Sex hormone levels in rural workers exposed to pesticides: A systematic review with meta-analysis
DOI:
https://doi.org/10.21527/2176-7114.2025.50.16289Palabras clave:
Sex hormones, Pesticides, Endocrine disruptorsResumen
The present study aims to analyze the excitatory and/or inhibitory effects of pesticide exposure on the production of male sex hormones in rural populations. The protocol for this systematic review was previously registered in PROSPERO (CRD42022354863) and follows the guidelines recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). The research question addressed was: Does pesticides exposure cause excitatory and/or inhibitory effects on the production of sex hormones? The literature search was conducted from July 1 to July 17, 2023, in the following databases: Public Medline (PubMed), Latin American and Caribbean Literature in Health Sciences (LILACS), Science Direct, and Scientific Electronic Library (Scielo). The results indicate that pesticides exposure was associated with a significant decrease in testosterone levels (mean difference: -1.60, 95% CI: -2.47 to -0.72) and prolactin levels (mean difference: -1.28, 95 %: CI -2.19 to -0.37). In constrast, there was significant increase in Sex Hormone Binding Globulin (SHBG) levels (mean difference: 4.24, 95% CI: 1.54 to 6.93). No significant changes were observed in the levels of Follicle Stimulating Hormone (FSH) (mean difference: 0.98, 95% CI: 0.74 to 1.21) and Luteinizing Hormone (LH, mean difference: 0.44; 95% CI: 0.25 to 0.64) between the groups studied. In conclusion, evidence suggests that pesticide exposure may alter the production of various sex hormones. Specifically, individuals exposed to pesticides tend to exhibit lower levels of testosterone and prolactin, while SHBG levels are increased compared to those without exposure.
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[1]. FAO – Food and Agriculture Organization of the United Nations. Pesticides Use Indicators. Rome: FAO, 2021. Disponível em: https://openknowledge.fao.org. Access at: 18 fev. 2023.
[2]. Ibama. Comercialização de agrotóxicos e afins. Série histórica 2000-2019, 2020 [Internet]. Available in : <https://www.gov.br/ibama/pt-br>. Access at: 7 set. 2022.
[3]. Food and Agriculture Organization of the United Nations (FAO). Pesticides Indicators. FAOSTAT, 23 de dezembro de 2022. Available in: https://www.fao.org/faostat/en/#data/EPA. Access at: 23 dez. 2022.
[4]. Silva YRA.Pesticide poisonings registered in the notification system and Brazilian toxicological information centers: an integrative review [Course Completion Work - Graduation - Health Sciences]. ITACOATIARA – AM; 2023.
[5]. Fucic A, Duca RC, Galea Ks, Maric T, Garcia K, Bloom MS, Andersen HR, Vena JE. Reproductive Health Risks Associated with Occupational and Environmental Exposure to Pesticides. Int J Environ Res Public Health. 2021 Jun 18;18(12):6576. doi: 10.3390/ijerph18126576. PMID: 34207279; PMCID: PMC8296378.
[6]. Paula IB, de Paula LB, de Paula LB. Exposição de gestantes aos agrotóxicos e suas consequências: uma revisão sistemática. Cuadernos de Educación y Desarrollo. 2024;16(2 Edição Especial). DOI: 10.55905/cuadv16n2-ed.esp.040. Available in: https://ojs.europubpublications.com/ojs/index.php/ced/article/view/2651. Access at: 8 abr. 2024.
[7]. Santos Barros SE, Moreira MB. Characterization of pesticides used in irrigated fruit growing agricultural areas in the São Francisco Valley. Irrigated Fruit Farming: vulnerabilities and prospects for sustainable production. Year 2023; Volume 1. Digital Scientific Editor.
[8]. Andersen RH, Vinggaard AM, Rasmussen TH, Gjermandsen IM, Bonefeld-Jorgensen EC. Effects of pesticides currently used in in vitro estrogenicity, androgenicity and aromatase activity assays. Toxicol Appl Pharmacol. 2002;179(1).
[9]. Kojima H, Katsura E, Takeuchi S, Niiyama K, Kobayashi K. Screening for estrogen and androgen receptor activities in 200 pesticides by reporter gene in vitro assays using Chinese hamster ovary cells. Environ Health Perspect. 2004;112(5):524-531.
[10]. Orton F, Rosivatz E, Scholze M, Kortenkamp A. Widely used pesticides with previously unknown endocrine activity revealed to be antiandrogens in vitro. Environ Health Perspect. 2011;119(6):794-800.
[11]. Saillenfait AM, Ndiaye D, Sabate JP. The estrogenic and androgenic potential of pyrethroids in vitro. Rev Toxicol In Vitro. 2016;34:321-332.
[12]. Ye X, Liu J. Efeitos de inseticidas piretróides no eixo hipotálamo-hipófise-gonadal: Uma perspectiva de saúde reprodutiva. Environ Pollut. 2019. doi:10.1016/j.envpol.2018.11.031
[13]. Otero MMMP, Rodrigues ERM, Yokoya ABA, Miyata GN, Gedolin BP, Pinto RS. Influência do Glifosato em distúrbios do sistema endócrino: um estudo de revisão narrativa. Brazilian J Health Rev. 2024;7(3):183. doi:10.34119/bjhrv7n3-183.
[14]. Mnif W, Hassine AI, Bouaziz A, Bartegi A, Thomas O, Roig B. Effect of endocrine disrupting pesticides: a review. Int J Environ Res Public Health. 2011;8(6):2265-2303.
[15]. Oliveira SM, López ML. Epidemiological overview of congenital malformations in Brazil (2013-2017). Rev Saúde Multidiscipl (Online). 2020;8(2):1-5.
[16]. Souza JP, Porto MJ, Credidio GC, Faria HA, Nepomuceno AFSF, Santos LO, Teles ALB. Changes in sex hormone levels caused by exposure to pesticides. RevIPI. 2022;11(2):VOL. 12.
[17]. Cavalier H, Trasande L, Porta M. Pesticide Exposures and Cancer Risk: Assessment of Recent Epidemiological Evidence in Humans and Ways Forward. Int J Cancer. 2023;152(5):879-912.
[18]. Pantaleon LP. Influence of exposure to atrazine during puberty on the sexual sphere of adult rats [Master's Dissertation in Experimental and Comparative Pathology]. São Paulo: University of São Paulo; 2021. doi:10.11606/D.10.2021.tde-14032022-145914. Access at: 8 abr. 2024.
[19]. Rawlings et al., 1998; Rocha VA. Effects of the Western diet and exposure to 2,4-dichlorophenoxyacetic acid (2,4-D) on the prostate of mice. Botucatu, 2023.
[20]. Freire C, Koifman RJ, Sarcinelli PN, Rosa ACS, Clapauch R, Koifman S. Association between serum levels of organochlorine pesticides and sex hormones in adults living in a heavily contaminated area in Brazil. Int J Hyg Environ Health. 2014;217:370–378.
[21]. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JPA, et al. A declaração PRISMA 2020: diretriz atualizada para relatar revisões sistemáticas e meta-análises de estudos que avaliam intervenções em saúde. BMJ. 2021;372:n71. doi:10.1136/bmj.n71.
[22]. Moher D, Liberati A, Tetzlaff J, Altman D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7). https://doi.org/10.1371/journal.pmed.1000097.
[23]. Fuchs SC, Paim BS. A Guide for Systematic Reviews of Observational Studies. Texto Contexto Enferm. 2024;33:e0221. doi:10.1590/1980-265X-TCE-2023-0221en.
[24]. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2000.
[25]. UnitsLab. Available in: https://unitslab.com/taxonomy/term/8. Accessed on: July 20, 2021. Scholten RJ, Clarke M, Hetherington J. The Cochrane Collaboration. Eur J Clin Nutr. 2005 Aug;59 Suppl 1:S147-9; discussion S195-6. doi: 10.1038/sj.ejcn.1602188. PMID: 16052183.
[26]. Scholten RJ, Clarke M, Hetherington J. The Cochrane Collaboration. Eur J Clin Nutr. 2005 Aug;59 Suppl 1:S147-9; discussion S195-6. doi: 10.1038/sj.ejcn.1602188. PMID: 16052183.
[27]. Celik-Ozenci C, Tasatargil A, Tekcan M, Sati L, Gungor E, Isbir M, Erler F. Effect of abamectin exposure on semen parameters indicative of reduced sperm maturity: a study with rural workers in Antalya (Turkey). Andrologia. 2012;44(6):388–395. doi: 10.1111/j.1439-0272.2012.01297.x.
[28]. Cunha TS, Moura MJCS, Reis LO. Níveis séricos de testosterona e globulina ligadora de hormônios sexuais em homens saudáveis: influência da idade e do índice de massa corporal. Revista Brasileira de Medicina do Esporte. 2022;26(4):314-318. doi:10.1590/1517-869220202604223202.
[29]. Nunes GS. Immunochemical methods for analyzing environmental contaminants: concepts, state of the art and perspectives. Quím Nova. 2005;28(3). https://doi.org/10.1590/S0100-40422005000300018.
[30]. Abbassy MA, et al. Adverse biochemical effects of various pesticides on cotton field sprayers in El-Behira Governorate, Egypt. Biomed Aging Pathol. 2014. http://dx.doi.org/10.1016/j.biomag.2014.04.004.
[31]. Yucra S, et al. Dialkyl phosphate metabolites of organophosphorus in applicators of agricultural pesticides in Majes - Arequipa (Peru). J Occup Med Toxicol. 2006;12(4):355-361.
[32]. Straube E, Straube W, Krüger E, Bradatsch M, Jacob-Meisel M, Rose HJ. Disruption of male sex hormones with regard to pesticides: pathophysiological and regulatory aspects. Toxicol Lett. 1999;107:225–231.
[33]. Czarnywojtek A,et al. The effect of endocrine disruptors on the reproductive system-current knowledge. European Review for Medical & Pharmacological Sciences, 2021; 25:15.
[34]. Freire C, Koifman RJ, Sarcinelli PN, Rosa ACS, Clapauch R, Koifman S. Association between serum levels of organochlorine pesticides and sex hormones in adults living in a heavily contaminated area in Brazil. Int J Hyg Environ Health. 2014;217:370–378.
[35]. Santos R, Piccoli C, Cremonese C, Freire C. Thyroid and reproductive hormones in relation to pesticide use in an agricultural population in Southern Brazil. Pesquisa Ambiental. 2019;173:221–23.
[36]. Krause W, Homola S. Alterations of the seminiferous epithelium and the Leydig cells of the rat testis after the application of dichlorvos (DDVP). Bull Environ Contam Toxicol. 1974 May;11(5):429-433. Springer Science and Business Media LLC. http://dx.doi.org/10.1007/bf01685299.
[37]. Fattahi, Parivar, Jorsaraei, Moghadamnia. The effects of diazinon on testosterone, FSH and LH levels and testicular tissue in mice. Int J Reprod Biomed. 2009 Nov;7(2):59-64.
[38]. Erthal RP, Siervo GEML, Frigoli GF, Zaninelli TH, Verri WA, Fernandes GSA.Exposure to malathion during the juvenile and peripubertal periods decreases the regulation of the androgen receptor and the expression of the testicular 17-ß-HSD gene and compromises sperm quality in rats. J Dev Orig Health Dis. 2023 Apr;14(2):286-293. DOI: 10.1017/S2040174422000599. EPub 2022 Nov 7. PMID: 36336997.
[39]. Erthal RP, Siervo GEML, Staurengo-Ferrari L, Fattori V, Pescim RR, Verri WA, Fernandes GSA. Impairment of postnatal epididymal development and immune microenvironment following administration of low doses of malathion during juvenile and peripubertal periods of rats. Hum Exp Toxicol. 2020 Jun 4;39(11):1487-1496. SAGE Publications. http://dx.doi.org/10.1177/0960327120930076.
[40]. Liu C, Qu J, Wu M, Huang X, Li L. Cypermethrin triggers YY1-mediated testosterone biosynthesis suppression. Ecotoxicol Environ Saf. 2021 Dec 1;225:112792. doi: 10.1016/j.ecoenv.2021.112792. Epub 2021 Sep 17. Erratum in: Ecotoxicol Environ Saf. 2022 Jul 8;242:113871. PMID: 34544022.
[41]. Vieira S. SHBG, obesity, diabetes and PCOS: more free and bound hormones. 2017. Available at: https://drasuzanavieira.med.br/2017/02/01/shbg-obesidade-diabetese-sop/. Accessed on: February 24, 2021.
[42]. Gineco Academy.2023 Principais condições que aumentam ou diminuem os níveis séricos de SHBG. Disponível em: https://app.ginecoacademy.com/principais-condicoes-que-aumentam-ou-diminuem-os-niveis-sericos-de-shbg/?utm_source=chatgpt.com. Acesso em: 21 fev. 2025.
[43]. MORAIS, Irani da Silva. Avaliação da puberdade e indução de neomachos de tambaqui Colossoma macropomum através da administração de esteroides sexuais na ração. 2023.
[44]. Cremonese C. Exposure to pesticides and reproductive disorders: study in rural workers, their families and young people in the municipality of FarroupilhaRS. 2014.
[45]. Ubaid ur Rahman, H., Asghar, W., Nazir, W., Sandhu, M. A., Ahmed, A., & Khalid, N. (2020). A comprehensive review on chlorpyrifos toxicity with special reference to endocrine disruption: Evidence of mechanisms, exposures and mitigation strategies. Science of The Total Environment, 142649. doi:10.1016/j.scitotenv.2020.1426.
[46]. Cremonese C, Piccoli C, Pasqualotto F, Clapauch R, Koifman RJ, Koifman S, Freire C. Occupational exposure to pesticides, reproductive hormone levels and sperm quality in young Brazilians. Reprod Toxicol. 2017;67:174-185. doi: 10.1016/j.reprotox.2017.01.001.
[47]. Kamijima M, Hibi H, Gotoh M, Taki K, Saito I, Wang H, Itohara S, Yamada T, Ichihara G, Shibata E, Nakajima T, Takeuchi Y. A Survey of Semen Indices in Insecticide Sprayers. J Occup Health. 2004;46:109–118.
[48]. Manfo FPT, Moundipa PF, Déchaud H, Tchana AN, Nantia EA, Zabot M-T, Pugeat M. Effect of agropesticide use on male reproductive function: A study in farmers in Djutitsa (Cameroon). Environ Toxicol. 2010;27(7):423-432. doi: 10.1002/tox.20656.
[49]. Bole-Feysot C, et al. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998;19(3):225-268.
[50]. Guelho D, et al. Prolactin and metabolism – a different perspective on a multifunctional hormone. Port J Endocrinol Diabetes Metab. 2016;11(2):268-276.
[51]. Petronilho, F; Giustina, A D; Danielski, L G. Chapter 4 - The role and function of specialized blood–neuronal barriers: Blood–CSF, blood–retinal, blood–spinal cord, blood–labyrinth, blood–nerve barriers, and blood–brain barrier (BBB).Neurobiology of Infectious Diseases. Neurobiology of Disease. 2025, Pages 49-69.
[52]. Snyder PJ. Causes of hyperprolactinemia [Internet]. Waltham (MA): UpToDate; 2017. Available from: https://www.uptodate.com/contents/causes-of-hyperprolactinemia. Accessed on: March 12, 2022.
[53]. SANTANA, Lidiana Bandeira de. Características clínicas e laboratoriais de mulheres com diagnóstico de artrite reumatóide e sua associação com as concentrações séricas de prolactina. 2021. 161 f., il. Dissertação (Mestrado em Ciências da Saúde) — Universidade de Brasília, Brasília, 2021.
[54]. Bapayeva G, Poddighe D, Terzic S, Zhumadilova A, Kulbayeva S, Terzic M. Exposure to organochlorine pesticides in adolescent females: potential impact on sex hormones and interleukin-1 levels. Pesquisa Immunológica. 2018. doi: 10.1007/s12026-018-9049-9.
[55]. Teresa U, et al. Dietary intake of potentially toxic elements and children's chemical exposure. Curr Opin Environ Sci Health. 2022;30:100393. doi:10.1016/j.coesh.2022.100393.
[56]. Koifman S, Hatagima A. Exposure to pesticides and environmental cancer. Available in: Accessed on: April 29, 2012.
[57]. Hernández, IB, Carrillo, RV, García, IC. (2009). Alteraciones en la fertilidad masculina por exposición a pesticidas.Rev Int Androl. , 7(2), 98–105. doi:10.1016/s1698-031x(09)71614-0
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