Abstract

Brazil is the main consumer of pesticides in the world. Large-scale use of these products is likely to contaminate major environmental compartments and expose more people to their toxic effects. Therefore, this literature review was carried out to seek supporting elements for a qualified discussion about the performance of Environmental Surveillance (HS) within the Brazilian Unified Health System (SUS) related to air contamination by pesticides and health risks. Twelve papers were selected and analyzed in this literature review. Of these, only one was published in a specialized public health journal. Notwithstanding this, two epidemiological studies published in the field of environmental sciences investigated the association between air contaminated by pesticides and specific outcomes such as non-Hodgkin’s lymphoma (NHL) and amyotrophic lateral sclerosis (ALS). Our findings reflect the lack of studies addressing such issue by public health. The discussion on air contamination by pesticides and potential risks to human health should be expanded by Brazilian science in order to further increase knowledge on the subject and support the HS performance capacity.

Pesticides; Air pollution; Environmental health; Public Health Surveillance

Introduction

Increased productivity, strong monoculture presence, field mechanization, export agribusiness and pesticides consumption are characteristics of the so-called Brazilian “agricultural modernization” begun in the 1960s and 1970s¹1. Porto MF, Milanez B. Eixos de desenvolvimento econômico e geração de conflitos socioambientais no Brasil: desafios para a sustentabilidade e a justiça ambiental. Cien Saude Colet 2009; 14(6):1983-1994.. However, the development of this agricultural model to current times has been responsible for impacts and damages to the environment and public health²2. Porto MF, Soares WL. Modelo de desenvolvimento, agrotóxicos e saúde: um panorama da realidade agrícola brasileira e propostas para uma agenda de pesquisa inovadora. Rev Bras Saúde Ocup 2012; 37(125):17-31..

The National Program of Agricultural Pesticides (PNDA) launched in 1975 and based on an official government policy to encourage the consumption of pesticides contributed to the intensified use of these products in the country. The policy thus fostered the adoption of measures such as exemption from levies and import taxes, in addition to expanded subsidized agricultural credit³3. Bull D, Hathaway D. Pragas e Venenos: Agrotóxicos no Brasil e no Terceiro Mundo. Petrópolis: Vozes, Oxfam, Fase; 1986..

In the 1990s, the Brazilian market-oriented and profit-driven Brazilian agricultural industry increased the consumption of pesticides. In 2008, Brazil became the world’s leading consumer of pesticides. This fact, combined with the poor management and control of consumption by the environmental agencies resulted in a worrisome national setting both from the environmental viewpoint and from public health, which is the focus of this review.

When used, pesticides can easily divert their primary purpose of fighting target species, also known as “pests”. The toxicity of these products is directly related to the undesirable effects observed in other living organisms, communities, ecosystems and to the contamination of the main environmental compartments: water, soil and air⁴4. van der Werf HMG. Assessing the impact of pesticides on the environment. Agric Ecosyst Environ 1996; 60(2-3):81-96.

5. Belden JB, Hanson BR, McMurry ST, Smith LM, Haukos DA. Assessment of the Effects of Farming and Conservation Programs on Pesticide Deposition in High Plains Wetlands. Environ Sci Technol 2012; 46(6):3424-3432.

6. Köck-Schulmeyer M, Ginebreda A, Postigo C, Garrido T, Fraile J, López de Alda M, Barceló D. Four-year advanced monitoring program of polar pesticides in groundwater of Catalonia (NE-Spain). Sci Total Environ 2014; 470-471:1087-1098.^-77. Peres F, Oliveira-Silva JJ, Della-Rosa HV, Lucca SR. Desafios ao estudo da contaminação humana e ambiental por agrotóxicos. Cien Saude Colet 2005; 10(Supl.):27-37..

Pesticides easily spread in the environment and can reach the atmosphere and contaminate the surroundings of the place of application thanks to its volatization potential from soil, water and vegetal surface (physicochemical property inherent to pesticides, which varies according to the active principle)⁵5. Belden JB, Hanson BR, McMurry ST, Smith LM, Haukos DA. Assessment of the Effects of Farming and Conservation Programs on Pesticide Deposition in High Plains Wetlands. Environ Sci Technol 2012; 46(6):3424-3432.^,88. Coscollà C, Colin P, Yahyaoui A, Petrique O, Yusà V, Mellouki A, Pastor A. Occurrence of currently used pesticides in ambient air of Centre Region (France). Atmos Environ 2010; 44(32):3915-3925.. Other physicochemical attributes and mechanisms that include the incineration of contaminated waste, temperature, weather conditions and type of management of these products may also be related to air contamination by pesticides⁹9. Breivik K, Alcock R, Li Y-F, Bailey RE, Fiedler H, Pacyna JM. Primary sources of selected POPs: regional and global scale emission inventories. Environ Pollut 2004; 128(1):3-16..

In 2000, the National Health Foundation (Funasa), an agency of the Ministry of Health, through Decree No. 3,450/2000, officially launched in Brazil the process of implementation of Environmental Surveillance (ES) in the SUS, focused on the refurbishment of Zoonosis Control Centers and structuring of the Drinking Water Quality Information System (SISAGUA). From that point on, some institutional restructuring was implemented and new normative instruments appeared to adjust the configuration of EHS to the model that is currently in force and that includes the surveillance of pesticide-exposed populations¹⁰10. Brasil. Decreto nº 3.450, de 9 de maio de 2000. Aprova o Estatuto e o Quadro Demonstrativo dos Cargos em Comissão e das Funções Gratificadas da Fundação Nacional de Saúde - FUNASA, e dá outras providências. Diário Oficial da União 2000; 10 maio..

Based on Normative Instruction N° 1 of the Health Surveillance Secretariat (SVS) of the Ministry of Health, established in 2005, the General Coordination Office of Environmental Surveillance (CGVAM), previously exercised within FUNASA, was reorganized and assumed a technical structure based on risk management: (i) Drinking Water Quality Surveillance (VIGIAGUA); (ii) Health Surveillance of Populations Exposed to Chemical Contaminants (VIGIPEQ), focused on priority chemical substances (pesticides, benzene, lead, asbestos and mercury), currently also involving VIGISOLO activities (contaminated areas); (iii) Air-exposed populations surveillance (VIGIAR), today unlinked from VIGIPEQ; and (iv) Environmental Surveillance of Risks Associated with Disasters (VIGIDESASTRES), encompassing VIGIFIS (related to physical factors) and also VIGIAPP (related to accidents with dangerous products)¹¹11. Rohlfs DB, Grigoletto JC, Netto GF, Rangel CF. A construção da Vigilância em Saúde Ambiental no Brasil. Cad Saúde Colet 2011; 19(4):391-398..

The development and application of methods to detect the presence of pesticides in the air is not a new subject in the field of environmental sciences. The risk to the environment and to human health due to the contamination by pesticides has also been investigated over the years and is therefore not an unprecedented agenda for science.

However, the problem of pesticides in the context of Health Surveillance has traditionally focused on worker’s health, soil and water. Thus, it is necessary to start the discussion on the matter in order to promote the improvement of Environmental Surveillance measures for population groups exposed to air contaminated by pesticides.

Thus, the dispersion of pesticides in the air consists of a transversal matter that requires permanent dialogue between VIGIPEQ and VIGIAR technical areas for the development of technical-scientific material that subsidizes the construction of adequate public policies to strengthen the EHS at the federal level. Therefore, the EHS’ primary scope is related to the instrumentalization of the SUS for the planning and execution of actions aimed at health promotion, prevention and control of damages associated with environmental factors, from the viewpoint of integrality.

Despite the relevance of this issue to Environmental Surveillance with regard to the risk to human health, environmental monitoring and entry routes of such substances into the body of exposed individuals, especially those belonging to more vulnerable population groups (children, the elderly and workers), we note a lack of Brazilian studies on this issue.

The scope of this review is not limited to exploring studies whose air contamination by pesticides has occurred by means of spraying processes and resulting drifts, nor does it intend to seek specific health outcomes potentially associated with pesticide contamination. The reason of this study is to expand the understanding of contamination mechanisms of the environmental matrix “air” and its effects on human health in the scope of Environmental Surveillance.

Therefore, the purpose of this bibliographic review is to gather and analyze the scientific publications of the last five years on air contamination by pesticides, the effects on human health and possible impacts on public health, in order to further reflect on the formulation of Environmental Surveillance strategies in the country on the subject, as well as the capacity to promote a qualified action supported by scientific evidence.

Methods

This is a systematic review of literature based on the online search in databases for the dissemination of scientific and technical knowledge in health sciences: PubMed – developed and maintained by the National Center for Biotechnology Information (NCBI) of the United States – and by the Virtual Health Library (BVS) / Regional Library of Medicine (Bireme) – specialized center of the Pan American Health Organization / World Health Organization (PAHO/WHO).

A preliminary search was conducted for subject descriptors that could result in a research with little noise and that satisfied the primary objective of the study. Thus, descriptors “pesticides”, “air pollutants”, “public health”, “risk” and their English correspondents were used in this study.

The research used the relationship of terms and identified 28 publications in the last five years exclusively from PubMed. From these, we resorted to reading the abstracts and titles to guide the selection of papers to be carefully analyzed and included in the review.

At this stage, the authors agreed, after extensive discussion, to exclude studies that were devoted to assessing exposure in work environments, given the specificity of certain occupational groups, whose nature of work presupposes a greater exposure than that observed in the general population, such as with farmers and workers in agrochemical industries, for example.

Of the 12 papers previously eligible for review, one could not be accessed, remaining 11 papers. On the other hand, we noticed that the bibliographic search was not able to capture one of three papers published in series, probably due to the specificity of the subject. Then, an independent search for that paper was carried out. After a preliminary review of the paper, authors agreed to include it in this review by completing the three-part series. Thus, the review was performed from 12 papers (n = 12), since that relevant paper was added in isolation to the 11 papers included in advance.

Finally, we performed a critical reading of the 12 papers included in the study, which were individually analyzed, according to the criteria of originality, relevance and adequacy to the purpose of this study (Figure 1).

In the analysis of the included studies, comparisons of the information available in each of them were made. The presentation and discussion of the results obtained focused on the following perspectives: potential health effects, exposure assessment and environmental monitoring of air contaminated by pesticides.

Results

The electronic search identified 28 studies. Of these, 12 papers were previously selected, and one was eliminated because it was in Chinese and was not published in Portuguese or English. In addition, this article was not available in the databases that we accessed in the conduction of this study. In contrast, a paper previously excluded by search engines and related to the other two of this review was added last.

Finally, of the 12 papers included in the review, six originated from the United States¹²12. Batterman S, Chin J-Y, Jia C, Godwin C, Parker E, Robins T, Max P, Lewis T. Sources, concentrations, and risks of naphthalene in indoor and outdoor air. Indoor Air 2012; 22(4):266-278.

13. Segawa R, Levine J, Neal R, Brattesani M. Community air monitoring for pesticides. Part 1: selecting pesticides and a community. Environ Monit Assess 2014; 186(3):1327-1341.

14. Hengel M, Lee P. Community air monitoring for pesticides - part 2: multiresidue determination of pesticides in air by gas chromatography, gas chromatography-mass spectrometry, and liquid chromatography-mass spectrometry. Environ Monit Assess 2014; 186(3):1343-1353.

15. Wofford P, Segawa R, Schreider J, Federighi V, Neal R, Brattesani M. Community air monitoring for pesticides. Part 3: Using health-based screening levels to evaluate results collected for a year. Environ Monit Assess 2014; 186(3):1355-1370.

16. Kumar S, Khodoun M, Kettleson EM, McKnight C, Reponen T, Grinshpun SA, Adhikari A. Glyphosate-rich air samples induce IL-33, TSLP and generate IL-13 dependent airway inflammation. Toxicology NIH Public Access 2014; 325:42-51.^-1717. Malek AM, Barchowsky A, Bowser R, Heiman-Patterson T, Lacomis D, Rana S, Ada Y, Talbott EO. Exposure to hazardous air pollutants and the risk of amyotrophic lateral sclerosis. Environ Pollut 2015; 197:181-186., one each from Australia¹⁸18. Stewart BW. Priorities for cancer prevention: Lifestyle choices versus unavoidable exposures. Lancet Oncol 2012; 13(3):e126-33., France¹⁹19. Viel J-F, Floret N, Deconinck E, Focant J-F, De Pauw E, Cahn J-Y. Increased risk of non-Hodgkin lymphoma and serum organochlorine concentrations among neighbors of a municipal solid waste incinerator. Environ Int 2011; 37(2):449-453., Armenia²⁰20. Dvorská A, Šír M, Honzajková Z, Komprda J, Čupr P, Petrlík J, Anakhasyan E, Simonyan L, Kubal M. Obsolete pesticide storage sites and their POP release into the environment - an Armenian case study. Environ Sci Pollut Res 2012; 19(6):1944-1952. and Portugal²¹21. Ratola N, Homem V, Silva JA, Araújo R, Amigo JM, Santos L, Alves A. Biomonitoring of pesticides by pine needles - Chemical scoring, risk of exposure, levels and trends. Sci Total Environ 2014; 476-477:114-124. and two in Pakistan²²22. Mahmood A, Malik RN, Li J, Zhang G. Human health risk assessment and dietary intake of organochlorine pesticides through air, soil and food crops (wheat and rice) along two tributaries of river Chenab, Pakistan. Food Chem Toxicol 2014; 71:17-25.^,2323. Sultana J, Syed JH, Mahmood A, Ali U, Rehman MYA, Malik RN, Li J5, Zhang G. Investigation of organochlorine pesticides from the Indus Basin, Pakistan: Sources, air-soil exchange fluxes and risk assessment. Sci Total Environ 2014; 497-498:113-122.. These were published in specialized journals in the areas of environmental sciences (n = 9), health (n = 1) and toxicology (n = 2) (Chart 1).

We observed that the only published work in the health area included a literature review addressing general concepts in environmental health and the possible environmental risk factors for the development of cancer, among them air pollution, pointed by the author as an example of causal association well established in literature¹⁸18. Stewart BW. Priorities for cancer prevention: Lifestyle choices versus unavoidable exposures. Lancet Oncol 2012; 13(3):e126-33..

Interestingly, two epidemiological case-control studies that sought to associate exposure of air contaminated with pesticides were not published in public health journals, commonly observed in investigations with this objective and approach¹⁷17. Malek AM, Barchowsky A, Bowser R, Heiman-Patterson T, Lacomis D, Rana S, Ada Y, Talbott EO. Exposure to hazardous air pollutants and the risk of amyotrophic lateral sclerosis. Environ Pollut 2015; 197:181-186.^,1919. Viel J-F, Floret N, Deconinck E, Focant J-F, De Pauw E, Cahn J-Y. Increased risk of non-Hodgkin lymphoma and serum organochlorine concentrations among neighbors of a municipal solid waste incinerator. Environ Int 2011; 37(2):449-453..

One of them¹⁹19. Viel J-F, Floret N, Deconinck E, Focant J-F, De Pauw E, Cahn J-Y. Increased risk of non-Hodgkin lymphoma and serum organochlorine concentrations among neighbors of a municipal solid waste incinerator. Environ Int 2011; 37(2):449-453. sought association between organochlorines (OC) from an incineration plant in Besançon, France, and development of non-Hodgkin’s lymphoma (NHL). Of the OCs evaluated, Beta-hexachlorocyclohexane [OR = 1.05; 95% CI: 1.00-1.2] and DDT (OR = 1.20, 95% CI: 1.01-1.45) were associated with NHL. However, another study with the same approach conducted by Malek et al.¹⁷17. Malek AM, Barchowsky A, Bowser R, Heiman-Patterson T, Lacomis D, Rana S, Ada Y, Talbott EO. Exposure to hazardous air pollutants and the risk of amyotrophic lateral sclerosis. Environ Pollut 2015; 197:181-186. found no association between pesticides and the development of amyotrophic lateral sclerosis (ALS).

Much in the same way as these, seven other papers¹²12. Batterman S, Chin J-Y, Jia C, Godwin C, Parker E, Robins T, Max P, Lewis T. Sources, concentrations, and risks of naphthalene in indoor and outdoor air. Indoor Air 2012; 22(4):266-278.^,1313. Segawa R, Levine J, Neal R, Brattesani M. Community air monitoring for pesticides. Part 1: selecting pesticides and a community. Environ Monit Assess 2014; 186(3):1327-1341.^,1515. Wofford P, Segawa R, Schreider J, Federighi V, Neal R, Brattesani M. Community air monitoring for pesticides. Part 3: Using health-based screening levels to evaluate results collected for a year. Environ Monit Assess 2014; 186(3):1355-1370.^,2020. Dvorská A, Šír M, Honzajková Z, Komprda J, Čupr P, Petrlík J, Anakhasyan E, Simonyan L, Kubal M. Obsolete pesticide storage sites and their POP release into the environment - an Armenian case study. Environ Sci Pollut Res 2012; 19(6):1944-1952.

21. Ratola N, Homem V, Silva JA, Araújo R, Amigo JM, Santos L, Alves A. Biomonitoring of pesticides by pine needles - Chemical scoring, risk of exposure, levels and trends. Sci Total Environ 2014; 476-477:114-124.

22. Mahmood A, Malik RN, Li J, Zhang G. Human health risk assessment and dietary intake of organochlorine pesticides through air, soil and food crops (wheat and rice) along two tributaries of river Chenab, Pakistan. Food Chem Toxicol 2014; 71:17-25.^-2323. Sultana J, Syed JH, Mahmood A, Ali U, Rehman MYA, Malik RN, Li J5, Zhang G. Investigation of organochlorine pesticides from the Indus Basin, Pakistan: Sources, air-soil exchange fluxes and risk assessment. Sci Total Environ 2014; 497-498:113-122. addressed the issue of air contamination by pesticides from the perspective of environmental sciences (environmental monitoring and risk analysis and assessment), while the methodology for assessing the impact and risk of exposure frequently observed in these studies includes, somehow, analyses of public health interest, such as the estimation of risk or carcinogenic potential related to exposure to pesticides, according to risk assessment methodologies proposed by international agencies of the environmental or health sector, such as the U.S. Environmental Protection Agency (US EPA) and the World Health Organization (WHO).

Discussion

This work was motivated by the need to better understand the potential routes, sources, mechanisms and possible health impacts of populations potentially exposed to air contaminated by pesticides, in order to initiate discussions among researchers, managers and interested stakeholders, given the relevance of this theme to the consolidation of Environmental Surveillance actions in the country.

Equally important would be to perform further studies on the issue addressed in order to consider the possibility of elaborating and adopting future Environmental Surveillance measures aiming at risk mitigation or elimination, prevention and control.

The agricultural sector is the main responsible for the release of pesticides in the environment. As shown by Ratola et al.²¹21. Ratola N, Homem V, Silva JA, Araújo R, Amigo JM, Santos L, Alves A. Biomonitoring of pesticides by pine needles - Chemical scoring, risk of exposure, levels and trends. Sci Total Environ 2014; 476-477:114-124., rural areas are potentially more polluted than areas close to industries, followed by urban areas, in terms of air pollution by pesticides.

Municipalities surrounded by large plantations or close to the rural area, as occurs in regions of Brazil with predominance of the agricultural model based on monoculture and focused on supplying the international market, should also be a priority in terms of Environmental Surveillance, including with regard to air contamination. This is because the distribution of risk occurs unevenly in the territory, especially affecting rural or urban communities influenced by this type of agriculture.

At the beginning of the search, we expected to find in scientific literature a sufficient number of papers that explored the issue of air contamination by pesticides related to the application method – spray drift of pesticides in plantations – contaminating populations and surrounding areas. This example may be related to the episode occurred in the Mato Grosso state’s municipality of Lucas do Rio Verde in March 2006, referred to as an expanded rural accident, which brought the theme of the issue to Brazilian public health, culminating with publication in scientific journals²⁴24. Pignati WA, Machado JMH, Cabral JF. Acidente rural ampliado: o caso das “chuvas” de agrotóxicos sobre a cidade de Lucas do Rio Verde - MT. Cien Saude Colet 2007; 12(1):105-114..

However, the bibliographic research that considered the environmental air contamination, excluding the specific work environments – occupational exposure – was scarce and returned 12 papers in the last five years. Surprisingly, none of them referred to studies carried out in Brazil, revealing a contradiction, given the prevailing agricultural production process model in the country, with a high dependence on agrochemicals (pesticides and fertilizers), as previously discussed.

In other countries, air pollution by pesticides is commonly addressed based on analysis by specific chemical classes of pesticides and possible health effects associated with them, and also it does not place the use of these products in the agro-industry associated with air pollution at the core of scientific investigations.

The legal definition of pesticides in Brazil was considered in this study. Thus, all identified studies explore the contamination of air by pesticides and the products of their degradation, regardless of release sources and routes of pesticides to the atmosphere.

In the analysis of the results, we observed that pesticide air pollution varied from the domestic use as repellent of undesirable animals, environmental deodorizer, to possible air contamination by solid waste incineration products.

Likewise, the health effects investigated in the analyzed studies considered the risk for cancer development in general¹⁸18. Stewart BW. Priorities for cancer prevention: Lifestyle choices versus unavoidable exposures. Lancet Oncol 2012; 13(3):e126-33. and more specific neoplasms¹⁹19. Viel J-F, Floret N, Deconinck E, Focant J-F, De Pauw E, Cahn J-Y. Increased risk of non-Hodgkin lymphoma and serum organochlorine concentrations among neighbors of a municipal solid waste incinerator. Environ Int 2011; 37(2):449-453., such as non-Hodgkin’s lymphoma (NHL).

The most likely route of exposure shown in the studies evaluated, though tacitly, was airways with inhalation of air contaminated by some pesticide or by-product, while the possibility of dermal exposure or intake of contaminated food has not been ruled out.

Our findings reflect the lack of studies addressing the theme by the health sector. Regarding Brazil, where profits generated by the agricultural sector are an important contribution to the current national economic setting, the lack of scientific studies and public sector’s neglect vis-à-vis the population potentially exposed to air contaminated by pesticides is even more worrying.

In addition, the country faces difficulties over the promotion of adequate migration to a more sustainable agricultural model, while at the same time producing a profit, which would result in long periods of exposure by the population. Developed countries tend to have a more advanced monitoring and surveillance system.

As we have seen in this study, the development of new techniques and methodologies for the monitoring of air contaminated by pesticides has unfolded in the world and points to a pathway to be followed by Brazil, both from the academic viewpoint and the improvement of health sector’s measures regarding Environmental Surveillance.

The expansion of the current traditional approach – focusing on health risks related to the presence and contamination of soil and water by pesticides, or occupational problems resulting from this type of chemical exposure – toward a more comprehensive Environmental Surveillance model that also considers air contamination is required within the SUS and could not start differently than through the bibliographic survey involving this theme.

References

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