Pesticide contamination of lactating mothers’ milk in Latin America: a systematic review

Thalyta Mota Figueiredo Jerusa da Mota Santana Fernando Henrique Basilio Granzotto Bianca Sampaio dos Anjos Danilo Guerra Neto Laylla Mirella Galvão Azevedo Marcos Pereira About the authors

ABSTRACT

OBJECTIVE

To identify the prevalence of contamination by pesticides and their metabolites in the milk of lactating mothers in Latin America.

METHODS

In this systematic review, the PubMed, LILACS, Embase, and Scopus databases were searched up to January 2022 to identify observational studies. The Mendeley software was used to manage these references. The risk of bias assessment was evaluated according to the checklist for prevalence studies and writing design, by the Prisma guidelines.

RESULTS

This study retrieved 1835 references and analyzed 49 studies. 69.38% of the analyzed studies found a 100% prevalence of breast milk contamination by pesticides among their sample. Main pesticides include dichlorodiphenyltrichloroethane (DDT) and its isomers (75.51%), followed by the metabolite dichlorodiphenyldichloroethylene (DDE) (69.38%) and hexachlorocyclohexane (HCH) (46.93%). This study categorized most (65.30%) studies as having a low risk of bias.

CONCLUSIONS

This review shows a high prevalence of pesticide contamination in the breast milk of Latin American women. Further investigations should be carried out to assess contamination levels in breast milk and the possible effects of these substances on maternal and child health.

Chemical Contamination; Agrochemicals; Breast Milk; Exposure; Human Health

INTRODUCTION

The World Health Organization (WHO) recommends exclusive breastfeeding (EBF) for infants up to six months of life and, after that period, complementing it with other foods up to two years of life or more11. World Health Organization. Guideline: protecting, promoting and supporting breastfeeding in facilities providing maternity and newborn services. Geneva: World Health Organization; 2017 [cited 2023 June 10]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK487819/pdf/Bookshelf_NBK487819.pdf
https://www.ncbi.nlm.nih.gov/books/NBK48...
,22. Brasil. Saúde da criança: aleitamento materno e alimentação complementar. 2. ed. Brasília, DF: Ministério da Saúde; 2015.. Scientific evidence shows the protective effects of breast milk for infants’ health as it contains energy; essential nutrients for their nutritional, metabolic, and physiological demands up to the sixth month of life; and immunological and cellular components33. Palmeira P, Carneiro-Sampaio M. Immunology of breast milk. Rev Assoc Med Bras. 2016 Sep;62(6):584-93. that protect children against diarrhea, respiratory infections, and infant morbi-mortality44. Paim JSL, Boiani MB, Freitas TS. Fatores associados a prática e a duração do aleitamento materno no Brasil contemporâneo. Investigação. 2018 Jul;17(3):66-74..

Despite breast milk being considered an ideal food for child nutrition and development, its composition and quality can change due to external environmental factors, such as mothers’ diet and lifestyle55. Ferronato G. Determinação de poluentes orgânicos persistentes (pops) em leite materno: desenvolvimento e aplicação de método analítico empregando GC-NCI-MS [dissertação de mestrado]. Santa Maria: Universidade Federal de Santa Maria; 2014..

Substances in pharmaceuticals, tobacco, alcohol, illicit drugs, and chemical products (such as pesticides) can be secreted into breast milk66. Sociedade Brasileira de Pediatria. Uso de medicamentos e outras substâncias pela mulher durante a amamentação. Rio de Janeiro: Sociedade Brasileira de Pediatria; 2017 [cited 2023 June 10]. Available from: https://portaldeboaspraticas.iff.fiocruz.br/wp-content/uploads/2021/06/Aleitamento_-__Uso_Medicam_durante_Amament.pdf
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,77. Sandes AS, Amorim TC, Queiroz VP, Matos LCP. Contaminação do leite materno por agrotóxicos e implicações na saúde infantil: uma revisão sistematizada. Saúde e meio ambient: rev interdiscip. 2022;11:43-58., interfering with the quality of this food regarding its composition, nutritional value, and aroma, hindering the milk ejection reflex and infants’ suction, which contributes to reducing breastfeeding time88. Borges CPG, Duarte CN, Gemelli CR, Santana JRS, Mendes RCD. Valor calórico do leite humano ordenhado pasteurizado de um banco de leite de Dourados-MS. Brazilian J Dev. 2020 Mar;6(3):14243-58.. For these reasons, exposure to such substances should be discouraged, especially during pregnancy and breastfeeding66. Sociedade Brasileira de Pediatria. Uso de medicamentos e outras substâncias pela mulher durante a amamentação. Rio de Janeiro: Sociedade Brasileira de Pediatria; 2017 [cited 2023 June 10]. Available from: https://portaldeboaspraticas.iff.fiocruz.br/wp-content/uploads/2021/06/Aleitamento_-__Uso_Medicam_durante_Amament.pdf
https://portaldeboaspraticas.iff.fiocruz...
.

Pesticides constitute chemical, physical, or biological products used to directly or indirectly control, destroy, or prevent pathogenic agents in plants and useful animals and people99. Nascimento BP, Silva RCGF, Ferreira AP, Silva EC, Figueiredo Junior JA, Oliveira Dias LL, et al. Impacto ambiental sobre a saúde humana devido à exposição aos agrotóxicos. UNICIÊNCIAS. 2021;25(1):44-56.. They serve as herbicides, fungicides, pesticides, rodenticides, nematicides, acaricides, molluscicides, termiticides, growth regulators and inhibitors, fumigants, fertilizers, wood preservatives, and some veterinary products1010. Peres F, Moreira JC, organizadores. É veneno ou é remédio? Agrotóxicos, saúde e ambiente. Rio de Janeiro: Fiocruz; 2003.,1111. Santana VS, Moura MCP, Nogueira FF. Occupational pesticide poisoning mortality, 2000-2009, Brazil. Rev Saude Publica. 2013 Jun;47(3):598-606. https://doi.org/10.1590/S0034-8910.2013047004306
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. The most commonly used compounds include organophosphates, carbamates, and halogenates, among others1010. Peres F, Moreira JC, organizadores. É veneno ou é remédio? Agrotóxicos, saúde e ambiente. Rio de Janeiro: Fiocruz; 2003.. These substances can contaminate breast milk if in direct contact with agricultural use1212. Corralo VS, Morais MM, Benedett A, Ferraz L. Presença de pesticidas organoclorados no leite materno: fatores de contaminação e efeitos à saúde humana. Hygeia. 2016 Jun;12(22):101-8., or indirectly, via exposure to its residues in the air, water, and animal, and vegetable foods77. Sandes AS, Amorim TC, Queiroz VP, Matos LCP. Contaminação do leite materno por agrotóxicos e implicações na saúde infantil: uma revisão sistematizada. Saúde e meio ambient: rev interdiscip. 2022;11:43-58..

Some of their chemical properties give pesticides the capacity to disperse and accumulate in the environment. Moreover, those with liposoluble properties may be present in foods of animal origin, indirectly contaminating and accumulating in the adipose tissue of human beings1212. Corralo VS, Morais MM, Benedett A, Ferraz L. Presença de pesticidas organoclorados no leite materno: fatores de contaminação e efeitos à saúde humana. Hygeia. 2016 Jun;12(22):101-8.. Breast milk, in turn, has a high concentration of fats in its composition, making it a potential vehicle for transferring pesticide residues1313. Brasil. Ministério da Saúde. Manual de Vigilância da Saúde de Populações Expostas a Agrotóxicos.Brasília, DF: Organização Pan-Americana da Saúde; 1996..

Studies conducted in Latin America since the 1990s show the presence of pesticides in the milk of women in that region. A study conducted1414. Matuo YK, Lopes JN, Casanova IC, Matuo T, Lopes JL. Organochlorine pesticide residues in human milk in the Ribeirão Preto region, state of São Paulo, Brazil. Arch Environ Contam Toxicol. 1992 Feb;22(2):167-75. https://doi.org/10.1007/BF00213281
https://doi.org/10.1007/BF00213281...
in Ribeirão Preto, São Paulo (Brazil) found residues of four types of pesticides, with dichlorodiphenyltrichloroethane (DDT) being identified in 100% of the analyzed breast milk samples, with higher mean levels of concentration in samples from occupationally exposed women than in those from non-exposed women. A study with women in Mexico1515. Chávez-Almazán LA, Saldarriaga-Noreña HA, Díaz-González L, Garibo-Ruiz D, Waliszewski SM. Dietary habits associated with the presence of organochlorine pesticides in human milk. J Environ Sci Health B. 2020 Jul;55(8):756-66. https://doi.org/10.1080/03601234.2020.1783169
https://doi.org/10.1080/03601234.2020.17...
found the presence of two compounds derived from pesticides in 76% of the analyzed milk samples.

The high prevalence of pesticide in breast milk is alarming due to the negative repercussions of pesticide to mothers’ and infants’ health. Amidst the wide range of chemical substances available in the market, estimates suggest that more than a 1000 can disrupt the endocrine system. Scientific evidence shows that pesticide exposure can lead to hormonal disorders and affect reproduction, contributing to the early onset of puberty, longer menstrual cycles, and anticipation of menopause1616. Gore AC, Crews D, Doan LL, La Merrill M, Patisaul H, Zota A. Introduction to endocrine disrupting chemicals (EDCs). A guide for public interest organizations and policy-makers. Washington, DC: Endocrine Society; 2014.. Furthermore, it is associated with the development of breast cancer; congenital disabilities; and impaired social, cognitive, and psychomotor development99. Nascimento BP, Silva RCGF, Ferreira AP, Silva EC, Figueiredo Junior JA, Oliveira Dias LL, et al. Impacto ambiental sobre a saúde humana devido à exposição aos agrotóxicos. UNICIÊNCIAS. 2021;25(1):44-56.,1717. Hernik A, Goralczyk K, Strucinski P, Czaja K, Korcz W, Minorczyk M, et al. Characterising the individual health risk in infants exposed to organochlorine pesticides via breast milk by applying appropriate margins of safety derived from estimated daily intakes. Chemosphere. 2014 Jan;94:158-63..

The importance of breast milk in infant nutrition and health the exposure of women in Latin America to chemical substances that can interfere with milk quality entail the need to systematize the scientific production in Latin America to identify the prevalence of contamination by pesticides and their metabolites in the breast milk of women directly or indirectly exposed to these compounds.

METHODS

Registration and Guiding Question

This is a systematic review (SR) of the literature aimed at finding studies developed in Latin America that evaluate the prevalence of pesticides and their metabolites in breast milk. This study followed the Prisma 2020 guidelines1818. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021 Mar;10(1):89. https://doi.org/10.1136/bmj.n71
https://doi.org/10.1136/bmj.n71...
and its protocol was registered in the Prospective Register of Systematic Reviews (PROSPERO) under number CRD42018106637.

Eligibility Criteria

Studies were selected following the PECOT acronym: P (Population) - studies with lactating mothers in Latin America; E (Exposure) - Human breast milk; C (Comparison) - no comparisons were made between groups in this systematic review; O (Outcome) - contamination of breast milk by pesticides; T (Study Type) - original articles, theses, and dissertations with observational study designs (cohort, cross-sectional, and case-control studies).

Search Strategy

The high sensitivity data search was independently carried out by two researchers on the PubMed, LILACS, Embase, and Scopus databases using the following descriptors: “breast feeding”, “breast milk”, “agrochemicals”, “pesticides”, “contamination”, and their respective terms in Portuguese and Spanish, which were combined with sensitive Boolean operators suited to each search platform (as described in Table 1).

Table 1
Search strategies in databases and main results, 2022.

Studies Selection

The Mendeley Desktop software (version 1803) was employed to manage the retrieved references, remove duplicates, and apply the inclusion criteria to the chosen studies. The titles were first read; then, the abstracts, and finally the whole manuscripts.

Risk of Bias

The 2017 Joanna Briggs Institute (JBI) Checklist for Prevalence Studies1919. Falcomer AL, Santos Araújo L, Farage P, Santos Monteiro J, Yoshio Nakano E, Puppin Zandonadi R. Gluten contamination in food services and industry: A systematic review. Crit Rev Food Sci Nutr. 2020 Dec;60(3):479-93. https://doi.org/10.1080/10408398.2018.1541864
https://doi.org/10.1080/10408398.2018.15...
was used to assess the rigor and methodological quality of all 49 studies chosen for this review. This instrument is composed of nine questions, including adequacy of the sample structure, recruitment of the population, adequacy of sample size, detailing the subjects and study setting, adequacy of data analysis, employment of validated methods, criteria for measuring variables, and adequacy of response rates.

Positive responses to any of the nine questions that compose the checklist were considered to classify risk of bias. Studies that had up to a 49% “yes” score were categorized as high risk of bias; those with a positive response for 50%-69% of the questions, as moderate risk; and studies that had a positive score for 70% or more of the questions, as low risk1919. Falcomer AL, Santos Araújo L, Farage P, Santos Monteiro J, Yoshio Nakano E, Puppin Zandonadi R. Gluten contamination in food services and industry: A systematic review. Crit Rev Food Sci Nutr. 2020 Dec;60(3):479-93. https://doi.org/10.1080/10408398.2018.1541864
https://doi.org/10.1080/10408398.2018.15...
.

Data Extraction and Analysis

Data were extracted by a reviewer and checked by another with the help of a standardized spreadsheet on Microsoft Excel containing the following variables: names of the authors, title of the article, year of publication, region of the study, country of origin, sample, age and income of participants, presence of pesticide contamination in breast milk, methodology used to identify pesticides in breast milk, types of pesticides and metabolites found in breast milk, and number of women exposed and not exposed to pesticides.

The prevalence of pesticide in breast milk was calculated according to the following formula: total number of breast milk samples contaminated by pesticides divided by the total number of samples multiplied by 100. Results were organized in graphs and tables.

RESULTS

Search Results

A total of 1835 references were identified. After reading their titles and abstracts and applying the eligibility criteria, 104 articles were selected to be read in full, of which 49 articles1414. Matuo YK, Lopes JN, Casanova IC, Matuo T, Lopes JL. Organochlorine pesticide residues in human milk in the Ribeirão Preto region, state of São Paulo, Brazil. Arch Environ Contam Toxicol. 1992 Feb;22(2):167-75. https://doi.org/10.1007/BF00213281
https://doi.org/10.1007/BF00213281...
,1515. Chávez-Almazán LA, Saldarriaga-Noreña HA, Díaz-González L, Garibo-Ruiz D, Waliszewski SM. Dietary habits associated with the presence of organochlorine pesticides in human milk. J Environ Sci Health B. 2020 Jul;55(8):756-66. https://doi.org/10.1080/03601234.2020.1783169
https://doi.org/10.1080/03601234.2020.17...
,2020. Chávez-Almazán LA, Diaz-Ortiz J, Alarcón-Romero M, Davila-Vazquez G, Saldarriaga-Noreña H, Sampedro-Rosas L, et al. Influence of Breastfeeding Time on Levels of Organochlorine Pesticides in Human Milk of a Mexican Population. Bull Environ Contam Toxicol [Internet]. 2016 Feb ;96(2):168-72. https://doi.org/10.1007/s00128-015-1702-6
https://doi.org/10.1007/s00128-015-1702-...

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https://doi.org/10.1007/s001289900928...

22. Torres-Arreola L, Lopez-Carrillo L, Torres-Sanchez L, Cebrian M, Rueda C, Reyes R, et al. Levels of dichloro-dyphenyl-trichloroethane (DDT) metabolites in maternal milk and their determinant factors. Arch Environ Health. 1999 Mar-Apr;54(2):124-9. https://doi.org/10.1080/00039899909602247
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26. Pardío VT, Waliszewski SM, Aguirre AA, Coronel H, Burelo GV, Infanzon RM, et al. DDT and its metabolites in human milk collected in Veracruz City and suburban areas (Mexico). Bull Environ Contam Toxicol. 1998 Jun;60(6):852-7. https://doi.org/10.1007/s001289900705
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59. Corcellas C, Feo ML, Torres JP, Malm O, Ocampo-Duque W, Eljarrat E, et al. Pyrethroids in human breast milk: occurrence and nursing daily intake estimation. Environ Int. 2012 Oct;47:17-22.

60. Paumgartten FJR, Cruz CM, Chahoud I, Palavinskas R, Mathar W. PCDDs, PCDFs, PCBs, and other organochlorine compounds in human milk from Rio de Janeiro, Brazil. Environ Res. 2000 Jul;83(3):293-7. https://doi.org/10.1006/enrs.2000.4062
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61. Costet N, Pele F, Comets E, Rouget F, Monfort C, Bodeau-Livinec F, et al. Perinatal exposure to chlordecone and infant growth. Environ Res. 2015 Oct;142:123-34. https://doi.org/10.1016/j.envres.2015.06.023
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62. Tamayo R, Matus N, Montes L, Cristi R. Determination of polychlorinated biphenyls (PCBs) in human milk samples collected in 3 provinces of the Tenth Region, Chile. 1990. Rev Med Chil. 1994 Jul;122(7):746-53.

63. Brunetto R, Leon A, Burguera JL, Burguera M. Levels of DDT residues in human milk of Venezuelan women from various rural populations. Sci Total Environ. 1996 Jul;186(3):203-7. https://doi.org/10.1016/0048-9697 (96)05112-1
https://doi.org/10.1016/0048-9697 (96)05...

64. Rojas-Squella X, Santos L, Baumann W, Landaeta D, Jaimes A, Correa JC, et al. Presence of organochlorine pesticides in breast milk samples from Colombian women. Chemosphere. 2013 May;91(6):733-9. https://doi.org/10.1016/j.chemosphere.2013.02.026
https://doi.org/10.1016/j.chemosphere.20...

65. Chávez-Almazán LA, Diaz-Ortiz JS, Alarcón-Romero M, Dávila-Vazquez G, Saldarriaga-Noreña H, Waliszewski SM. Organochlorine pesticide levels in breast milk in guerrero, Mexico. Bull Environ Contam Toxicol. 2014 Sep;93(3):294-8. https://doi.org/10.1007/s00128-014-1308-4
https://doi.org/10.1007/s00128-014-1308-...

66. Polanco Rodríguez ÁG, Inmaculada Riba López M, Angel DelValls Casillas T, León JAA, Anjan Kumar Prusty B, Álvarez Cervera FJ. Levels of persistent organic pollutants in breast milk of Maya women in Yucatan, Mexico. Environ Monit Assess. 2017 Feb;189(2):59. https://doi.org/10.1007/s10661-017-5768-y
https://doi.org/10.1007/s10661-017-5768-...
-6767. Chávez-Almazán LA, Díaz-Ortiz JA, Saldarriaga-Noreña HA, Dávila-Vazquez G, Santiago-Moreno A, Rosas-Acevedo JL, et al. Análisis regional de la contaminación por plaguicidas organoclorados en leche humana en guerrero, México. Rev Int Contam Ambient. 2018 May;34(2):225-35. https://doi.org/10.20937/rica.2018.34.02.04
https://doi.org/10.20937/rica.2018.34.02...
were selected for study (Figure 1). The main reasons for excluding articles referred to their failure to meet the established regionality criteria (n = 29), research of pesticides in media other than breast milk (n = 23), and review studies (n = 3).

Figure 1
Flowchart of the search strategy used in this systematic review.

Characteristics of the Eligible Studies

All the studies included in this review were published from 1973 to 2020, most of which were from 1988 to 1999 (32.65%), conducted in Mexico (44.89%) and in Brazil (20.4%), with a cross-sectional design (79.59%), and a sample size smaller than 100 (65.3%). Most samples were collected from 1993 to 2002 (24.48%) and contemplated a rural and urban zone population (30.61%). Study participants’ age ranged from 13 to 44 years (Table 2).

Table 2
Characteristics of the studies included in this systematic review, 2022.

Risk of Bias Results

This review individually assessed risk of bias by the JBI Checklist for Prevalence Studies. After the methodological assessment following the JBI criteria, this systematic review included all 49 studies, categorizing most (65.30%) of them as having a low risk of bias; 26.53%, as with a medium risk of bias; and 8.16%, as with a high risk of bias (Figure 2). The criteria that scored most negatively among the selected studies referred to sample size adequacy (85.71%), analysis with sufficient sample coverage (85.71%), and recruitment of study participants (16.32%).

Figure 2
Risk of bias of the studies included in this systematic review using the Instituto Joanna Briggs critical appraisal tool for prevalence studies.

Prevalence and Main Pesticides Found in the Breast Milk of Women in Latin America

This review found pesticide contamination in the milk of lactating mothers in all included studies and a prevalence of pesticides ranging from < 30% (n = 1), 70 to 99.9% (n = 10), and 100% (n = 34), with the most frequent pesticides including dichlorodiphenyltrichloroethane (DDT) (75.51%), followed by dichlorodiphenyldichloroethylene (DDE) (69.38%) and hexachlorocyclohexane (HCH) (46.93%) (Table 3).

Table 3
Prevalence and types of pesticide contamination of lactating mothers’ milk in Latin America in the studies included in this systematic review, 2022.

DISCUSSION

This systematic review found a high prevalence of pesticide contamination in women’s breast milk in 11 Latin American countries from 1973 to 2020, of which 69.38% of the included studies found a 100% prevalence of pesticide contamination of breast milk among their sample. Of these, de Campos and Olszyna-Marzys4040. Campos M, Olszyna-Marzys AE. Contamination of human milk with chlorinated pesticides in Guatemala and in El Salvador. Arch Environ Contam Toxicol. 1979 Jan;8(1):43-58. https://doi.org/10.1007/BF01055139
https://doi.org/10.1007/BF01055139...
(carried out in Guatemala and El Salvador) stands out for its alarming data, in which, with the exception of one sample, all others showed pesticide contamination levels above the adequate limits for human consumption.

This high prevalence of pesticide contamination may be related to the unrestricted use of these substances in agricultural production since Latin American countries produce commodities for the international market6868. Carneiro FF, Augusto LGS, Rigotto RM, Friedrich K, Búrigo AC, organizadores. Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde. Rio de Janeiro: Escola Politécnica de Saúde Joaquim Venânico; São Paulo: Expressão Popular; 2015.. Among them, Brazil stands out as the biggest consumer of agrochemicals in the world since 20086868. Carneiro FF, Augusto LGS, Rigotto RM, Friedrich K, Búrigo AC, organizadores. Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde. Rio de Janeiro: Escola Politécnica de Saúde Joaquim Venânico; São Paulo: Expressão Popular; 2015. and as the second biggest buyer of substances already banned in Europe6969. Gaberell L, Hoinkes C. Lucros altamente perigosos: como a Syngenta ganha bilhões vendendo agrotóxicos nocivos. Lausanne: Public Eye; 2019.. Moreover, the number of pesticides released in the country has increased since 2015, reaching the highest rate of pesticide release in a year in 20197070. Lima MBS. Aspectos sociobiodiversos do novo marco regulatório para agrotóxicos publicado pela Agência Nacional de Vigilância Sanitária (ANVISA) [Trabalho de Conclusão de Curso]. Salvador: Universidade Católica do Salvador; 2020;.

In this systematic review, Brazil had the second highest production of data in relation to the presence of pesticides in breast milk, with most studies finding a high prevalence of contamination1414. Matuo YK, Lopes JN, Casanova IC, Matuo T, Lopes JL. Organochlorine pesticide residues in human milk in the Ribeirão Preto region, state of São Paulo, Brazil. Arch Environ Contam Toxicol. 1992 Feb;22(2):167-75. https://doi.org/10.1007/BF00213281
https://doi.org/10.1007/BF00213281...
,4242. Sant'Ana LS, Vassilieff I, Jokl L. Levels of organochlorine insecticides in milk of mothers from urban and rural areas of Botucatu, SP, Brazil. Bull Environ Contam Toxicol. 1989 Jun;42(6):911-8. https://doi.org/10.1007/BF01701635
https://doi.org/10.1007/BF01701635...
,4343. Beretta M, Dick T. Organochlorine compounds in human milk, Porto Alegre, Brazil. Bull Environ Contam Toxicol. 1994 Sep;53(3):357-60. https://doi.org/10.1007/BF00197226
https://doi.org/10.1007/BF00197226...
,4545. Azeredo A, Torres JPM, de Freitas Fonseca M, Britto JL, Bastos WR, Silva CE, et al. DDT and its metabolites in breast milk from the Madeira River basin in the Amazon, Brazil. Chemosphere [Internet]. 2008;73(1 Suppl.):S246-51. https://doi.org/10.1016/j.chemosphere.2007.04.090
https://doi.org/10.1016/j.chemosphere.20...

46. Lara WH, Barretto HHC, Inomata ONK. Residuos de pesticidas organoclorados em leite humano, Sao Paulo, Brasil, 1979-1981. Rev Inst Adolfo Lutz [Internet]. 1982 [cited 2023 June 15];42(1-2):45-52. Available from: https://www.scopus.com/inward/record.uri?eid=2-s2.0-0020273458&partnerID=40&md5=f6ef726d6551920da74ce82d492fd6ff
https://www.scopus.com/inward/record.uri...

47. Ferronato G, Viera MS, Prestes OD, Adaime MB, Zanella R. Determination of organochlorine pesticides (OCPs) in breast milk from Rio Grande do Sul, Brazil, using a modified QuEChERS method and gas chromatography-negative chemical ionisation-mass spectrometry. Int J Environ Anal Chem. 2018;98(11):1005-16. https://doi.org/10.1080/03067319.2018.1518441
https://doi.org/10.1080/03067319.2018.15...
-4848. Matuo YK. Níveis de praguicidas organoclorados no leite humano colostro da regiäo de Ribeiräo Preto TT - Levels of organochlorine pesticide in humana milk (colostrum) of Ribeiräo Preto region [Thesis].São Paulo: Universidade de São Paulo; 1987 [cited 2023 June 17]. Available from: http://pesquisa.bvsalud.org/portal/resource/pt/lil-67534
http://pesquisa.bvsalud.org/portal/resou...
,5555. Freguglia RMO, Moura Andrade GCR, Tornisielo VL. Determination of organochlorine pesticide residues in human milk in Piracicaba, SP. Eclet Quim [Internet]. 2011 [cited 2023 June 17];36(4):21-7. Available from: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85045264183&partnerID=40&md5=f5dfa5b85f51d24953cd66f45ec8fce0
https://www.scopus.com/inward/record.uri...
,5757. Souza RC, Portella RB, Almeida PVNB, Pinto CO, Gubert P, Santos da Silva JD, et al. Human milk contamination by nine organochlorine pesticide residues (OCPs). J Environ Sci Health B. 2020;55(6):530-8. https://doi.org/10.1080/03601234.2020.1729630
https://doi.org/10.1080/03601234.2020.17...
. The study by Souza et al.5757. Souza RC, Portella RB, Almeida PVNB, Pinto CO, Gubert P, Santos da Silva JD, et al. Human milk contamination by nine organochlorine pesticide residues (OCPs). J Environ Sci Health B. 2020;55(6):530-8. https://doi.org/10.1080/03601234.2020.1729630
https://doi.org/10.1080/03601234.2020.17...
(carried out in western Bahia, Brazil) stands out as they found two or more pesticide residues in all 34 analyzed samples, with methoxychlor, dieldrin, and endosulfan in highest mean concentrations.

The flexibilization of the legislation that regulates the use and sale of agrochemicals in Brazil may be reflected in the data from the analyzed studies since the prevalence of breast milk contamination varied from 65% to 100%.

On the other hand, Mexico has produced the most data on the presence of pesticides in breast milk, with a prevalence of contamination ranging from 76% to 100%. The pesticides registered and authorized for use in the country by its Federal Commission for Protection against Sanitary Risks in 2016 include 140 active ingredients that other countries have banned or unauthorized. Of these, 65 pesticides are considered highly dangerous according to the criteria established by the FAO and WHO7171. González FB, editor. Los plaguicidas altamente peligrosos en México. Texcoco: RAPAM; 2015..

Although the workers that directly handle these products (whether in transport/commerce, formulation, or application in farming and livestock) suffer more intense exposure, the general population also finds itself susceptible to contact with these chemical substances, primarily by food via the intake of residues in both unprocessed and processed foods7272. Instituto Nacional de Câncer José Alencar Gomes da Silva. Ambiente, trabalho e câncer: aspectos epidemiológicos, toxicológicos e regulatórios [Internet]. Rio de Janeiro: INCA; 2021 [cited 2023 June 15]. Available from: http://fi-admin.bvsalud.org/document/view/j9cnv
http://fi-admin.bvsalud.org/document/vie...
. This occurs because these substances not only persist in the environment for prolonged periods, but most also have a bioaccumulation capacity, contributing to the contamination of the soil, water, and foods1212. Corralo VS, Morais MM, Benedett A, Ferraz L. Presença de pesticidas organoclorados no leite materno: fatores de contaminação e efeitos à saúde humana. Hygeia. 2016 Jun;12(22):101-8..

Unprocessed and minimally processed foods, the basis for a nutritious diet, are recommended for mothers who are in the phase of producing breast milk and have a greater demand for energy and micronutrients7373. Ribeiro ECD, Moraes PMO, Moraes LP. Caracterização nutricional de nutrizes na segunda etapa do método canguru de um hospital amigo da criança. Rev Para Med. 2015 Jul-Set;29(3):21-8.. However, studies show that pesticide residues are increasingly contaminating these foods.

In all the years analyzed, data from the reports of the Program for Analyzing Pesticide Residues in Foods from 2008 to 2015 recorded pesticide residues above the maximum permitted residue limit or residues of unauthorized pesticides in pepper and cucumber crops, whereas more than half of pepper crop samples showed irregularities in all years7474. Balleste VM, Mantelli J. Presença de resíduos de agrotóxicos nos alimentos: um enfoque no pimentão e pepino. Geogr em Atos. 2020 Abr;2(17):44-63. https://doi.org/10.35416/geoatos.v2i17.6480
https://doi.org/10.35416/geoatos.v2i17.6...
.

Other studies also show pesticide contamination in foods frequently consumed by the Brazilian population, such as those conducted by Lemes et al7575. Lemes VRR, Kussumi TA, Nakano VE, Rocha SB, Oliveira MCC, Rodrigues MP, et al. Avaliação de resíduos de agrotóxicos em arroz e feijão e sua contribuição para prevenção de riscos à saúde da população consumidora. Rev Inst Adolfo Lutz. 2011;70(2):113-21., which found pesticide residues in 26 (59%) rice samples and in 11 (25%) bean samples, and Silva et al.7676. Rezende RAE, Nicoletti MA, Pereira AGA, Serafim BO, Paixão DF, Diniz JS, et al. Determinação de Paraquate em maçãs do tipo Gala, Fuji, Argentina e Verde. Vigil Sanit Debate. 2020;8(1):106-10., which found pesticide residues in Fuji- and Argentina-type apples sold in the Mooca region in the municipality of São Paulo.

Such chemical substances also widely contaminate processed foods. A study conducted by the Brazilian Consumer Defense Institute found at least one type of pesticide in 16 (59.3%) of the 27 analyzed ultra-processed foods, of which all those that contained wheat in their composition included pesticide residues7777. Instituto Brasileiro de Defesa do Consumidor. Tem veneno nesse pacote [Internet]. São Paulo: IDEC; 2021 [cited 2023 June 15]. Available from: https://idec.org.br/system/files/ferramentas/idec_cartilha_tem-veneno-nesse-pacote.pdf
https://idec.org.br/system/files/ferrame...
. It warrants highlighting that products derived from wheat are well accepted and widespread in the diet of Latin American populations.

Some studies in this review found higher levels of pesticides in women’s breast milk in rural and suburban areas, which may be associated with occupational exposure on large farms. Large-scale food production can create farmer dependency on agrochemicals for cultivation1515. Chávez-Almazán LA, Saldarriaga-Noreña HA, Díaz-González L, Garibo-Ruiz D, Waliszewski SM. Dietary habits associated with the presence of organochlorine pesticides in human milk. J Environ Sci Health B. 2020 Jul;55(8):756-66. https://doi.org/10.1080/03601234.2020.1783169
https://doi.org/10.1080/03601234.2020.17...
,2222. Torres-Arreola L, Lopez-Carrillo L, Torres-Sanchez L, Cebrian M, Rueda C, Reyes R, et al. Levels of dichloro-dyphenyl-trichloroethane (DDT) metabolites in maternal milk and their determinant factors. Arch Environ Health. 1999 Mar-Apr;54(2):124-9. https://doi.org/10.1080/00039899909602247
https://doi.org/10.1080/0003989990960224...
,2525. Elvia LF, Sioban HD, Bernardo HP, Constanza SC. Organochlorine pesticide exposure in rural and urban areas in Mexico. J Expo Sci Environ Epidemiol. 2000 Aug;10(4):394-9. https://doi.org/10.1038/sj.jea.7500103
https://doi.org/10.1038/sj.jea.7500103...
,2626. Pardío VT, Waliszewski SM, Aguirre AA, Coronel H, Burelo GV, Infanzon RM, et al. DDT and its metabolites in human milk collected in Veracruz City and suburban areas (Mexico). Bull Environ Contam Toxicol. 1998 Jun;60(6):852-7. https://doi.org/10.1007/s001289900705
https://doi.org/10.1007/s001289900705...
,3131. Waliszewski SM, Bermúdez MT, Infanzón RM. DDT levels in maternal adipose tissue, blood serum and milk of mothers living in Veracruz, Mexico. Study 1997-1999. Rev Int Contam Ambient. 2002 Jan;18(1):17-25.,4242. Sant'Ana LS, Vassilieff I, Jokl L. Levels of organochlorine insecticides in milk of mothers from urban and rural areas of Botucatu, SP, Brazil. Bull Environ Contam Toxicol. 1989 Jun;42(6):911-8. https://doi.org/10.1007/BF01701635
https://doi.org/10.1007/BF01701635...
,4848. Matuo YK. Níveis de praguicidas organoclorados no leite humano colostro da regiäo de Ribeiräo Preto TT - Levels of organochlorine pesticide in humana milk (colostrum) of Ribeiräo Preto region [Thesis].São Paulo: Universidade de São Paulo; 1987 [cited 2023 June 17]. Available from: http://pesquisa.bvsalud.org/portal/resource/pt/lil-67534
http://pesquisa.bvsalud.org/portal/resou...
,5252. Waliszewski SM, Pardio Sedas VT, Chantiri JN, Infanzon RM, Rivera J. Organochlorine pesticide residues in human breast milk from tropical areas in Mexico. Bull Environ Contam Toxicol. 1996 Jul;57(1):22-8. https://doi.org/10.1007/s001289900150
https://doi.org/10.1007/s001289900150...
,5959. Corcellas C, Feo ML, Torres JP, Malm O, Ocampo-Duque W, Eljarrat E, et al. Pyrethroids in human breast milk: occurrence and nursing daily intake estimation. Environ Int. 2012 Oct;47:17-22.. However, other studies4242. Sant'Ana LS, Vassilieff I, Jokl L. Levels of organochlorine insecticides in milk of mothers from urban and rural areas of Botucatu, SP, Brazil. Bull Environ Contam Toxicol. 1989 Jun;42(6):911-8. https://doi.org/10.1007/BF01701635
https://doi.org/10.1007/BF01701635...
,4444. Limon-Miro AT, Aldana-Madrid ML, Alvarez-Hernandez G, Antunez-Roman LE, Rodriguez-Olibarria G, Valencia Juillerat ME. Breast milk intake and mother to infant pesticide transfer measured by deuterium oxide dilution in agricultural and urban areas of Mexico. Chemosphere. 2017 Aug;181:682-9. https://doi.org/10.1016/j.chemosphere.2017.04.110
https://doi.org/10.1016/j.chemosphere.20...
found higher levels of DDT in breast milk samples derived from women in the urban zone. These findings are associated with the dietary habits of that population, which show higher meat consumption than rural populations4242. Sant'Ana LS, Vassilieff I, Jokl L. Levels of organochlorine insecticides in milk of mothers from urban and rural areas of Botucatu, SP, Brazil. Bull Environ Contam Toxicol. 1989 Jun;42(6):911-8. https://doi.org/10.1007/BF01701635
https://doi.org/10.1007/BF01701635...
.

Amidst the intense use of pesticides for food production, organic farming offers an excellent alternative to traditional means of production. By adopting sustainable practices without the use of pesticides and chemical inputs, it contributes not only to protecting the health and healthy development of future generations, but also to preserving biodiversity and the environment7878. Terra SB, Costa JEL. Nível de informação e consumo da população sobre produtos orgânicos em Santana do Livramento, Rio Grande do Sul. Rev Verde Agroecol Desenvolv Sustentável. 2017;12(2):311-8. https://doi.org/10.18378/rvads.v12i2.4822
https://doi.org/10.18378/rvads.v12i2.482...
. This agricultural approach based on agroecological principles reduces the risks associated with pesticide contamination and promotes the preservation of local ecosystems.

It is also important to place greater value on food production derived from small farmers that use alternative inputs instead of the conventional methods adopted by agribusiness (pesticides, transgenic seeds, and chemical fertilizers)7979. Almeida EW, Stumpf MT, Porto CRP, Rolon AS, Trentin G. Potencial agroecológico de propriedades agrícolas familiares do município de São Lourenço do Sul, Rio Grande do Sul. Rev Verde Agroecol e Desenvolv Sustentável. 2019;14(4):546-53..

Notably, the Dietary Guide for the Brazilian population8080. Brasil. Guia alimentar para a população brasileira. 2. ed. Brasília, DF: Ministério da Saúde; 2014., for children aged under two years8181. Brasil. Guia Alimentar para crianças brasileiras menores de 2 anos. Brasília, DF: Ministério da Saúde; 2019., and the Mexican8282. Arenas AB, Fernández-Gaxiola AC, Belausteguigoitia MP, Kaufer-Horwitz M, Pérez-Lizaur AB, Dommarco JR. Guías alimentarias y de actividad física: en contexto de sobrepeso y obesidad en la población mexicana: documento de postura. Ciudad de México: CONACYT; 2015. and Guatemalan8383. Alonzo AF, Mendoza A, Nuñez E, Mejía V, Pérez A, López S. Guías alimentarias para Guatemala: Recomendaciones para una alimentación saludable. Ciudad de Guatemala: Ministerio de Salud Publica y Asistencia Social; 2012. dietary guides recommend that unprocessed and minimally processed foods should constitute the basis for an adequate and healthy diet and that the consumption of processed and ultra-processed foods should be limited. These recommendations, adapted to regional dietary habits, contribute to making appropriate food choices and strengthening more sustainable production systems8181. Brasil. Guia Alimentar para crianças brasileiras menores de 2 anos. Brasília, DF: Ministério da Saúde; 2019..

Regarding pesticides and their metabolites, most studies (75.51%) found DDT and its isomers, followed by its metabolite DDE (69.38%) and HCH (46.93%). Contamination by DDT has a greater relation with its inhalation and food contamination given its high topical toxicity8484. D'amato C, Torres JPM, Malm O. DDT (dicloro difenil tricloroetano): toxicidade e contaminação ambiental-uma revisão. Quim Nova. 2002 Nov;25(6a):995-1002., representing more recent exposure to the substance. In turn, the metabolite DDE represents prior exposure to DDT and its persistence in the environment8585. Marques JPLD. Resíduos de pesticidas Organoclorados em leite materno. Coimbra: Universidade de Coimbra; 2016..

HCH exposure, in turn, more frequently occurs by inhalation due to occupational use or via the digestive tract from the consumption of contaminated foods by people not occupationally exposed, most often affecting liver functions. Also, despite a lack of evidence of its carcinogenicity in human beings, experimental studies show positive findings for malignant neoplasias8686. Mendes R. Hexaclorociclohexano (HCH) e a Saúde Humana: síntese do estágio atual do conhecimento e identificação das principais questões controversas. Brasília, DF: Ministério da Saúde; 2001..

Exposure to these toxic substances negatively affects the population’s health, especially more vulnerable groups such as pregnant women, infants, and breastfeeding children. Various studies relate pesticide exposure with adverse effects on leukocyte growth and development, thus interfering with bodily immune functions8787. Lee GH, Choi KC. Adverse effects of pesticides on the functions of immune system. Comp Biochem Physiol Part C Toxicol Pharmacol. 2020 Sep;235:108789., causing dysfunctions to the nervous, reproductive, and endocrine system1212. Corralo VS, Morais MM, Benedett A, Ferraz L. Presença de pesticidas organoclorados no leite materno: fatores de contaminação e efeitos à saúde humana. Hygeia. 2016 Jun;12(22):101-8. and increasing the risk of developing breast, digestive, genital, urinary, and respiratory cancer8888. Silva AC, Camponogara S, Viero CM, Menegat RP, Dias GL, Miorin JD. Perfil socioeconômico de Trabalhadores Rurais portadores de neoplasia Socioeconomic profile of Rural Workers cancer sufferers. Rev Pesqui. 2016 Jul;8(3):4891-7. https://doi.org/10.9789/2175-5361.2016.v8i3.4891-4897
https://doi.org/10.9789/2175-5361.2016.v...
.

Considering the different possibilities of pesticide exposure, it is plausible to infer that breast milk contamination could be substantially higher than currently estimated, especially if we consider that most existing studies tend to focus on a limited set of pesticides, which may underestimate the reality of exposure. Therefore, more comprehensive research is essential to identify and quantify these chemical compounds, providing a more accurate view of potential risks to maternal and child health.

Breast milk is the ideal food for child nutrition and development, especially in the first months of children’s lives, and it should not contain undesirable chemical substances. Pesticides and the health problems related to their use configure a serious public health problem because child and breastfeeding infant exposure to pesticides may be associated with various health problems, such as the development of leukemia and other types of cancer, low birth weight, birth defects, cognitive deficit, and a low intelligence quotient8989. Rozas ME. Revisión de estudios epidemiológicos sobre efectos de los plaguicidas en niñas, niños e infantes en América Latina. Retos para la salud pública. Santiago de Chile: Red de Acción en Plaguicidas y sus Alternativas de América Latina; 2021..

Results of a longitudinal study suggest that fetal exposure to DDE during the first trimester of pregnancy can negatively affect children’s psychomotor development during their first year of life9090. Torres-Sánchez L, Rothenberg SJ, Schnaas L, Cebrián ME, Osorio E, del Carmen Hernández M, et al. In utero p, p'-DDE exposure and infant neurodevelopment: a perinatal cohort in Mexico. Environ Health Perspect. 2007 Jan;115(3):435-9. https://doi.org/10.1289/ehp.9566
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. Several studies have also shown an association between fathers who were exposed to pesticides and congenital malformations in their children, especially those related to the male reproductive system9191. Michalakis M, Tzatzarakis MN, Kovatsi L, Alegakis AK, Tsakalof AK, Heretis I, et al. Hypospadias in offspring is associated with chronic exposure of parents to organophosphate and organochlorine pesticides. Toxicol Lett. 2014 Oct;230(2):139-45. https://doi.org/10.1016/j.toxlet.2013.10.015
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, central nervous system outcomes9292. Kalra S, Dewan P, Batra P, Sharma T, Tyagi V, Banerjee BD. Organochlorine pesticide exposure in mothers and neural tube defects in offsprings. Reprod Toxicol. 2016 Dec;66:56-60. https://doi.org/10.1016/j.reprotox.2016.09.005
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, and fetal growth restrictions9393. Sharma E, Mustafa M, Pathak R, Guleria K, Ahmed RS, Vaid NB, et al. A case control study of gene environmental interaction in fetal growth restriction with special reference to organochlorine pesticides. Eur J Obstet Gynecol Reprod Biol. 2012 Apr;161(2):163-9. https://doi.org/10.1016/j.ejogrb.2012.01.008
https://doi.org/10.1016/j.ejogrb.2012.01...
.

In women, this exposure is associated with endocrine/hormonal dysregulation, breast cancer, risk of depression99. Nascimento BP, Silva RCGF, Ferreira AP, Silva EC, Figueiredo Junior JA, Oliveira Dias LL, et al. Impacto ambiental sobre a saúde humana devido à exposição aos agrotóxicos. UNICIÊNCIAS. 2021;25(1):44-56., kidney diseases, predisposition to ovarian and thyroid cancer, diabetes, and an increased likelihood of polycystic ovary syndrome9494. Fernandino SSG. (In)visibilidade dos agrotóxicos na saúde integral de mulheres rurais [dissertação de mestrado]. Viçosa: Universidade Federal de Visoça; 2019..

Although beyond the scope of this study, some factors worsen the toxic effects of pesticides, such as malnutrition — 53.7 million people lived in poverty and under severe food insecurity in Latin America from 2016 and 20188989. Rozas ME. Revisión de estudios epidemiológicos sobre efectos de los plaguicidas en niñas, niños e infantes en América Latina. Retos para la salud pública. Santiago de Chile: Red de Acción en Plaguicidas y sus Alternativas de América Latina; 2021.. These numbers tend to increase given the COVID-19 pandemic and the related political and economic instability that resumed food and nutritional insecurity—with a significant expression of hunger in Latin American countries—and should thus be considered in this discussion9595. Food and Agriculture Organization of the United Nations. The state of food security and nutrition in the world 2020: transforming food systems for affordable healthy diets. Rome: FAO; 2020..

Strengths and Limitations

Some limitations of this systematic review are related to the relative need for up-to-date studies in Latin America. Most of the available studies that show the levels of contamination of breast milk in these countries are old. So, more studies must be carried out to identify current contamination levels, covering sample numbers that represent the studied population since the risk of bias analysis in this study showed inadequate sample sizes that may raise the risk of bias in the sample of this review. Therefore, we ignored a meta-analysis with the data from these studies.

Nonetheless, we believe that there is no interference in the results of this review since it involves prevalence studies without an associative purpose; includes the methodological rigor employed by its independent reviewers; and involves the databases recommended by systematic review guidelines, gray literature, and the assessment of the risk of bias in the studies that met its eligibility criteria, rendering a consistent study that produced useful results for public health.

Recommendations

The systematization of scientific production in Latin America showed a high prevalence of pesticides and their metabolites in the breast milk of women in that region, suggesting that direct or indirect exposure to pesticides configures a condition in these women’s everyday lives that can be considered a serious public health problem in the studied group given its negative impact on maternal and infant health. We should highlight that these results are unable to support the interruption of exclusive breastfeeding since contamination reflects environmental and occupational exposure and the consumption of foods containing pesticide residues.

Results may contribute to broadening the knowledge on the topic and educating the population about the violation of rights associated with the indiscriminate release of pesticides in the studied countries. However, additional epidemiological investigations with adequate sample sizes are recommended for the evaluation of breast milk contamination levels and the identification of the possible potentiators of the effects of these metabolites on maternal and infant health over time.

Moreover, public health interventions are needed for the pre-natal and post-partum period to guide women toward strategies to prevent and minimize pesticide exposure and guarantee the stimulation of exclusive breastfeeding up to the sixth month of infants’ lives (complemented up to two years or more) to ensure children’s healthy growth and development.

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  • Funding: None.

Publication Dates

  • Publication in this collection
    13 May 2024
  • Date of issue
    2024

History

  • Received
    20 Mar 2023
  • Accepted
    15 Oct 2023
Faculdade de Saúde Pública da Universidade de São Paulo São Paulo - SP - Brazil
E-mail: revsp@org.usp.br