An updated systematic review on the maternal exposure to environmental pesticides and involved mechanisms of autism spectrum disorder (ASD) progression risk in children
-
Maryam Maleki
, Zahra Noorimotlagh, Seyyed Abbas Mirzaee
, Neemat Jaafarzadeh
, Susana Silva Martinez , Fakher Rahimand Mohammadreza Kaffashian
Abstract
Autism spectrum disorder (ASD) increased dramatically over the past 25 years because of genetic and environmental factors. This systematic review (SR) aimed to determine the association between maternal exposure during pregnancy to environmental pesticides and other associations with the risk of ASD progression in children. PubMed (MEDLINE), Scopus (Elsevier) and the Institute for Scientific Information (ISI) Web of Science were searched using appropriate keywords up to March 2021. Twenty-four studies met the inclusion/exclusion criteria and were selected. Most studies reported that ASD increases the risk of offspring after prenatal exposure to environmental pesticides in pregnant mother’s residences, against offspring of women from the same region without this exposure. The main potential mechanisms inducing ASD progressions are ROS and prostaglandin E2 synthesis, AChE inhibition, voltage-gated sodium channel disruption, and GABA inhibition. According to the included studies, the highest rates of ASD diagnosis increased relative to organophosphates, and the application of the most common pesticides near residences might enhance the prevalence of ASD.
Funding source: Ilam University of Medical Sciences
Award Identifier / Grant number: IR.MEDILAM.REC.1399.171
-
Research funding: This present work has been funded by Ilam University of Medical Sciences (IR.MEDILAM.REC.1399.171).
-
Author contributions: Maryam Maleki: Methodology, Validation, Writing – review & editing. Neemat Jaafarzadeh: Methodology, Validation, Writing – review & editing. Fakher Rahim: Conceptualization, Validation, Writing – review & editing. Mohamadreza Kaffashian: Methodology, Validation, Writing – review & editing. Susana Silva Martinez: Validation, Writing – review & editing. Zahra Noorimotlagh: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Supervision. Seyyed Abbas Mirzaee: Conceptualization, Methodology, Validation, Resources, Writing – original draft, Writing – review & editing, Project administration.
-
Competing interests: The authors declare that they have no actual or potential competing financial interests.
-
Informed consent: Not applicable.
-
Ethical approval: The local Institutional Review Board deemed the study exempt from review.
References
1. Ye, BS, Leung, AOW, Wong, MH. The association of environmental toxicants and autism spectrum disorders in children. Environ Pollut 2017;227:234–42. https://doi.org/10.1016/j.envpol.2017.04.039.Search in Google Scholar PubMed
2. Kalkbrenner, AE, Schmidt, RJ, Penlesky, AC. Environmental chemical exposures and autism spectrum disorders: a review of the epidemiological evidence. Curr Probl Pediatr Adolesc Health Care 2014;44:277–318. https://doi.org/10.1016/j.cppeds.2014.06.001.Search in Google Scholar PubMed PubMed Central
3. Cheng, J, Eskenazi, B, Widjaja, F, Cordero, JF, Hendren, RL. Improving autism perinatal risk factors: a systematic review. Med Hypotheses 2019;127:26–33. https://doi.org/10.1016/j.mehy.2019.03.012.Search in Google Scholar PubMed
4. Ongono, JS, Béranger, R, Baghdadli, A, Mortamais, M. Pesticides used in Europe and autism spectrum disorder risk: can novel exposure hypotheses be formulated beyond organophosphates, organochlorines, pyrethroids and carbamates?-A systematic review. Environ Res 2020;187:109646. https://doi.org/10.1016/j.envres.2020.109646.Search in Google Scholar PubMed
5. Colle, D, Farina, M, Ceccatelli, S, Raciti, M. Paraquat and maneb exposure alters rat neural stem cell proliferation by inducing oxidative stress: new insights on pesticide-induced neurodevelopmental toxicity. Neurotox Res 2018;34:820–33. https://doi.org/10.1007/s12640-018-9916-0.Search in Google Scholar PubMed
6. Shelton, JF, Geraghty, EM, Tancredi, DJ, Delwiche, LD, Schmidt, RJ, Ritz, B, et al.. Neurodevelopmental disorders and prenatal residential proximity to agricultural pesticides: the CHARGE study. Environ Health Perspect 2014;122:1103–9. https://doi.org/10.1289/ehp.1307044.Search in Google Scholar PubMed PubMed Central
7. Sagiv, SK, Harris, MH, Gunier, RB, Kogut, KR, Harley, KG, Deardorff, J, et al.. Prenatal organophosphate pesticide exposure and traits related to autism spectrum disorders in a population living in proximity to agriculture. Environ Health Perspect 2018;126:47012. https://doi.org/10.1289/EHP2580.Search in Google Scholar PubMed PubMed Central
8. De Felice, A, Greco, A, Calamandrei, G, Minghetti, L. Prenatal exposure to the organophosphate insecticide chlorpyrifos enhances brain oxidative stress and prostaglandin E 2 synthesis in a mouse model of idiopathic autism. J Neuroinflammation 2016;13:149. https://doi.org/10.1186/s12974-016-0617-4.Search in Google Scholar PubMed PubMed Central
9. Banks, CN, Lein, PJ. A review of experimental evidence linking neurotoxic organophosphorus compounds and inflammation. Neurotoxicology 2012;33:575–84. https://doi.org/10.1016/j.neuro.2012.02.002.Search in Google Scholar PubMed PubMed Central
10. Rauh, VA, Perera, FP, Horton, MK, Whyatt, RM, Bansal, R, Hao, X, et al.. Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proc Natl Acad Sci 2012;109:7871–6. https://doi.org/10.1073/pnas.1203396109.Search in Google Scholar PubMed PubMed Central
11. Roberts, EM, English, PB, Grether, JK, Windham, GC, Somberg, L, Wolff, C. Maternal residence near agricultural pesticide applications and autism spectrum disorders among children in the California Central Valley. Environ Health Perspect 2007;115:1482–9. https://doi.org/10.1289/ehp.10168.Search in Google Scholar PubMed PubMed Central
12. Domingues, VF, Nasuti, C, Piangerelli, M, Correia-Sá, L, Ghezzo, A, Marini, M, et al.. Pyrethroid pesticide metabolite in urine and microelements in hair of children affected by autism spectrum disorders: a preliminary investigation. Int J Environ Res Publ Health 2016;13:388. https://doi.org/10.3390/ijerph13040388.Search in Google Scholar PubMed PubMed Central
13. Perez-Fernandez, C, Morales-Navas, M, Aguilera-Sáez, LM, Abreu, AC, Guardia-Escote, L, Fernández, I, et al.. Medium and long-term effects of low doses of Chlorpyrifos during the postnatal, preweaning developmental stage on sociability, dominance, gut microbiota and plasma metabolites. Environ Res 2020;184:109341. https://doi.org/10.1016/j.envres.2020.109341.Search in Google Scholar PubMed
14. Windham, GC, Sumner, A, Li, SX, Anderson, M, Katz, E, Croen, LA, et al.. Use of birth certificates to examine maternal occupational exposures and autism spectrum disorders in offspring. Autism Res 2013;6:57–63. https://doi.org/10.1002/aur.1275.Search in Google Scholar PubMed
15. Moher, D, Shamseer, L, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, et al.. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 2015;4:1. https://doi.org/10.1186/2046-4053-4-1.Search in Google Scholar PubMed PubMed Central
16. Liberati, A, Altman, DG, Tetzlaff, J, Mulrow, C, Gøtzsche, PC, Ioannidis, JPA, et al.. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 2009;6:e1000100. https://doi.org/10.1371/journal.pmed.1000100.Search in Google Scholar PubMed PubMed Central
17. Noorimotlagh, Z, Azizi, M, Pan, H-F, Mami, S, Mirzaee, SA. Association between air pollution and Multiple Sclerosis: a systematic review. Environ Res 2021;196:110386. https://doi.org/10.1016/j.envres.2020.110386.Search in Google Scholar PubMed
18. Mirzaee, SA, Noorimotlagh, Z, Ahmadi, M, Rahim, F, Martinez, SS, Nourmohammadi, A, et al.. The possible oxidative stress and DNA damage induced in Diclofenac-exposed Non-target organisms in the aquatic environment: a systematic review. Ecol Indic [Internet] 2021;131:108172. https://doi.org/10.1016/j.ecolind.2021.108172.Search in Google Scholar
19. Noorimotlagh, Z, Mirzaee, SA, Martinez, SS, Rachoń, D, Hoseinzadeh, M, Jaafarzadeh, N. Environmental exposure to nonylphenol and cancer progression Risk–A systematic review. Environ Res 2020;184:109263. https://doi.org/10.1016/j.envres.2020.109263.Search in Google Scholar PubMed
20. Palmer, RF, Heilbrun, L, Camann, D, Yau, A, Schultz, S, Elisco, V, et al.. Organic compounds detected in deciduous teeth: a replication study from children with autism in two samples. J Environ Public Health 2015;2015:1–9. https://doi.org/10.1155/2015/862414.Search in Google Scholar PubMed PubMed Central
21. Pearson, BL, Simon, JM, McCoy, ES, Salazar, G, Fragola, G, Zylka, MJ. Identification of chemicals that mimic transcriptional changes associated with autism, brain aging and neurodegeneration. Nat Commun 2016;7:1–12. https://doi.org/10.1038/ncomms11173.Search in Google Scholar PubMed PubMed Central
22. Jusko, TA, van den Dries, MA, Pronk, A, Shaw, PA, Guxens, M, Spaan, S, et al.. Organophosphate pesticide metabolite concentrations in urine during pregnancy and offspring nonverbal IQ at age 6 years. Environ Health Perspect 2019;127:17007. https://doi.org/10.1289/EHP3024.Search in Google Scholar PubMed PubMed Central
23. von Ehrenstein, OS, Ling, C, Cui, X, Cockburn, M, Park, AS, Yu, F, et al.. Prenatal and infant exposure to ambient pesticides and autism spectrum disorder in children: population based case-control study. Bmj 2019;364:1–10. https://doi.org/10.1136/bmj.l962.Search in Google Scholar PubMed PubMed Central
24. Philippat, C, Barkoski, J, Tancredi, DJ, Elms, B, Barr, DB, Ozonoff, S, et al.. Prenatal exposure to organophosphate pesticides and risk of autism spectrum disorders and other non-typical development at 3 years in a high-risk cohort. Int J Hyg Environ Health 2018;221:548–55. https://doi.org/10.1016/j.ijheh.2018.02.004.Search in Google Scholar PubMed PubMed Central
25. Schmidt, RJ, Kogan, V, Shelton, JF, Delwiche, L, Hansen, RL, Ozonoff, S, et al.. Combined prenatal pesticide exposure and folic acid intake in relation to autism spectrum disorder. Environ Health Perspect 2017;125:97007. https://doi.org/10.1289/EHP604.Search in Google Scholar PubMed PubMed Central
26. Millenson, ME, Braun, JM, Calafat, AM, Barr, DB, Huang, Y-T, Chen, A, et al.. Urinary organophosphate insecticide metabolite concentrations during pregnancy and children’s interpersonal, communication, repetitive, and stereotypic behaviors at 8 years of age: the home study. Environ Res 2017;157:9–16. https://doi.org/10.1016/j.envres.2017.05.008.Search in Google Scholar PubMed PubMed Central
27. Hicks, SD, Wang, M, Fry, K, Doraiswamy, V, Wohlford, EM. Neurodevelopmental delay diagnosis rates are increased in a region with aerial pesticide application. Front Pediatr 2017;5:116. https://doi.org/10.3389/fped.2017.00116.Search in Google Scholar PubMed PubMed Central
28. De Felice, A, Scattoni, ML, Ricceri, L, Calamandrei, G. Prenatal exposure to a common organophosphate insecticide delays motor development in a mouse model of idiopathic autism. PLoS One 2015;10: e0121663. https://doi.org/10.1371/journal.pone.0121663.Search in Google Scholar PubMed PubMed Central
29. Braun, JM, Kalkbrenner, AE, Just, AC, Yolton, K, Calafat, AM, Sjödin, A, et al.. Gestational exposure to endocrine-disrupting chemicals and reciprocal social, repetitive, and stereotypic behaviors in 4-and 5-year-old children: the HOME study. Environ Health Perspect 2014;122:513–20. https://doi.org/10.1289/ehp.1307261.Search in Google Scholar PubMed PubMed Central
30. Keil, AP, Daniels, JL, Hertz-Picciotto, I. Autism spectrum disorder, flea and tick medication, and adjustments for exposure misclassification: the CHARGE (CHildhood Autism Risks from Genetics and Environment) case–control study. Environ Heal 2014;13:1–10. https://doi.org/10.1186/1476-069X-13-3.Search in Google Scholar PubMed PubMed Central
31. Cheslack-Postava, K, Rantakokko, PV, Hinkka-Yli-Salomäki, S, Surcel, H-M, McKeague, IW, Kiviranta, HA, et al.. Maternal serum persistent organic pollutants in the Finnish Prenatal Study of Autism: a pilot study. Neurotoxicol Teratol 2013;38:1–5. https://doi.org/10.1016/j.ntt.2013.04.001.Search in Google Scholar PubMed PubMed Central
32. Mullen, BR, Khialeeva, E, Hoffman, DB, Ghiani, CA, Carpenter, EM. Decreased reelin expression and organophosphate pesticide exposure alters mouse behaviour and brain morphology. ASN Neuro 2013;5: AN20120060. https://doi.org/10.1042/an20120060.Search in Google Scholar PubMed PubMed Central
33. D’amelio, M, Ricci, I, Sacco, R, Liu, X, D’agruma, L, Muscarella, LA, et al.. Paraoxonase gene variants are associated with autism in North America, but not in Italy: possible regional specificity in gene–environment interactions. Mol Psychiatry 2005;10:1006–16. https://doi.org/10.1038/sj.mp.4001714.Search in Google Scholar PubMed
34. Lyall, K, Croen, LA, Sjödin, A, Yoshida, CK, Zerbo, O, Kharrazi, M, et al.. Polychlorinated biphenyl and organochlorine pesticide concentrations in maternal mid-pregnancy serum samples: association with autism spectrum disorder and intellectual disability. Environ Health Perspect 2017;125:474–80. https://doi.org/10.1289/ehp277.Search in Google Scholar
35. Lan, A, Kalimian, M, Amram, B, Kofman, O. Prenatal chlorpyrifos leads to autism-like deficits in C57Bl6/J mice. Environ Heal 2017;16:43. https://doi.org/10.1186/s12940-017-0251-3.Search in Google Scholar PubMed PubMed Central
36. Patriquin, MA, DeRamus, T, Libero, LE, Laird, A, Kana, RK. Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder. Hum Brain Mapp 2016;37:3957–78. https://doi.org/10.1002/hbm.23288.Search in Google Scholar PubMed PubMed Central
37. Wigle, DT, Arbuckle, TE, Walker, M, Wade, MG, Liu, S, Krewski, D. Environmental hazards: evidence for effects on child health. J Toxicol Environ Health part B 2007;10:3–39. https://doi.org/10.1080/10937400601034563.Search in Google Scholar PubMed
38. Croonenberghs, J, Verkerk, R, Scharpe, S, Deboutte, D, Maes, M. Serotonergic disturbances in autistic disorder: L-5-hydroxytryptophan administration to autistic youngsters increases the blood concentrations of serotonin in patients but not in controls. Life Sci 2005;76:2171–83. https://doi.org/10.1016/j.lfs.2004.06.032.Search in Google Scholar PubMed
39. Sonzogni, SV, Ogara, MF, Belluscio, LM, Castillo, DS, Scassa, ME, Cánepa, ET. Is involved in the cellular senescence mechanism contributing to heterochromatin formation. Biochim Biophys Acta, Gen Subj 2014;1840:2171–83. https://doi.org/10.1016/j.bbagen.2014.03.015.Search in Google Scholar PubMed
40. Weinberg, RA. The retinoblastoma protein and cell cycle control. Cell 1995;81:323–30. https://doi.org/10.1016/0092-8674(95)90385-2.Search in Google Scholar PubMed
41. Dyson, N. The regulation of E2F by pRB-family proteins. Genes Dev 1998;12:2245–62. https://doi.org/10.1101/gad.12.15.2245.Search in Google Scholar PubMed
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/reveh-2022-0092).
© 2022 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Reviews
- A meta-analysis of the risk of salivary gland tumors associated with mobile phone use: the importance of correct exposure assessment
- An investigation into the present levels of contamination in children’s toys and jewelry in different countries: a systematic review
- Analysis of physiological markers and risk factors for the development of rhabdomyolysis in military personnel: a systematic review
- Cell proliferation assay for determination of estrogenic components in food: a systematic review
- Investigation ways of causes needle sticks injuries, risk factors affecting on health and ways to preventive
- The impact of nature-led recovery initiatives for individual and community health post disaster: a systematic literature review
- Acrylamide; a neurotoxin in popcorns: a systematic review and meta-analysis
- Havana syndrome: a scoping review of the existing literature
- Emerging trends and knowledge domain of research on urban green open spaces and wellbeing: A scientometric review
- A critical review on global CO2 emission: where do industries stand?
- Global systematic review and meta-analysis on prevalence and concentration of aflatoxins in peanuts oil and probabilistic risk assessment
- Noise exposure and the risk of cancer: a comprehensive systematic review
- An updated systematic review on the maternal exposure to environmental pesticides and involved mechanisms of autism spectrum disorder (ASD) progression risk in children
- Exploring the links between indoor air pollutants and health outcomes in South Asian countries: a systematic review
- Letter to the Editor
- The influence of Maslow’s hammer. Response to: electromagnetic hypersensitivity close to mobile phone base stations – a case study in Stockholm, Sweden
Articles in the same Issue
- Frontmatter
- Reviews
- A meta-analysis of the risk of salivary gland tumors associated with mobile phone use: the importance of correct exposure assessment
- An investigation into the present levels of contamination in children’s toys and jewelry in different countries: a systematic review
- Analysis of physiological markers and risk factors for the development of rhabdomyolysis in military personnel: a systematic review
- Cell proliferation assay for determination of estrogenic components in food: a systematic review
- Investigation ways of causes needle sticks injuries, risk factors affecting on health and ways to preventive
- The impact of nature-led recovery initiatives for individual and community health post disaster: a systematic literature review
- Acrylamide; a neurotoxin in popcorns: a systematic review and meta-analysis
- Havana syndrome: a scoping review of the existing literature
- Emerging trends and knowledge domain of research on urban green open spaces and wellbeing: A scientometric review
- A critical review on global CO2 emission: where do industries stand?
- Global systematic review and meta-analysis on prevalence and concentration of aflatoxins in peanuts oil and probabilistic risk assessment
- Noise exposure and the risk of cancer: a comprehensive systematic review
- An updated systematic review on the maternal exposure to environmental pesticides and involved mechanisms of autism spectrum disorder (ASD) progression risk in children
- Exploring the links between indoor air pollutants and health outcomes in South Asian countries: a systematic review
- Letter to the Editor
- The influence of Maslow’s hammer. Response to: electromagnetic hypersensitivity close to mobile phone base stations – a case study in Stockholm, Sweden