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Infection by Trypanosoma cruzi in the central nervous system in non-human mammals: a systematic review

Published online by Cambridge University Press:  15 March 2019

Evaristo Villalba-Alemán ,
Mariáurea Matias Sarandy ,
Mônica Morais-Santos ,
Rômulo Dias Novaes Open the ORCID record for Rômulo Dias Novaes [Opens in a new window]  and
Reggiani Vilela Gonçalves Open the ORCID record for Reggiani Vilela Gonçalves [Opens in a new window]
Evaristo Villalba-Alemán
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Mariáurea Matias Sarandy
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Mônica Morais-Santos
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Rômulo Dias Novaes
Affiliation:
Department of Structural Biology, Federal University of Alfenas, Alfenas, Minas Gerais, Brazil
Reggiani Vilela Gonçalves*
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
*
Author for correspondence: Vilela Gonçalves, E-mail: reggiani.goncalves@ufv.br
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Abstract

Currently, the types and distribution of the lesions induced in the central nervous system (CNS) by Trypanosoma cruzi remain unclear as the available evidence is based on fragmented data. Therefore, we developed a systematic review to analyse the main characteristics of the CNS lesions in non-human hosts infected. From a structured search on the PubMed/Medline and Scopus platforms, 32 studies were retrieved, subjected to data extraction and methodological bias analysis. Our results show that the most frequent alterations in the CNS are the presence of different forms of T. cruzi and intense lymphocytes infiltrates. The encephalon is the main target of T. cruzi, and inflammatory changes in the CNS are more frequent and severe in the acute phase of infection. The parasite's genotype and phenotype are associated with the tropism and severity of the CNS lesions. The methodological limitations found in the studies were divergences in inoculation pathways, under-reporting of animal age and weight, sample calculation strategies and histopathological characterization. Since the changes were dependent on the pathogenicity and virulence of the T. cruzi strains, the genotype and phenotype characterization of the parasite are extremely relevant to predict changes in the CNS and the neurological manifestations associated with Chagas’ disease.

Keywords

Chagas diseaseencephalongenotypesspinal cordTrypanosoma cruzi
Type
Review Article
Information
Parasitology , Volume 146 , Issue 8 , July 2019 , pp. 983 - 1005
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Copyright
Copyright © Cambridge University Press 2019 

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References

Abolis, NG, De Araujo, SM, Toledo, MJ, Fernandez, MA and Gomes, ML (2011) Trypanosoma cruzi I–III in southern Brazil causing individual and mixed infections in humans, sylvatic reservoirs and triatomines. Acta Tropica 120, 167–172.Google Scholar
Alves, RT, Regasini, LO, Funari, CS, Young, MCM, Rimoldi, A, Bolzani, VDS, Silva, DHS, Albuquerque, S and Rosa, JAD (2012) Trypanocidal activity of Brazilian plants against epimastigote forms from Y and Bolivia strains of Trypanosoma cruzi. Revista Brasileira de Farmacognosia 22, 528–534.Google Scholar
Andrade, SG, Filho, AC, De Souza, AJM, De Lima, ES and Andrade, ZA (1997) Influence of treatment with immunosuppressive drugs in mice chronically infected with Trypanosoma cruzi. International Journal of Experimental Pathology 78, 391–399.Google Scholar
Andrade, LO, Machado, CR, Chiari, E, Pena, SD and Macedo, AM (1999) Differential tissue distribution of diverse clones of Trypanosoma cruzi in infected mice. Molecular and Biochemical Parasitology 100, 163–172.Google Scholar
Andrade, LO, Machado, CR, Chiari, E, Pena, SD and Macedo, AM (2002) Trypanosoma cruzi: role of host genetic background in the differential tissue distribution of parasite clonal populations. Experimental Parasitology 100, 269–275.Google Scholar
Andrade, LO, Galvão, L, Meirelles, MDNS, Chiari, E, Pena, SD and Macedo, AM (2010) Differential tissue tropism of Trypanosoma cruzi strains: an in vitro study. Memorias do Instituto Oswaldo Cruz 105, 834–837.Google Scholar
Añez, N, Crisante, G and Soriano, PJ (2009) Trypanosoma cruzi congenital transmission in wild bats. Acta Tropica 109, 78–80.Google Scholar
Antinori, S, Galimberti, L, Bianco, R, Grande, R, Galli, M and Corbellino, M (2017) Chagas disease in Europe: a review for the internist in the globalized world. European Journal of Internal Medicine 43, 6–15.Google Scholar
Banks, WA (2009) The blood–brain barrier in psychoneuroimmunology. Immunology and Allergy Clinics 29, 223–228.Google Scholar
Barrios, P, Más, M, Giachetto, G, Basjmadjián, Y, Rodríguez, M, Viera, AL, Baroloco, AL and Sayaguez, B (2015) Enfermedad de Chagas: transmisión vertical. Descripción de casos clínicos. Revista Médica del Uruguay 31, 209–213.Google Scholar
Bombeiro, AL, Gonçalves, LA, Penha-Gonçalves, C, Marinho, CRF, Lima, MRDI, Chadi, G and Álvarez, JM (2012) IL-12p40 deficiency leads to uncontrolled Trypanosoma cruzi dissemination in the spinal cord resulting in neuronal death and motor dysfunction. PLoS ONE 7, 1–11.Google Scholar
Botero, LA, Mejía, AM and Triana, O (2007) Caracterización biológica y genética de dos clones pertenecientes a los grupos I y II de Trypanosoma cruzi de Colombia. Biomédica 27, 64–74.Google Scholar
Brisse, S, Dujardin, JC and Tibayrenc, M (2000) Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Molecular and Biochemical Parasitology 111, 95–105.Google Scholar
Bryan, LK, Hamer, SA, Shaw, S, Curtis-Robles, R, Auckland, LD, Hodo, CL, Chaffin, K and Rech, RR (2016) Chagas disease in a Texan horse with neurologic deficits. Veterinary Parasitology 216, 13–17.Google Scholar
Buckner, FS, Wilson, AJ and Van Voorhis, WC (1999) Detection of live Trypanosoma cruzi in tissues of infected mice by using histochemical stain for β-galactosidase. Infection and Immunity 67, 403–409.Google Scholar
Cabral-Piccin, MP, Guillermo, LV, Vellozo, NS, Filardy, AA, Pereira-Marques, ST, Rigoni, TS, Pereira-Manfro, WF, DosReis, GA and Lopes, MF (2016) Apoptotic CD8 T-lymphocytes disable macrophage-mediated immunity to Trypanosoma cruzi infection. Cell Death & Disease 2016, 1–14.Google Scholar
Caradonna, K and PereiraPerrin, M (2009) Preferential brain homing following intranasal administration of Trypanosoma cruzi. Infection and Immunity 77, 1349–1356.Google Scholar
Castro-Sesquen, YE, Gilman, RH, Yauri, V, Angulo, N, Verastegui, M, Velásquez, DE, Sterling, CR, Martin, D and Bern, C (2011) Cavia porcellus as a model for experimental infection by Trypanosoma cruzi. The American Journal of Pathology 179, 281–288.Google Scholar
Chagas, C (1909) Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memórias do Instituto Oswaldo Cruz 1, 159–218.Google Scholar
Chatelain, E and Konar, N (2015) Translational challenges of animal models in Chagas disease drug development: a review. Drug Design, Development and Therapy 9, 4807–4823.Google Scholar
Chizzolini, C and Brembilla, NC (2009) Prostaglandin E2: igniting the fire. Immunology and Cell Biology 87, 510–511.Google Scholar
Costa, GC, da Costa Rocha, MO, Moreira, PR, Menezes, AS, Silva, MR, Gollob, KJ and Dutra, WO (2009) Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. The Journal of Infectious Diseases 199, 451–454.Google Scholar
Coura, JR and Viñas, PA (2010) Chagas disease: a new worldwide challenge. Nature 465, S6–S7.Google Scholar
De Diego, JA, Penin, P, Del Rey, J, Mayer, R and Gamallo, C (1991) A comparative pathological study of three strains of Trypanosoma cruzi in an experimental model. Histology and Histopathology Journal 6, 199–206.Google Scholar
De Diego, JA, Palau, MT, Gamallo, C and Penin, P (1998) Relationships between histopathological findings and phylogenetic divergence in Trypanosoma cruzi. Tropical Medicine & International Health 3, 222–233.Google Scholar
de Queiroz, AC and Castro Filho, BG (1985) The choroid plexus in experimental Chagas infection in mice. Acta Medica Portuguesa 6, 181–182.Google Scholar
De Scorza, C, Urdaneta-Morales, S and Sampson-Ward, L (1989) Urban Trypanosoma (schizotrypanum) cruzi: pathology in white mice of isolates from Panstrongylus geniculatus. Annales De La Societe Belge De Medecine Tropicale 69, 283–289.Google Scholar
Dias, JC (2006) Notas sobre o Trypanosoma cruzi e suas características bio-ecológicas, como agente de enfermidades transmitidas por alimentos. Revista da Sociedade Brasileira de Medicina Tropical 39, 370–375.Google Scholar
Di Noia, JM, Buscaglia, CA, De Marchi, CR, Almeida, IC and Frasch, AC (2002) A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas’ disease is due to a single parasite lineage. Journal of Experimental Medicine 195, 401–413.Google Scholar
Domingues, CS, Hardoim, DJ, Souza, CSF, Cardoso, FO, Mendes, VG, Previtalli-Silva, H, Abreu-Silva, AL, Pelajo-Machado, CMSCG and Calabrese, KS (2015) Oral outbreak of Chagas disease in Santa Catarina, Brazil: experimental evaluation of a patient's strain. PLoS ONE 10, 1–18.Google Scholar
Flores-Vieira, CLL and Barreira, AA (1997) Experimental benznidazole encephalopathy: I. Clinical-neurological alterations. Journal of Neurological Sciences 150, 3–11.Google Scholar
Flores-Vieira, CLL, Chimelli, L, Fernandes, RMF and Barreira, AA (1997) Experimental benznidazole encephalopathy: II. Electroencephalographic and morphological alterations. Journal of Neurological Sciences 150, 13–25.Google Scholar
Freitas, JM, Lages-Silva, E, Crema, E, Pena, SDJ and Macedo, AM (2005) Real time PCR strategy for the identification of major lineages of Trypanosoma cruzi directly in chronically infected human tissues. International Journal for Parasitology 35, 411–417.Google Scholar
Galea, I, Bechmann, I and Perry, VH (2007) What is immune privilege (not)? Trends in Immunology 28, 12–18.Google Scholar
Gironès, N and Fresno, M (2003) Etiology of Chagas disease myocarditis: autoimmunity, parasite persistence, or both? Trends in Parasitology 19, 19–22.Google Scholar
Guarner, J, Bartlett, J, Zaki, SR, Colley, DG, Grijalva, MJ and Powell, MR (2001) Mouse model for Chagas disease: immunohistochemical distribution of different stages of Trypanosoma cruzi in tissues throughout infection. The American Journal of Tropical Medicine and Hygiene 65, 152–158.Google Scholar
Guillamón-Vivancos, T, Gómez-Pinedo, U and Matías-Guiu, J (2015) Astrocitos en las enfermedades neurodegenerativas (I): función y caracterización molecular. Neurología 30, 119–129.Google Scholar
Guimarães-Pinto, K, Nascimento, DO, Corrêa-Ferreira, A, Morro, A, Freire-de-Lima, CG, Lopes, MF, DosReis, GF and Filardy, AA (2018) Trypanosoma cruzi infection induces cellular stress response and senescence-like phenotype in murine fibroblasts. Frontiers in Immunology 9, 1–11.Google Scholar
Gupta, E, Bhalla, P, Khurana, N and Singh, T (2009) Histopathology for the diagnosis of infectious diseases. Indian Journal of Medical Microbiology 27, 100–106.Google Scholar
Gutierrez, FR, Mineo, TW, Pavanelli, WR, Guedes, PM and Silva, JS (2009) The effects of nitric oxide on the immune system during Trypanosoma cruzi infection. Memórias do Instituto Oswaldo Cruz 104, 236–245.Google Scholar
Hanson, WL and Roberson, EL (1974) Density of parasites in various organs and the relation to numbers of trypomastigotes in the blood during acute infections of Trypanosoma cruzi in mice. Journal of Eukaryotic Microbiology 21, 512–517.Google Scholar
Herrera, L (2010) Una revisión sobre reservorios de Trypanosoma (schizotrypanum) cruzi (chagas, 1909), agente etiológico de la Enfermedad de Chagas. Boletín de Malariología y Salud Ambiental 50, 3–15.Google Scholar
Jeganathan, S, Sanderson, L, Dogruel, M, Rodgers, J, Croft, S and Thomas, SA (2010) The distribution of Nifurtimox across the healthy and trypanosome-infected murine blood-brain and blood-cerebrospinal fluid barriers. The Journal of Pharmacology and Experimental Therapeutics 336, 506–515.Google Scholar
Kawai, T and Akira, S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunology 11, 373–384.Google Scholar
Kilkenny, C, Browne, W, Cuthill, IC, Emerson, M and Altman, DG (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. British Journal of Pharmacology 160, 1577–1579.Google Scholar
Kuhn, RE, Vaughn, RT and Iannuzzi, NP (1974) The in vivo distribution of 51Cr-labeled Trypanosoma cruzi in mice. International Journal for Parasitology 4, 585–588.Google Scholar
Lana, M and Tafuri, WL (2016) Trypanosoma cruzi e doença de Chagas. In Neves, DP, De Melo, AL, Linardi, PM and Vitor, RWA (eds), Parasitologia Humana. São Paulo, Brazil: Atheneu, pp. 89–114.Google Scholar
León, CM, Montilla, M, Vanegas, R, Castillo, M, Parra, E and Ramírez, JD (2017) Murine models susceptibility to distinct Trypanosoma cruzi I genotypes infection. Parasitology 144, 512–519.Google Scholar
Lisboa, CV, das Chagas, XSC, Herrera, HM and Jansen, AM (2009) The ecology of the Trypanosoma cruzi transmission cycle: dispersion of zymodeme 3 (Z3) in wild hosts from Brazilian biomes. Veterinary Parasitology 165, 19–24.Google Scholar
Macedo, AM and Pena, SDJ (1998) Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitology Today 14, 119–124.Google Scholar
Macedo, AM, Machado, CR, Oliveira, RP and Pena, SD (2004) Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of Chagas disease. Memorias do Instituto Oswaldo Cruz 99, 1–12.Google Scholar
Magalhães-Santos, IF, Souza, MM, Lima, CSC and Andrade, SG (2004) Infection of Calomys callosus (Rodentia Cricetidae) with strains of different Trypanosoma cruzi biodemes: pathogenicity, histotropism, and fibrosis induction. Memórias do Instituto Oswaldo Cruz 99, 407–413.Google Scholar
Manoel-Caetano, FDS and Silva, AE (2007) Implications of genetic variability of Trypanosoma cruzi for the pathogenesis of Chagas disease. Cadernos de Saúde Pública 23, 2263–2274.Google Scholar
Marin-Neto, JA, Cunha-Neto, E, Maciel, BC and Simões, MV (2007) Pathogenesis of chronic Chagas heart disease. Circulation 115, 1109–1123.Google Scholar
Márquez, E, Crespo, M, Mir, M, Pérez-Sáez, MJ, Quintana, S, Barbosa, F and Pascual, J (2013) Chagas’ disease and kidney donation. Nefrologia 33, 128–133.Google Scholar
Masocha, W and Kristensson, K (2012) Passage of parasites across the blood-brain barrier. Virulence 3, 202–212.Google Scholar
Mescher, AL (2016) Junqueira's Basic Histology: Text and Atlas. New York, USA: Mcgraw-hill.Google Scholar
Meza, SKL, Kaneshima, EN, de Oliveira Silva, S, Gabriel, M, de Araújo, SM, Gomes, ML, Monteiro, WM, Barbosa, MGV and de Ornelas Toledo, MJ (2014) Comparative pathogenicity in Swiss mice of Trypanosoma cruzi IV from northern Brazil and Trypanosoma cruzi II from southern Brazil. Experimental Parasitology 146, 34–42.Google Scholar
Michailowsky, V, Silva, NM, Rocha, CD, Vieira, LQ, Lannes-Vieira, J and Gazzinelli, RT (2001) Pivotal role of interleukin-12 and interferon-γ axis in controlling tissue parasitism and inflammation in the heart and central nervous system during Trypanosoma cruzi infection. The American Journal of Pathology 159, 1723–1733.Google Scholar
Minning, TA, Weatherly, DB, Flibotte, S and Tarleton, RL (2011) Widespread, focal copy number variations (CNV) and whole chromosome aneuploidies in Trypanosoma cruzi strains revealed by array comparative genomic hybridization. BMC Genomics 12, 1–11.Google Scholar
Mirkin, GA, Jones, M, Sanz, OP, Rey, R, Sica, RE and Cappa, SUG (1994) Experimental Chagas’ disease: electrophysiology and cell composition of the neuromyopathic inflammatory lesions in mice infected with a myotropic and a pantropic strain of Trypanosoma cruzi. Clinical Immunology and Immunopathology 73, 69–79.Google Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of Internal Medicine 151, 264–269.Google Scholar
Molina, HA, Cardoni, RL and Rimoldi, MT (1987) The neuromuscular pathology of experimental Chagas’ disease. Journal of the Neurological Sciences 81, 287–300.Google Scholar
Monteiro, WM, Magalhães, LKC, Oliveira, JC, Guerra, JADO, Silveira, H, Ferreira, LCDL, Toledo, MJO and Barbosa, MDGV (2012) Biological behavior of Trypanosoma cruzi stocks obtained from the State of Amazonas, Western Brazilian Amazon, in mice. Revista da Sociedade Brasileira de Medicina Tropical 45, 209–214.Google Scholar
Montenegro, VM, Jiménez, M, Dias, JC and Zeledón, R (2002) Chagas disease in dogs from endemic areas of Costa Rica. Memórias do Instituto Oswaldo Cruz 97, 491–494.Google Scholar
Moraes-Souza, H and Ferreira-Silva, MM (2011) Control of transfusional transmission. Revista da Sociedade Brasileira de Medicina Tropical 44, 64–67.Google Scholar
Morocoima, A, Socorro, G, Ávila, R, Hernández, A, Merchán, S, Ortiz, D, Primavera, G, Chique, J, Herrera, L and Urdaneta-Morales, S (2012) Trypanosoma cruzi: experimental parasitism in the central nervous system of albino mice. Parasitology Research 111, 2099–2107.Google Scholar
Nisimura, LM, Estato, V, De Souza, EM, Reis, PA, Lessa, MA, Castro-Faria-Neto, HC, Pereira, MCS, Tibiriçá, E and Garzoni, LR (2014) Acute Chagas disease induces cerebral microvasculopathy in mice. PLoS Neglected Tropical Diseases 8, 1–9.Google Scholar
Oliveira, NK, Ferreira, RN, Lopes, SDN, Chiari, E, Camargos, ERDS and Martinelli, PM (2017) Cardiac autonomic denervation and expression of neurotrophins (NGF and BDNF) and their receptors during experimental Chagas disease. Growth Factors 35, 161–170.Google Scholar
Pereira, RM, Greco, GM, Moreira, AM, Chagas, PF, Caldas, IS, Goncalves, RV and Novaes, RD (2017) Applicability of plant-based products in the treatment of Trypanosoma cruzi and Trypanosoma brucei infections: a systematic review of preclinical in vivo evidence. Parasitology 144, 1275–1287.Google Scholar
Perin, L, Moreira da Silva, R, Fonseca, KD, Cardoso, JM, Mathias, FA, Reis, LE, Molina, I, Correa-Oliveira, R, Vieira, PM and Carneiro, CM (2017) Pharmacokinetics and tissue distribution of benznidazole after oral administration in mice. Antimicrobial Agents Chemother 61, 2410–2416.Google Scholar
Pittella, JEH (2013) Pathology of CNS parasitic infections. Handbook of Clinical Neurology Elsevier 114, 65–88.Google Scholar
Prata, A (2001) Clinical and epidemiological aspects of Chagas disease. The Lancet Infectious Diseases 1, 92–100.Google Scholar
Procop, GW and Wilson, M (2001) Infectious disease pathology. Clinical Infectious Diseases 32, 1589–1601.Google Scholar
Prost, JO, Morikone, AM, Polo, G and Bosch, AM (2000) Evidence of cerebral involvement in the chronic stage of Chagas disease obtained using the P300 potential and quantified electroencephalography. Arquivos de neuro-psiquiatria 58, 262–271.Google Scholar
Rassi, A Jr., Rassi, A and Marin-Neto, JA (2010) Chagas disease. The Lancet 375, 1388–1402.Google Scholar
Rocha, A, de Meneses, ACO, De Meneses, O, da Silva, AM, Ferreira, MS, Nishioka, SA, Burgarelli, MKN, Almeida, E, Turcato, GJ, Metze, K and Lopes, ER (1994) Pathology of patients with Chagas’ disease and acquired immunodeficiency syndrome. The American Journal of Tropical Medicine and Hygiene 50, 261–268.Google Scholar
Rocha, FL, Roque, ALR, de Lima, JS, Cheida, CC, Lemos, FG, de Azevedo, FC, Arrais, RC, Bilac, D, Herrera, HM, Mourão, G and Jansen, AM (2013) Trypanosoma cruzi infection in neotropical wild carnivores (Mammalia: Carnivora): at the top of the T. cruzi transmission chain. PLoS ONE 8, e67463.Google Scholar
Roffê, E, Silva, AA, Marino, APM, dos Santos, PV and Lannes-Vieira, J (2003) Essential role of VLA-4/VCAM-1 pathway in the establishment of CD8+ T-cell-mediated Trypanosoma cruzi-elicited meningoencephalitis. Journal of Neuroimmunology 142, 17–30.Google Scholar
Schmunis, GA (2007) Epidemiology of Chagas disease in non endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 75–85.Google Scholar
Shikanai-Yasuda, MA and Carvalho, NB (2012) Oral transmission of Chagas disease. Clinical Infectious Diseases 54, 845–852.Google Scholar
Silva, AA, Roffê, E, Marino, AP, dos Santos, PV, Quirico-Santos, T, Paiva, CN and Lannes-Vieira, J (1999 a) Chagas’ disease encephalitis: intense CD8+ lymphocytic infiltrate is restricted to the acute phase, but is not related to the presence of Trypanosoma cruzi antigens. Clinical Immunology 92, 56–66.Google Scholar
Silva, AA, Roffe, E and Lannes-Vieira, J (1999 b) Expression of extracellular matrix components and their receptors in the central nervous system during experimental Toxoplasma gondii and Trypanosoma cruzi infection. Brazilian Journal of Medical and Biological Research 32, 593–600.Google Scholar
Silva, AA, Roffê, E, Santiago, H, Marino, AP, Kroll-Palhares, K, Teixeira, MM, Gazzinelli, RT and Lannes-Vieira, J (2007) Trypanosoma cruzi-triggered meningoencephalitis is a CCR1/CCR5-independent inflammatory process. Journal of Neuroimmunology 184, 156–163.Google Scholar
Silva, AAD, Pereira, GV, Souza, ASD, Silva, RR, Rocha, MS and Lannes-Vieira, J (2010) Trypanosoma cruzi-induced central nervous system alterations: from the entry of inflammatory cells to potential cognitive and psychiatric abnormalities. Journal of Neuropathology 1, 1–13.Google Scholar
Snary, D, Flint, JE, Wood, JN, Scott, MT, Chapman, MD, Dodd, J, Jessell, TM and Miles, MA (1983) A monoclonal antibody with specificity for Trypanosoma cruzi, central and peripheral neurones and glia. Clinical and Experimental Immunology 54, 617–624.Google Scholar
Sangster, NC and Dobson, RJ (2002) Anthelmintic resistance. In Lee, DL (ed.), The Biology of Nematodes. London and New York: Taylor and Francis, pp. 531–567.Google Scholar
Storino, R, Jörg, M and Auger, S (2003) Atención médica del paciente chagásico. Manual Práctico, un enfoque biológico, antropológico y social. Buenos Aires, Argentina: Editorial Ediprof.Google Scholar
Tanowitz, HB, Davies, P, Factor, SM, Minase, T, Herskowitz, A and Wittner, M (1981) Trypanosoma cruzi: choline acetyltransferase activity in tissues of susceptible and resistant mice infected with the Brazil strain. Experimental Parasitology 51, 269–278.Google Scholar
Tanowitz, HB, Davies, P and Wittner, M (1983) Alterations in acetylcholine receptors in experimental Chagas’ disease. Journal of Infectious Diseases 147, 460–466.Google Scholar
Teixeira, AR, Nascimento, RJ and Sturm, NR (2006) Evolution and pathology in Chagas disease: a review. Memórias do Instituto Oswaldo Cruz 101, 463–491.Google Scholar
Tekiel, VS, Mirkin, GA and Cappa, SG (1997) Chagas’ disease: reactivity against homologous tissues induced by different strains of Trypanosoma cruzi. Parasitology 115, 495–502.Google Scholar
Tekiel, V, Oliveira, GC, Correa-Oliveira, R, Sánchez, D and González-Cappa, SM (2005) Chagas’ disease: TCRBV9 over-representation and sequence oligoclonality in the fine specificity of T lymphocytes in target tissues of damage. Acta tropica 94, 15–24.Google Scholar
Trajkovic, V, Vuckovic, O, Stosic-Grujicic, S, Miljkovic, D, Popadic, D, Markovic, M, Bumbasirevic, V, Backovic, A, Cvetkovic, I, Harhaji, L, Ramic, Z and Stojkovic, MM (2004) Astrocyte-induced regulatory T cells mitigate CNS autoimmunity. Glia 47, 168–179.Google Scholar
Vago, AR, andrade, LO, Leite, AA, Reis, DDÁ, Macedo, AM, Adad, SJ, Tostes, SJ, Moreira, MCV, Filho, GB and Pena, SD (2000) Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. The American Journal of Pathology 156, 1805–1809.Google Scholar
Vilar-Pereira, G, da Silva, AA, Pereira, IR, Silva, RR, Moreira, OC, de Almeida, LR, de Souza, AS, Rocha, MS and Lannes-Vieira, J (2012) Trypanosoma cruzi-induced depressive-like behavior is independent of meningoencephalitis but responsive to parasiticide and TNF-targeted therapeutic interventions. Brain, Behavior, and Immunity 26, 1136–1149.Google Scholar
Vitkovic, L, Konsman, JP, Bockaert, J, Dantzer, R, Homburger, V and Jacque, C (2000) Cytokine signals propagate through the brain. Molecular Psychiatry 5, 604–615.Google Scholar
Volpato, FCZ, Sousa, GR, D’Ávila, DA, Galvão, LMDC and Chiari, E (2017) Combined parasitological and molecular-based diagnostic tools improve the detection of Trypanosoma cruzi in single peripheral blood samples from patients with Chagas disease. Revista da Sociedade Brasileira de Medicina Tropical 50, 506–515.Google Scholar
Woods, GL and Walker, DH (1996) Detection of infection or infectious agents by use of cytologic and histologic stains. Clinical Microbiology Reviews 9, 382–404.Google Scholar
World Health Organization (2017) Chagas disease (American trypanosomiasis): Epidemiology. Retrieved from http://www.who.int/chagas/epidemiology/en/.Google Scholar
Yauri, V, Castro-Sesquen, YE, Verastegui, M, Angulo, N, Recuenco, F, Cabello, I, Malaga, E, Bern, C, Gavidia, CM and Gilman, RH (2016) Domestic pig (Sus scrofa) as an animal model for experimental Trypanosoma cruzi infection. The American Journal of Tropical Medicine and Hygiene 94, 1020–1027.Google Scholar
Yeo, M, Acosta, N, Llewellyn, M, Sánchez, H, Adamson, S, Miles, GA, López, E, González, N, Patterson, JS, Gaunt, MW, Arias, AR and Miles, MA (2005) Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. International Journal for Parasitology 35, 225–233.Google Scholar
Zingales, B (2018) Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Tropica 184, 38–52.Google Scholar
Zingales, B, Andrade, SG, Briones, MRS, Campbell, DA, Chiari, E, Fernandes, O, Guhl, F, Lages-Silva, E, Macedo, AM, Machado, CR, Miles, MA, Romanha, AJ, Sturm, NR, Tibayrenc, M and Schijman, AG (2009) A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memórias do Instituto Oswaldo Cruz 104, 1051–1054.Google Scholar
Zingales, B, Miles, MA, Campbell, DA, Tibayrenc, M, Macedo, AM, Teixeira, MM, Schijman, AG, Llewellyn, MS, Lages-Silva, E, Machado, CR, Andrade, SG and Sturm, NR (2012) The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infection, Genetics and Evolution 12, 240–253.Google Scholar
Ziv, Y, Ron, N, Butovsky, O, Landa, G, Sudai, E, Greenberg, N, Cohen, H, Kipnis, J and Schwartz, M (2006) Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nature Neuroscience 9, 268–275.Google Scholar
Zoltowski, APC, Costa, AB, Teixeira, MAP and Koller, SH (2014) Qualidade metodológica das revisões sistemáticas em periódicos de psicologia brasileiros. Psicologia: teoria e Pesquisa 30, 97–104.Google Scholar
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