The use of pesticides and the development of cancer in farmers: A scoping reviewABSTRACT
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.
RESUMO
Diante da problemática que envolve a complexa relação entre o uso de agrotóxicos e o aparecimento de câncer, diversos estudos vêm sendo desenvolvidos no mundo em busca de evidências que a comprovem. Objetivou-se analisar a relação entre a utilização de agrotóxicos e o aparecimento de câncer em agricultores, segundo a bibliografia especializada. Trata-se de uma revisão de escopo. A busca foi realizada em três bases de dados, e os artigos foram analisados por dois pesquisadores e um terceiro, para as discordancias. Foi testado o valor de Kappa de Cohen para avaliar concordância quanto aos dados extraídos dos estudos. Um total de 29 bibliografias compuseram a amostra. Os estudos foram provenientes de cinco continentes. Pesquisas de caso-controle e coorte dominaram o cenário da revisão, utilizando estatística inferencial com diferentes tipos de testes estatísticos. Uma variedade de tipologias de câncer foi estudada, e grande parte dos artigos apontou para uma predisposição ao câncer, remetendo a biomarcadores para previsão precoce dessa doença crônica. Conclui-se que ser agricultor e estar exposto aos agrotóxicos conferem um maior risco de desenvolvimento de câncer em relação aos não expostos.
PALAVRAS-CHAVES
Agroquímicos; Neoplasias; Agricultores; Risco à saúde humana; Saúde ambiental
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 beings1. They are used to maintain control or eliminate insects, larvae, weeds and other pests that can affect plantations2,3, 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%4. 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 world5, 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 regions6.
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 use5,7.
Chronic damage resulting from exposure includes different types of cancer8. 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 body8.
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 Health9 and by different authors2,5,10. Some of these studies seek evidence that indicates the relationship between specific types of pesticides and genetic mutations11,12 or the carcinogenic potential of certain types of products13,14; others still research the relationship between the use of pesticides and cancer morbidity and mortality rates15,16. It is important to emphasize that the probability increases when these farmers do not use PPE properly17.
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 review18,19,20 was conducted following the PRISMA-ScR (Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews) approach21. The study protocol for the scoping review was registered on the Open Science Framework (OSF) platform on August 22, 202222.
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 evaluators23,24. A Kappa value between 0.6 and 0.825 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 interpretation26.
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 damage30,40,41,42,44,45,52 and/or oxidative stress42,44,45,52,55, in addition to metabolic disorders46 and immunological profile53, all factors that contribute to the development of cancer.
Other studies are aimed at specific types of cancer, such as breast47, prostate33,40, central nervous system27,37,49, lung32,36,43, in addition to risk or incidence for any type of cancer38,39,41,48,52.
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 lung32,36, hematological34, breast47 and prostate54 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 future56. 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 harvested57. Soybeans are the crop with the highest use of pesticides and accounted for 55.69% of total pesticide sales58. 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)5 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 gender27,28,29,38,39, being an agricultural worker28,35,37,38,39, frequency and duration of exposure to pesticides29,30,31,43, specific types of pesticides32,34,36,47,54 and the use of pesticides33,47,48,52 as variables that predispose the onset of this disease. The vast majority of studies indicated exposure to pesticides35,40,41,42,44,45,46,49,50,51,52,53,55 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 workers28,37, that is, the greater the exposure, the greater the risk29. 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 country33,42,44,47,48,52,53. 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 harvesting33,37, as well as their lifestyle30,31,33,36,39,45,51,54 and environmental characteristics, may be factors that increase the risk of the disease27,28. Other studies, in smaller numbers, have not observed any difference in the incidence of cancer between farmers and the general population38,39.
Several authors conclude that exposure to pesticides increases the chance of developing cancer29,32,33,34,49 or present them as the main inducer of tumors37. 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 worldwide5.
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 disease28,29,49. 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 studies35,38,39, but were not considered in this analysis, due to the strong relationship with sun exposure38, 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.
-
Financial support:
non-existent
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Editor in charge:
Maria Lucia Frizon Rizzotto
Source: Prepared by the authors based on PRISMA-ScR