EXPOSURE TO TOXIC AGROCHEMICALS AND DEVELOPMENT OF CONGENITAL MALFORMATIONS: A SCOPING REVIEW

Costa, Nathalia Zorzo; Nora, Carlise Rigon Dalla; Souto, Lucia Helena Donini; Carlotto, Franciela Delazeri; Afonso, Richard dos Santos; Riquinho, Deise Lisboa

doi:10.1590/1980-265X-TCE-2020-0372

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Texto & Contexto - Enfermagem

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Sumário

Literature Review • Texto contexto - enferm. 30 • 2021 • https://doi.org/10.1590/1980-265X-TCE-2020-0372 copy

EXPOSURE TO TOXIC AGROCHEMICALS AND DEVELOPMENT OF CONGENITAL MALFORMATIONS: A SCOPING REVIEW

EXPOSICIÓN A AGROTÓXICOS Y DESARROLLO MALFORMACIONES CONGÉNITAS: REVISIÓN DE ALCANCE

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objective:

to assess whether maternal and paternal exposure to toxic agrochemicals throughout life causes congenital malformations.

Method:

a scoping review was carried out on the PUBMED, CINAHL, EBSCO, MEDLINE, LILACS, SciELO, BDENF, Web of Science and ATHENA databases between August and September 2019 and updated in December 2020. A cohort and case control study were included, which addressed the effects of parents' exposure throughout their lives to toxic agrochemicals which caused congenital malformation outcomes.

Results:

the review covered 32 studies published between 2005 and 2020. The main malformations presented are related to the reproductive system, nervous system, musculoskeletal system, transverse limb deficiencies, digestive system and other malformations such as fetal growth restrictions, cleft palate and congenital heart disease. The most investigated toxic agrochemicals in the studies were the herbicides represented by atrazine.

Conclusion:

maternal and paternal exposure to toxic agrochemicals can be associated with greater chances of children being born with congenital malformations, especially those related to the male reproductive system.

DESCRIPTORS:
Congenital, hereditary and neonatal diseases and anomalies; Toxic agrochemicals; Pesticides; Review

Country	Type of study	Description of the sample	Assessed outcome	Evidence level
France1010. Rouget F, Kadhel P, Monfort C, Viel JF, Thome JP, Cordier S, et al. Chlordecone exposure and risk of congenital anomalies: the Timoun Mother-Child Cohort Study in Guadeloupe (French West Indies). Environ Sci Pollut Res Int [Internet]. 2020 Nov [cited 2020 Jul 06];27(33):40992-8. Available from: https://doi.org/10.1007/s11356-019-06031-y https://doi.org/10.1007/s11356-019-06031...	cohort	1,068 pregnant women	Malformations of the reproductive system	IV
Brazil88. Gaspari L, Sampaio DR, Paris F, Audran F, Orsini M, Neto JB, Sulatn C. High prevalence of micropenis in 2710 male newborns from na intensive-use pesticide area of Northeastern Brazil. Int J Androl [Internet]. 2012 [cited 2020 Jul 6];35(3):253-64. Available from: https://doi.org/10.1111/j.1365-2605.2011.01241.x https://doi.org/10.1111/j.1365-2605.2011...	cohort	2710 male born	Cryptorchidism, hypospadias and micropenis	IV
France2727. Chevrier C, Limon G, Monfort C, Rouget F, Garlantézec R, Petit C, et al. Urinary biomarkers of prenatal atrazine exposure and adverse birth outcomes in the PELAGIE birth cohort. Environ Health Perspect [Internet]. 2011 [cited 2020 Jul 03];119(7):1034-41. Available from: https://doi.org/doi:10.1289/ehp.1002775 https://doi.org/doi:10.1289/ehp.1002775...	cohort	579 pregnant women	Fetal growth restriction	IV
USA1919. Addissie YA, Kruszka P, Troia A, Wong ZC, Everson JL, Kozel BA, et al. Prenatal exposure to pesticides and risk for holoprosencephaly: a case control study. Environ Health [Internet]. 2020 [cited 2020 Dec 08];19(1):65. Available from: https://doi.org/10.1186/s12940-020-00611-z https://doi.org/10.1186/s12940-020-00611...	control case	92 cases and 56 controls	Holoprosencephaly	IV
USA1111. Axelsson J, Scott K, Dillner J, Lindh CH, Zhang H, Rylander L, et al. Exposure to polychlorinated compounds and cryptorchidism; A nested case-control study. PLoS One [Internet]. 2020 Jul 23 [cited 2020 Dec 08];15(7):e0236394. Available from: https://doi.org/10.1371/journal.pone.0236394 https://doi.org/10.1371/journal.pone.023...	control case	165 cases and 165 controls	Cryptorchidism	IV
USA2424. Pettigrew SM, Bell EM, Van Zutphen AR, Rocheleau CM, Shaw GM, Romitti PA, et al. Paternal and joint parental occupational pesticide exposure and spina bifida in the National Birth Defects Prevention Study, 1997 to 2002. Birth Defects Res A Clin Mol Teratol [Internet]. 2016 [cited 2020 Jul 06];106(11):963-71. Available from: https://doi.org/10.1002/bdra.23551 https://doi.org/10.1002/bdra.23551...	control case	291 cases for 2,745 controls	Spina bifida	IV
USA1717. Winston JJ, Emch M, Meyer RE, Langlois P, Weyer P, Mosley B, et al. Hypospadias and maternal exposure to atrazine via drinking water in the National Birth Defects Prevention study. Environ Health [Internet]. 2016 [cited 2020 Jul 06];15(1):76. Available from: https://doi.org/10.1186/s12940-016-0161-9 https://doi.org/10.1186/s12940-016-0161-...	control case	343 cases of hypospadias and 1,422 male controls	Hypospadias	IV
USA2929. Agopian AJ, Cai Y, Langlois PH, Canfield MA, Lupo PJ. Maternal residential atrazine exposure and risk for choanal atresia and stenosis in offspring. J Pediatr [Internet]. 2013 [cited 2020 Jul 6];162(3):581-6. Available from: https://doi.org/10.1016/j.jpeds.2012.08.012 https://doi.org/10.1016/j.jpeds.2012.08....	control case	372 cases for 3,720 controls	Choanal atresia or stenosis	IV
USA2626. Kielb C, Lin S, Herdt-Losavio M, Bell E, Chapman B, Rocheleau CM, et al. Maternal periconceptional occupational exposure to pesticides and selected musculoskeletal birth defects. Int J Hyg Environ Health [Internet] 2014 [cited 2020 Jul 06];217(2-3):248-54. Available from: https://doi.org/10.1016/j.ijheh.2013.06.003 https://doi.org/10.1016/j.ijheh.2013.06....	control case	871 cases and 2,857 controls	Craniosynostosis, gastroschisis, diaphragmatic hernia and transverse limb deficiencies	IV
USA2121. Makelarski JA, Romitti PA, Rocheleau CM, Burns TL, Stewart PA, Waters MA, et al. Maternal periconceptional occupational pesticide exposure and neural tube defects. Birth Defects Res A Clin Mol Teratol [Internet]. 2014 [cited 2020 Jul 06];100(11):877-86. Available from: https://doi.org/10.1002/bdra.23293 https://doi.org/10.1002/bdra.23293...	control case	502 cases and 2950 controls	Neural tube defects	IV
USA2323. Yang W, Carmichael SL, Roberts EM, Kegley SE, Padula AM, English PB, et al. Residential agricultural pesticide exposures and risk of neural tube defects and orofacial clefts among offspring in the San Joaquin Valley of California. Am J Epidemiol [Internet]. 2014 [cited 2020 Jul 06];179(6):740-8. Available from: https://doi.org/10.1093/aje/kwt324 https://doi.org/10.1093/aje/kwt324...	control case	367 cases and 785 controls	Anencephaly, spina bifida with and without cleft palate	IV
USA3232. Shaw GM, Yang W, Roberts E, Kegley SE, Padula A, English PB, Carmichael SL. Early pregnancy agricultural pesticide exposures and risk of gastroschisis among offspring in the San Joaquin Valley of California. Birth Defects Res A Clin Mol Teratol [Internet]. 2014 [cited 2020 Jul 06];100(9):686-94. Available from: https://doi.org/10.1002/bdra.23263 https://doi.org/10.1002/bdra.23263...	control case	156 cases for 785 controls	Gastroschisis	IV
USA1515. Rocheleau CM, Romitti PA, Sanderson WT, Sun L, Lawson CC, Waters MA, et al. Maternal occupational pesticide exposure and risk of hypospadias in the National birth defects prevention study. Birth Defects Res A Clin Mol Teratol [Internet]. 2011 [cited 2020 Jul 06];91(11):927-36. Available from: https://doi.org/10.1002/bdra.22860 https://doi.org/10.1002/bdra.22860...	control case	646 cases and 1493 controls	Hypospadias	IV
USA77. Carmichael SL, Herring AH, Sjödin A, Jones R, Larry N, Ma C, et al. Hypospadias and halogenated organic pollutant levels in maternal mid-pregnancy serum samples. Chemosphere [Internet]. 2010 [cited 2020 Jul 06]; 80(6):641-6. Available from: https://doi.org/10.1016/j.chemosphere.2010.04.055 https://doi.org/10.1016/j.chemosphere.20...	control case	20 cases and 28 controls	Hypospadias	IV
USA3333. Waller SA, Paul K, Peterson SE, Hitti JE. Agricultural-related chemical exposures, season of conception, and risk of gastroschisis in Washington State. Am J Obstet Gynecol [Internet]. 2010 [cited 2020 Jul 06];202(3): p241.e1-241.e6. Available from: https://doi.org/10.1016/j.ajog.2010.01.023 https://doi.org/10.1016/j.ajog.2010.01.0...	control case	4 controls for one case, with 805 cases for 3,616 controls	Gastroschisis and abdominal wall defects	IV
Brazil2525. Oliveira NP, Moi GP, Atanaka-Santos M, Silva AMC, Pignati WA. Malformações congênitas em municípios de grande utilização de agrotóxicos em Mato Grosso, Brasil. Ciênc Saúde Coletiva [Internet]. 2014 [cited 2020 Jul 06];19(10):4123-30. Available from: https://doi.org/10.1590/1413-812320141910.08512014 https://doi.org/10.1590/1413-81232014191...	control case	219 cases for 862 controls	Congenital malformations	IV
Brazil3838. Ueker ME, Silva VM, Moi GP, Pignati WA, Mattos IE, Silva AMC. Parenteral exposure to pesticides and occurence of congenital malformations: hospital-based case-control study. BMC Pediatr [Internet]. 2016 [cited 2020 Jul 06];16(1):125. Available from: https://doi.org/10.1186/s12887-016-0667-x https://doi.org/10.1186/s12887-016-0667-...	control case	137 cases for 274 controls	<5 years with congenital malformations	IV
Brazil and India2020. Kalra S, Dewan P, Batra P, Sharma T, Tyagi V, Banerjee BD. Organochlorine pesticide exposure in mothers and neural tube defects in offsprings. Reprod Toxicol [Internet]. 2016 [cited 2020 Jul 06];66:56-60. Available from: https://doi.org/10.1016/j.reprotox.2016.09.005 https://doi.org/10.1016/j.reprotox.2016....	control case	35 cases 35 controls (mother and baby)	Congenital anomaly due to neural tube defects	IV
India1616. ShekharYadav C, Bajpai M, Kumar V, Ahmed RS, Gupta P, Banerjee BD. Polymorphism in CYP1A1, GSTMI, GSTT1 genes and organochlorine pesticides in the etiology of hypospadias. Hum Exp Toxicol [Internet] 2011 [cited 2020 Jul 06];30(10):1464-74. Available from: https://doi.org/10.1177/0960327110392402 https://doi.org/10.1177/0960327110392402...	control case	80 boys with hypospadias and 120 controls	Hypospadias	IV
India3131. Sharma E, Mustafa M, Pathak R, Ahmed RS, Vaid NB, Baneriee BD. A case control study of gene environmental interaction in fetal growth restriction with special reference to organochlorine pesticides. Eur J Obstet Gynecol Reprod Biol [Internet]. 2012 [cited 2020 Jul 06];161(2):163-9. Available from: https://doi.org/10.1016/j.ejogrb.2012.01.008 https://doi.org/10.1016/j.ejogrb.2012.01...	control case	cases of fetal growth restriction: 50; control: 50	Fetal growth restriction	IV
France1414. Morera AM, Valmalle AF, Asensio MJ, Chauvin MA, Durand P. A study of risk factors for hypospadias in the Rhône-Alpes region (France). J Pediatr Urol [Internet] 2006 [cited 2020 Jul 06];2(3):169-77. Available from: https://doi.org/10.1016/j.jpurol.2005.09.008 https://doi.org/10.1016/j.jpurol.2005.09...	control case	225 cases of hypospadias and 225 controls	Hypospadias	IV
Netherlands3636. Spinder N, Bergman JEH, Kromhout H, Vermeulen R, Corsten-Janssen N, Boezen HM, et al. Maternal occupational exposure and congenital heart defects in offspring. Scand J Work Environ Health [Internet]. 2020 [cited 2020 Dec 4];46(6):588-608. Available from: https://doi.org/10.5271/sjweh.3912 https://doi.org/10.5271/sjweh.3912...	control case	1174 cases and 5602 controls	Congenital heart diseases	IV
Netherlands3737. Spinder N, Bergman JE, Boezen HM, Vermeulen RC, Kromhout H, Walle HE. Maternal occupational exposure and oral clefts in offspring. Environ Health [Internet] 2017 [cited 2020 Jul 06]; 16:83. Available from: https://doi.org/10.1186/s12940-017-0294-5 https://doi.org/10.1186/s12940-017-0294-...	control case	387 cases were defined as non-syndromic clefts, 1,135 chromosomal and 4,352 malformed non-chromosomal controls	Cleft lip	IV
Mexico1313. Montes LPB, WaliszewskiII S, Hernández-ValeroIII M, Sanín-Aguirre L, Infanzón-Ruiz R, Jañas AG. Exposición prenatal a los plaguicidas organoclorados y criptorquidia. Ciênc Saúde Coletiva [Internet]. 2010 [cited 2020 Jul 06];15(Suppl 1):1169-74. Available from: https://doi.org/10.1590/S1413-81232010000700025 https://doi.org/10.1590/S1413-8123201000...	control case	Mother-baby binomial Newborns diagnosed with cryptorchidism (n=41). 41 controls with deciduous testicles	Cryptorchidism	IV
Mexico1818. Brender JD, Felkner M, Suarez L, Canfield MA, Henry JP. Maternal pesticide exposure and neural tube defects in Mexican Americans. Ann Epidemiol. [Internet]. 2010 [cited 2020 Jul 06];20(1):16-22. Available from: https://doi.org/10.1016/j.annepidem.2009.09.011 https://doi.org/10.1016/j.annepidem.2009...	control case	184 case women and 225 control women	Neural tube defects	IV
Ethiopia3535. Mekonnen AG, Hordofa AG, Kitila TT, Sav A. Modifiable risk factors of congenital malformations in bale zone hospitals, Southeast Ethiopia: an unmatched case-control study. BMC Pregnancy Childbirth [Internet]. 2020 [cited 2020 Dec 04];20(1):129. Available from: https://doi.org/10.1186/s12884-020-2827-0 https://doi.org/10.1186/s12884-020-2827-...	control case	136 cases and 273 control	Congenital malformations	IV
Hungary3434. Fazekas-Pongor V, Csáky-Szunyogh M, Fekete M, Mészáros A, Cseh K, Pénzes M. Congenital heart diseases and parental occupational exposure in a Hungarian case-control study in 1997 to 2002. Congenit Anom (Kyoto) [Internet]. 2021 Mar [cited 2020 Dec 04];61(2):55-62. Available from: Available from: Available from: https://doi.org/10.1111/cga.12401. https://doi.org/10.1111/cga.12401....	control case	2,263 cases and 6,789 controls	Congenital heart diseases	IV
Paraguay3030. Ojeda CL, Leite SB. Factores de riesgo prenatales y su asociación a malformaciones congénitas en un hospital universitario de referência. Pediatr (Asunción) [Internet]. 2018 [cited 2020 Jul 06];45(1):8-16. Available from: https://doi.org/10.31698/ped.45012018002 https://doi.org/10.31698/ped.45012018002...	control case	66 cases and 66 controls	Congenital malformations	IV
Greece1212. Michalakis M, Tzatzarakis MN, Kovatsi L, Alegakis KA, Tsakalof AK, Heretise I, et al. Hypospadias in offspring is associated with chronic exposure of parents to organophosphate and organochlorine pesticides. Toxicol Lett [Internet] 2014 [cited 2020 Jul 06];230(2):139-45. Available from: https://doi.org/10.1016/j.toxlet.2013.10.015 https://doi.org/10.1016/j.toxlet.2013.10...	control case	29 children with hypospadias and 49 fathers	Hypospadias	IV
Egypt2828. El-Helaly M, Abdel-Elah K, Haussein A, Shalaby H. Paternal occupational exposures and the risk of congenital malformations--a case-control study. Int J Occup Med Environ Health [Internet] 2011 [cited 2020 Jul 06];24(2):218-27. Available from: https://doi.org/10.2478/s13382-011-0019-x https://doi.org/10.2478/s13382-011-0019-...	control case	242 cases of congenital malformations and 270 controls	Congenital malformations	IV
China2222. Ren A, Qiu X, Jin L, Ma J, Zhiwen L, Zhang L, et al. Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc Natl Acad Sci USA [Internet]. 2011 [cited 2020 Jul 06];108(31):12770-5. Available from: https://doi.org/10.1073/pnas.1105209108 https://doi.org/10.1073/pnas.1105209108...	control case	80 fetuses or newborns with NTDs, while the controls were 50 healthy newborns	Neural tube defects (NTDs)
Italy99. Giordano F, Abballe A, De Felip E, di Domenico A, Ferro F, Grammatico P et al. Maternal exposures to endocrine disrupting chemicals and hypospadias in offspring. Birth Defects Res A Clin Mol Teratol [Internet] 2010 [cited 2020 Jul 6];88(4):241-50. Available from: https://doi.org/10.1002/bdra.20657 https://doi.org/10.1002/bdra.20657...	control case	80 mothers with babies with hypospadias and 80 mothers with healthy controls	Hypospadias	IV

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[1] CORRESPONDING AUTHOR
Nathalia Zorzo Costa nzorzo@gmail.com