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Piassaba Palm Extractivism As an Associated Factor with Chagas Disease: Seroprevalence and Immunological Profile in Native Inhabitants of the Central Amazonia, Brazil

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Piassaba Palm Extractivism As an Associated Factor with Chagas Disease: Seroprevalence and Immunological Profile in Native Inhabitants of the Central Amazonia, Brazil ORIGINAL ARTICLE | ARTIGO ORIGINAL | ARTÍCULO ORIGINAL doi: 10.5123/S2176-62232015000300005 Piassaba palm extractivism as an associated factor with Chagas disease: seroprevalence and immunological profile in native inhabitants of the Central Amazonia, Brazil O extrativismo da piaçaba como um fator associado à doença de Chagas: soroprevalência e perfil imunológico em habitantes da Amazônia Central, Brasil La extracción de la piasaba como un factor asociado a la enfermedad de Chagas: seroprevalencia y perfil inmunológico en habitantes de la Amazonía Central, Brasil Wallice Paxiúba Duncan Adriana Malheiro Laboratório de Morfologia Funcional, Departamento de Morfologia, Laboratório de Imunologia Celular, Departamento de Parasitologia, Universidade Federal do Amazonas, Manaus, Amazonas, Brasil Universidade Federal do Amazonas, Manaus, Amazonas, Brasil Juliana Leal Danilow Faculdade de Medicina, Universidade Federal do Amazonas, Manaus, Amazonas, Brasil ABSTRACT In the Brazilian Amazon, Chagas disease is considered a zoonosis with low virulence and pathogenicity that primarily appears in chronic latent infections. To examine the seroprevalence, epidemiological and immunological profiles of Chagas disease in the microregion of the Negro river (Central Amazonia), an observational and cross-sectional study was conducted on native people from the Municipality of Barcelos, the most important piassaba (Leopoldinia piassaba) fibre extractivism site in the Amazonas State. Serology tests were performed using both ELISA and indirect immunofluorescence tests. Immunophenotyping and profiles of Th1, Th2 and Th17 cytokines were determined. The seroprevalence in native inhabitants ranged from 2.6 to 6.5%. The low level of circulating INF-γ was associated to the low percentage of T-helper CD3+ CD4+ lymphocytes. As INF-γ is an important factor associated with the development of severe cardiomyopathy, the low levels INF-γ in seropositive individuals from the Central Amazonia suggests the downregulation of the Th1 immune response, which might explain the long and latent asymptomatic phase of Trypanosoma cruzi infections. Keywords: Chagasic Infection; Leopoldinia piassaba; Serology; Immunophenotyping. INTRODUCTION resulting from dilated cardiomyopathy in autochthonous 6,7 The epidemiological, immunological, and clinical patients from the Middle Negro river basin . aspects of Chagas disease in the Brazilian Amazon Chagas disease is caused by the protozoan differ from those in other Brazilian regions in several Trypanosoma cruzi and is naturally transmitted through aspects. Firstly, the main triatomine vector in the Brazilian triatomine haematophagous bugs1. Rhodnius brethesi is Amazon belongs to the genus Rhodnius1, whereas a sylvatic triatomine originating from the native palm tree 2,3 Triatoma is prevalent in other regions . Secondly, as piassaba Leopoldinia piassaba in the Barcelos region, disease transmission does not typically occur in dwellings Amazonas State, Brazil4,8. The epidemiological aspects in the Brazilian Amazon, Chagas disease is sometimes of Chagas disease transmission are characterised by 4 considered an occupational disease in this region . the absence of vector domiciliation, suggesting that However, acute outbreaks due to contaminated food have this condition is an occupational disease4. However, being commonly reported in endemic areas of the Western uncontrolled deforestation in the Amazon tends to increase Amazon5. Thirdly, the chronic phase is characterised by the house invasion by sylvatic triatomines and the risk of low morbidity2, with the exception of some fatal cases T. cruzi infection transmission9. Despite the high prevalence, some clinical studies have reported that the acute phase is marked with high morbidity, including Correspondence / Correspondência / Correspondencia: 6 Wallice Paxiúba Duncan some fatal cases of dilated cardiomyopathy . However, Laboratório de Morfologia Funcional, Departamento de Morfologia, the results of several studies based on clinical and Instituto de Ciências Biológicas, Universidade Federal do Amazonas electrocardiographic analyses of seropositive Chagas Av. General Rodrigo Octávio Jordão Ramos, 6200. Bairro: Coroado I disease patients from the Amazon basin suggest low CEP: 69077-000 Manaus-Amazonas-Brazil Phone #: +55 (92) 98112-3169 morbidity, likely reflecting circulating T. cruzi strains and E-mail: [email protected] low parasitaemia7,10,11,12,13. http://revista.iec.pa.gov.br Rev Pan-Amaz Saude 2015; 6(1):35-42 35 Duncan, WP, et al. Piassaba palm extractivism as an associated factor with Chagas disease Many immunoregulatory mechanisms have been epidemiological and socioeconomic aspects, such as proposed for T. cruzi infections, including those that occupation, recognition of triatomines, and other risk involve regulatory T cells and regulatory cytokines14. factors associated with Chagas disease, was conducted. Patients with cardiac Chagas disease develop a strong The study was approved by the Ethical Review Board immune response against the parasite, showing of the Universidade Federal do Amazonas (approval high levels of interferon gamma and low levels of number CAAE#0139.0.115.000-10) on June 16, 2010. interleukin-1015. With this background, it is important to examine whether low morbidity of the Chagas disease BLOOD COLLECTION AND SEROLOGY in the Brazilian Amazon is due to downregulation of After obtaining written consent, blood sample was the Th1 immune response, which maintain the infected collected from each participant through venipuncture individual in a long asymptomatic period. into heparinised vacuum tubes. An aliquot of total blood was used for flow cytometric analysis based on the MATERIALS AND METHODS expression of surface markers. Subsequently, the blood samples were centrifuged for 10 min at 3,000 rpm. STUDY AREA The plasma samples were analysed for the presence of The Municipality of Barcelos (S00o42'/W62o58') IgG antibodies using an immunoenzymatic assay (ELISA) covers an area of 122,476.123 km2, located at 490 km and the indirect immunofluorescence method (IIF). For from Manaus, Amazonas State (Figure 1). In 2010, ELISA, the Chagas test ELISA III kit (Abbott Laboratórios according to the Brazilian Institute for Geography and do Brasil LTDA, São Paulo, Brazil) was used. All assay Statistics (IBGE)16, this region contains a population procedures were automated, and the ELISA reactions of 25,718 individuals, with 14,561 residents in the were measured at 450 nm using an Asys Expert Plus rural area (56.6%) and 11,157 (43.4%) residents in microplate reader. The reactive, inconclusive and the Municipality. The economy of Barcelos is based on undetermined samples were subjected to IIF analysis. extractivism activities, fishing, subsistence agriculture, These analyses were conducted using anti-human and tourism. Piassaba (Leopoldinia piassaba) fibres globulin anti-IgG (Imuno-CON Chagas®; Wana obtained through the extractivism activity are important Diagnóstica, São Carlos, Brazil) at a 1:40 dilution. for rural populations as a source of economic income. Individuals seropositive for both methods (ELISA and IIF The fibres of this palm are used in the manufacture of test) were considered as positive for chagasic infection. handicrafts, baskets and brooms. MEASUREMENTS OF CYTOKINES 78º0'0''W 72º0'0''W 66º0'0''W 60º0'0''W 54º0'0''W Serum cytokines-related Th1/Th2/Th17 were measured using a Cytometric Bead Array Kit (CBA, VENEZUELA GUYANA BD Pharmingen, San Diego, CA, USA) according to the manufacturer's instructions. Briefly, samples 6º0'0''N SURINAME 6º0'0''N and standards were incubated with capture beads COLOMBIA for 1 h at room temperature, followed by incubation with phycoerythrobilin-labelled IL-2, IL-4, IL-10, IL-17, IFN-γ and TNF-α detection antibodies for 2 h 0º0'0'' Barcelos 0º0'0'' Manaus at room temperature to achieve complex formation. Subsequently, the samples were washed, and the mean Amazonas State fluorescence intensity was detected using flow cytometry (FACSCaliburTM, Becton Dickinson, CA, USA). The data 6º0'0''S BRAZIL 6º0'0''S were analysed using BD Cytometric Bead Array analysis software. PERU FLOW CYTOMETRY 12º0'0''S 12º0'0''S The blood samples were stained with anti-CD8, anti-CD4, anti-CD3, anti-CD69 and anti-CD25 antibodies labelled with phycoerythrin or fluoresce Figure 1 – Map of the Municipality of Barcelos in Amazonas in isothiocyanate at concentrations titrated State, Brazil for optimal staining. The cell suspensions and fluorochrome-conjugated antibodies were incubated for 15 min at room temperature in the dark. After SAMPLING POPULATION incubation, the cell suspensions were incubated with a fixative in lysing solution for 10 min, followed The present study was conducted in the residential by centrifugation for 7 min at 1,300 rpm. The district of the Municipality of Barcelos as an immunophenotyping was analysed by the fluorescence- observational and cross-sectional analysis of 155 activated cell sorting (FACSCaliburTM, Becton Dickinson, native inhabitants and their households. A survey of the CA, USA) according to fluorescence intensity. 36 Rev Pan-Amaz Saude 2015; 6(3):35-42 Duncan, WP, et al. Piassaba palm extractivism as an associated factor with Chagas disease STATISTICS ANALYSES PLASMA CYTOKINES The values were tested for normality and equal The levels of all cytokines did not differ between variance (Kolmogorov-Smirnov and F-test, respectively). seropositive and seronegative individuals (Table 2), Based on serological reactivity (ELISA
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