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https://doi.org/10.1007/s11356-023-26420-8 RESEARCH ARTICLE Exposure to pesticides and breast cancer in the city of Petrópolis, Brazil Louise Moura de Rezende1 · Sabrina da Silva Santos1 · Gina Torres Rego Monteiro1 Received: 24 August 2022 / Accepted: 8 March 2023 © The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023 Abstract To investigate the association between pesticide use and breast cancer. A hospital-based case–control study was conducted in Petrópolis city, Brazil. The study data were obtained through interviews, and the magnitude of the association between self-reported pesticide exposure and breast cancer was determined using unconditional logistic regression. A higher esti- mated risk for breast cancer was found in women exposed to pesticides for 10 or more years, where this association was not statistically significant after adjusting for potential confounders (OR = 1.40; 95% CI 0.85–2.49). A positive statistically significant association was found between breast cancer and higher educational level or previous use of hormone replacement therapy (HRT), whereas having had 2 or more pregnancies to term proved a protective factor. Further studies elucidating the contribution of pesticide exposure to the development of breast cancer are needed, given that current findings in the literature are conflicting. Keywords Breast cancer · Pesticides · Case–control study · Self-reported exposure · Petrópolis city · Brazil Introduction Breast cancer is a public health issue worldwide and a dis- ease which requires prevention and control owing to its high rates of incidence and mortality. Rates of breast cancer incidence and mortality have been rising significantly over the years. In fact, since 2020, according to IARC estimates, breast cancer has become the most incident cancer in the world, exceeding lung cancer, with an incidence rate of 58.5 cases per 10,000 population (Sung et al. 2021). Most cases of cancer are associated with environmen- tal exposure, including pesticides. A wide range of these compounds is classified as carcinogenic by the International Agency for Research on Cancer (WHO and IARC 2014). The action mechanisms can be a genotoxic effect, as can be seen for organochlorine and organophosphorus compounds (Jamil et al. 2004). Farther, a broad number of pesticides are considered as endocrine disruptors (Mnif et al. 2011) and some, such as atrazine, organophosphorus compounds, carbamates, and pyrethroids, were shown to be immunotoxic (Lee and Choi 2020). These mechanisms are involved in the physiopathology of breast cancer (Wan et al. 2022; Souza et al. 2022; Arévalo-Jaramillo et al. 2019). Corroborating these relationships, many studies have shown that individu- als who work in farming and agriculture, and those who live in rural communities or that are exposed to pesticides, carry a higher risk of developing breast cancer (Eldakroory et al. 2017; Huang et al. 2019; Paydar et al. 2019; Silva et al. 2019; Engel et al. 2017; Huang et al. 2019; Paydar et al. 2019; Silva et al. 2019). However, these associations remain unclear since some studies have identified higher risk, but without statistical significance (Aronson et al. 2000; Demers et al. 2000; Farooq et al. 2010; Wolff et al. 2000; Zota et al. 2010; Werder et al. 2020). Since 2008, Brazil has been ranked as one of the larg- est users of pesticides worldwide (Carneiro et al. 2015; Worldometer 2022; FAO 2022; Almeida et al. 2017; Pig- nati et al. 2017). In the state for Rio de Janeiro, around 1,800,000 hectares of land are dedicated to agriculture. In the state’s Mountain Region, where the cities of Petrópolis, Teresópolis, and São José do Vale do Rio Preto comprise the main agricultural center, 7% of the population is engaged in Responsible Editor: Lotfi Aleya * Sabrina da Silva Santos sabrina_ssantos@hotmail.com 1 National School of Public Health (ENSP, Escola Nacional de Saúde Pública), Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro, RJ, Brazil / Published online: 15 March 2023 Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 http://crossmark.crossref.org/dialog/?doi=10.1007/s11356-023-26420-8&domain=pdf http://orcid.org/0000-0001-8327-3546 farming activities (IBGE 2006). Pesticide use in the region amounts to 56 kg per agricultural worker annually, exceed- ing the state average (Peres and Moreira 2007). Against this background, the objective of the present study was to investigate the association between self- reported pesticide exposure and female breast cancer, according to risk factors related to exposure to estrogen, in women hospitalized in the city of Petropolis, a city where this relationship has not previously been investigated. Materials and methods Study design and participants This is a hospital-based case–control study with newly diag- nosed female breast cancer cases confirmed by histopatho- logical tests and classified according to the IDC-10 of the World Health Organization (WHO 1993), at the Oncology Treatment Center in the city of Petrópolis between Decem- ber 2014 and March 2020. Control subjects were female inpatients of a general hos- pital, the Alcides Carneiro Municipal Hospital, during the study period, in the same age range of controls. Cases and control individuals with a previous history of cancer, at terminal stage of the disease or that presented cognitive impairment precluding communication or compre- hension of the study questionnaire, were excluded. Female inpatients admitted for the treatment of any type of cancer or for symptoms potentially associated with the clinical picture of breast cancer were also excluded. A total sample of 191 cases and 185 controls was inter- viewed by trained personnel at the health clinic where they were undergoing treatment. A structured questionnaire cov- ering sociodemographic, lifestyle, and previous contact with pesticides information was applied. These research instru- ment initially presented a series of questions about the use of pesticides in general (applications at home, in gardens, on pets, in commercial buildings, and on farm crops, storage of grain or other agricultural products, and forestry applica- tions). When the interviewee answered in the affirmative to any of them, a list of trade names for specific products was presented. For each used product, data about quantity, fre- quency, and protective equipment were requested. Addition- ally, individuals involved in agricultural activities answered questions about characteristics of the property and the crops produced on it. Statistical analysis The magnitude of the association between pesticide expo- sure and breast cancer was determined by calculating crude odds ratio (OR) or by OR adjusted for potential confounders, using the unconditional logistic regression method. Analy- ses were performed for estimated confidence intervals with a 5% level of significance (p = 0.05). The multiple logistic regression model was constructed by testing all variables with a p value < 0.20 on crude analysis and retaining in the final model only variables which statistical significance (p value < 0.05), after adjusting for the other variables in the model, or changed the effect of the variable of interest by more than 10%. Lastly, the quality of the final model was verified by residual analysis. All statistical analyses were carried out using the SPSS 20.0 software package (IBM). With a sample size of 190 cases and 184 controls, consid- ering a 95% significance level and a population prevalence of self-reported pesticide exposure, for over 10 years, of 17.7%, this study has a power of 80% to detect an OR = 2.0 between such exposure and female breast cancer, as calcu- lated by EpiInfo 7.2.4.0. Ethical considerations The procedures adopted in this project conformed with the recommendations of Resolution no. 466/12 of the National Boardof Health, of 12th December 2012, and the study was approved by the Research Ethics Committee of the ENSP (CAAE permit: 31,126,514.0.0000.5240) and by the com- mittees of the participating hospitals. Results The population characteristics are presented in Table 1. Cases had a mean age of 58.16 (SD ± 12.4) years, while controls had a mean age of 50.89 (SD ± 17.0) years. Although age-frequency matching was employed, there was a statistically significant difference in age between the two groups (p < 0.001). Age was therefore used as an adjustment variable in the final model. Cases and controls were predominantly white, low-educated, and overweight (mean BMI = 28.1 for cases and 26.6 for controls). Most participants reported no history of alcohol or tobacco use, and the two groups differed significantly for smoking status (p = 0.032). There was no difference between case and control groups for age at menarche or use of oral contraceptives, family history of breast cancer, or breastfeeding, where most women reported hav- ing practiced breastfeeding. However, the menopause started later in cases than in controls (p < 0.001), and statistically significant dif- ferences were observed for use of HRT (p < 0.001) and for number of children (p = 0.006), even though the first pregnancy occurred before the age of 30 years in most women for both groups. Regarding environmental and occupational exposure to pesticides (Table 2), the groups were similar for pesticide use, largely for domestic purposes and also for lifetime use 56535Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 of these substances. Among women reporting residential use of pesticides, 80% of cases and 75% of controls stated that they used no personal protective equipment, such as gloves, when handling the products. Similarly, in the group of women reporting agricultural use, 85.7% of cases and 60% of controls used no protection when applying pesticide products (data not shown). A statistically significant differ- ence was detected between the group that used pesticides for over 10 years relative to the groups which had never used the products or had used them for fewer years (p = 0.014). The strength of the association of exposure to pest icides, and other selected r isk factors , with breast cancer in the final logistic regression model is presented in Table 3. After adjusting for all the var iables present in the model, the var iables age (p < 0.001), education (p = 0.019), number of chil- dren (p = 0.003), and HRT (p = 0.039) remained statistically signif icant, whereas duration of pes- ticide use showed a higher, non-signif icant, r isk (p = 0.177). Table 1 Distribution of cases (n = 192) and controls (n = 188) according to selected variables, Petrópolis, Brazil, 2014–2020 Statistically significant values are shown in bold OR, odds ratio; CI, confidence interval; HRT, hormone replacement therapy a Totals differ due to missing data b Chi-square test Variables Cases N (%) Controls N (%) OR (95% CI) pb Agea < 45 years 31 (16.1) 69 (36.9) 1.00 < 0.001 45–54 46 (24.0) 39 (20.9) 2.6 (1.4–4.8) 55–64 52 (27.1) 35 (18.7) 3.3 (1.8–6.0) ≥ 65 years 63 (32.8) 44 (23.5) 3.2 (1.8–5.6) Skin colora White 129 (67.9) 110 (58.5) 1.00 0.059 Non-white 61 (32.1) 78 (41.5) 0.7 (0.4–1.02) Educationa ≤ 8 years 99 (52.1) 114 (60.6) 1.00 0.094 > 8 years 91 (47.9) 74 (39.4) 1.4 (0.9–2.1) BMIa Underweight/normal 66 (35.7) 66 (43.1) 1.00 0.097 Overweight 53 (28.6) 49 (32.0) 1.08 (0.6–1.8) Obese 66 (35.7) 38 (24.8) 1.7 (1.03–2.9) Alcohol use Non-drinker 98 (51.0) 104 (55.3) 1.00 0.387 Former drinker 58 (30.2) 45 (23.9) 1.4 (0.8–2.2) Drinker 36 (18.8) 39 (20.7) 0.9 (0.6–1.7) Tobacco usea Non-smoker 134 (71.3) 123 (66.1) 1.00 0.032 Former smoker 47 (25.0) 43 (23.1) 1.0 (0.6–1.6) Smoker 7 (3.7) 20 (10.8) 0.3 (0.1–0.8) Menarchea ≤ 12 years 84 (44.2) 75 (40.3) 1.00 0.445 > 12 years 106 (55.8) 111 (59.7) 0.8 (0.6–1.3) Menopausea No 41 (22.0) 75 (40.8) 1.00 < 0.001 ≤ 45 years 53 (28.5) 56 (30.4) 1.7 (1.01–2.9) > 45 years 92 (49.5) 53 (28.8) 3.2 (1.9–5.3) Years using oral contraceptivesa Never used 36 (19.4) 39 (21.0) 1.00 0.816 ≤ 5 years 65 (34.9) 68 (36.6) 1.04 (0.6–1.8) > 5 years 85 (45.7) 79 (42.5) 1.2 (0.7–2.0) HRT usea No 154 (82.8) 170 (94.4) 1.00 < 0.001 Yes 32 (17.2) 10 (5.6) 3.5 (1.7–7.4) Number of childrena 0–2 136 (71.6) 108 (58.1) 1.00 0.006 > 2 54 (28.4) 78 (41.9) 0.5 (0.3–0.8) Breastfeedinga Never breastfed 46 (25.1) 41 (22.5) 1.00 0.427 ≤ 12 months 89 (48.6) 82 (45.1) 1.0 (0.6–1.6) > 12 months 48 (26.2) 59 (32.4) 0.7 (0.4–1.3) Family history of cancer No 170 (88.5) 171 (91.0) 1.00 0.438 Yes 22 (11.5) 17 (9.0) 1.3 (0.7–2.5) 56536 Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 Discussion The self-reported use of pesticides for over 10 years was associated with a greater estimated risk of developing breast cancer compared to non-use or shorter periods of use, although this relationship was not significant after adjusting for selected variables. Some studies have shown a positive association between this type of exposure and breast cancer. A case–control study which included 1169 cases and 1743 controls, interviewed in Australia from 2009 to 2011, showed an increased risk (OR = 1.51; 95% CI 1.18–1.94) among women who reported noticing pes- ticide spray drift, and who lived close to an agricultural area, for 10 years or more, compared to women who reported not observing pesticide use (El-Zaemey et al. 2013). Another case–control study, involving 85 cases and 266 controls recruited between 2017 and 2018 in Ron- donópolis, Mato Grosso state, Brazil, also found a higher odds ratio (OR: 2.37; 95% CI 1.78–3.16) for the develop- ment of breast cancer among women reporting residing close to agricultural areas in which pesticides were used, compared to women not living close to these sites (Silva et al. 2019). Similarly, a case–control study of 1505 cases and 1553 controls living in New York between 1996 and 1997 found a higher risk of breast cancer (OR 1.39, 95 CI% 1.15–1.68) among women reporting ever lifetime pesticide use compared with women who reported never having used pesticides (Teitelbaum et al. 2007). A case–control study conducted in China found a higher chance (OR = 1.63; 95% CI 1.15–2.85) of DDE exposure in women who had breast cancer when comparing tissue concentrations of the compounds in cases and controls (Huang et al. 2019). Similarly, another case–control study also found a higher risk of DDE exposure (OR = 1.72; 95% CI 1.11–3.13) in breast cancer cases relative to controls (Arrebola et al. 2015). However, some studies, including the present investiga- tion, have identified greater estimated risk for developing breast cancer in women exposed to pesticides, but found this relationship to be non-significant on statistical analyses. This was the case for a case–control study conducted in Canada comparing women in the last quintile of exposure to DDT, with those in the first quintile (OR: 1.37; 95% CI 0.73–2.56) (Demers et al. 2000). A hospital-based case–control study comprising 447 cases and 758 controls, interviewed between 1994 and 1996 in New York city, found a higher, non-sig- nificant, risk (OR 1.25; 95% CI 0.79–1.98) among women reporting residential pesticide use compared to those who never used these products (Farooq et al. 2010). Table 2 Distribution of cases (n = 192) and controls (n = 188) according to variables related to pesticide exposure, Petrópolis, Brazil, 2014–2020 Statistically significant values are shown in bold OR, odds ratio; CI, confidence interval a Totals differ due to missing data b Chi-square test Variables Cases N (%) Controls N (%) OR (95% CI) pb Pesticide use Never used 60 (31.2) 52 (27.7) 1.00 0.744 Domestic 125 (65.1) 129 (68.6) 0.8 (0.5–1.3) Agricultural 7 (3.6) 7 (3.7) 0.9 (0.3–2.6) Time using pesticidesa 0–10 years 136(71.6) 153 (82.3) 1.00 0.014 > 10 years 54 (28.4) 33 (17.7) 1.8 (1.1–3.0) Lifetime pesticide usea < 30 days 92 (49.5) 91 (50.8) 1.00 0.810 30–235 49 (26.3) 42 (23.5) 1.1 (0.7–1.9) > 235 45 (24.2) 46 (25.7) 1.0 (0.6–1.6) Table 3 Final model of association of pesticide exposure, and other variables of interest, with developing breast cancer, Petrópolis, Brazil, 2014–2020 Statistically significant values are shown in bold OR, odds ratio; CI, confidence interval; HRT, hormone replacement therapy a Adjusted for all variables included in model b Wald test Variables Adjusted ORa 95% CI pb Age 1.04 1.03–1.06 < 0.001 Time using pesticides ≤ 10 years 1.00 > 10 years 1.40 0.85–2.49 0.177 Education ≤ 8 years 1.00 > 8 years 1.81 1.10–2.97 0.019 Number of children 0–2 1.00 > 2 0.47 0.29–0.78 0.003 HRT use No 1.00 Yes 2.29 1.04–5.03 0.039 56537Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 A case–control study which included 787 cases and 721 controls residing for at least 6 months in the city of Cape Cod, USA, between 1988 and 1995, found a slightly higher breast cancer risk (OR = 1.2; 95% CI 0.80–1.60) in women who reported using any type of pesticide 10 times or more compared to those who never used the products, although this association did not reach statistical signifi- cance (Zota et al. 2010). Similar results were reported by a nested case–control study conducted in New York, where higher risk of developing breast cancer was found for the last quartile of DDE exposure (OR: 1.30; 95% CI 0.51–3.35) compared to the first quartile (Wolff et al. 2000). Two cross-sectional studies reported a positive asso- ciation between previous pesticide and the breast cancer, although this was not statistically significant. The first, a study by Xu et al. (2010) conducted in the USA, found a higher risk of breast cancer (OR = 1.19; 95% CI 0.40–3.50) among women in the last quartile of exposure to DDE, while a study by Engel et al. (2017), also in the USA, found a higher risk (OR = 1.5; 95% CI 0.70–2.90) for exposure to heptachlor, an organochlorine. Regarding exposure to the other factors related to estro- gen metabolism, such as HRT, in the present study, the odds of cases having used this treatment was higher relative to controls. Similarly, a cohort study in Denmark found a higher risk of breast cancer (OR 1.56; 95% CI 1.19–2.04) in women who reported having used HRT (Azam et al. 2018). This same relationship had previously been reported in the Nurses Health Study cohort, which found an elevated risk of breast cancer (OR 1.32; 95% CI 1.14–1.54) in women that used estrogen alone and in users of estrogen plus proges- tin (OR = 1.41; 95% CI 1.15–1.74), compared to individu- als that used no hormones (Colditz et al. 1995). The nested case–control study of Chen (2002) also found a higher risk (OR = 1.70; 95% CI 1.15–2.50) of developing breast cancer in women on HRT for longer than 4 years. Number of pregnancies was also a factor associated with breast cancer but, unlike HRT, this acted as a protective fac- tor, providing the body with a pause in exposure to estrogen (Liu et al. 2019). The present study found a lower chance of developing breast cancer among women who had more than two children, relative to those who had no children or two pregnancies to term. This finding corroborates the results of a cohort study performed in the USA, in which a lower risk (OR = 0.84; 95% CI 0.80–0.89) of breast cancer was evident in women who were mothers compared to those who had no children (Fortner et al. 2019). In another study, con- ducted in Japan, a lower risk (OR = 0.43; 95% CI 0.19–0.97) was identified in women who had 5 children compared to those who had only one pregnancy (Liu et al. 2019). In a nested case–control study conducted in Norway, the chance of developing breast cancer was lower (OR = 0.59; 95% CI 0.51–0.68) for women who had 4 or more pregnancies, each lasting at least 6 months, compared to women who had never been pregnant (Ellingjord-Dale et al. 2017). The present study also found a higher odds ratio for women with > 8 years of education compared to those who had not studied or had ≤ 8 years of education. This result corroborates other studies showing greater risk for breast cancer among women with higher educational level, a char- acteristic also associated with other factors related to the disease, such as later age at first pregnancy to term, fewer pregnancies, and use of HRT for menopausal symptoms (Fujino et al. 2008; Hussain et al. 2008; Larsen et al. 2011; Menvielle et al. 2011; Mouw et al. 2008). Additionally, the greater adherence to screening in this group explains the higher number of cases of cancer diagnosed in high-edu- cated women (Damiani et al. 2015; Dong and Qin 2020). Regarding associations with other risk factors, such as race, alcohol and tobacco use, radiation exposure, age at menarche, age at menopause, use of oral contraceptives, family history for cancer, and other characteristics, these either did not differ statistically between the two groups from the outset or lost statistical significance after adjusting for the other variables included in the logistic regression model. The present case–control study has some limitations. The sample size was relatively small compared to other studies that identified greater, statistically significant, risk for developing breast cancer associated with self-reported pesticide exposure (El-Zaemey et al. 2013; Engel et al. 2017; Farooq et al. 2010; Silva et al. 2019; Zota et al. 2010). It was not possible to increase the sample size and to obtain an aged-frequency-matched distribution between cases and controls once the interviews of the subjects was interrupted by the COVID-19 pandemic. The estimation of exposure through self-report instead of quantifying actual levels of exposure using biological samples is also a limitation. Even so, in simple analyses, it was shown a higher odds of developing breast cancer among women who reported using pesticides that has been pointed as a risk for this type of cancer in literature (Wan et al. 2022; Darbre 2021; Kahn et al. 2020; Loomis et al. 2015). Con- sidering the high use of pesticides in the region where the study was carried out, the association with breast cancer may be underestimated since both cases and con- trols may be highly exposed to pesticides due to the broad background environmental contamination. On the other hand, recently, we show that the average concentrations of organochlorines, in no cancer hospitalized individu- als of Petropolis city, are below those observed by other studies (de Rezende et al. 2023), which was unexpected since organochlorine pesticides continues to occur in the region, possibly obtained through illegal trade (Guida et al. 2021; Meire et al. 2012; Peres and Moreira 2007). This lower concentrations of organochlorines may not only explain, in part, the fact that the present study did not find 56538 Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 a statistically significant association between pesticide use and breast cancer after adjusting for potential confounders but also draws attention to the importance of future studies to make a more in-depth assessment of pesticides that dif- ferentiate persistent pesticides that is known carcinogenic (Loomis et al. 2015) from those that are not persistent, more difficult to access and with less data in the literature (Fernández et al. 2020; Yildizdas et al. 2019; Bakke et al. 2009). Nonetheless, the present study assessed incident cases and hospital controls, conferring greater reliability of events reported by cases and lower likelihood of mem- ory bias or lack of response by control subjects. Another strength of this study is its investigation of a population and region for which the relationship between pesticide exposure and breast cancer hadnot previously been studied. Conclusion The results showed a higher odds of developing breast cancer among women who reported using pesticides for over 10 years, although these findings were not statisti- cally significant after adjusting for potential confounders. Moreover, a positive, statistically significant, association was found between breast cancer and higher educational level or previous HRT use, whereas more than 2 pregnan- cies proved a protective factor against the disease. Fur- ther studies involving larger samples and more in-depth assessment of pesticide exposure are needed to elucidate the contribution of this exposure to the development of breast cancer, given that current findings in the literature are conflicting. Acknowledgements The authors thank the patients of the Hospital Municipal Alcides Carneiro and of the Centro de Terapia Oncológica de Petrópolis. Author contribution All authors contributed to the study conception and design. Data collection was performed by Louise Moura Rezende and Gina Torres Rego Monteiro. Analysis was performed by Louise Moura Rezende and Sabrina da Silva Santos. The first draft of the manuscript was written by Louise Moura de Rezende. All authors com- mented on previous versions and approved the final manuscript. Funding This work was supported by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ—process no. 110.287/2014 and project E-26./210.882/2021) and by the Sergio Arouca National School of Public Health (ENSP/FIOCRUZ—research grant bid 2016–2018). Data availability The data that support the findings of this study are available on request from the corresponding author, SSS. 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Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. 56541Environmental Science and Pollution Research (2023) 30:56534–56541 1 3 https://www.worldometers.info/food-agriculture/pesticides-by-country/ https://www.worldometers.info/food-agriculture/pesticides-by-country/ Exposure to pesticides and breast cancer in the city of Petrópolis, Brazil Abstract Introduction Materials and methods Study design and participants Statistical analysis Ethical considerations Results Discussion Conclusion Acknowledgements References
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