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PREVALENCE OF CHAGAS DISEASE ASSOCIATED WITH THE MODE OF INFECTION

ABSTRACT

Objective:

analyze the prevalence of acute Chagas disease and association with mode of infection.

Method:

descriptive, quantitative study conducted in the health region of Tocantins - Pará - Brazil, with 346 cases of acute Chagas disease. The data were obtained in September 2017 and correspond to 2012-2016, from the Information system for health notification diseases. They were analyzed by Pearson’s chi-square (χ2), p≤0.05, in Excel® 2013.

Results:

greater involvement of males (56.93%) and rural residents (56.35%). In urban areas, 110 (94%) contracted the disease orally and seven (6%) by vectorial route. In rural areas, 137 (84%) were infected orally and 26 (16%) vectorially (p=0.010).

Conclusion:

the control of the disease demands specific public policies aligned to locoregional specificities. Acute Chagas disease was shown to be prevalent with an association between oral infection and urban area residents.

DESCRIPTORS
Chagas Disease; Epidemiology; Health Information Systems; Nursing; Public Health

RESUMO

Objetivo:

analisar a prevalência da doença de Chagas aguda e associação com o modo de infecção.

Método:

estudo descritivo, quantitativo realizado na região de saúde do Tocantins - Pará - Brasil, com 346 casos da doença de Chagas aguda. Os dados foram obtidos em setembro de 2017 e correspondem a 2012-2016, oriundos do Sistema de Informação de Agravos de Notificação. Foram analisados pelo Qui-quadrado de Pearson, p≤0,05, no Excel® 2013.

Resultados:

maior acometimento do sexo masculino (56,93%) e moradores da zona rural (56,35%). Na zona urbana, 110 (94%) contraíram a doença por via oral e sete (6%) por via vetorial. Na rural, 137 (84%) foram infectados por via oral e 26 (16%) por via vetorial (p=0,010).

Conclusão:

o controle da doença demanda políticas públicas específicas alinhadas às especificidades locorregionais. A doença de Chagas aguda mostrou-se prevalente com associação entre a infecção oral e residente de área urbana.

DESCRITORES
Doença de Chagas; Epidemiologia; Sistemas de Informação em Saúde; Enfermagem; Saúde Pública

RESUMEN

Objetivo:

analizar la prevalencia de la enfermedad de Chagas aguda y su asociación con el modo de infección.

Método:

estudio descriptivo y cuantitativo realizado en la región sanitaria de Tocantins - Pará - Brasil, con 346 casos de enfermedad de Chagas aguda. Los datos se obtuvieron en septiembre de 2017 y corresponden al periodo 2012-2016, a partir del Sistema de Información de Agravios de Notificación. Se analizaron mediante el chi-cuadrado de Pearson (χ2), p≤0,05, en Excel® 2013.

Resultados:

mayor acometimiento del sexo masculino (56,93%) y moradores de la zona rural (56,35%). En las zonas urbanas, 110 (94%) contrajeron la enfermedad por vía oral y siete (6%) por vía vectorial. En la zona rural, 137 (84%) se infectaron por vía oral y 26 (16%) por vía vectorial (p=0,010).

Conclusión:

el control de la enfermedad requiere políticas públicas específicas adaptadas a las especificidades loco-regionales. La enfermedad de Chagas aguda es más prevalente con la asociación entre la infección oral y los residentes de zonas urbanas.

PALABRAS CLAVE
Enfermedad de Chagas; Epidemiología; Sistemas de Información en Salud; Enfermería; Salud Pública

INTRODUCTION

Chagas disease (CD) is a highly prevalent antropozoonosis with expressive morbidity and mortality, constituting a serious public health problem, and the human being is an important reservoir of the protozoan Trypanosoma cruzi. The clinical evolution of the disease is divided into an acute and a chronic phase, which may manifest in the indeterminate, cardiac, digestive or cardiodigestive forms(11 Simões MV, Romano MMD, Schmidt A, Martins KSM, Marin-Neto JA. Cardiomiopatia da doença de Chagas. Int J Cardiovasc Sci [Internet]. 2018 [acesso em 13 jul 2019]; 31(2). Disponível em: https://doi.org/10.5935/2359-4802.20180011.
https://doi.org/10.5935/2359-4802.201800...
). According to the World Health Organization (WHO), it is one of the most neglected tropical diseases in the world, with a prevalence of 16 to 18 million people infected by the parasite worldwide(22 Pereira CML, Azevedo AP, Marinho S da SB, Prince KA de, Gonçalves JTT, Costa MR, et al. Perfil clínico e epidemiológico da doença de Chagas aguda no estado de Minas Gerais. Rev. Aten. Saúde [Internet]. 2017 [acesso em 13 jul 2019]; 15(52). Disponível em: http://doi.org/10.13037/ras.vol15n52.4523.
https://doi.org/10.13037/ras.vol15n52.45...
).

Most infected patients develop the chronic form, accompanied by cardiopathy that causes severe consequences to the patient and a high mortality rate(33 Ministério da Saúde. Portaria n. 264, de 17 de fevereiro de 2020. Altera a Portaria de Consolidação nº 4/GM/MS, de 28 de setembro de 2017, para incluir a doença de Chagas crônica, na Lista Nacional de Notificação Compulsória de doenças, agravos e eventos de saúde pública nos serviços de saúde públicos e privados em todo o território nacional. Diário Oficial da União, 19 fev 2020.). It is a disease that has been monitored by the Brazilian Ministry of Health and has recently been included in the National Compulsory Notification List, by means of Ordinance no. 264 of February 17th, 2020(33 Ministério da Saúde. Portaria n. 264, de 17 de fevereiro de 2020. Altera a Portaria de Consolidação nº 4/GM/MS, de 28 de setembro de 2017, para incluir a doença de Chagas crônica, na Lista Nacional de Notificação Compulsória de doenças, agravos e eventos de saúde pública nos serviços de saúde públicos e privados em todo o território nacional. Diário Oficial da União, 19 fev 2020.).

Corroborating the global scenario, in Brazil, most cases diagnosed with CD show the chronic form, although in recent years, the notification of acute Chagas disease (ACD) has been increasing, raising new concerns, especially because it is attributed to the consumption of contaminated food, i.e., oral infection(44 Dias JCP, Ramos Júnior. AN, Gontijo ED, Luquetti A, Shikanai-Yasuda MA, Coura JR, et al. II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiol. Serv. Saúde [Internet]. 2016 [acesso em 13 jul 2019]; 25(spe). Disponível em: http://doi.org/10.5123/S1679-49742016000500002.
https://doi.org/10.5123/S1679-4974201600...
). The ACD affects mainly people with low purchasing power and more difficult access to health services, especially in the North region of Brazil(44 Dias JCP, Ramos Júnior. AN, Gontijo ED, Luquetti A, Shikanai-Yasuda MA, Coura JR, et al. II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiol. Serv. Saúde [Internet]. 2016 [acesso em 13 jul 2019]; 25(spe). Disponível em: http://doi.org/10.5123/S1679-49742016000500002.
https://doi.org/10.5123/S1679-4974201600...
).

The social and geographical characteristics of the region, together with cultural diversity, have enabled the identification of cases of ACD in municipalities that have açaí as a local economic force. According to data available on the Tabnet/Datasus platform, between 2007 and 2016, 1,579 cases of ACD were confirmed in the state of Pará (PA), with the Metropolitan I, Tocantins, and Marajó II health regions having the highest number of confirmed cases of the disease(55 Andrade NC de S de. Epidemiological profile of Chagasic patients attended in reference cardiology hospital in Belém/PA. Multidisciplinary Core scientific journal of knowledge [Internet]. 2016 [acesso em 14 jul 2019]; 1(9). Disponível em: https://www.nucleodoconhecimento.com.br/health/chagasic-patients.
https://www.nucleodoconhecimento.com.br/...
).

Of the 1,579 cases of ACD in the state, there was a significant concentration of notification between the months of July and December, a period that coincides with the açaí harvest(66 Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Boletim Epidemiológico. Doença de Chagas aguda no Brasil: série histórica de 2000 a 2013 [Internet]. Brasília: Ministério da Saúde; 2015 [acesso em 14 jul 2019]; 46(21). Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/agosto/03/2014-020..pdf.
http://portalarquivos.saude.gov.br/image...
). Acai is a typical fruit from the tropical climate and is widely consumed by the general population, rich in protein, fiber, lipids, vitamin E, and minerals such as manganese, copper, boron, and chromium, with a high caloric value(77 Sousa Junior A da S, Palácios VR da CM, Miranda C do S, Costa RJF da, Catete CP, Chagasteles EJ, et al Space-temporal analysis of Chagas disease and its environmental and demographic risk factors in the municipality of Barcarena, Pará, Brazil. Rev Bras Epidemiol [Internet]. 2017 [acesso em 14 jul 2019]; 20(4). Disponível em: https://doi.org/10.1590/1980-5497201700040015.
https://doi.org/10.1590/1980-54972017000...
). In addition, açaí is one of the main foods of the riverside populations, often being the main meal(88 Nogueira AKM, Santana AC de. Análise de sazonalidade de preços de varejo de açaí, cupuaçu e bacaba no estado do Pará. Revista de Estudos Sociais [Internet]. 2009 [acesso em 18 jul 2019]; 21(1). Disponível em: http://periodicoscientificos.ufmt.br/ojs/index.php/res/article/view/232/221.
http://periodicoscientificos.ufmt.br/ojs...
).

An alternative for ACD prevention, implemented as a public policy, was the blanching of the fruits, which leads to the inactivation of the protozoan. It is a technique of immersing the açaí in natura in water with a temperature of 80ºC for ten seconds and, soon after, immersed in cold water for rapid cooling(99 Governo do Estado do Pará. Decreto n. 326, de 20 de janeiro de 2012: establece regras para cadastramento dos batedores artesanais de açaí e bacaba; padrões para instalações, materiais, máquinas e equipamentos; condições higiênico-sanitárias e boas práticas de processamento, e atividade de inspeções e fiscalização. Diário Oficial do Estado do Pará, [Internet]. 24 jan 2012 [acesso em 18 jul 2019]. Disponível em: https://www.legisweb.com.br/legislacao/?id=148207.
https://www.legisweb.com.br/legislacao/?...
). This process has become mandatory throughout the state for the artisanal beaters (people who extract the juice from the fruit), who spread throughout all localities, aiming to ensure quality to the product to be marketed and consumed domestically.

In this context, the objective of this study was to analyze the prevalence of acute Chagas disease and its association with the mode of infection in the health region of Tocantins-PA.

METHOD

A descriptive, retrospective study with a quantitative approach, developed with secondary data from ACD in the Tocantins-PA-BR health region, consisting of the municipalities: Abaetetuba, Baião, Barcarena, Cametá, Igarapé-Miri, Limoeiro do Ajuru, Moju, Mocajuba, Oeiras do PA and Tailândia. The state of PA is made up of 13 health regions, namely: Araguaia, Baixo Amazonas, Carajás, Lago de Tucuruí, Marajó I, Marajó II, Metropolitana I, Metropolitana II, Metropolitana III, Rio Caetés, Tapajós, Tocantins and Xingu, which congregate 144 municipalities and an average area of 8,664.50 km2.

The Tocantins health region has 605,119 inhabitants, distributed in nine municipalities, all of which have riverine and floodplain populations with significant production and consumption of açaí. Thus, the choice of the region was due to its epidemiological profile, since it has a high prevalence of ACD and geographical, economic, and cultural characteristics that favor the cultivation and consumption of the fruit.

The data were obtained in September 2017 and concern the cases of ACD notified and confirmed in the Information system for health notification diseases (SINAN), made available by the Regional Office of the State Secretary of Public Health, in a bank format. All notified and confirmed cases of ACD in the Tocantins-PA health region between 2012 and 2016 were included, and there was no exclusion of data.

The variables studied were: i) socio-demographic - age, gender, race/color, and place of residence; and ii) epidemiological - year of occurrence, means of contamination, and evolution of the disease.

Data were transported and stored in electronic spreadsheets in Excel® 2013 software and analyzed using Pearson’s chi-square test (χ2) to verify possible association between variables, with p≤0.05 being considered. The study was approved by the Ethics and Research Committee of the Undergraduate Nursing Course of the Pará State University, under opinion number 2,449,156.

RESULTS

From the 346 cases studied, there was a predominance of disease in males with 197 (56.93%) cases, mulattoes with 272 (78.61%) cases, and in the 20 to 39 age group with 123 (35.54%) cases. As for the place of residence, 195 (56.35%) cases were reported among rural residents (Table 1).

Table 1
Sociodemographic profile of cases of acute Chagas disease in the Tocantins-PA health region, from 2012 to 2016. Belém, PA, Brazil, 2020

The most frequent mode of infection was the oral route, with 255 (73.59%) cases, and in 55 notifications (15.89%) there was no record of the form of contamination. There was laboratory confirmation of the diagnosis in 330 (95.37%) cases, and regarding the clinical evolution, it can be observed that 309 (89.30%) evolved to remission of disease manifestations, while seven (2.02%) resulted in death (Table 2).

Table 2
Clinical-epidemiological information of cases of acute Chagas disease in the Tocantins-PA health region, from 2012 to 2016. Belém, PA, Brazil, 2020

In Table 3, it is observed that 195 cases were residents of rural areas and 140 of urban perimeters. Among the residents in rural areas, 137 were infected by ingesting food contaminated with Trypanosoma cruzi and 26 by penetration of the etiologic agent at the time of the bite by the “barbeiro” (Triatoma brasiliensis). In urban areas, 110 cases of oral transmission and seven cases of vectorial transmission were identified.

Table 3
Confirmed cases per zone of residence according to mode of infection of acute Chagas disease in the Tocantins-PA health region, from 2012 to 2016. Belém, PA, Brazil, 2020

In the distribution, eight cases had no record of place of residence, of which one was of vector transmission and seven of oral transmission, besides, three cases being from peri-urban areas, two with no record of the mode of infection and one of oral transmission. In total, oral infection was more prevalent with 255 (73.69%) cases.

From the data in Table 3, it was possible to select 280 cases that correspond to the sum of the two main forms of contamination, oral and vectorial, of residents in urban and rural areas. Table 4 shows that oral infection is more prevalent, with 247 (88%) cases. Among the cases that live in urban areas, 110 (94%) contracted the disease orally and seven (6%) by vectorial route, and among those who live in rural areas, 137 (84%) were infected orally, and 26 (16%) by vectorial route. The data indicate an association between place of residence and route of infection for ACD.

Table 4
Distribution of confirmed cases of acute Chagas disease in the Tocantins-PA health region, from 2012 to 2016. Belém, PA, Brazil, 2020

DISCUSSION

ACD was highly prevalent in the region studied and there was evidence of an association between oral infection and living in urban areas. In the sociodemographic profile, most infected individuals were male, in the age range of 20 to 39 years, which strengthens the relationship between Chagas infection and açaí extraction activity, predominant in the region, performed primarily by males, configuring greater exposure to Trypanosoma cruzi than those who work in the extraction of other products(1010 Cardoso EJ de S, Cavalcanti MAF, Nascimento EGC do, Barreto MAF. Perfil epidemiológico dos portadores de doença de Chagas: dos indicadores de risco ao processo de enfrentamento da doença. Arq. Ciênc. Saúde [Internet]. 2017 [acesso em 20 jan 2020]; 24(1) 41-46. Disponível em: http://www.cienciasdasaude.famerp.br/index.php/racs/article/view/545/274.
http://www.cienciasdasaude.famerp.br/ind...
).

Regarding race, those who declared themselves as brown showed a higher percentage of illness (78.61%), like the findings of a study conducted in the city of Barcarena-PA, which identified 74.7% of brown people. In the study conducted in the city of Salvador-BA, there was a predominance of blacks associated with the prevalence of the disease(77 Sousa Junior A da S, Palácios VR da CM, Miranda C do S, Costa RJF da, Catete CP, Chagasteles EJ, et al Space-temporal analysis of Chagas disease and its environmental and demographic risk factors in the municipality of Barcarena, Pará, Brazil. Rev Bras Epidemiol [Internet]. 2017 [acesso em 14 jul 2019]; 20(4). Disponível em: https://doi.org/10.1590/1980-5497201700040015.
https://doi.org/10.1590/1980-54972017000...
). The ethnic profile identified in the studies corresponds to the racial characteristics of the places studied. The miscegenation with blacks is more prevalent in Salvador, and in PA, and besides the black, there is a strong presence of indigenous people, especially in the ancestry.

In the studied health region, the cases of ACD are distributed throughout the geographic space, with predominance in rural areas. However, the urbanization process has been contributing to the displacement of the disease from rural areas to urbanized spaces, favoring its dissemination(1111 Guariento ME, Carrijo CM, Almeida EA de, Magna LA. Perfil clínico de idosos portadores de doença de Chagas atendidos em serviço de referência. Rev. Bras Clin Med [Internet]. 2011 [acesso em 23 jan 2020]; 9(1). Disponível em: http://files.bvs.br/upload/S/1679-1010/2011/v9n1/a1717.pdf.
http://files.bvs.br/upload/S/1679-1010/2...
). It is noteworthy that, besides this change in the profile of reported cases according to the zone of residence, which has already been appearing for the years 2017 and 2018 on the DATASUS website with the data studied, one can establish a relationship between the variables zone of residence and mode of infection of ACD, confirming an association.

Thus, the high oral contamination is related to eating and hygiene habits, essentially the consumption of foods contaminated with the vector’s excrements(1212 Carvalho GLB, Galdino R da S, Cavalcante WM de A, Aquino DS de. Doença e Chagas: sua transmissão através do consumo do açaí. Acta de Ciências e Saúde [Internet]. 2018 [acesso em 12 out 2020]; 1(1). Disponível em: https://www2.ls.edu.br/actacs/index.php/ACTA/article/view/174/150.
https://www2.ls.edu.br/actacs/index.php/...
). The açaí was the food with the highest association with Chagas disease in the North region in recent years, either by contamination of the fruit or the pulp through vector droppings or infected reservoir animals in endemic areas(44 Dias JCP, Ramos Júnior. AN, Gontijo ED, Luquetti A, Shikanai-Yasuda MA, Coura JR, et al. II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiol. Serv. Saúde [Internet]. 2016 [acesso em 13 jul 2019]; 25(spe). Disponível em: http://doi.org/10.5123/S1679-49742016000500002.
https://doi.org/10.5123/S1679-4974201600...
). This is a scenario that has demanded a response from the public health surveillance system, due to its wide consumption and commercialization, both in the domestic and international markets.

A study on the risk of oral infection associated with the consumption of contaminated food concluded that the oral transmission of ACD is related to the consumption of poorly sanitized food, such as the juice of açaí and bacaba, typical fruits of the region(1212 Carvalho GLB, Galdino R da S, Cavalcante WM de A, Aquino DS de. Doença e Chagas: sua transmissão através do consumo do açaí. Acta de Ciências e Saúde [Internet]. 2018 [acesso em 12 out 2020]; 1(1). Disponível em: https://www2.ls.edu.br/actacs/index.php/ACTA/article/view/174/150.
https://www2.ls.edu.br/actacs/index.php/...
). Trypanosoma cruzi can survive in açaí pulp for different periods, and by ingesting sugarcane juice contaminated by infected triatomines, as evidenced in a study conducted in the city of Marcelino Vieira(1313 Vargas A, Malta JMAS, Costa VM da, Cláudio LDG, Alves RV, Cordeiro G da S, et al. Investigação de surto de doença de Chagas aguda na região extra-amazônica, Rio Grande do Norte, Brasil, 2016. Cad. Saúde Pública [Internet]. 2018 [acesso em 12 out 2020]; 34(1). Disponível em: http://dx.doi.org/10.1590/0102-311x00006517.
https://doi.org/10.1590/0102-311x0000651...
).

In this context, a study on factors that contribute to the increase in contamination and illness by ACD, especially in the state of PA, concluded that the high number of cases may be associated with the ingestion of açaí contaminated by triatomine feces, which deposits trypanosomes in the fruit(99 Governo do Estado do Pará. Decreto n. 326, de 20 de janeiro de 2012: establece regras para cadastramento dos batedores artesanais de açaí e bacaba; padrões para instalações, materiais, máquinas e equipamentos; condições higiênico-sanitárias e boas práticas de processamento, e atividade de inspeções e fiscalização. Diário Oficial do Estado do Pará, [Internet]. 24 jan 2012 [acesso em 18 jul 2019]. Disponível em: https://www.legisweb.com.br/legislacao/?id=148207.
https://www.legisweb.com.br/legislacao/?...
). The increase in the number of cases, whose first symptoms occur in the months from August to November, strengthens the thesis of transmission through the ingestion of contaminated açaí, since it corresponds to the harvest period of the fruit, leading to increased consumption and wide manipulation.

Given the severity, in 2012 a sanitary policy measure was established by the State Department of Public Health, for the registration of handmade beaters of açaí, with determination of hygienic-sanitary requirements for handling, in order to prevent outbreaks of Foodborne Diseases (FTS) and thus minimizing the risk of illness(99 Governo do Estado do Pará. Decreto n. 326, de 20 de janeiro de 2012: establece regras para cadastramento dos batedores artesanais de açaí e bacaba; padrões para instalações, materiais, máquinas e equipamentos; condições higiênico-sanitárias e boas práticas de processamento, e atividade de inspeções e fiscalização. Diário Oficial do Estado do Pará, [Internet]. 24 jan 2012 [acesso em 18 jul 2019]. Disponível em: https://www.legisweb.com.br/legislacao/?id=148207.
https://www.legisweb.com.br/legislacao/?...
). Regarding the vectorial transmission, it is possible to relate it to the forest areas still present in the region, configuring greater susceptibility to disease. This is because individuals living in rural areas are susceptible to contracting Chagas disease due to the poor infrastructure of their homes(44 Dias JCP, Ramos Júnior. AN, Gontijo ED, Luquetti A, Shikanai-Yasuda MA, Coura JR, et al. II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiol. Serv. Saúde [Internet]. 2016 [acesso em 13 jul 2019]; 25(spe). Disponível em: http://doi.org/10.5123/S1679-49742016000500002.
https://doi.org/10.5123/S1679-4974201600...
).

In this study, 95.37% of the ACD cases were laboratory confirmed, according to data made available by the Regional Office of the Secretary of State for Public Health, like the findings of a survey conducted in three states (PA, Amapá, and Maranhão) that included 233 acute cases of the disease, all confirmed by laboratory tests. Thus, it is identified that the backlog for confirmation of cases is available, which favors the use of the recommended therapeutic conduct(44 Dias JCP, Ramos Júnior. AN, Gontijo ED, Luquetti A, Shikanai-Yasuda MA, Coura JR, et al. II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiol. Serv. Saúde [Internet]. 2016 [acesso em 13 jul 2019]; 25(spe). Disponível em: http://doi.org/10.5123/S1679-49742016000500002.
https://doi.org/10.5123/S1679-4974201600...
).

The limitations of this study are that it was conducted with data from secondary sources, which may imply underreporting of cases, as well as possible inconsistencies in the records made in the various health services. In addition, the high number of ignored and/or blank variables limited the knowledge of the real situation of ACD in the studied region. Another limitation was that the study was carried out in only one health region of the state, lacking expansion.

CONCLUSION

The Tocantins health region draws attention for concentrating a significant number of cases of ACD throughout the studied period. In the state of PA, it was the region that most contributed to the magnitude of the morbidity and mortality indicators of the disease, demanding specific public policies that are aligned with the locoregional specificities.

The epidemiological data of the disease indicated oral transmission as the most responsible for the spread of the disease, attributable to the consumption of açaí, given the economic and cultural specificities of the region. This fact leads to the urgent need to establish inter-institutional partnerships to face the problem, reaching all its aspects, from the production, transportation, packing, and handling of the açaí.

A plan to address the problem is necessary to reduce the occurrence of cases, considering the possibility of chronicity of the disease, requiring specialized assistance for long periods, causing burden to the Health System and greater human suffering. Thus, investing in the agricultural and commercial area is essential to strengthen health practices of health promotion and disease prevention.

HOW TO REFERENCE THIS ARTICLE:

  • Nascimento LPGR do, Nogueira LMV, Rodrigues ILA, André SR, Graça VV da, Monteiro NJ. Prevalence of chagas disease associated with the mode of infection. Cogit. Enferm. [Internet]. 2021 [accessed “insert day, monh and year”]; 26. Available from: http://dx.doi.org/10.5380/ce.v26i0.73951.

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    » https://doi.org/10.5935/2359-4802.20180011
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    » https://doi.org/10.1590/1980-5497201700040015
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    » http://periodicoscientificos.ufmt.br/ojs/index.php/res/article/view/232/221
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    » https://doi.org/10.1590/0102-311x00006517

Edited by

Associate editor: Cremilde Aparecida Trindade Radovanovic

Publication Dates

  • Publication in this collection
    05 Nov 2021
  • Date of issue
    2021

History

  • Received
    21 May 2020
  • Accepted
    29 Jan 2021
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