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In utero exposure to organochlorine pesticide residues and their potential impact on birth outcomes and fetal gender

Environmental Science and Pollution Research volume 27, pages 33703–33711 (2020)Cite this article

Abstract

Being the largest agriculture country in the Arab world, Egypt was one of the major consumer of organochlorine pesticides (OCPs) in this area, continued to have a heavy burden of OCPs in the environment. There is growing concern that OCPs could pass from the maternal circulation through the placenta to the fetal circulation and pose several health risks to their fetuses. The current study was intended to identify OCPs residue exposure in healthy pregnant women and to justify the potential impacts of these residues on their fetuses. In this study, the prevalence of 18 OCPs was estimated in 81 maternal and cord blood samples, using Agilent 7890, gas chromatograph equipped with micro-electron capture detector (GC-μECD). Our data signposted that the heptachlor epoxide has the highest detection rate among all residues in both maternal (32%) and cord blood serum (27.16%). DDTs were still quantifiable, but with the lowest quantifiable percentage. More than 85% of mothers' serum with detectable residues transfer OCPs residue to their fetuses in a statistically significant manner (x = 42.9, p value < 0.001). The present findings showed no significant growth retardation, or preterm delivery induced by in utero exposure to the most abundant residues. There is growing evidence that exposure to OCPs residue has profound impact on sex ratio. Methoxychlor, in this study be deemed as testosterone triggers which yields high boys ratio (x = 4.37, p < 0.05). In conclusion, Egypt continued to have a heavy burden of OCPs residues, and fetuses and infants are especially the most vulnerable groups to their adverse health effects. Exposure to OCPs may disrupt the maternal hormones, which regulate the offspring gender, but these results need to be validated in larger sample sizes.

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References

  • Abou-Arab AAK, Soliman KM, Naguib KH (1998) Pesticide residue contents in Egyptian vegetables and fruits and removal by washing. Bull Natl. Nutr. Inst. Arab   Rep. Egypt 18:117–138

  • 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

    CAS  Article  Google Scholar 

  • Apgar V, Holaday DA, James LS, Weisbrot IM, Berrien C (1958) Evaluation of the newborn infant-second report. J Am Med Assoc 168(15):1985–1988

    CAS  Article  Google Scholar 

  • ATSDR (Agency for Toxic Substances and Disease Registry) (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

  • Barakat AO, Khairy M, Aukaily I (2013) Persistent organochlorine pesticide and PCB residues in surface sediments of Lake Qarun, a protected area of Egypt. Chemosphere 90(9):2467–2476

    CAS  Article  Google Scholar 

  • Chao HR, Wang SL, Lin LY, Lee WJ, Päpke O (2007) Placental transfer of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in Taiwanese mothers in relation to menstrual cycle characteristics. Food Chem Toxicol 45(2):259–265

    CAS  Article  Google Scholar 

  • 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(5):1704–1710

    CAS  Article  Google Scholar 

  • El Nemr A, El-Said GF, Khaled A (2016) Risk assessment of Organochlorines in mollusk from the Mediterranean and Red Sea coasts of Egypt. Water Environ Res 88(4):325–337

    Article  Google Scholar 

  • Eldakroory SA, El Morsi DA, Abdel-Rahman RH, Roshdy S, Gouida MS, Khashaba EO (2017) Correlation between toxic organochlorine pesticides and breast cancer. Hum Exp Toxicol 36(12):1326–1334

    CAS  Article  Google Scholar 

  • Evseenko D, Paxton JW, Keelan JA (2006) Active transport across the human placenta: impact on drug efficacy and toxicity. Expert Opin Drug Metab Toxicol 2(1):51–69

    CAS  Article  Google Scholar 

  • Farhang L, Weintraub JM, Petreas M, Eskenazi B, Bhatia R (2005) Association of DDT and DDE with birth weight and length of gestation in the child health and development studies, 1959–1967. Am J Epidemiol 162(8):717–725

    Article  Google Scholar 

  • Frías MM, Torres MJ, Frenich AG, Martínez Vidal JL, Olea-Serrano F, Olea N (2004) Determination of organochlorine compounds in human biological samples by GC-MS/MS. Biomed Chromatogr 18(2):102–111

    Article  Google Scholar 

  • Ghazy HA, Abdel-Razek MA, El Nahas AF, Mahmoud S (2017) Assessment of complex water pollution with heavy metals and Pyrethroid pesticides on transcript levels of metallothionein and immune related genes. Fish Shellfish Immunol 68:318–326

    CAS  Article  Google Scholar 

  • Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences 96 (9):5001-5006

  • Grant VJ (2007) Could maternal testosterone levels govern mammalian sex ratio deviations? J Theor Biol 246(4):708–719

    CAS  Article  Google Scholar 

  • Guo H, Jin Y, Cheng Y, Leaderer B, Lin S, Holford TR, Qiu J, Zhang Y, Shi K, Zhu Y, Niu J, Bassig BA, Xu S, Zhang B, Li Y, Hu X, Chen Q, Zheng T (2014) Prenatal exposure to organochlorine pesticides and infant birth weight in China. Chemosphere 110:1–7

    CAS  Article  Google Scholar 

  • Jaga K, Dharmani C (2003) Global surveillance of DDT and DDE levels in human tissues. Int J Occup Med Environ Health 16(1):7–20

    Google Scholar 

  • James WH (2006) Possible constraints on adaptive variation in sex ratio at birth in humans and other primates. J Theor Biol 238(2):383–394

    Article  Google Scholar 

  • Khairy MAEH, Kolb M, Mostafa AR, Anwar EF, Bahadir M (2012) Risk posed by chlorinated organic compounds in Abu Qir Bay, East Alexandria, Egypt. Environ Sci Pollut Res 19(3):794–811

    Article  Google Scholar 

  • Lancz K, Murínová Ľ, Patayová H, Drobná B, Wimmerová S, Šovčíková E, Trnovec T (2015) Ratio of cord to maternal serum PCB concentrations in relation to their congener-specific physicochemical properties. Int J Hyg Environ Health 218(1):91–98

    CAS  Article  Google Scholar 

  • Longnecker MP, Klebanoff MA, Zhou H, Brock JW (2001) Association between maternal serum concentration of the DDT metabolite DDE and preterm and small-for-gestational-age babies at birth. Lancet 358(9276):110–114

    CAS  Article  Google Scholar 

  • Lopez-Espinosa MJ, Murcia M, Iñiguez C, Vizcaino E, Llop S, Vioque J, Ballester F (2011) Prenatal exposure to organochlorine compounds and birth size. Pediatrics 128(1):e127–e134

    Article  Google Scholar 

  • Luo D, Pu Y, Tian H, Cheng J, Zhou T, Tao Y, Yuan J, Sun X, Mei S (2016) Concentrations of organochlorine pesticides in umbilical cord blood and related lifestyle and dietary intake factors among pregnant women of the Huaihe River basin in China. Environ Int 92:276–283

    Article  Google Scholar 

  • Mansour SA (2008) Environmental impact of pesticides in Egypt. In: Reviews of Environmental Contamination and Toxicology Vol 196. Springer, New York, pp 1–51

    Google Scholar 

  • Mori C, Nakamura N, Todaka E, Fujisaki T, Matsuno Y, Nakaoka H, Hanazato M (2014) Correlation between human maternal–fetal placental transfer and molecular weight of PCB and dioxin congeners/isomers. Chemosphere 114:262–267

    CAS  Article  Google Scholar 

  • Myllynen P, Vähäkangas K (2013) Placental transfer and metabolism: an overview of the experimental models utilizing human placental tissue. Toxicol in Vitro 27(1):507–512

    CAS  Article  Google Scholar 

  • Myllynen P, Pasanen M, Pelkonen O (2005) Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26(5):361–371

    CAS  Article  Google Scholar 

  • Patayová H, Wimmerová S, Lancz K, Palkovičová Ľ, Drobná B, Fabišiková A, Trnovec T (2013) Anthropometric, socioeconomic, and maternal health determinants of placental transfer of organochlorine compounds. Environ Sci Pollut Res 20(12):8557–8566

    Article  Google Scholar 

  • Pereg D, Dewailly É, Poirier GG, Ayotte P (2002) Environmental exposure to polychlorinated biphenyls and placental CYP1A1 activity in Inuit women from northern Quebec. Environ Health Perspect 110(6):607–612

    CAS  Article  Google Scholar 

  • Rogan WJ, Gladen BC, McKinney JD, Carreras N, Hardy P, Thullen J, Tully M (1986) Neonatal effects of transplacental exposure to PCBs and DDE. J Pediatr 109(2):335–341

    CAS  Article  Google Scholar 

  • Rylander L, Nilsson-Ehle P, Hagmar L (2006) A simplified precise method for adjusting serum levels of persistent organohalogen pollutants to total serum lipids. Chemosphere 62(3):333–336

    CAS  Article  Google Scholar 

  • Sharaf NE, Elserougy SM, Hussein AS, Abou-Arab AA, Ahmed SB (2008) Organochlorine pesticides in breast milk and other tissues of some Egyptian mothers. Am Eurasian J Agric Environ Sci 4(4):434–442

    Google Scholar 

  • Sharaf NE, Amer NM, Ibrahim KS, El-Tahlawy EM, Abdelgelil KS (2013) Pesticides usage in agriculture among rural women in Egypt: association between serum organo-chlorine pesticide residues and occurrence of diabetes. World J. Med. Sci 9(1):08–15

  • Shonkoff JP, Garner AS (2012) The lifelong effects of early childhood adversity and toxic stress. Pediatr 129(1): e232–e246.

  • Siddiqui M, Srivastava S, Mehrotra P, Mathur N, Tandon I (2003) Persistent chlorinated pesticides and intra-uterine foetal growth retardation: a possible association. Int Arch Occup Environ Health 76(1):75–80

    CAS  Article  Google Scholar 

  • 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(3):428–433

    CAS  Article  Google Scholar 

  • Tyagi V, Garg N, Mustafa MD, Banerjee BD, Guleria K (2015) Organochlorine pesticide levels in maternal blood and placental tissue with reference to preterm birth: a recent trend in north Indian population. Environ Monit Assess 187(7):471

    Article  Google Scholar 

  • Umeda K, Kotake Y, Miyara M, Ishida K, Sanoh S, Ohta S (2016) Methoxychlor and fenvalerate induce neuronal death by reducing GluR2 expression. J Toxicol Sci 41(2):255–264

    CAS  Article  Google Scholar 

  • UNEP. Stockholm Convention on Persistent Organic Pollutants.2001 <http://chm.pops.int>

  • Vizcaino E, Grimalt JO, Fernández-Somoano A, Tardon A (2014) Transport of persistent organic pollutants across the human placenta. Environ Int 65:107–115

    CAS  Article  Google Scholar 

  • Wolff MS, Engel S, Berkowitz G, Teitelbaum S, Siskind J, Barr DB, Wetmur J (2007) Prenatal pesticide and PCB exposures and birth outcomes. Pediatr Res 61(2):243–250

    CAS  Article  Google Scholar 

  • World Health Organization (1995) Physical status: The use and interpretation of anthropometry. Technical Report Series no. 854: Geneva

  • World Health Organization (2006) WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development

  • Zhang X, Wu X, Lei B, Jing Y, Jiang ZA, Zhang X, Yu Y (2018) Transplacental transfer characteristics of organochlorine pesticides in paired maternal and cord sera, and placentas and possible influencing factors. Environ Pollut 233:446–454

    CAS  Article  Google Scholar 

Download references

Funding

The authors thank the National Research Centre (NRC), Giza, Egypt for supporting this study within the project “Immunological Profile in Cord Blood and Growth Assessment of the Newborn about Maternal Exposure to Environmental Contaminant” Project No. 11010140.

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Affiliations

  1. Department of Child Health, National Research Centre, Giza, Egypt

    Enas R. Abdel Hamid

  2. Department of Environmental and Occupational Medicine, National Research Centre, Giza, Egypt

    Nevin E. Sharaf

  3. Hormones Department, National Research Centre, Giza, Egypt

    Hanaa H. Ahmed

  4. Al-Galaa Teaching Hospital, Cairo, Egypt

    Amira Ahmed

  5. Pesticide Chemistry Department, Chemical Industries Research Division, National Research Centre (NRC), 33 El Bohouth Street (former El Tahrir St.), Giza, P.O. 12622,, Egypt

    Abdel-Tawab H. Mossa

Authors
  1. Enas R. Abdel Hamid
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  2. Nevin E. Sharaf
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  3. Hanaa H. Ahmed
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  4. Amira Ahmed
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  5. Abdel-Tawab H. Mossa
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Correspondence to Abdel-Tawab H. Mossa.

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Abdel Hamid, E.R., Sharaf, N.E., Ahmed, H.H. et al. In utero exposure to organochlorine pesticide residues and their potential impact on birth outcomes and fetal gender. Environ Sci Pollut Res 27, 33703–33711 (2020). https://doi.org/10.1007/s11356-020-09411-x

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  • DOI: https://doi.org/10.1007/s11356-020-09411-x

Keywords

  • In utero exposure
  • Organochlorine pesticide residues
  • Birth outcomes
  • Methoxychlor
  • Gender of fetuses