Skip to main content

Advertisement

Log in

Pesticides as endocrine disruptors: programming for obesity and diabetes

  • Mini Review
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

Exposure to pesticides has been associated with obesity and diabetes in humans and experimental models mainly due to endocrine disruptor effects. First contact with environmental pesticides occurs during critical phases of life, such as gestation and lactation, which can lead to damage in central and peripheral tissues and subsequently programming disorders early and later in life.

Methods

We reviewed epidemiological and experimental studies that associated pesticide exposure during gestation and lactation with programming obesity and diabetes in progeny.

Results

Maternal exposure to organochlorine, organophosphate and neonicotinoids, which represent important pesticide groups, is related to reproductive and behavioral dysfunctions in offspring; however, few studies have focused on glucose metabolism and obesity as outcomes.

Conclusion

We provide an update regarding the use and metabolic impact of early pesticide exposure. Considering their bioaccumulation in soil, water, and food and through the food chain, pesticides should be considered a great risk factor for several diseases. Thus, it is urgent to reformulate regulatory actions to reduce the impact of pesticides on the health of future generations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. P.D. Gluckman, M.A. Hanson, Developmental plasticity and human disease: research directions. J Intern Med 261(5), 461–471 (2007). https://doi.org/10.1111/j.1365-2796.2007.01802.x

    Article  CAS  PubMed  Google Scholar 

  2. T. Bianco-Miotto, J.M. Craig, Y.P. Gasser, S.J. van Dijk, S.E. Ozanne, Epigenetics and DOHaD: from basics to birth and beyond. J Dev Orig Health Dis 8(5), 513–519 (2017). https://doi.org/10.1017/S2040174417000733

    Article  CAS  PubMed  Google Scholar 

  3. D.J. Barker, J.G. Eriksson, T. Forsen, C. Osmond, Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31(6), 1235–1239 (2002). https://doi.org/10.1093/ije/31.6.1235

    Article  CAS  PubMed  Google Scholar 

  4. J.J. Heindel, The developmental basis of disease: Update on environmental exposures and animal models. Basic Clin Pharm Toxicol 125(Suppl 3), 5–13 (2019). https://doi.org/10.1111/bcpt.13118

    Article  CAS  Google Scholar 

  5. J.J. Heindel, J. Balbus, L. Birnbaum, M.N. Brune-Drisse, P. Grandjean, K. Gray, P.J. Landrigan, P.D. Sly, W. Suk, D. Cory Slechta, C. Thompson, M. Hanson, Developmental origins of health and disease: integrating environmental influences. Endocrinology 156(10), 3416–3421 (2015). https://doi.org/10.1210/EN.2015-1394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. P.F. Baillie-Hamilton, Chemical toxins: a hypothesis to explain the global obesity epidemic. J Alter Complement Med 8(2), 185–192 (2002). https://doi.org/10.1089/107555302317371479

    Article  Google Scholar 

  7. J.J. Heindel, B. Blumberg, M. Cave, R. Machtinger, A. Mantovani, M.A. Mendez, A. Nadal, P. Palanza, G. Panzica, R. Sargis, L.N. Vandenberg, F. Vom Saal, Metabolism disrupting chemicals and metabolic disorders. Reprod Toxicol 68, 3–33 (2017). https://doi.org/10.1016/j.reprotox.2016.10.001

    Article  CAS  PubMed  Google Scholar 

  8. B.S. Silva, I.M. Bertasso, C.B. Pietrobon, B.P. Lopes, T.R. Santos, N. Peixoto-Silva, J.C. Carvalho, S. Claudio-Neto, A.C. Manhaes, S.S. Cabral, G.E.G. Kluck, G.C. Atella, E. Oliveira, E.G. Moura, P.C. Lisboa, Effects of maternal bisphenol A on behavior, sex steroid and thyroid hormones levels in the adult rat offspring. Life Sci 218, 253–264 (2019). https://doi.org/10.1016/j.lfs.2018.12.039

    Article  CAS  PubMed  Google Scholar 

  9. J.F.P. de Araujo, P.L. Podratz, G.C. Sena, E. Merlo, L.C. Freitas-Lima, J.G.M. Ayub, A.F.Z. Pereira, A.P. Santos-Silva, L. Miranda-Alves, I.V. Silva, J.B. Graceli, The obesogen tributyltin induces abnormal ovarian adipogenesis in adult female rats. Toxicol Lett 295, 99–114 (2018). https://doi.org/10.1016/j.toxlet.2018.06.1068

    Article  CAS  PubMed  Google Scholar 

  10. S. Ghosh, L. Murinova, T. Trnovec, C.A. Loffredo, K. Washington, P.S. Mitra, S.K. Dutta, Biomarkers linking PCB exposure and obesity. Curr Pharm Biotechnol 15(11), 1058–1068 (2014). https://doi.org/10.2174/1389201015666141122203509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. M. Czajka, M. Matysiak-Kucharek, B. Jodlowska-Jedrych, K. Sawicki, B. Fal, B. Drop, M. Kruszewski, L. Kapka-Skrzypczak, Organophosphorus pesticides can influence the development of obesity and type 2 diabetes with concomitant metabolic changes. Environ Res 178, 108685 (2019). https://doi.org/10.1016/j.envres.2019.108685

    Article  CAS  PubMed  Google Scholar 

  12. B. Weiss, S. Amler, R.W. Amler, Pesticides. Pediatrics 113(4 Suppl), 1030–1036 (2004)

    Article  PubMed  Google Scholar 

  13. K.P. Dubois, Insecticides, rodenticides, herbicides; household hazards. Postgrad Med 24(3), 278–288 (1958). https://doi.org/10.1080/00325481.1958.11692212

    Article  CAS  PubMed  Google Scholar 

  14. W. Mnif, A.I. Hassine, A. Bouaziz, A. Bartegi, O. Thomas, B. Roig, Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health 8(6), 2265–2303 (2011). https://doi.org/10.3390/ijerph8062265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. International Agency for Research on Cancer (IARC), World Health Organization (WHO). IARCMonographs evaluate DDT, lindane, and 2,4-D. Press release 236. 2015. https://monographs.iarc.who.int/wpcontent/uploads/2018/07/QA_ENG.pdf

  16. D.A. John, G.R. Babu, Lessons from the aftermaths of green revolution on food system and health. Front Sustain Food Syst 5, 644559 (2021). https://doi.org/10.3389/fsufs.2021.644559

    Article  PubMed  PubMed Central  Google Scholar 

  17. Carson, R.: Silent spring. Pub. Houghton Mifflin, USA (1962).

  18. A.F. Hernandez, T. Parron, R. Alarcon, Pesticides and asthma. Curr Opin Allergy Clin Immunol 11(2), 90–96 (2011). https://doi.org/10.1097/ACI.0b013e3283445939

    Article  CAS  PubMed  Google Scholar 

  19. A. Ascherio, M.A. Schwarzschild, The epidemiology of Parkinson’s disease: risk factors and prevention. Lancet Neurol 15(12), 1257–1272 (2016). https://doi.org/10.1016/S1474-4422(16)30230-7

    Article  PubMed  Google Scholar 

  20. Miani, A., Imbriani, G., De Filippis, G., De Giorgi, D., Peccarisi, L., Colangelo, M., Pulimeno, M., Castellone, M.D., Nicolardi, G., Logroscino, G., Piscitelli, P.: Autism spectrum disorder and prenatal or early life exposure to pesticides: a short review. Int J Environ Res Public Health 18(20) (2021). https://doi.org/10.3390/ijerph182010991

  21. D. Montes-Grajales, J. Olivero-Verbel, Structure-based identification of endocrine disrupting pesticides targeting breast cancer proteins. Toxicology 439, 152459 (2020). https://doi.org/10.1016/j.tox.2020.152459

    Article  CAS  PubMed  Google Scholar 

  22. C. Yang, A.P.S. Kong, Z. Cai, A.C.K. Chung, Persistent organic pollutants as risk factors for obesity and diabetes. Curr DiabRep 17(12), 132 (2017). https://doi.org/10.1007/s11892-017-0966-0

    Article  CAS  Google Scholar 

  23. M.E. Miller, M. Hamann, F.J. Kroon, Bioaccumulation and biomagnification of microplastics in marine organisms: A review and meta-analysis of current data. PLoS One 15(10), e0240792 (2020). https://doi.org/10.1371/journal.pone.0240792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. M. Collotta, P.A. Bertazzi, V. Bollati, Epigenetics and pesticides. Toxicology 307, 35–41 (2013). https://doi.org/10.1016/j.tox.2013.01.017

    Article  CAS  PubMed  Google Scholar 

  25. S. Mostafalou, M. Abdollahi, Pesticides and human chronic diseases: evidences, mechanisms, and perspectives. Toxicol Appl Pharm 268(2), 157–177 (2013). https://doi.org/10.1016/j.taap.2013.01.025

    Article  CAS  Google Scholar 

  26. E. Evangelou, G. Ntritsos, M. Chondrogiorgi, F.K. Kavvoura, A.F. Hernandez, E.E. Ntzani, I. Tzoulaki, Exposure to pesticides and diabetes: A systematic review and meta-analysis. Environ Int 91, 60–68 (2016). https://doi.org/10.1016/j.envint.2016.02.013

    Article  CAS  PubMed  Google Scholar 

  27. L.E. Gray Jr., J. Ostby, Effects of pesticides and toxic substances on behavioral and morphological reproductive development: endocrine versus nonendocrine mechanisms. Toxicol Ind Health 14(1-2), 159–184 (1998). https://doi.org/10.1177/074823379801400111

    Article  CAS  PubMed  Google Scholar 

  28. L.G. Rosas, B. Eskenazi, Pesticides and child neurodevelopment. Curr Opin Pediatr 20(2), 191–197 (2008). https://doi.org/10.1097/MOP.0b013e3282f60a7d

    Article  PubMed  Google Scholar 

  29. J.J. Heindel, History of the obesogen field: looking back to look forward. Front Endocrinol 10, 14 (2019). https://doi.org/10.3389/fendo.2019.00014

    Article  Google Scholar 

  30. P.D. Darbre, Endocrine disruptors and obesity. Curr Obes Rep 6(1), 18–27 (2017). https://doi.org/10.1007/s13679-017-0240-4

    Article  PubMed  PubMed Central  Google Scholar 

  31. M. Anand, A. Taneja, Organochlorine pesticides residue in placenta and their influence on anthropometric measures of infants. Environ Res 182, 109106 (2020). https://doi.org/10.1016/j.envres.2019.109106

    Article  CAS  PubMed  Google Scholar 

  32. Y. Jeong, S. Lee, S. Kim, J. Park, H.J. Kim, G. Choi, S. Choi, S. Kim, S.Y. Kim, S. Kim, K. Choi, H.B. Moon, Placental transfer of persistent organic pollutants and feasibility using the placenta as a non-invasive biomonitoring matrix. Sci Total Environ 612, 1498–1505 (2018). https://doi.org/10.1016/j.scitotenv.2017.07.054

    Article  CAS  PubMed  Google Scholar 

  33. Witczak, A., Pohorylo, A., Abdel-Gawad, H.: Endocrine-disrupting organochlorine pesticides in human breast milk: changes during lactation. Nutrients 13 (1) (2021). https://doi.org/10.3390/nu13010229

  34. C.L.F. Fernandes, L.M. Volcao, P.F. Ramires, R.R. Moura, F.M.R. Da Silva Junior, Distribution of pesticides in agricultural and urban soils of Brazil: a critical review. Environ Sci Process Impacts 22(2), 256–270 (2020). https://doi.org/10.1039/c9em00433e

    Article  CAS  PubMed  Google Scholar 

  35. C. Pelletier, P. Imbeault, A. Tremblay, Energy balance and pollution by organochlorines and polychlorinated biphenyls. Obes Rev 4(1), 17–24 (2003). https://doi.org/10.1046/j.1467-789x.2003.00085.x

    Article  CAS  PubMed  Google Scholar 

  36. S. Karami-Mohajeri, M. Abdollahi, Toxic influence of organophosphate, carbamate, and organochlorine pesticides on cellular metabolism of lipids, proteins, and carbohydrates: a systematic review. Hum Exp Toxicol 30(9), 1119–1140 (2011). https://doi.org/10.1177/0960327110388959

    Article  CAS  PubMed  Google Scholar 

  37. E. Vizcaino, J.O. Grimalt, A. Fernandez-Somoano, A. Tardon, Transport of persistent organic pollutants across the human placenta. Environ. Int 65, 107–115 (2014). https://doi.org/10.1016/j.envint.2014.01.004

    Article  CAS  PubMed  Google Scholar 

  38. D.J. Wilson, D.J. Locker, C.A. Ritzen, J.T. Watson, W. Schaffner, DDT concentrations in human milk. Am J Dis Child 125(6), 814–817 (1973). https://doi.org/10.1001/archpedi.1973.04160060026005

    Article  CAS  PubMed  Google Scholar 

  39. E. Junque, S. Garcia, M.A. Martinez, J. Rovira, M. Schuhmacher, J.O. Grimalt, Changes of organochlorine compound concentrations in maternal serum during pregnancy and comparison to serum cord blood composition. Environ Res 182, 108994 (2020). https://doi.org/10.1016/j.envres.2019.108994

    Article  CAS  PubMed  Google Scholar 

  40. F. Konradsen, W. van der Hoek, F.P. Amerasinghe, C. Mutero, E. Boelee, Engineering and malaria control: learning from the past 100 years. Acta Trop 89(2), 99–108 (2004). https://doi.org/10.1016/j.actatropica.2003.09.013

    Article  PubMed  Google Scholar 

  41. S. Sudharshan, R. Naidu, M. Mallavarapu, N. Bolan, DDT remediation in contaminated soils: a review of recent studies. Biodegradation 23(6), 851–863 (2012). https://doi.org/10.1007/s10532-012-9575-4

    Article  CAS  PubMed  Google Scholar 

  42. F.D. Martinez, A. Trejo-Acevedo, A.F. Betanzos, G. Espinosa-Reyes, J.A. Alegria-Torres, I.N. Maldonado, Assessment of DDT and DDE levels in soil, dust, and blood samples from Chihuahua, Mexico. Arch Environ Contam Toxicol 62(2), 351–358 (2012). https://doi.org/10.1007/s00244-011-9700-0

    Article  CAS  PubMed  Google Scholar 

  43. J.R. Harley, V.A. Gill, S. Lee, K. Kannan, V. Santana, K. Burek-Huntington, T.M. O’Hara, Concentrations of organohalogens (PCBs, DDTs, PBDEs) in hunted and stranded Northern sea otters (Enhydra lutris Kenyon) in Alaska from 1992 to 2010: Links to pathology and feeding ecology. Sci Total Environ 691, 789–798 (2019). https://doi.org/10.1016/j.scitotenv.2019.07.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. I. Al-Saleh, I. Al-Doush, A. Alsabbaheen, D. Mohamed Gel, A. Rabbah, 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 (2012). https://doi.org/10.1016/j.scitotenv.2011.11.020

    Article  CAS  PubMed  Google Scholar 

  45. Fruge, A.D., Cases, M.G., Schildkraut, J.M., Demark-Wahnefried, W.: Associations between obesity, body fat distribution, weight loss and weight cycling on serum pesticide concentrations. J Food Nutr Disord 5(3) (2016). https://doi.org/10.4172/2324-9323.1000198

  46. G. Cano-Sancho, A.G. Salmon, M.A. La Merrill, Association between exposure to p,p’-DDT and Its Metabolite p,p’-DDE with obesity: Integrated systematic review and meta-analysis. Environ Health Perspect. 125(9), 096002 (2017). https://doi.org/10.1289/EHP527

    Article  PubMed  PubMed Central  Google Scholar 

  47. N. Tawar, B.D. Banerjee, B.K. Mishra, T. Sharma, S. Tyagi, S.V. Madhu, V. Agarwal, S. Gupta, Adipose tissue levels of DDT as risk factor for obesity and Type 2 Diabetes Mellitus. Indian J Endocrinol Metab 25(2), 160–165 (2021). https://doi.org/10.4103/ijem.ijem_198_21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. N. Stratakis, S. Rock, M.A. La Merrill, M. Saez, O. Robinson, D. Fecht, M. Vrijheid, D. Valvi, D.V. Conti, R. McConnell, V.L. Chatzi, Prenatal exposure to persistent organic pollutants and childhood obesity: A systematic review and meta-analysis of human studies. Obes Rev 23(Suppl 1), e13383 (2022). https://doi.org/10.1111/obr.13383

    Article  CAS  PubMed  Google Scholar 

  49. S.L. Verhulst, V. Nelen, E.D. Hond, G. Koppen, C. Beunckens, C. Vael, G. Schoeters, K. Desager, Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect 117(1), 122–126 (2009). https://doi.org/10.1289/ehp.0800003

    Article  CAS  PubMed  Google Scholar 

  50. D. Valvi, M.A. Mendez, D. Martinez, J.O. Grimalt, M. Torrent, J. Sunyer, M. Vrijheid, Prenatal concentrations of polychlorinated biphenyls, DDE, and DDT and overweight in children: a prospective birth cohort study. Environ Health Perspect 120(3), 451–457 (2012). https://doi.org/10.1289/ehp.1103862

    Article  CAS  PubMed  Google Scholar 

  51. M. Warner, M. Ye, K. Harley, K. Kogut, A. Bradman, B. Eskenazi, Prenatal DDT exposure and child adiposity at age 12: The CHAMACOS study. Environ Res 159, 606–612 (2017). https://doi.org/10.1016/j.envres.2017.08.050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. M.A. La Merrill, N.Y. Krigbaum, P.M. Cirillo, B.A. Cohn, Association between maternal exposure to the pesticide dichlorodiphenyltrichloroethane (DDT) and risk of obesity in middle age. Int J Obes 44(8), 1723–1732 (2020). https://doi.org/10.1038/s41366-020-0586-7

    Article  CAS  Google Scholar 

  53. P.M. Cirillo, M.A. La Merrill, N.Y. Krigbaum, B.A. Cohn, Grandmaternal perinatal serum DDT in Relation to granddaughter early menarche and adult obesity: three generations in the child health and development studies cohort. Cancer Epidemiol Biomark Prev 30(8), 1480–1488 (2021). https://doi.org/10.1158/1055-9965.EPI-20-1456

    Article  Google Scholar 

  54. M.K. Skinner, M. Manikkam, R. Tracey, C. Guerrero-Bosagna, M. Haque, E.E. Nilsson, Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med 11, 228 (2013). https://doi.org/10.1186/1741-7015-11-228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. S. Cox, A.S. Niskar, K.M. Narayan, M. Marcus, Prevalence of self-reported diabetes and exposure to organochlorine pesticides among Mexican Americans: Hispanic health and nutrition examination survey, 1982-1984. Environ Health Perspect 115(12), 1747–1752 (2007). https://doi.org/10.1289/ehp.10258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. A.A. Al-Othman, S.H. Abd-Alrahman, N.M. Al-Daghri, DDT and its metabolites are linked to increased risk of type 2 diabetes among Saudi adults: a cross-sectional study. Environ Sci Pollut Res Int 22(1), 379–386 (2015). https://doi.org/10.1007/s11356-014-3371-0

    Article  CAS  PubMed  Google Scholar 

  57. M. La Merrill, E. Karey, E. Moshier, C. Lindtner, M.R. La Frano, J.W. Newman, C. Buettner, Perinatal exposure of mice to the pesticide DDT impairs energy expenditure and metabolism in adult female offspring. PLoS One 9(7), e103337 (2014). https://doi.org/10.1371/journal.pone.0103337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. J.R. Lakowicz, D. Hogen, G. Omann, Diffusion and partitioning of a pesticide, lindane, into phosphatidylcholine bilayers. A new fluorescence quenching method to study chlorinated hydrocarbon-membrane interactions. Biochim Biophys Acta 471(3), 401–411 (1977). https://doi.org/10.1016/0005-2736(77)90045-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. A. Ferro, D. Teixeira, D. Pestana, R. Monteiro, C.C. Santos, V.F. Domingues, J. Polonia, C. Calhau, POPs’ effect on cardiometabolic and inflammatory profile in a sample of women with obesity and hypertension. Arch Environ Occup Health 74(6), 310–321 (2019). https://doi.org/10.1080/19338244.2018.1535480

    Article  PubMed  Google Scholar 

  60. S. Li, X. Wang, L. Yang, S. Yao, R. Zhang, X. Xiao, Z. Zhang, L. Wang, Q. Xu, S.L. Wang, Interaction between beta-hexachlorocyclohexane and ADIPOQ genotypes contributes to the risk of type 2 diabetes mellitus in East Chinese adults. Sci Rep 6, 37769 (2016). https://doi.org/10.1038/srep37769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. A. Al-Othman, S. Yakout, S.H. Abd-Alrahman, N.M. Al-Daghri, Strong associations between the pesticide hexachlorocyclohexane and type 2 diabetes in Saudi adults. Int J Environ Res Public Health 11(9), 8984–8995 (2014). https://doi.org/10.3390/ijerph110908984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. R. Criswell, V. Lenters, S. Mandal, H. Stigum, N. Iszatt, M. Eggesbo, Persistent environmental toxicants in breast milk and rapid infant growth. Ann Nutr Metab 70(3), 210–216 (2017). https://doi.org/10.1159/000463394

    Article  CAS  PubMed  Google Scholar 

  63. C. Calciu, S. Kubow, H.M. Chan, Interactive dysmorphogenic effects of toxaphene or toxaphene congeners and hyperglycemia on cultured whole rat embryos during organogenesis. Toxicology 175(1-3), 153–165 (2002). https://doi.org/10.1016/s0300-483x(02)00075-6

    Article  CAS  PubMed  Google Scholar 

  64. R.J. Kavlock, N. Chernoff, E. Rogers, D. Whitehouse, B. Carver, J. Gray, K. Robinson, An analysis of fetotoxicity using biochemical endpoints of organ differentiation. Teratology 26(2), 183–194 (1982). https://doi.org/10.1002/tera.1420260211

    Article  CAS  PubMed  Google Scholar 

  65. I.S. Che Sulaiman, B.W. Chieng, M.J. Osman, K.K. Ong, J.I.A. Rashid, W.M.Z. Wan Yunus, S.A.M. Noor, N.A.M. Kasim, N.A. Halim, A. Mohamad, A review on colorimetric methods for determination of organophosphate pesticides using gold and silver nanoparticles. Mikrochim Acta 187(2), 131 (2020). https://doi.org/10.1007/s00604-019-3893-8

    Article  CAS  PubMed  Google Scholar 

  66. S. Suratman, J.W. Edwards, K. Babina, Organophosphate pesticides exposure among farmworkers: pathways and risk of adverse health effects. Rev Environ Health 30(1), 65–79 (2015). https://doi.org/10.1515/reveh-2014-0072

    Article  CAS  PubMed  Google Scholar 

  67. J.E. Casida, Organophosphorus xenobiotic toxicology. Annu Rev Pharm Toxicol 57, 309–327 (2017). https://doi.org/10.1146/annurev-pharmtox-010716-104926

    Article  CAS  Google Scholar 

  68. S. Thapa, M. Lv, H. Xu, Acetylcholinesterase: A primary target for drugs and insecticides. Mini Rev Med Chem 17(17), 1665–1676 (2017). https://doi.org/10.2174/1389557517666170120153930

    Article  CAS  PubMed  Google Scholar 

  69. Singh, S., Kumar, V., Gill, J.P.K., Datta, S., Singh, S., Dhaka, V., Kapoor, D., Wani, A.B., Dhanjal, D.S., Kumar, M., Harikumar, S.L., Singh, J.: Herbicide Glyphosate: Toxicity and Microbial Degradation. Int J Environ Res Public Health 17(20) (2020). https://doi.org/10.3390/ijerph17207519

  70. M.M. Milesi, V. Lorenz, M. Durando, M.F. Rossetti, J. Varayoud, Glyphosate herbicide: reproductive outcomes and multigenerational effects. Front Endocrinol 12, 672532 (2021). https://doi.org/10.3389/fendo.2021.672532

    Article  Google Scholar 

  71. V. Lorenz, G. Pacini, E.H. Luque, J. Varayoud, M.M. Milesi, Perinatal exposure to glyphosate or a glyphosate-based formulation disrupts hormonal and uterine milieu during the receptive state in rats. Food Chem Toxicol 143, 111560 (2020). https://doi.org/10.1016/j.fct.2020.111560

    Article  CAS  PubMed  Google Scholar 

  72. M.M. Milesi, V. Lorenz, G. Pacini, M.R. Repetti, L.D. Demonte, J. Varayoud, E.H. Luque, Perinatal exposure to a glyphosate-based herbicide impairs female reproductive outcomes and induces second-generation adverse effects in Wistar rats. Arch Toxicol 92(8), 2629–2643 (2018). https://doi.org/10.1007/s00204-018-2236-6

    Article  CAS  PubMed  Google Scholar 

  73. J.L. Teleken, E.C.Z. Gomes, C. Marmentini, M.B. Moi, R.A. Ribeiro, S.L. Balbo, E.M.P. Amorim, M.L. Bonfleur, Glyphosate-based herbicide exposure during pregnancy and lactation malprograms the male reproductive morphofunction in F1 offspring. J Dev Orig Health Dis 11(2), 146–153 (2020). https://doi.org/10.1017/S2040174419000382

    Article  CAS  PubMed  Google Scholar 

  74. M.A. Romano, R.M. Romano, L.D. Santos, P. Wisniewski, D.A. Campos, P.B. de Souza, P. Viau, M.M. Bernardi, M.T. Nunes, C.A. de Oliveira, Glyphosate impairs male offspring reproductive development by disrupting gonadotropin expression. Arch Toxicol 86(4), 663–673 (2012). https://doi.org/10.1007/s00204-011-0788-9

    Article  CAS  PubMed  Google Scholar 

  75. Y. Ait-Bali, S. Ba-M’hamed, G. Gambarotta, M. Sassoe-Pognetto, M. Giustetto, M. Bennis, Pre- and postnatal exposure to glyphosate-based herbicide causes behavioral and cognitive impairments in adult mice: evidence of cortical ad hippocampal dysfunction. Arch Toxicol 94(5), 1703–1723 (2020). https://doi.org/10.1007/s00204-020-02677-7

    Article  CAS  PubMed  Google Scholar 

  76. Y. Pu, L. Ma, J. Shan, X. Wan, B.D. Hammock, K. Hashimoto, Autism-like behaviors in male juvenile offspring after maternal glyphosate exposure. Clin Psychopharmacol Neurosci 19(3), 554–558 (2021). https://doi.org/10.9758/cpn.2021.19.3.554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. D. Kubsad, E.E. Nilsson, S.E. King, I. Sadler-Riggleman, D. Beck, M.K. Skinner, Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Sci Rep 9(1), 6372 (2019). https://doi.org/10.1038/s41598-019-42860-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. S.B. Panza, R. Vargas, S.L. Balbo, M.L. Bonfleur, D.C.T. Granzotto, D.M.G. Sant’Ana, G.A. Nogueira-Melo, Perinatal exposure to low doses of glyphosate-based herbicide combined with a high-fat diet in adulthood causes changes in the jejunums of mice. Life Sci 275, 119350 (2021). https://doi.org/10.1016/j.lfs.2021.119350

    Article  CAS  PubMed  Google Scholar 

  79. O.E. Kale, M. Vongdip, T.F. Ogundare, O. Osilesi, The use of combined high-fructose diet and glyphosate to model rats type 2 diabetes symptomatology. Toxicol Mech Methods 31(2), 126–137 (2021). https://doi.org/10.1080/15376516.2020.1845889

    Article  CAS  PubMed  Google Scholar 

  80. R. Mesnage, M.N. Antoniou, Facts and fallacies in the debate on glyphosate toxicity. Front Public Health 5, 316 (2017). https://doi.org/10.3389/fpubh.2017.00316

    Article  PubMed  PubMed Central  Google Scholar 

  81. Z. Lin, S. Pang, W. Zhang, S. Mishra, P. Bhatt, S. Chen, Degradation of acephate and its intermediate methamidophos: mechanisms and biochemical pathways. Front Microbiol 11, 2045 (2020). https://doi.org/10.3389/fmicb.2020.02045

    Article  PubMed  PubMed Central  Google Scholar 

  82. C.P. do Nascimento, G.X. Maretto, G.L.M. Marques, L.M. Passamani, A.P. Abdala, L.C. Schenberg, V. Beijamini, K.N. Sampaio, Methamidophos, an organophosphorus insecticide, induces pro-aggressive behaviour in mice. Neurotox Res 32(3), 398–408 (2017). https://doi.org/10.1007/s12640-017-9750-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. M. Uriostegui-Acosta, I. Hernandez-Ochoa, M. Sanchez-Gutierrez, B. Pina-Guzman, L. Rafael-Vazquez, M.J. Solis-Heredia, G. Martinez-Aguilar, B. Quintanilla-Vega, Methamidophos alters sperm function and DNA at different stages of spermatogenesis in mice. Toxicol Appl Pharm 279(3), 391–400 (2014). https://doi.org/10.1016/j.taap.2014.06.017

    Article  CAS  Google Scholar 

  84. V. Lucia Scherholz de Castro, S. Heloisa Chiorato, Effects of separate and combined exposure to the pesticides methamidophos and chlorothalonil on the development of suckling rats. Int J Hyg Environ Health 210(2), 169–176 (2007). https://doi.org/10.1016/j.ijheh.2006.09.003

    Article  CAS  PubMed  Google Scholar 

  85. T.A. Ribeiro, K.V. Prates, A. Pavanello, A. Malta, L.P. Tofolo, I.P. Martins, J.C. Oliveira, R.A. Miranda, R.M. Gomes, E. Vieira, C.C. Franco, L.F. Barella, F.A. Francisco, V.S. Alves, S.D. Silveira, V.M. Moreira, G.S. Fabricio, K. Palma-Rigo, D.M. Sloboda, P.C. Mathias, Acephate exposure during a perinatal life program to type 2 diabetes. Toxicology 372, 12–21 (2016). https://doi.org/10.1016/j.tox.2016.10.010

    Article  CAS  PubMed  Google Scholar 

  86. A.R. Nandhini, M. Harshiny, S.N. Gummadi, Chlorpyrifos in environment and food: a critical review of detection methods and degradation pathways. Environ Sci Process Impacts 23(9), 1255–1277 (2021). https://doi.org/10.1039/d1em00178g

    Article  CAS  PubMed  Google Scholar 

  87. T. Farkhondeh, A. Amirabadizadeh, S. Samarghandian, O. Mehrpour, Impact of chlorpyrifos on blood glucose concentration in an animal model: a systematic review and meta-analysis. Environ Sci Pollut Res Int 27(3), 2474–2481 (2020). https://doi.org/10.1007/s11356-019-07229-w

    Article  CAS  PubMed  Google Scholar 

  88. E.N. Ndonwi, B. Atogho-Tiedeu, E. Lontchi-Yimagou, T.S. Shinkafi, D. Nanfa, E.V. Balti, J.C. Katte, A. Mbanya, T. Matsha, J.C. Mbanya, A. Shakir, E. Sobngwi, Metabolic effects of exposure to pesticides during gestation in female Wistar rats and their offspring: a risk factor for diabetes. Toxicol Res 36(3), 249–256 (2020). https://doi.org/10.1007/s43188-019-00028-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. M.M. Lasram, K. Bouzid, I.B. Douib, A. Annabi, N. El Elj, S. El Fazaa, J. Abdelmoula, N. Gharbi, Lipid metabolism disturbances contribute to insulin resistance and decrease insulin sensitivity by malathion exposure in Wistar rat. Drug Chem Toxicol 38(2), 227–234 (2015). https://doi.org/10.3109/01480545.2014.933348

    Article  CAS  PubMed  Google Scholar 

  90. W. Han, Y. Tian, X. Shen, Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: An overview. Chemosphere 192, 59–65 (2018). https://doi.org/10.1016/j.chemosphere.2017.10.149

    Article  CAS  PubMed  Google Scholar 

  91. C.S. Anjos, R.N. Lima, A.L.M. Porto, An overview of neonicotinoids: biotransformation and biodegradation by microbiological processes. Environ Sci Pollut Res Int 28(28), 37082–37109 (2021). https://doi.org/10.1007/s11356-021-13531-3

    Article  PubMed  Google Scholar 

  92. Y. Park, Y. Kim, J. Kim, K.S. Yoon, J. Clark, J. Lee, Y. Park, Imidacloprid, a neonicotinoid insecticide, potentiates adipogenesis in 3T3-L1 adipocytes. J Agric Food Chem 61(1), 255–259 (2013). https://doi.org/10.1021/jf3039814

    Article  CAS  PubMed  Google Scholar 

  93. Q. Sun, W. Qi, X. Xiao, S.H. Yang, D. Kim, K.S. Yoon, J.M. Clark, Y. Park, Imidacloprid promotes high fat diet-induced adiposity in female C57BL/6J mice and enhances Adipogenesis in 3T3-L1 Adipocytes via the AMPKalpha-mediated pathway. J Agric Food Chem 65(31), 6572–6581 (2017). https://doi.org/10.1021/acs.jafc.7b02584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Q. Sun, X. Xiao, Y. Kim, D. Kim, K.S. Yoon, J.M. Clark, Y. Park, Imidacloprid promotes high fat diet-induced adiposity and insulin resistance in male C57BL/6J Mice. J Agric Food Chem 64(49), 9293–9306 (2016). https://doi.org/10.1021/acs.jafc.6b04322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. S. Yan, S. Tian, Z. Meng, J. Yan, M. Jia, R. Li, Z. Zhou, W. Zhu, Imbalance of gut microbiota and fecal metabolites in offspring female mice induced by nitenpyram exposure during pregnancy. Chemosphere 260, 127506 (2020). https://doi.org/10.1016/j.chemosphere.2020.127506

    Article  CAS  PubMed  Google Scholar 

  96. S. Yan, S. Tian, Z. Meng, M. Teng, W. Sun, M. Jia, Z. Zhou, S. Bi, W. Zhu, Exposure to nitenpyram during pregnancy causes colonic mucosal damage and non-alcoholic steatohepatitis in mouse offspring: The role of gut microbiota. Environ Pollut 271, 116306 (2021). https://doi.org/10.1016/j.envpol.2020.116306

    Article  CAS  PubMed  Google Scholar 

  97. S. Kitauchi, M. Maeda, T. Hirano, Y. Ikenaka, M. Nishi, A. Shoda, M. Murata, Y. Mantani, T. Yokoyama, Y. Tabuchi, N. Hoshi, Effects of in utero and lactational exposure to the no-observed-adverse-effect level (NOAEL) dose of the neonicotinoid clothianidin on the reproductive organs of female mice. J Vet Med Sci 83(4), 746–753 (2021). https://doi.org/10.1292/jvms.21-0014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. M. Shamsi, M. Soodi, S. Shahbazi, A. Omidi, Effect of Acetamiprid on spatial memory and hippocampal glutamatergic system. Environ Sci Pollut Res Int 28(22), 27933–27941 (2021). https://doi.org/10.1007/s11356-020-12314-6

    Article  CAS  PubMed  Google Scholar 

  99. National Toxicology, P.: Bioassay of nithiazide for possible carcinogenicity. Natl Cancer Inst Carcinog Tech Rep Ser 146, 1–107 (1979).

Download references

Author contributions

R.A.M., B.S.S., E.G.M., and P.C.L. designed, wrote, and approve the final version of this mini-review.

Funding

This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico- CNPq, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior- CAPES, and Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro- FAPERJ.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrícia Cristina Lisboa.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miranda, R.A., Silva, B.S., de Moura, E.G. et al. Pesticides as endocrine disruptors: programming for obesity and diabetes. Endocrine 79, 437–447 (2023). https://doi.org/10.1007/s12020-022-03229-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-022-03229-y

Keywords

Navigation