ABSTRACT

Giving the problem that involves the complex relationship between the use of pesticides and the onset of cancer, several studies have been developed around the world searching for evidence to prove it. The objective is to analyze the relationship between the use of pesticides and the onset of cancer in farmers, according to specialized literature. It is a scoping review. The search was carried out in three databases, and the articles were analyzed by two researchers and a third, for dealing with disagreements. Cohen's Kappa value was tested to assess agreement regarding the data extracted from the studies. A total of 29 bibliographies made up the sample. The studies came from five continents. Case-control and cohort research dominated the review landscape, using inferential statistics with different types of statistical tests. A variety of cancer types were studied, and most of the articles pointed to a predisposition to cancer, referring to biomarkers for early prediction of this chronic disease. In conclusion, being a farmer and being exposed to pesticides confers a greater risk of developing cancer compared to those who are not exposed.

KEYWORDS
Pesticides; Neoplasms; Farmers; Health risk; Environmental health

Introduction

Pesticides are products, according to Law No. 14,785, whose purpose is to modify the composition of flora or fauna, with the aim of protecting them from the harmful interference of other living beings¹1 Presidência da República (BR). Lei n° 14.785, de 27 de dezembro de 2023. Dispõe sobre a pesquisa, a experimentação, a produção, a embalagem, a rotulagem, o transporte, o armazenamento, a comercialização, a utilização, a importação, a exportação, o destino final dos resíduos e das embalagens, o registro, a classificação, o controle, a inspeção e a fiscalização de agrotóxicos, de produtos de controle ambiental, de seus produtos técnicos e afins; revoga as Leis nos 7.802, de 11 de julho de 1989, e 9.974, de 6 de junho de 2000, e partes de anexos das Leis nos 6.938, de 31 de agosto de 1981, e 9.782, de 26 de janeiro de 1999. Diário Oficial da União, Brasília, DF. 2023 dez 28; Edição 246; Seção I:28.. They are used to maintain control or eliminate insects, larvae, weeds and other pests that can affect plantations²2 Kim KH, Kabir E, Jahan SA. Exposure to pesticides and the associated human health effects. Sci Total Environ. 2017;575:525-535. DOI: https://doi.org/10.1016/j.scitotenv.2016.09.009
https://doi.org/10.1016/j.scitotenv.2016... ,³3 Instituto Nacional de Câncer José Alencar Gomes da Silva. Ambiente, trabalho e câncer: aspectos epidemiológicos, toxicológicos e regulatórios [Internet]. Rio de Janeiro: INCA; 2021 [acesso em 2024 jan 31]. 293 p. Disponível em: https://www.inca.gov.br/sites/ufu.sti.inca.local/files//media/document//ambiente_trabalho_e_cancer_-_aspectos_epidemiologicos_toxicologicos_e_regulatorios.pdf
https://www.inca.gov.br/sites/ufu.sti.in... , however, their effects are not selective and affect flora and fauna in general.

The use of pesticides has increased by 93% worldwide in recent years, with the increase in Brazil corresponding to 190%⁴4 Secretaria de Estado da Saúde do Paraná (PR). Superintendência de Atenção à Saúde. Linha Guia da Atenção às Populações Expostas aos Agrotóxicos [Internet]. 1. ed. Curitiba: Sesa; 2018 [acesso em 2022 out 14]. Disponível em: https://www.saude.pr.gov.br/sites/default/arquivos_restritos/files/documento/2020-04/linhaguiaagrotoxicos.pdf.
https://www.saude.pr.gov.br/sites/defaul... . Brazil is considered one of the largest agricultural producers in the world and the second largest exporter of these products5. In 2008, it rose to the ranking of the largest consumer of pesticides in the world⁵5 Carneiro FF, Augusto LGS, Rigotto ARM, et al. Dossiê ABRASCO: um alerta sobre os impactos dos agro-tóxicos na saúde [Internet]. Rio de Janeiro, São Paulo: Expressão Popular; 2015 [acesso em 2024 fev 1]. 628 p. Disponível em: https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/
https://abrasco.org.br/download/dossie-a... , maintaining this position since then. Its excessive use increases the risks to Public Health, Occupational Health and the Environment.

Study mapped the use of pesticides in Brazil, demonstrating that, while the consumption of pesticides in the world, between 2000 and 2010, increased by 100%, in Brazil, it reached 200%; and that from 2012 to 2014, approximately 8.33 kg per hectare were applied, with glyphosate being the most consumed in all Brazilian regions⁶6 Bombardi LM. Geografia do Uso de Agrotóxicos no Brasil e Conexões com a União Europeia [Internet]. São Paulo: FFLCH - USP; 2017 [acesso em 2024 fev 1]. 296 p. Disponível em: https://conexaoagua.mpf.mp.br/arquivos/agrotoxicos/05-larissa-bombardi-atlas-agrotoxico-2017.pdf
https://conexaoagua.mpf.mp.br/arquivos/a... .

Pesticides are classified based on their purpose, chemical group and toxicity. After exposure to pesticides, poisoning may occur, which, depending on the time of onset of symptoms, may be: i) acute, resulting from exposure to concentrations of one or more toxic agents capable of causing damage within 24 hours; ii) chronic, resulting from continued exposure to relatively low doses of one or more products, the symptoms of which may appear weeks, months, years or generations after their use⁵5 Carneiro FF, Augusto LGS, Rigotto ARM, et al. Dossiê ABRASCO: um alerta sobre os impactos dos agro-tóxicos na saúde [Internet]. Rio de Janeiro, São Paulo: Expressão Popular; 2015 [acesso em 2024 fev 1]. 628 p. Disponível em: https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/
https://abrasco.org.br/download/dossie-a... ,⁷7 Londres F. Agrotóxicos no Brasil: um guia para ação em defesa da vida [Internet]. Rio de Janeiro: ASPTA - Assessoria e Serviços a Projetos em Agricultura Alternativa; 2011 [acesso em 2024 jan 14]. 191 p. Disponível em: https://br.boell.org/sites/default/files/agrotoxicos-no-brasil-mobile.pdf
https://br.boell.org/sites/default/files... .

Chronic damage resulting from exposure includes different types of cancer⁸8 Ministério da Saúde (BR); Instituto Nacional do Câncer. O que é câncer? [Internet]. Brasília, DF: Ministério da Saúde; 2022 [acesso em 2024 jan 24]. Disponível em: https://www.gov.br/inca/pt-br/assuntos/cancer/o-que-e-cancer#
https://www.gov.br/inca/pt-br/assuntos/c... . Cancer appears as a result of the disorderly growth of cells, which can invade adjacent tissues or distant organs. Because they divide rapidly, cancer cells tend to be very aggressive and uncontrollable, forming tumors that can spread to other areas of the body⁸8 Ministério da Saúde (BR); Instituto Nacional do Câncer. O que é câncer? [Internet]. Brasília, DF: Ministério da Saúde; 2022 [acesso em 2024 jan 24]. Disponível em: https://www.gov.br/inca/pt-br/assuntos/cancer/o-que-e-cancer#
https://www.gov.br/inca/pt-br/assuntos/c... .

The potential for cancer development -despite the large number of variables to be considered (types of substances and their associations, handling, use of Personal Protective Equipment (PPE), genetic factors, among others) - is recognized by the Ministry of Health⁹9 Ministério da Saúde (BR); Instituto Nacional do Câncer. Agrotóxico [Internet]. Brasília, DF: Ministério da Saúde; 2023 [acesso em 2024 jan 24]. Disponível em: https://www.gov.br/inca/pt-br/assuntos/causas-e-prevencao-do-cancer/exposicao-no-trabalho-e-no-ambiente/agrotoxico.
https://www.gov.br/inca/pt-br/assuntos/c... and by different authors²2 Kim KH, Kabir E, Jahan SA. Exposure to pesticides and the associated human health effects. Sci Total Environ. 2017;575:525-535. DOI: https://doi.org/10.1016/j.scitotenv.2016.09.009
https://doi.org/10.1016/j.scitotenv.2016... ,⁵5 Carneiro FF, Augusto LGS, Rigotto ARM, et al. Dossiê ABRASCO: um alerta sobre os impactos dos agro-tóxicos na saúde [Internet]. Rio de Janeiro, São Paulo: Expressão Popular; 2015 [acesso em 2024 fev 1]. 628 p. Disponível em: https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/
https://abrasco.org.br/download/dossie-a... ,¹⁰10 Sarpa M, Friedrich K. Exposição a agrotóxicos e desenvolvimento de câncer no contexto da saúde coletiva: o papel da agroecologia como suporte às políticas públicas de prevenção do câncer. Saúde debate. 2022;46(esp2):407-425. DOI: https://doi.org/10.1590/0103-11042022E227
https://doi.org/10.1590/0103-11042022E22... . Some of these studies seek evidence that indicates the relationship between specific types of pesticides and genetic mutations¹¹11 Bellei TT, Stedile NLR. Relação entre risco de câncer e trabalho na agricultura: uma análise a partir dos dados do Instituto Nacional do Câncer. Rev Sul-Bras Enferm. 2020;32:26-35.,¹²12 Pluth TB, Zanini LAG, Battisti IDE. Pesticide exposure and cancer: an integrative literature review. Saúde debate. 2019;43(122):906-924. DOI: https://doi.org/10.1590/0103-1104201912220
https://doi.org/10.1590/0103-11042019122... or the carcinogenic potential of certain types of products¹³13 Friedrich K, Silveira GR, Amazonas JC, et al. Situação regulatória internacional de agrotóxicos com uso autorizado no Brasil: potencial de danos sobre a saúde e impactos ambientais. Cad Saúde Pública. 2021;37(4):e00061820. DOI: https://doi.org/10.1590/0102-311X00061820
https://doi.org/10.1590/0102-311X0006182... ,¹⁴14 Costa VIB, Mello MSC, Friedrich K. Exposição ambiental e ocupacional a agrotóxicos e o linfoma não Hodgkin. Saúde debate. 2017;41(112):49-62. DOI: https://doi.org/10.1590/0103-1104201711205
https://doi.org/10.1590/0103-11042017112... ; others still research the relationship between the use of pesticides and cancer morbidity and mortality rates¹⁵15 Pluth TB, Zanini LAG, Battisti IDE, et al. Epidemiological profile of cancer patients from an area with high pesticide use. Saúde debate. 2020;44(127):1005-1017. DOI: https://doi.org/10.1590/0103-1104202012705
https://doi.org/10.1590/0103-11042020127... ,¹⁶16 Silva AMC, Soares MR, Silva NA, et al. Environmental and occupational exposure among cancer patients in Mato Grosso, Brazil. Rev Bras Epidemiol. 2022;25:e220018. DOI: https://doi.org/10.1590/1980-549720220018.supl.1
https://doi.org/10.1590/1980-54972022001... . It is important to emphasize that the probability increases when these farmers do not use PPE properly¹⁷17 Brust RS, Oliveira LPM, Silva ACSS, et al. Epidemiological profile of farmworkers from the state of Rio de Janeiro. Rev Bras Enferm. 2019;72:122-128. DOI: https://doi.org/10.1590/0034-7167-2017-0555
https://doi.org/10.1590/0034-7167-2017-0... .

Given the evidence presented, the objective of this review is to analyze the relationship between the use of pesticides and the appearance of cancer in farmers, according to specialized bibliography.

Material and methods

A scoping review¹⁸18 Cordeiro L, Soares CB. Revisão de escopo: potencialidades para a síntese de metodologias utilizadas em pesquisa primária qualitativa [Internet]. BIS. 2019 [acesso em 2024 jan 31];20(2):37-43. Disponível em: https://pesquisa.bvsalud.org/portal/resource/pt/biblio-1021863
https://pesquisa.bvsalud.org/portal/reso... ,¹⁹19 Munn Z, Peters MDJ, Stern C, et al. Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach. BMC Med Res Methodol. 2018;18(1):143. DOI: https://doi.org/10.1186/s12874-018-0611-x
https://doi.org/10.1186/s12874-018-0611-... ,²⁰20 Tricco AC, Lillie E, Zarin W, et al. A scoping review on the conduct and reporting of scoping reviews. BMC Med Res Methodol. 2016;16:15. DOI: https://doi.org/10.1186/s12874-016-0116-4
https://doi.org/10.1186/s12874-016-0116-... was conducted following the PRISMA-ScR (Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews) approach²¹21 Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. DOI: http://dx.doi.org/10.1136/bmj.n71
http://dx.doi.org/10.1136/bmj.n71... . The study protocol for the scoping review was registered on the Open Science Framework (OSF) platform on August 22, 2022²²22 Lucas JIP, Stedile NLR, Cioato FM. Protocolo de Revisão de Escopo. OSF. 2024. DOI: https://doi.org/10.17605/OSF.IO/8RC4Z
https://doi.org/10.17605/OSF.IO/8RC4Z... .

Inclusion criteria

The inclusion criteria for selecting articles were: original articles; applied research articles; published in full, from 2012 to 2021; with open access; in English and Portuguese; that addressed the relationship between the use of pesticides and the onset of cancer in the farming population. Systematic reviews; editorials; experience reports; annals; theses and dissertations; government manuals and documents; studies with other types of workers other than agricultural workers or that treated cancer in animals; and those that focused on acute damage or other chronic damage other than cancer were excluded. It was decided to include in the analysis original articles, published in journals and submitted to peer review, as they directly seek to contribute to the construction of responses regarding the effects of pesticides on the health of farmers.

Search scheme

The data search was developed in the BVS, Scopus and ScienceDirect databases, from the CAFe access of the CAPES' Portal of Journals, using the keywords indexed in the Health Sciences Descriptors (DeCS) and with Boolean expressions, on 07/14/2021: "agrotóxicos OR agrochemicals OR pesticides", AND "câncer", AND "agricultores OR farmers".

Study selection

Figure 1 presents the search results, inclusions and exclusions of articles that deal with the relationship between cancer and the use of pesticides, with the respective justifications.

The search for articles in the databases yielded 1,401 references. Using the Parsifal and Orange Data Mining tools, the search resulted in 1,192 studies. After screening (Kappa 0.774, p = <0.01) and reading the articles in full (Kappa 0.627), based on the criteria defined for this study, a total of 29 bibliographies were pre-selected, with the final sample comprising of articles that presented statistical significance (n = 29) for the relationship between the onset of cancer in farmers and the use of pesticides.

As a strategy for screening the articles, the Orange Data Mining platform was used in the first phase for 'text mining', with descriptors assigned based on the analysis of titles, abstracts and keywords. The selection of studies in the screening and eligibility phases was carried out by two researchers who were experts in the subject and a third reviewer in case of disagreements.

As a parameter for the evaluation - inclusion/exclusion criteria and selection of articles by researchers -, Cohen's Kappa test was applied to verify the agreements between the evaluators²³23 Kottner J, Audigé L, Brorson S, et al. Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. J Clin Epidemiol. 2011;64(1):96-106. DOI: https://doi.org/10.1016/j.jclinepi.2010.03.002
https://doi.org/10.1016/j.jclinepi.2010.... ,²⁴24 McHugh ML. Interrater reliability: the kappa statistic. Biochem Med (Zagreb). 2012;22(3):276-282.. A Kappa value between 0.6 and 0.8²⁵25 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-174 was considered satisfactory.

Data analysis

After extracting the data of interest, they were organized into tables and treated using thematic analysis. Thematic analysis consists of three stages: a) pre-analysis, which is subdivided into skimming, corpus formation, and formulation and reformulation of hypotheses and objectives; b) exploration of the material; and c) processing of the results obtained and interpretation²⁶26 Minayo MCS. O desafio do conhecimento: pesquisa qualitativa em saúde. 13. ed. São Paulo: Hucitec; 2013. 269 p..

The study is part of the research project 'The use of pesticides in family farming and its implications for farmers' health and environmental health', approved by the Research Ethics Committee, Opinion No. 3,481,277 (CAAE 17010519.1.0000.5341).

Results

The characteristics related to the studies, such as authors and year, title, country of origin, journal and qualis are described in table 1, only for the studies that presented statistical significance for the association between pesticides and cancer 81% (n=29).

A geographic distribution of publications was identified that covers almost all continents. Most studies were concentrated in the American continent (22, with n = 12 in North America and n = 10 in South America). The United States of America (n = 9) and Brazil (n = 8) are worth highlighting, as they concentrated the largest number of published articles. In Europe, France had the largest number (n = 4). Publications in Africa and Asia were less prominent. There were no publications in Oceania. This distribution suggests that the use of pesticides and their effects on health is a concern that deserves attention at a global level.

The papers selected for the research are distributed across international and national scientific journals. The 29 articles come from 24 different journals, with 24 articles also published in journals included in the Qualis/ CAPES system, with significant impact metrics, and the majority published in A1 and A2 journals.

The characteristics relating to methodological aspects, such as design, participants and statistical analyses used, are described in table 2.

Case-control and cohort studies dominated the review scenario. There was a diverse number of participants in each study, sources and forms of data collection, which shows diversity in the number and types of methodologies used, making the analysis of the studies as a whole complex.

As for statistical tests, different and diverse types of tests were used, especially for quantitative data. Most studies used descriptive and inferential statistics.

The objectives and conclusions of the studies are presented in table 3.

Regarding the objectives of the studies presented in the bibliographies, most refer to: 1) biomarkers for early prediction of cancer (case-control studies and clinical trials); and 2) risk associations (sociodemographic data, use of pesticides, types of pesticides, exposure to products, frequency and duration of exposure and agricultural tasks).

Most of the articles point to a predisposition to cancer (n = 14), including epidemiological, case-control and experimental studies, through clinical trials. They use laboratory tests to verify genetic damage³⁰30 Andreotti G, Hoppin JA, Hou L, et al. Pesticide Use and Relative Leukocyte Telomere Length in the Agricultural Health Study. PLoS One. 2015;10(7):e0133382. DOI: https://doi.org/10.1371/journal.pone.0133382
https://doi.org/10.1371/journal.pone.013... ,⁴⁰40 Rusiecki JA, Beane Freeman LE, Bonner MR, et al. High pesticide exposure events and DNA methylation among pesticide applicators in the agricultural health study. Environ Mol Mutagen. 2017;58(1):19-29. DOI: https://doi.org/10.1002/em.22067
https://doi.org/10.1002/em.22067... ,⁴¹41 Ahluwalia M, Kaur A. Modulatory role of GSTT1 and GSTM1 in Punjabi agricultural workers exposed to pesticides. Environ Sci Pollut Res Int. 2018;25(12):11981-11986. DOI: https://doi.org/10.1007/s11356-018-1459-7
https://doi.org/10.1007/s11356-018-1459-... ,⁴²42 Benedetti D, Lopes Alderete B, Souza CT, et al. DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides. Mutagenesis. 2018;33(1):87-95. DOI: https://doi.org/10.1093/mutage/gex035
https://doi.org/10.1093/mutage/gex035... ,⁴⁴44 Jacobsen-Pereira CH, Santos CR, Maraslis FT, et al. Markers of genotoxicity and oxidative stress in farmers exposed to pesticides. Ecotoxicol Environ Saf. 2018;148:177-183. DOI: https://doi.org/10.1016/j.ecoenv.2017.10.004
https://doi.org/10.1016/j.ecoenv.2017.10... ,⁴⁵45 Tomiazzi JS, Judai MA, Nai GA, et al. Evaluation of genotoxic effects in Brazilian agricultural workers exposed to pesticides and cigarette smoke using machine-learning algorithms. Environ Sci Pollut Res Int. 2018;25(2):1259-1269. DOI: https://doi.org/10.1007/s11356-017-0496-y
https://doi.org/10.1007/s11356-017-0496-... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... and/or oxidative stress⁴²42 Benedetti D, Lopes Alderete B, Souza CT, et al. DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides. Mutagenesis. 2018;33(1):87-95. DOI: https://doi.org/10.1093/mutage/gex035
https://doi.org/10.1093/mutage/gex035... ,⁴⁴44 Jacobsen-Pereira CH, Santos CR, Maraslis FT, et al. Markers of genotoxicity and oxidative stress in farmers exposed to pesticides. Ecotoxicol Environ Saf. 2018;148:177-183. DOI: https://doi.org/10.1016/j.ecoenv.2017.10.004
https://doi.org/10.1016/j.ecoenv.2017.10... ,⁴⁵45 Tomiazzi JS, Judai MA, Nai GA, et al. Evaluation of genotoxic effects in Brazilian agricultural workers exposed to pesticides and cigarette smoke using machine-learning algorithms. Environ Sci Pollut Res Int. 2018;25(2):1259-1269. DOI: https://doi.org/10.1007/s11356-017-0496-y
https://doi.org/10.1007/s11356-017-0496-... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... ,⁵⁵55 Salazar-Flores J, Pacheco-Moisés FP, Ortiz GG, et al. Occupational exposure to organophosphorus and carbamates in farmers in La Cienega, Jalisco, Mexico: oxidative stress and membrane fluidity markers. J Occup Med Toxicol. 2020;15:32. DOI: https://doi.org/10.1186/s12995-020-00283-y
https://doi.org/10.1186/s12995-020-00283... , in addition to metabolic disorders⁴⁶46 Ch R, Singh AK, Pathak MK, et al. Saliva and urine metabolic profiling reveals altered amino acid and energy metabolism in male farmers exposed to pesticides in Madhya Pradesh State, India. Chemosphere. 2019;226:636-644. DOI: https://doi.org/10.1016/j.chemosphere.2019.03.157
https://doi.org/10.1016/j.chemosphere.20... and immunological profile⁵³53 Jacobsen-Pereira CH, Cardoso CC, Gehlen TC, et al. Immune response of Brazilian farmers exposed to multiple pesticides. Ecotoxicol Environ Saf. 2020;202:110912. DOI: https://doi.org/10.1016/j.ecoenv.2020.110912
https://doi.org/10.1016/j.ecoenv.2020.11... , all factors that contribute to the development of cancer.

Other studies are aimed at specific types of cancer, such as breast⁴⁷47 Mills PK, Dodge JL, Bush J, et al. Agricultural Exposures and Breast Cancer Among Latina in the San Joaquin Valley of California. J Occup Environ Med. 2019;61(7):552-558. DOI: https://doi.org/10.1097/JOM.0000000000001598
https://doi.org/10.1097/JOM.000000000000... , prostate³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,⁴⁰40 Rusiecki JA, Beane Freeman LE, Bonner MR, et al. High pesticide exposure events and DNA methylation among pesticide applicators in the agricultural health study. Environ Mol Mutagen. 2017;58(1):19-29. DOI: https://doi.org/10.1002/em.22067
https://doi.org/10.1002/em.22067... , central nervous system²⁷27 Miranda-Filho AL, Monteiro GT, Meyer A. Brain cancer mortality among farm workers of the State of Rio de Janeiro, Brazil: a population-based case-control study, 1996-2005. Int J Hyg Environ Health. 2012;215(5):496-501. DOI: https://doi.org/10.1016/j.ijheh.2011.10.007
https://doi.org/10.1016/j.ijheh.2011.10.... ,³⁷37 Fallahi P, Foddis R, Cristaudo A, et al. High risk of brain tumors in farmers: a mini-review of the literature, and report of the results of a case control study. Clin Ter. 2017;168(5):e290-e292. DOI: https://doi.org/10.7417/T.2017.2022
https://doi.org/10.7417/T.2017.2022... ,⁴⁹49 Piel C, Pouchieu C, Carles C, et al. Agricultural exposures to carbamate herbicides and fungicides and central nervous system tumour incidence in the cohort AGRICAN. Environ Int. 2019;130:104876. DOI: https://doi.org/10.1016/j.envint.2019.05.070
https://doi.org/10.1016/j.envint.2019.05... , lung³²32 Jones RR, Barone-Adesi F, Koutros S, et al. Incidence of solid tumours among pesticide applicators exposed to the organophosphate insecticide diazinon in the Agricultural Health Study: an updated analysis. Occup Environ Med. 2015;72(7):496-503. DOI: https://doi.org/10.1136/oemed-2014-102728
https://doi.org/10.1136/oemed-2014-10272... ,³⁶36 Bonner MR, Freeman LE, Hoppin JA, et al. Occupational Exposure to Pesticides and the Incidence of Lung Cancer in the Agricultural Health Study. Environ Health Perspect. 2017;125(4):544-551. DOI: https://doi.org/10.1289/EHP456
https://doi.org/10.1289/EHP456... ,⁴³43 Boulanger M, Tual S, Lemarchand C, et al. Lung cancer risk and occupational exposures in crop farming: results from the AGRIculture and CANcer (AGRICAN) cohort. Occup Environ Med. 2018;75(11):776-785. DOI: https://doi.org/10.1136/oemed-2017-104976
https://doi.org/10.1136/oemed-2017-10497... , in addition to risk or incidence for any type of cancer³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... ,⁴¹41 Ahluwalia M, Kaur A. Modulatory role of GSTT1 and GSTM1 in Punjabi agricultural workers exposed to pesticides. Environ Sci Pollut Res Int. 2018;25(12):11981-11986. DOI: https://doi.org/10.1007/s11356-018-1459-7
https://doi.org/10.1007/s11356-018-1459-... ,⁴⁸48 Ordoñez-Beltrán V, Frías-Moreno MN, Parra-Acosta H, et al. Estudio sobre el uso de plaguicidas y su posible relación con daños a la salud. Rev Toxicol [Internet]. 2019 [acesso em 2024 fev 1];36(2):148-153. Disponível em: https://dialnet.unirioja.es/servlet/articulo?codigo=7180172
https://dialnet.unirioja.es/servlet/arti... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... .

There is a diversity of pesticides used by farmers, with results associated with the use of products in isolation or in combination. The use of different types of pesticides has been shown to be associated with lung³²32 Jones RR, Barone-Adesi F, Koutros S, et al. Incidence of solid tumours among pesticide applicators exposed to the organophosphate insecticide diazinon in the Agricultural Health Study: an updated analysis. Occup Environ Med. 2015;72(7):496-503. DOI: https://doi.org/10.1136/oemed-2014-102728
https://doi.org/10.1136/oemed-2014-10272... ,³⁶36 Bonner MR, Freeman LE, Hoppin JA, et al. Occupational Exposure to Pesticides and the Incidence of Lung Cancer in the Agricultural Health Study. Environ Health Perspect. 2017;125(4):544-551. DOI: https://doi.org/10.1289/EHP456
https://doi.org/10.1289/EHP456... , hematological³⁴34 Presutti R, Harris SA, Kachuri L, et al. Pesticide exposures and the risk of multiple myeloma in men: An analysis of the North American Pooled Project. Int J Cancer. 2016;139(8):1703-1714. DOI: https://doi.org/10.1002/ijc.30218
https://doi.org/10.1002/ijc.30218... , breast⁴⁷47 Mills PK, Dodge JL, Bush J, et al. Agricultural Exposures and Breast Cancer Among Latina in the San Joaquin Valley of California. J Occup Environ Med. 2019;61(7):552-558. DOI: https://doi.org/10.1097/JOM.0000000000001598
https://doi.org/10.1097/JOM.000000000000... and prostate⁵⁴54 Pardo LA, Beane Freeman LE, Lerro CC, et al. Pesticide exposure and risk of aggressive prostate cancer among private pesticide applicators. Environ Health. 2020;19(1):30. DOI: https://doi.org/10.1186/s12940-020-00583-0
https://doi.org/10.1186/s12940-020-00583... cancer.

Discussion

It is important to highlight the following cohorts: the Agricultural Health Study (AHS), in the USA, of licensed pesticide applicators enrolled between 1993 and 1997; and the AGRIculture and CANcer (AGRICAN), in France, of members of the agricultural health insurance scheme, enrolled between 2005 and 2007, from which several studies in this review were derived. Cohort studies are the most capable of raising etiological hypotheses, providing incidence and risk measures, and, for the most part, are based on groups exposed to a risk factor presumed to be the cause of a disease to be detected in the future⁵⁶56 Madalosso G, Alexandre LBSP. A aplicação da metodologia de pesquisa epidemiológica. In: Alexandre LBSP. Epidemiologia aplicada nos serviços de saúde. São Paulo: Martinari; 2012. p. 89-112.. In this context, they constitute predictive factors that, if controlled, can delay or even prevent the onset of a disease.

Brazil stands out for its large agricultural market. The April 2023 estimate for the Brazilian harvest of cereals, legumes, and oilseeds reached 302.1 million tons, which corresponds to an increase of 14.8% compared to 2022, growth of 39.0 million tons. Rice, corn, and soybeans are the three main products in this group, which together account for 92.3% of the production estimate and occupy 87.3% of the area expected to be harvested⁵⁷57 Instituto Brasileiro de Geografia e Estatística. Levantamento Sistemático da Produção Agrícola Estatística da Produção Agrícola [Internet]. Rio de Janeiro: IBGE; 2023 [acesso em 2023 maio 12]. Disponível em: https://biblioteca.ibge.gov.br/visualizacao/periodicos/2415/epag_2023_abr.pdf
https://biblioteca.ibge.gov.br/visualiza... . Soybeans are the crop with the highest use of pesticides and accounted for 55.69% of total pesticide sales⁵⁸58 Carbonar A, Andrade A, Lenat A, et al. Impactos do aumento de impostos de defensivos agrícolas [Internet]. Estudo realizado para o Sindicato Nacional da Indústria de Produtos para Defesa Vegetal - SINDIVEG. Brasília, DF: Barral M Jorge Consultores Associados; 2017 [acesso em 2023 ago 11]. 160 p. Disponível em: https://pt.scribd.com/document/416339142/evento-206-3
https://pt.scribd.com/document/416339142... . The number of hectares cultivated and large monocultures are responsible for the consumption of most pesticides used in the country, which justifies the significant number of studies developed and the warning produced by the Brazilian Association of Public Health (ABRASCO)⁵5 Carneiro FF, Augusto LGS, Rigotto ARM, et al. Dossiê ABRASCO: um alerta sobre os impactos dos agro-tóxicos na saúde [Internet]. Rio de Janeiro, São Paulo: Expressão Popular; 2015 [acesso em 2024 fev 1]. 628 p. Disponível em: https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/
https://abrasco.org.br/download/dossie-a... regarding the cumulative and gradually increased use of pesticides and their consequent risks, including the development of different types of cancer.

It can be seen that most studies presented statistical significance for the association between pesticides and cancer, 81% (n = 29). The predominant number of articles that validate the existence of this relationship points to the increased risk of cancer for those exposed to these products.

In the articles analyzed, the association between cancer development and pesticide use highlighted factors such as male gender²⁷27 Miranda-Filho AL, Monteiro GT, Meyer A. Brain cancer mortality among farm workers of the State of Rio de Janeiro, Brazil: a population-based case-control study, 1996-2005. Int J Hyg Environ Health. 2012;215(5):496-501. DOI: https://doi.org/10.1016/j.ijheh.2011.10.007
https://doi.org/10.1016/j.ijheh.2011.10.... ,²⁸28 Boccolini PMM, Asmus CIRF, Chrisman JR, et al. Stomach cancer mortality among agricultural workers: results from a death certificate-based case-control study. Cad Saúde Colet. 2014;22(1):86-92. DOI: https://doi.org/10.1590/1414-462X201400010013
https://doi.org/10.1590/1414-462X2014000... ,²⁹29 Amr S, Dawson R, Saleh DA, et al. Pesticides, gene polymorphisms, and bladder cancer among Egyptian agricultural workers. Arch Environ Occup Health. 2015;70(1):19-26. DOI: https://doi.org/10.1080/19338244.2013.853646
https://doi.org/10.1080/19338244.2013.85... ,³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... , being an agricultural worker²⁸28 Boccolini PMM, Asmus CIRF, Chrisman JR, et al. Stomach cancer mortality among agricultural workers: results from a death certificate-based case-control study. Cad Saúde Colet. 2014;22(1):86-92. DOI: https://doi.org/10.1590/1414-462X201400010013
https://doi.org/10.1590/1414-462X2014000... ,³⁵35 Salerno C, Carcagnì A, Sacco S, et al. An Italian population-based case-control study on the association between farming and cancer: Are pesticides a plausible risk factor?. Arch Environ Occup Health. 2016;71(3):147-156. DOI: https://doi.org/10.1080/19338244.2015.1027808
https://doi.org/10.1080/19338244.2015.10... ,³⁷37 Fallahi P, Foddis R, Cristaudo A, et al. High risk of brain tumors in farmers: a mini-review of the literature, and report of the results of a case control study. Clin Ter. 2017;168(5):e290-e292. DOI: https://doi.org/10.7417/T.2017.2022
https://doi.org/10.7417/T.2017.2022... ,³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... , frequency and duration of exposure to pesticides²⁹29 Amr S, Dawson R, Saleh DA, et al. Pesticides, gene polymorphisms, and bladder cancer among Egyptian agricultural workers. Arch Environ Occup Health. 2015;70(1):19-26. DOI: https://doi.org/10.1080/19338244.2013.853646
https://doi.org/10.1080/19338244.2013.85... ,³⁰30 Andreotti G, Hoppin JA, Hou L, et al. Pesticide Use and Relative Leukocyte Telomere Length in the Agricultural Health Study. PLoS One. 2015;10(7):e0133382. DOI: https://doi.org/10.1371/journal.pone.0133382
https://doi.org/10.1371/journal.pone.013... ,³¹31 Gómez-Martín A, Altakroni B, Lozano-Paniagua D, et al. Increased N7-methyldeoxyguanosine DNA adducts after occupational exposure to pesticides and influence of genetic polymorphisms of paraoxonase-1 and glutathione S-transferase M1 and T1. Environ Mol Mutagen. 2015;56(5):437-445. DOI: https://doi.org/10.1002/em.21929
https://doi.org/10.1002/em.21929... ,⁴³43 Boulanger M, Tual S, Lemarchand C, et al. Lung cancer risk and occupational exposures in crop farming: results from the AGRIculture and CANcer (AGRICAN) cohort. Occup Environ Med. 2018;75(11):776-785. DOI: https://doi.org/10.1136/oemed-2017-104976
https://doi.org/10.1136/oemed-2017-10497... , specific types of pesticides³²32 Jones RR, Barone-Adesi F, Koutros S, et al. Incidence of solid tumours among pesticide applicators exposed to the organophosphate insecticide diazinon in the Agricultural Health Study: an updated analysis. Occup Environ Med. 2015;72(7):496-503. DOI: https://doi.org/10.1136/oemed-2014-102728
https://doi.org/10.1136/oemed-2014-10272... ,³⁴34 Presutti R, Harris SA, Kachuri L, et al. Pesticide exposures and the risk of multiple myeloma in men: An analysis of the North American Pooled Project. Int J Cancer. 2016;139(8):1703-1714. DOI: https://doi.org/10.1002/ijc.30218
https://doi.org/10.1002/ijc.30218... ,³⁶36 Bonner MR, Freeman LE, Hoppin JA, et al. Occupational Exposure to Pesticides and the Incidence of Lung Cancer in the Agricultural Health Study. Environ Health Perspect. 2017;125(4):544-551. DOI: https://doi.org/10.1289/EHP456
https://doi.org/10.1289/EHP456... ,⁴⁷47 Mills PK, Dodge JL, Bush J, et al. Agricultural Exposures and Breast Cancer Among Latina in the San Joaquin Valley of California. J Occup Environ Med. 2019;61(7):552-558. DOI: https://doi.org/10.1097/JOM.0000000000001598
https://doi.org/10.1097/JOM.000000000000... ,⁵⁴54 Pardo LA, Beane Freeman LE, Lerro CC, et al. Pesticide exposure and risk of aggressive prostate cancer among private pesticide applicators. Environ Health. 2020;19(1):30. DOI: https://doi.org/10.1186/s12940-020-00583-0
https://doi.org/10.1186/s12940-020-00583... and the use of pesticides³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,⁴⁷47 Mills PK, Dodge JL, Bush J, et al. Agricultural Exposures and Breast Cancer Among Latina in the San Joaquin Valley of California. J Occup Environ Med. 2019;61(7):552-558. DOI: https://doi.org/10.1097/JOM.0000000000001598
https://doi.org/10.1097/JOM.000000000000... ,⁴⁸48 Ordoñez-Beltrán V, Frías-Moreno MN, Parra-Acosta H, et al. Estudio sobre el uso de plaguicidas y su posible relación con daños a la salud. Rev Toxicol [Internet]. 2019 [acesso em 2024 fev 1];36(2):148-153. Disponível em: https://dialnet.unirioja.es/servlet/articulo?codigo=7180172
https://dialnet.unirioja.es/servlet/arti... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... as variables that predispose the onset of this disease. The vast majority of studies indicated exposure to pesticides³⁵35 Salerno C, Carcagnì A, Sacco S, et al. An Italian population-based case-control study on the association between farming and cancer: Are pesticides a plausible risk factor?. Arch Environ Occup Health. 2016;71(3):147-156. DOI: https://doi.org/10.1080/19338244.2015.1027808
https://doi.org/10.1080/19338244.2015.10... ,⁴⁰40 Rusiecki JA, Beane Freeman LE, Bonner MR, et al. High pesticide exposure events and DNA methylation among pesticide applicators in the agricultural health study. Environ Mol Mutagen. 2017;58(1):19-29. DOI: https://doi.org/10.1002/em.22067
https://doi.org/10.1002/em.22067... ,⁴¹41 Ahluwalia M, Kaur A. Modulatory role of GSTT1 and GSTM1 in Punjabi agricultural workers exposed to pesticides. Environ Sci Pollut Res Int. 2018;25(12):11981-11986. DOI: https://doi.org/10.1007/s11356-018-1459-7
https://doi.org/10.1007/s11356-018-1459-... ,⁴²42 Benedetti D, Lopes Alderete B, Souza CT, et al. DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides. Mutagenesis. 2018;33(1):87-95. DOI: https://doi.org/10.1093/mutage/gex035
https://doi.org/10.1093/mutage/gex035... ,⁴⁴44 Jacobsen-Pereira CH, Santos CR, Maraslis FT, et al. Markers of genotoxicity and oxidative stress in farmers exposed to pesticides. Ecotoxicol Environ Saf. 2018;148:177-183. DOI: https://doi.org/10.1016/j.ecoenv.2017.10.004
https://doi.org/10.1016/j.ecoenv.2017.10... ,⁴⁵45 Tomiazzi JS, Judai MA, Nai GA, et al. Evaluation of genotoxic effects in Brazilian agricultural workers exposed to pesticides and cigarette smoke using machine-learning algorithms. Environ Sci Pollut Res Int. 2018;25(2):1259-1269. DOI: https://doi.org/10.1007/s11356-017-0496-y
https://doi.org/10.1007/s11356-017-0496-... ,⁴⁶46 Ch R, Singh AK, Pathak MK, et al. Saliva and urine metabolic profiling reveals altered amino acid and energy metabolism in male farmers exposed to pesticides in Madhya Pradesh State, India. Chemosphere. 2019;226:636-644. DOI: https://doi.org/10.1016/j.chemosphere.2019.03.157
https://doi.org/10.1016/j.chemosphere.20... ,⁴⁹49 Piel C, Pouchieu C, Carles C, et al. Agricultural exposures to carbamate herbicides and fungicides and central nervous system tumour incidence in the cohort AGRICAN. Environ Int. 2019;130:104876. DOI: https://doi.org/10.1016/j.envint.2019.05.070
https://doi.org/10.1016/j.envint.2019.05... ,⁵⁰50 Saad-Hussein A, Beshir S, Taha MM, et al. Early prediction of liver carcinogenicity due to occupational exposure to pesticides. Mutat Res Genet Toxicol Environ Mutagen. 2019;838:46-53. DOI: https://doi.org/10.1016/j.mrgentox.2018.12.004
https://doi.org/10.1016/j.mrgentox.2018.... ,⁵¹51 Cepeda S, Forero-Castro M, Cárdenas-Nieto D, et al. Chromosomal instability in farmers exposed to pesticides: High prevalence of clonal and non-clonal chromosomal alterations. Risk Manag Healthc Policy. 2020;13:97-110. DOI: https://doi.org/10.2147/RMHP.S230953
https://doi.org/10.2147/RMHP.S230953... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... ,⁵³53 Jacobsen-Pereira CH, Cardoso CC, Gehlen TC, et al. Immune response of Brazilian farmers exposed to multiple pesticides. Ecotoxicol Environ Saf. 2020;202:110912. DOI: https://doi.org/10.1016/j.ecoenv.2020.110912
https://doi.org/10.1016/j.ecoenv.2020.11... ,⁵⁵55 Salazar-Flores J, Pacheco-Moisés FP, Ortiz GG, et al. Occupational exposure to organophosphorus and carbamates in farmers in La Cienega, Jalisco, Mexico: oxidative stress and membrane fluidity markers. J Occup Med Toxicol. 2020;15:32. DOI: https://doi.org/10.1186/s12995-020-00283-y
https://doi.org/10.1186/s12995-020-00283... as a cause or determining factor for cellular damage contributing to the onset of cancer.

Thus, being a farmer confers a higher risk of developing cancer compared to non-agricultural workers²⁸28 Boccolini PMM, Asmus CIRF, Chrisman JR, et al. Stomach cancer mortality among agricultural workers: results from a death certificate-based case-control study. Cad Saúde Colet. 2014;22(1):86-92. DOI: https://doi.org/10.1590/1414-462X201400010013
https://doi.org/10.1590/1414-462X2014000... ,³⁷37 Fallahi P, Foddis R, Cristaudo A, et al. High risk of brain tumors in farmers: a mini-review of the literature, and report of the results of a case control study. Clin Ter. 2017;168(5):e290-e292. DOI: https://doi.org/10.7417/T.2017.2022
https://doi.org/10.7417/T.2017.2022... , that is, the greater the exposure, the greater the risk²⁹29 Amr S, Dawson R, Saleh DA, et al. Pesticides, gene polymorphisms, and bladder cancer among Egyptian agricultural workers. Arch Environ Occup Health. 2015;70(1):19-26. DOI: https://doi.org/10.1080/19338244.2013.853646
https://doi.org/10.1080/19338244.2013.85... . Several studies that confirm the relationship between exposure to pesticides and the risk of developing cancer indicate that this is increased when farmers do not use the personal protective equipment recommended in each country³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,⁴²42 Benedetti D, Lopes Alderete B, Souza CT, et al. DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides. Mutagenesis. 2018;33(1):87-95. DOI: https://doi.org/10.1093/mutage/gex035
https://doi.org/10.1093/mutage/gex035... ,⁴⁴44 Jacobsen-Pereira CH, Santos CR, Maraslis FT, et al. Markers of genotoxicity and oxidative stress in farmers exposed to pesticides. Ecotoxicol Environ Saf. 2018;148:177-183. DOI: https://doi.org/10.1016/j.ecoenv.2017.10.004
https://doi.org/10.1016/j.ecoenv.2017.10... ,⁴⁷47 Mills PK, Dodge JL, Bush J, et al. Agricultural Exposures and Breast Cancer Among Latina in the San Joaquin Valley of California. J Occup Environ Med. 2019;61(7):552-558. DOI: https://doi.org/10.1097/JOM.0000000000001598
https://doi.org/10.1097/JOM.000000000000... ,⁴⁸48 Ordoñez-Beltrán V, Frías-Moreno MN, Parra-Acosta H, et al. Estudio sobre el uso de plaguicidas y su posible relación con daños a la salud. Rev Toxicol [Internet]. 2019 [acesso em 2024 fev 1];36(2):148-153. Disponível em: https://dialnet.unirioja.es/servlet/articulo?codigo=7180172
https://dialnet.unirioja.es/servlet/arti... ,⁵²52 Hutter HP, Poteser M, Lemmerer K, et al. Indicators of genotoxicity in farmers and laborers of ecological and conventional banana plantations in Ecuador. Int J Environ Res Public Health. 2020;17(4):1435. DOI: https://doi.org/10.3390/ijerph17041435
https://doi.org/10.3390/ijerph17041435... ,⁵³53 Jacobsen-Pereira CH, Cardoso CC, Gehlen TC, et al. Immune response of Brazilian farmers exposed to multiple pesticides. Ecotoxicol Environ Saf. 2020;202:110912. DOI: https://doi.org/10.1016/j.ecoenv.2020.110912
https://doi.org/10.1016/j.ecoenv.2020.11... . The number of studies that show the non-use of this protective equipment as one of the determinants of the development of cancer allows us to state that this is a behavior that needs to be changed worldwide (regardless of the level of development), through appropriate and effective educational actions and technological support.

In addition to exposure to pesticides, the professional activities carried out by farmers at each stage of planting, such as preparing the spray, applying it, spraying it, and harvesting³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,³⁷37 Fallahi P, Foddis R, Cristaudo A, et al. High risk of brain tumors in farmers: a mini-review of the literature, and report of the results of a case control study. Clin Ter. 2017;168(5):e290-e292. DOI: https://doi.org/10.7417/T.2017.2022
https://doi.org/10.7417/T.2017.2022... , as well as their lifestyle³⁰30 Andreotti G, Hoppin JA, Hou L, et al. Pesticide Use and Relative Leukocyte Telomere Length in the Agricultural Health Study. PLoS One. 2015;10(7):e0133382. DOI: https://doi.org/10.1371/journal.pone.0133382
https://doi.org/10.1371/journal.pone.013... ,³¹31 Gómez-Martín A, Altakroni B, Lozano-Paniagua D, et al. Increased N7-methyldeoxyguanosine DNA adducts after occupational exposure to pesticides and influence of genetic polymorphisms of paraoxonase-1 and glutathione S-transferase M1 and T1. Environ Mol Mutagen. 2015;56(5):437-445. DOI: https://doi.org/10.1002/em.21929
https://doi.org/10.1002/em.21929... ,³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,³⁶36 Bonner MR, Freeman LE, Hoppin JA, et al. Occupational Exposure to Pesticides and the Incidence of Lung Cancer in the Agricultural Health Study. Environ Health Perspect. 2017;125(4):544-551. DOI: https://doi.org/10.1289/EHP456
https://doi.org/10.1289/EHP456... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... ,⁴⁵45 Tomiazzi JS, Judai MA, Nai GA, et al. Evaluation of genotoxic effects in Brazilian agricultural workers exposed to pesticides and cigarette smoke using machine-learning algorithms. Environ Sci Pollut Res Int. 2018;25(2):1259-1269. DOI: https://doi.org/10.1007/s11356-017-0496-y
https://doi.org/10.1007/s11356-017-0496-... ,⁵¹51 Cepeda S, Forero-Castro M, Cárdenas-Nieto D, et al. Chromosomal instability in farmers exposed to pesticides: High prevalence of clonal and non-clonal chromosomal alterations. Risk Manag Healthc Policy. 2020;13:97-110. DOI: https://doi.org/10.2147/RMHP.S230953
https://doi.org/10.2147/RMHP.S230953... ,⁵⁴54 Pardo LA, Beane Freeman LE, Lerro CC, et al. Pesticide exposure and risk of aggressive prostate cancer among private pesticide applicators. Environ Health. 2020;19(1):30. DOI: https://doi.org/10.1186/s12940-020-00583-0
https://doi.org/10.1186/s12940-020-00583... and environmental characteristics, may be factors that increase the risk of the disease²⁷27 Miranda-Filho AL, Monteiro GT, Meyer A. Brain cancer mortality among farm workers of the State of Rio de Janeiro, Brazil: a population-based case-control study, 1996-2005. Int J Hyg Environ Health. 2012;215(5):496-501. DOI: https://doi.org/10.1016/j.ijheh.2011.10.007
https://doi.org/10.1016/j.ijheh.2011.10.... ,²⁸28 Boccolini PMM, Asmus CIRF, Chrisman JR, et al. Stomach cancer mortality among agricultural workers: results from a death certificate-based case-control study. Cad Saúde Colet. 2014;22(1):86-92. DOI: https://doi.org/10.1590/1414-462X201400010013
https://doi.org/10.1590/1414-462X2014000... . Other studies, in smaller numbers, have not observed any difference in the incidence of cancer between farmers and the general population³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... .

Several authors conclude that exposure to pesticides increases the chance of developing cancer²⁹29 Amr S, Dawson R, Saleh DA, et al. Pesticides, gene polymorphisms, and bladder cancer among Egyptian agricultural workers. Arch Environ Occup Health. 2015;70(1):19-26. DOI: https://doi.org/10.1080/19338244.2013.853646
https://doi.org/10.1080/19338244.2013.85... ,³²32 Jones RR, Barone-Adesi F, Koutros S, et al. Incidence of solid tumours among pesticide applicators exposed to the organophosphate insecticide diazinon in the Agricultural Health Study: an updated analysis. Occup Environ Med. 2015;72(7):496-503. DOI: https://doi.org/10.1136/oemed-2014-102728
https://doi.org/10.1136/oemed-2014-10272... ,³³33 Lemarchand C, Tual S, Levêque-Morlais N, et al. Cancer incidence in the AGRICAN cohort study (2005-2011). Cancer Epidemiol. 2017;49:175-185. DOI: https://doi.org/10.1016/j.canep.2017.06.003
https://doi.org/10.1016/j.canep.2017.06.... ,³⁴34 Presutti R, Harris SA, Kachuri L, et al. Pesticide exposures and the risk of multiple myeloma in men: An analysis of the North American Pooled Project. Int J Cancer. 2016;139(8):1703-1714. DOI: https://doi.org/10.1002/ijc.30218
https://doi.org/10.1002/ijc.30218... ,⁴⁹49 Piel C, Pouchieu C, Carles C, et al. Agricultural exposures to carbamate herbicides and fungicides and central nervous system tumour incidence in the cohort AGRICAN. Environ Int. 2019;130:104876. DOI: https://doi.org/10.1016/j.envint.2019.05.070
https://doi.org/10.1016/j.envint.2019.05... or present them as the main inducer of tumors³⁷37 Fallahi P, Foddis R, Cristaudo A, et al. High risk of brain tumors in farmers: a mini-review of the literature, and report of the results of a case control study. Clin Ter. 2017;168(5):e290-e292. DOI: https://doi.org/10.7417/T.2017.2022
https://doi.org/10.7417/T.2017.2022... . In this sense, research must be developed to produce substances that are increasingly less aggressive to the environment and to living beings in general, in addition to producing international protocols that prohibit extremely toxic pesticides from being used worldwide⁵5 Carneiro FF, Augusto LGS, Rigotto ARM, et al. Dossiê ABRASCO: um alerta sobre os impactos dos agro-tóxicos na saúde [Internet]. Rio de Janeiro, São Paulo: Expressão Popular; 2015 [acesso em 2024 fev 1]. 628 p. Disponível em: https://abrasco.org.br/download/dossie-abrasco-um-alerta-sobre-os-impactos-dos-agrotoxicos-na-saude/
https://abrasco.org.br/download/dossie-a... .

It is important to highlight that 12 of the 29 studies analyzed made adjustments for risk factors for the development of cancer. This is important to increase the quality of the evidence and attests to the researchers' concern with the accuracy of the data presented. Thus, due to the complexity of the topic in question, the adjustment of variables allows analyses that reinforce the evidence between occupational exposure and the development of the disease²⁸28 Boccolini PMM, Asmus CIRF, Chrisman JR, et al. Stomach cancer mortality among agricultural workers: results from a death certificate-based case-control study. Cad Saúde Colet. 2014;22(1):86-92. DOI: https://doi.org/10.1590/1414-462X201400010013
https://doi.org/10.1590/1414-462X2014000... ,²⁹29 Amr S, Dawson R, Saleh DA, et al. Pesticides, gene polymorphisms, and bladder cancer among Egyptian agricultural workers. Arch Environ Occup Health. 2015;70(1):19-26. DOI: https://doi.org/10.1080/19338244.2013.853646
https://doi.org/10.1080/19338244.2013.85... ,⁴⁹49 Piel C, Pouchieu C, Carles C, et al. Agricultural exposures to carbamate herbicides and fungicides and central nervous system tumour incidence in the cohort AGRICAN. Environ Int. 2019;130:104876. DOI: https://doi.org/10.1016/j.envint.2019.05.070
https://doi.org/10.1016/j.envint.2019.05... . The most commonly used adjustments were for sociodemographic data: age, sex, ethnicity, education; smoking and alcohol habits; and family history of cancer.

It is worth noting that skin cancer, such as melanoma, non-melanoma and lip cancer, were evidenced in three of the studies³⁵35 Salerno C, Carcagnì A, Sacco S, et al. An Italian population-based case-control study on the association between farming and cancer: Are pesticides a plausible risk factor?. Arch Environ Occup Health. 2016;71(3):147-156. DOI: https://doi.org/10.1080/19338244.2015.1027808
https://doi.org/10.1080/19338244.2015.10... ,³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... ,³⁹39 Lemarchand C, Tual S, Boulanger M, et al. Prostate cancer risk among French farmers in the AGRICAN cohort. Scand J Work Environ Health. 2016;42(2):144-152. DOI: https://doi.org/10.5271/sjweh.3552
https://doi.org/10.5271/sjweh.3552... , but were not considered in this analysis, due to the strong relationship with sun exposure³⁸38 Kachuri L, Harris MA, MacLeod JS, et al. Cancer risks in a population-based study of 70,570 agricultural workers: results from the Canadian census health and Environment cohort (CanCHEC). BMC Cancer. 2017;17(1):343. DOI: https://doi.org/10.1186/s12885-017-3346-x
https://doi.org/10.1186/s12885-017-3346-... , which may result in another analysis bias, compromising the results obtained in the aforementioned studies.

Conclusions

The relationship between the use of pesticides and the development of cancer has been the subject of several studies on different continents over the last decade. For the present study, were selected 36 bibliographies, of which 81% (n = 29) obtained statistical significance for this relationship, which demonstrates the possibility of a cause-and-effect link, especially with adjustments for confounding factors.

Thus, the data set of this scoping review shows that being a farmer and being exposed to pesticides confers a greater risk of developing cancer compared to unexposed individuals.

Different types of cancer have been reported, in particular lung, hematopoietic and prostate cancer. It is also important to highlight that farmers used a variety of products and combinations of compounds.

In addition to the types of cancer highlighted, n = 14 (48%) studies indicated biomarkers for early cancer prediction. Therefore, there is evidence of the differentiations (or cellular impairment) that the products can cause in the human body, especially in relation to cellular metabolism, such as DNA damage and oxidative stress.

Case-control and cohort studies dominated the review scenario, using inferential statistics with several different types of statistical tests. There were a diverse number of participants in each study.

It is important to emphasize that it is the responsibility of health professionals to relate the various risk factors that involve the health condition of users, such as the profession of being a farmer. Professionals must be able to identify, analyze and implement measures that minimize risks based on the evidence found and knowledge of professional practice, as well as to diagnose early and offer appropriate treatment to this population.

Given the problem involving public health due to the incorrect use of pesticides, Public Policies need to be implemented in order to control and guarantee safety in the handling of products by farmers, considering that, according to the literature, the relationship between the use of pesticides and the development of cancer is established.

References

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