • Colles A, Koppen G, Hanot V, Nelen V, Dewolf MC, Noël E, Malisch R, Kotz A, Kypke K, Biot P, Vinkx C, Schoeters G (2008) Fourth WHO-coordinated survey of human milk for persistent organic pollutants (POPs): Belgian results. Chemosphere 73:907–914. https://doi.org/10.1016/j.chemosphere.2008.07.002

    Article  CAS  Google Scholar 

  • Croes K, Colles A, Koppen G, Govarts E, Bruckers L, Van de Mieroop E, Nelen V, Covaci A, Dirtu AC, Thomsen C, Haug LS, Becher G, Mampaey M, Schoeters G, Van Larebeke N, Baeyens W (2012) Persistent organic pollutants (POPs) in human milk: a biomonitoring study in rural areas of Flanders (Belgium). Chemosphere 89:988–994. https://doi.org/10.1016/j.chemosphere.2012.06.058

    Article  CAS  Google Scholar 

  • Devanathan G, Subramanian A, Someya M, Sudaryanto A, Isobe T, Takahashi S, Chakraborty P, Tanabe S (2009) Persistent organochlorines in human breast milk from major metropolitan cities in India. Environ Pollut 157:148–154. https://doi.org/10.1016/j.envpol.2008.07.011

    Article  CAS  Google Scholar 

  • Ennaceur S, Ridha D, Marcos R (2008) Genotoxicity of the organochlorine pesticides 1,1-dichloro-2,2- bis(p-chlorophenyl)ethylene (DDE) and hexachlorobenzene (HCB) in cultured human lymphocytes. Chemosphere 71:1335–1339. https://doi.org/10.1016/j.chemosphere.2007.11.040

    Article  CAS  Google Scholar 

  • FAO/WHO (2005) Joint meeting of the panel of experts on pesticide residues. www.who.int/ipcs/publications/jmpr/en/. Assessed 10 Aug 2017

  • FAO/WHO (2008) Food standards Programme, Codex alimentarius commission, Vol. 11, Pesticde residues in food. www.fao.org/input/download/report/728/al32REPe.pdf. Assessed 10 Aug 2017

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Gill JPS (2000) Studies in pesticide residues in milk and milk products and its public health significance (Ph.D. Dissertation). Punjab Agricultural University, Ludhiana, India

  • Guo YL, Lambert GH, Hsu CC, Hsu MM (2004) Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int Arch Occup Environ Health 77:153–158

    Article  CAS  Google Scholar 

  • Howsam M, Grimalt JO, Guinó E, Navarro M, Martí-Ragué J, Peinado MA, Capellá G, Moreno V, Bellvitge Colorectal Cancer Group (2004) Organochlorine exposure and colorectal cancer risk. Environ Health Perspect 112:1460–1466

    Article  CAS  Google Scholar 

  • Hoyer AP, Jørgensen T, Rank F, Grandjean P (2001) Organochlorine exposures influence on breast cancer risk and survival according to estrogen receptor status: a Danish cohort-nested case-control study. BMC Cancer 1:8. https://doi.org/10.1186/1471-2407-1-8

    Article  CAS  Google Scholar 

  • Jacobson JL, Jacobson SW (1996) Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N Engl J Med 335:783–789. https://doi.org/10.1056/NEJM199609123351104

    Article  CAS  Google Scholar 

  • Kalra RL, Singh B, Battu RS (1994) Organochlorine pesticide residues in human milk in Punjab, India. Environ Pollut 85:147–151. https://doi.org/10.1016/0269-7491(94)90080-9

    Article  CAS  Google Scholar 

  • Kumar A, Dayal P, Shukla G, Singh G, Joseph PE (2006) DDT and HCH residue load in mother’s breast milk: a survey of lactating mother’s from remote villages in Agra region. Environ Int 32:248–251. https://doi.org/10.1016/j.envint.2005.08.019

    Article  CAS  Google Scholar 

  • La Merrill M, Emond C, Kim MJ, Antignac JP, Le Bizec B, Clément K, Birnbaum LS, Barouki R (2013) Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect 121:162–169. https://doi.org/10.1289/ehp.1205485

    Article  CAS  Google Scholar 

  • Li Q, Loganath A, Chong Y, Tan J, Obbard J (2006) Persistent organic pollutants and adverse health effects in humans. J Toxicol Environ Health Part A 69:1987–2005. https://doi.org/10.1080/15287390600751447

    Article  CAS  Google Scholar 

  • Lutter C, Iyengar V, Barnes R, Chuvakova T, Kazbekova G, Sharmanov T (1998) Breast milk contamination in Kazakhstan: implications for infant feeding. Chemosphere 37:1761–1772. https://doi.org/10.1016/S0045-6535(98)00241-0

    Article  CAS  Google Scholar 

  • Luzardo OP, Ruiz-Suárez N, Almeida-González M, Henríquez-Hernández LA, Zumbado M, Boada LD (2013) Multi-residue method for the determination of 57 persistent organic pollutants in human milk and colostrum using a QuEChERS-based extraction procedure. Anal Bioanal Chem 405:9523–9536. https://doi.org/10.1007/s00216-013-7377-0

    Article  CAS  Google Scholar 

  • Minh NH, Someya M, Minh TB, Kunisue T, Iwata H, Watanabe M, Tanabe S, Viet PH, Tuyen BC (2004) Persistent organochlorine residues in human breast milk from Hanoi and Hochiminh City, Vietnam: contamination, accumulation kinetics and risk assessment for infants. Environ Pollut 129:431–441. https://doi.org/10.1016/j.envpol.2003.11.012

    Article  CAS  Google Scholar 

  • Mishra K, Sharma RC (2011) Assessment of organochlorine pesticides in human milk and risk exposure to infants from North-East India. Sci Total Environ 409:4939–4949. https://doi.org/10.1016/j.scitotenv.2011.07.038

    Article  CAS  Google Scholar 

  • Müller MHB, Polder A, Brynildsrud OB, Karimi M, Lie E, Manyilizu WB, Mdegela RH, Mokiti F, Murtadha M, Nonga HE, Skaare JU, Lyche JL (2017) Organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) in human breast milk and associated health risks to nursing infants in Northern Tanzania. Environ Res 154:425–434. https://doi.org/10.1016/j.envres.2017.01.031

    Article  CAS  Google Scholar 

  • Newsome WH, Ryan JJ (1999) Toxaphene and other chlorinated compounds in human milk from northern and southern Canada: a comparison. Chemosphere 39:519–526. https://doi.org/10.1016/S0045-6535(98)00600-6

    Article  CAS  Google Scholar 

  • Noren K, Meironyte D ( 2000) Certain organochlorine and organobromine contaminants in the Swedish human milk in the perspective of past 20-30 years. Chemosphere 40:1111–1143

    Article  CAS  Google Scholar 

  • Parks CG, Walitt BT, Pettinger M, Chen JC, de Roos AJ, Hunt J, Sarto G, Howard BV (2011) Insecticide use and risk of rheumatoid arthritis and systemic lupus erythematosus in the Women’s Health Initiative Observational Study. Arthritis Care Res 63:184–194. https://doi.org/10.1002/acr.20335

    Article  Google Scholar 

  • Polder A, Skaare JU, Skjerve E, Løken KB, Eggesbø 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. https://doi.org/10.1016/j.scitotenv.2009.04.032

    Article  CAS  Google Scholar 

  • Quintana PJ, Delfino RJ, Korrick S, Ziogas A, Kutz FW, Jones EL, Laden F, Garshick E (2004) Adipose tissue levels of organochlorine pesticides and polychlorinated biphenyls and risk of non-Hodgkin’s lymphoma. Environ Health Perspect 112:854–861

    Article  CAS  Google Scholar 

  • Ribas-Fitó N, Torrent M, Carrizo D, Muñoz-Ortiz L, Júlvez J, Grimalt JO, Sunyer J (2006) In utero exposure to background concentrations of DDT and cognitive functioning among preschoolers. Am J Epidemiol 164:955–962. https://doi.org/10.1093/aje/kwj299

    Article  Google Scholar 

  • Sharma KK (2007) Pesticide residue analytical manual. Directorate of Information and Publication of Agriculture, New Delhi

    Google Scholar 

  • Singh KP, Malik A, Mohan D, Takroo R (2005) Distribution of persistent organochlorine pesticide residues in Gomti River, India. Bull Environ Contam Toxicol 74:146–154. https://doi.org/10.1007/s00128-004-0561-3

    Article  CAS  Google Scholar 

  • Solomon GM, Weiss PM (2002) Chemical contaminants in breast milk: time trends and regional variability. Environ Health Perspect 110:339–347

    Article  Google Scholar 

  • Someya M, Ohtake M, Kunisue T, Subramanian A, Takahashi S, Chakraborty P, Ramachandran R, Tanabe S (2010) Persistent organic pollutants in breast milk of mothers residing around an open dumping site in Kolkata, India: specific dioxin-like PCB levels and fish as a potential source. Environ Int 36:27–35. https://doi.org/10.1016/j.envint.2009.09.003

    Article  CAS  Google Scholar 

  • Subramanian A, Ohtake M, Kunisue T, Tanabe S (2007) High levels of organochlorines in mothers’ milk from Chennai (Madras) city, India. Chemosphere 68:928–939. https://doi.org/10.1016/j.chemosphere.2007.01.041

    Article  CAS  Google Scholar 

  • Sudaryanto A, Kunisue T, Tanabe S, Niida M, Hashim H (2005) Persistent organochlorine compounds in human breast milk from mothers living in Penang and Kedah, Malaysia. Arch Environ Contam Toxicol 49:429–437. https://doi.org/10.1007/s00244-004-0208-8

    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. https://doi.org/10.1016/S0048-9697(99)00036-4

    Article  Google Scholar 

  • Vreugdenhil HJI, Slijper FME, Mulder PGH, Weisglas-Kuperus N (2002) Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age. Environ Health Perspect 110:593–598

    Article  Google Scholar 

  • Walkowiak J, Wiener JA, Fastabend A, Heinzow B, Krämer U, Schmidt E, Steingrüber HJ, Wundram S, Winneke G (2001) Environmental exposure to polychlorinated biphenyls and quality of the home environment: effects on psychodevelopment in early childhood. Lancet 358:1602–1607. https://doi.org/10.1016/S0140-6736(01)06654-5

    Article  CAS  Google Scholar 

  • WHO (2007) Biomonitoring of breast milk for persistent organic pollutants. http://www.who.int/foodsafety/chem/pops/en. Accessed 11 Aug 2017

  • Yadav I, Devi N, Syed J, Cheng Z, Li J, Zhang G, Jones KC (2015) Current status of persistent organic pesticides residues in air, water, and soil, and their possible effect on neighboring countries: a comprehensive review of India. Sci Total Environ 511:123–137. https://doi.org/10.1016/j.scitotenv.2014.12.041

    Article  CAS  Google Scholar 

  • Zhang G, Chakraborty P, Li J, Sampathkumar P, Balasubramanian T, Kathiresan K, Takahashi S, Subramanian A, Tanabe S, Jones KC (2008) Passive atmospheric sampling of organochlorine pesticides, polychlorinated biphenyls, and polybrominated diphenyl ethers in Urban, Rural, and Wetland Sites along the Coastal Length of India. Environ Sci Technol 42:8218–8223. https://doi.org/10.1021/es8016667

    Article  CAS  Google Scholar 

  • Zhao G, Xu Y, Han G, Ling B (2006) Biotransfer of persistent organic pollutants from a large site in China used for the disassembly of electronic and electrical waste. Environ Geochem Health 28:341–351. https://doi.org/10.1007/s10653-005-9003-3

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the volunteers who took part in the study. We also thank the doctors and hospital staff for their cooperation and help provided during interaction with the sample donors and collection of samples. We express gratitude towards University Grants Commission, New Delhi, India (Grant Number UGC No. 42-635 (2013) SR Sr. no. 5) for funding this research work.

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Bawa, P., Bedi, J.S., Gill, J.P.S. et al. Persistent Organic Pollutants Residues in Human Breast Milk from Bathinda and Ludhiana Districts of Punjab, India. Arch Environ Contam Toxicol 75, 512–520 (2018). https://doi.org/10.1007/s00244-018-0512-3

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