Exposure to Pesticides and Breast Cancer in an Agricultural Region in Brazil

Abstract

Rural workers are disproportionally exposed to pesticides and might be at an increased risk of developing chronic diseases. Here, we investigated the impact of pesticide exposure on breast cancer (BC) risk and disease profile in rural female workers. This is a case-control study that prospectively included 758 individuals. The study was conducted in the Southwest region of Paraná state in Brazil, a region characterized by family-based agriculture and intensive use of pesticides. We found that this region has a 41% higher BC diagnosis rate and 14% higher BC mortality rate than the mean rates in Brazil, as well as a pesticide trade volume about 6 times higher than the national average. We showed substantial exposure in this population and found that even women who did not work in the fields but performed equipment decontamination and clothes washing of male partners who worked in the fields had urine samples positive for glyphosate, atrazine, and/or 2,4-D. The crude association showed a significantly higher risk of BC among women exposed to pesticides (OR: 1.58, 95% CI 1.18-2.13). Adjusted analyses showed a lower and nonstatistically significant association (OR: 1.30, 95% CI 41 0.87-1.95). Stratification on disease profile showed a significantly higher risk of lymph node metastasis (adjusted OR: 2.19, 95% CI 1.31-3.72) in women exposed to pesticides. Our findings suggest that female populations exposed to pesticides are at a higher risk of developing BC with a more aggressive profile and draw attention to the need to monitor rural populations potentially exposed to pesticides in the field or at home.

Keywords: breast cancer risk; breast metastasis; pesticides.

Figure 1

Breast cancer epidemiology and pesticide trade in Brazil and Paraná state. Mean breast cancer (BC) cases among the 27 Brazilian States from 2009 to 2018. The black bar highlights Paraná state as the fourth state with higher BC incidence. The dotted line represents the mean of BC cases in Brazil (per million people). The comparative mean percentage incidence (B) and mortality (C) are presented for Brazil, Paraná state, and the Paraná Southwest region from 2016 to 2019 (the period of data collection for this study). (D) Map of Brazil showing the mean pesticide trade for each state during the 2016–2019 interval; Paraná state is the third biggest consumer of pesticides. (E) the 27 municipalities from Paraná Southwest regions were distributed according to their pesticide trade for 2016–2019; the darker the color, the larger the amount of pesticides used by the municipality. Acre—AC; Alagoas—AL; Amapá—AP; Amazonas—AM; Bahia—BA; Ceará—CE; Distrito Federal—DF; Espírito Santo—ES; Goiás—GO; Maranhão—MA; Mato Grosso—MT; Mato Grosso do Sul—MS; Minas Gerais—MG; Pará—PA; Paraíba—PB; Paraná—PR; Pernambuco—PE; Piauí—PI; Roraima—RR; Rondônia—RO; Rio de Janeiro—RJ; Rio Grande do Norte—RN; Rio Grande do Sul—RS; Santa Catarina—SC; São Paulo—SP; Sergipe—SE; Tocantins—TO.

Figure 2

Design of the study. A total of 775 women, who attended a public hospital (Francisco Beltrão Cancer Hospital—Ceonc, Francisco Beltrão—Paraná, Brazil), were screened. After signing consent forms, patients were interviewed to obtain their pesticide exposure profiles. Seventeen women were excluded from the study due to THE lack of follow-up or insufficient information regarding pesticide exposure. Thus, 758 women were included in the study. Urine samples from 30 women were collected in the exposure assessment (contamination) study, aiming to measure glyphosate, atrazine, and 2,4-D residues. For the cancer risk study (n = 728), a total of 373 women were characterized as exposed and 355 as unexposed. Based on the biopsy result, patients were categorized into four groups: Women exposed to pesticides diagnosed with breast cancer (n = 215), women exposed to pesticides without breast cancer (n = 158), women not exposed to pesticides diagnosed with breast cancer (n = 164), and women not exposed to pesticides without breast cancer (n = 191). Data obtention included patient characteristics (age at diagnosis, weight, height, body mass index, menopausal status, disease onset), tumor features molecular subtypes, hormonal receptors status, human epidermal growth factor 2 receptor amplification (HER2), the presence of tumor emboli or lymph nodal metastasis, distant metastasis, chemoresistance, and tumor recurrence.

Figure 3

Pesticide contamination study. A total of 10 farms were chosen to conduct the exposure assessment (contamination) study, as shown on the map. This step was carried out during the peak of pulverization of the three most traded pesticides in the region (glyphosate, atrazine, and 2,4-D). An interview was conducted to obtain their occupational exposure profile to pesticides, and the results are shown in Box A. Urine samples were collected to evaluate pesticide concentration after its pulverization, and the results are shown in Box B. ND = not detected, ppb = parts per billion.

Figure 4

Correlation matrix of select variables for all breast cancer patients. BMI = body mass index, LN = lymph nodal. * p-value < 0.1, **p-value < 0.05, and ***p-value < 0.01.