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Haematological alterations in non-human hosts infected with Trypanosoma cruzi: a systematic review

Published online by Cambridge University Press:  02 August 2018

Evaristo Villalba-Alemán ,
David L. Justinico ,
Mariáurea M. Sarandy ,
Rômulo D. Novaes ,
Mariella B. Freitas  and
Reggiani V. Gonçalves Open the ORCID record for Reggiani V. Gonçalves [Opens in a new window]
Evaristo Villalba-Alemán
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
David L. Justinico
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Mariáurea M. Sarandy
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Rômulo D. Novaes
Affiliation:
Department of Structural Biology, Federal University of Alfenas, Alfenas, Minas Gerais, Brazil
Mariella B. Freitas
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Reggiani V. Gonçalves*
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
*
Author for correspondence: Reggiani V. Gonçalves, E-mail: [email protected]
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Abstract

American trypanosomiasis is a neglected tropical disease whose spectrum has not been quite understood, including the impact of Trypanosoma cruzi infection on the haematological parameters of different vertebrate hosts. Thus, this study was designed to compare the pattern of haematological changes induced by T. cruzi infection in order to identify possible species-specific differences among taxons. We also aimed at evaluating the use of this parameter as a tool for diagnosis during the acute phase, when symptoms are usually masked. For this purpose, we performed a systematic search on PubMed and Scopus databases to retrieve original studies published until August 2016. Thirty-one studies were selected using Prisma strategy, which were then submitted to data extraction and methodological bias analysis. Half of the studies showed that the number of erythrogram decreased in infected animals, indicating anaemia. In 68.2% of the studies, the total amount of leukogram values increased, suggesting infection. The main methodological limitations were insufficient information for T. cruzi strains identification, inoculation routes and parasitological characterization. Most of the mammalian species analysed showed the same pattern of haematological changes following T. cruzi infection, indicating that haematological parameters might direct the diagnosis of Chagas disease in the initial phase.

Keywords

Chagas diseaseerythrocyteshaematologyleucocytesTrypanosoma cruzi
Type
Review Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 142 - 160
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Copyright © Cambridge University Press 2018 

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References

Acharya, KR and Ackerman, SJ (2014) Eosinophil granule proteins: form and function. Journal of Biological Chemistry 289, 17406–17415.Google Scholar
Alves, FM, Olifiers, N, Bianchi, RDC, Duarte, AC, Cotias, PMT, D'Andrea, PS and Jansen, AM (2011) Modulating variables of Trypanosoma cruzi and Trypanosoma evansi transmission in free-ranging coati (Nasua nasua) from the Brazilian Pantanal region. Vector-Borne and Zoonotic Diseases 11, 835–841.Google Scholar
Andrade, SG, Mesquita, IMO, Jambeiro, JF, Santos, IFM and Portella, RS (2003) Treatment with benznidazole in association with immunosuppressive drugs in mice chronically infected with Trypanosoma cruzi: investigation into the possible development of neoplasias. Revista da Sociedade Brasileira de Medicina Tropical 36, 441–447.Google Scholar
Andrews, NW and Whitlow, MB (1989) Secretion by Trypanosoma cruzi of a hemolysin active at low pH. Molecular and Biochemical Parasitology 33, 249–256.Google Scholar
Añez, N, Crisante, G and Soriano, PJ (2009) Trypanosoma cruzi congenital transmission in wild bats. Acta Tropica 109, 78–80.Google Scholar
Arantes, JM, Pedrosa, ML, Martins, HR, Veloso, VM, de Lana, M, Bahia, MT, Tafuri, WL and Carneiro, CM (2007) Trypanosoma cruzi: treatment with the iron chelator desferrioxamine reduces parasitemia and mortality in experimentally infected mic. Experimental Parasitology 117, 43–50.Google Scholar
Artis, D and Spits, H (2015) The biology of innate lymphoid cells. Nature 517, 293–301.Google Scholar
Barretto, MP (1964) Reservatórios de Trypanosoma cruzi nas Américas. Revista Brasileira de Malariología e Doenças Tropicais 16, 527–552.Google Scholar
Beldomenico, PM, Telfer, S, Gebert, S, Lukomski, L, Bennett, M and Begon, M (2008) The dynamics of health in wild field vole populations: a haematological perspective. Journal of Animal Ecology 77, 984–997.Google Scholar
Bern, C (2015) Chagas’ disease. New England Journal of Medicine 373, 456–466.Google Scholar
Berra, HH, Piaggio, E, Revelli, SS and Luquita, A (2005) Blood viscosity changes in experimentally Trypanosoma cruzi-infected rats. Clinical Hemorheology and Microcirculation 32, 175–182.Google Scholar
Bonecine-Almeida, MDG, Galvão-Castro, B, Pessoa, MHR, Piramez, C and Laranja, F (1990) Experimental Chagas’ disease in rhesus monkeys. I. Clinical parasitological, hematological and anatomo-pathological studies in the acute and indeterminate phase of the disease. Memórias do Instituto Oswaldo Cruz 85, 163–171.Google Scholar
Brener, Z and Gazzinelli, RT (1997) Immunological control of Trypanosoma cruzi infection and pathogenesis of Chagas’ disease. International Archives of Allergy and Immunology 114, 103–110.Google Scholar
Calabrese, KDS, Paradela, ASRC, do Valle, TZ, Tedesco, RC, Silva, S, Mortara, RA and da Costa, SG (1999) Study of acute Chagasic mice under immunosuppressive therapy by cyclosporin A: modulation and confocal analysis of inflammatory reaction. Immunopharmacology 47, 1–11.Google Scholar
Calabrese, KS, Lagrange, PH and Da Costa, SCG (1996) Chagas’ disease: enhancement of systemic inflammatory reaction in cyclophosphamide treated mice. International Journal of Immunopharmacology 18, 505–514.Google Scholar
Camargo, IJB, Araujo, PMF, Sakurada, JK, Stach-machado, DR, Rancel, HA and Silva, P (1991) Trypanosoma cruzi: early resistance induced by culture-derived trypomastigotes. Experimental Parasitology 268, 260–268.Google Scholar
Cardoso, J and Brener, Z (1980) Hematological changes in mice experimentally infected with Trypanosoma cruzi. Memorias Instituto Oswaldo Cruz, Rio de Janeiro 75, 97–104.Google Scholar
Carvalho, LS, Camargos, ER, Almeida, CT, Peluzio, MDCG, Alvarez-Leite, JI, Chiari, E and Reis, DDÁ (2006) Vitamin E deficiency enhances pathology in acute Trypanosoma cruzi-infected rats. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1025–1031.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
Cintra, IP, Silva, ME, Silva, ME, Silva, ME, Afonso, LCC, Nicoli, JR, Bambirra, EA and Vieira, EC (1998) Influence of dietary protein content on Trypanosoma cruzi infection in germfree and conventional mice. Revista do Instituto de Medicina Tropical de São Paulo 40, 355–362.Google Scholar
Coura, JR and Dias, JCP (2009) Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Memórias do Instituto Oswaldo Cruz 104, 31–40.Google Scholar
Coura, JR and Viñas, PA (2010) Chagas disease: a new worldwide challenge. Nature 465, S6–S7.Google Scholar
de Bonilla, L, Ewald, MD and Negrette, A (1973) Morphology and leukocyte values in the experimental Chagas disease. Investigación Clínica 14, 129–149.Google Scholar
de Castro, SL, Araújo-Jorge, TC, Rivera, MT and Junqueira, ACV (2000) Avaliação de parâmetros parasitológicos e de mortalidade. In de Araújo-Jorge, TC and de Castro, SL (eds), Doença de Chagas: Manual Para Experimentação Animal. Rio de Janeiro, Brasil: SciELO-Editora FIOCRUZ, pp. 219–236.Google Scholar
Deane, LM (1964) Animal reservoirs of Trypanosoma cruzi in Brazil. Revista Brasileira de Malariología e Doenças Tropicais 16, 27–48.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
Domingues, CS, Hardoim, DJ, Souza, CSF, Cardoso, FO, Mendes, VG, Previtalli-Silva, H, Abreu-Silva, AL, Pelajo-Machado, M, da Costa, SCG 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
dos Santos, CD, Toldo, MP and do Prado, JJC (2005) Trypanosoma cruzi: the effects of dehydroepiandrosterone (DHEA) treatment during experimental infection. Acta Tropica 95, 109–115.Google Scholar
Dotiwala, F, Mulik, S, Polidoro, RB, Ansara, JA, Burleigh, BA, Walch, M, Gazzinelli, RT and Lieberman, J (2016) Killer lymphocytes use granulysin, perforin and granzymes to kill intracellular parasites. Nature Medicine 22, 210–216.Google Scholar
Duz, ALC, Vieira, PMDA, Roatt, BM, Aguiar-Soares, RDO, Cardoso, JMDO, Oliveira, FCBD, Reis, LES, Tafuri, WL, Veloso, VM, Reis, AB and Carneiro, CM (2014) The TcI and TcII Trypanosoma cruzi experimental infections induce distinct immune responses and cardiac fibrosis in dogs. Memórias do Instituto Oswaldo Cruz 109, 1005–1013.Google Scholar
Elias, MCQ, Marques-Porto, R, Freymüller, E and Schenkman, S (2001) Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Molecular and Biochemical Parasitology 112, 79–90.Google Scholar
Fabrino, DL, Leon, LL, Parreira, GG, Genestra, M, Almeida, PE and Rossana, RC (2004) Peripheral blood monocytes show morphological pattern of activation and decreased nitric oxide production during acute Chagas’ disease in rats. Nitric Oxide – Biology and Chemistry 11, 166–174.Google Scholar
Feldman, AM and McNamara, D (2000) Myocarditis. New England Journal of Medicine 343, 1388–1398.Google Scholar
Ferraz, FN, Bilotti, CC, Aleixo, DL, Herrero, JCM, do Nascimento, JAD and de Araújo, SM (2014) Hematological and parasitological changes in mice experimentally infected by Trypanosoma cruzi and treated with biotherapy 7dH. European Journal of Integrative Medicine 6, 664–671.Google Scholar
Francisco, AF, de Abreu Vieira, PM, Arantes, JM, Pedrosa, ML, Martins, HR, Silva, M, Velosa, M, de Lana, M, Bahia, MT, Tafuri, WL and Carneiro, CM (2008) Trypanosoma cruzi: effect of benznidazole therapy combined with the iron chelator desferrioxamine in infected mice. Experimental Parasitology 120, 314–319.Google Scholar
Gascón, J, Albajar, P, Cañas, E, Flores, M, Herrera, RN, Lafuente, CA, Luciardi, HL, Moncayo, A, Molina, L, Muñoz, J and Puente, S (2008) Diagnosis, management and treatment of chronic Chagas’ heart disease in areas where Trypanosoma cruzi infection is not endemic. Enfermedades Infecciosas y Microbiologia Clinica 26, 99–106.Google Scholar
Green, AM, DiFazio, R and Flynn, JL (2013) IFN-γ from CD4 T cells is essential for host survival and enhances CD8 T cell function during Mycobacterium tuberculosis infection. The Journal of Immunology 190, 270–277.Google Scholar
Guedes, PMM, Veloso, VM, Afonso, LC, Caliari, MV, Carneiro, CM, Diniz, LF, Marques-da-Silva, EA, Caldas, IS, Do Valle Matta, MA, Souza, SM, Lana, M, Chiari, E, Galvão, LMC and Bahia, MT (2009) Development of chronic cardiomyopathy in canine Chagas disease correlates with high IFN-γ, TNF-α, and low IL-10 production during the acute infection phase. Veterinary Immunology and Immunopathology 130, 43–52.Google Scholar
Guedes, PMM, Veloso, VM, Mineo, TWP, Santiago-Silva, J, Crepalde, G, Caldas, IS and Bahia, MT (2012) Hematological alterations during experimental canine infection by Trypanosoma cruzi. Revista Brasileira de Parasitologia Veterinária 21, 151–156.Google Scholar
Hamilton, PB, Teixeira, MM and Stevens, JR (2012) The evolution of Trypanosoma cruzi: the ‘bat seeding’ hypothesis. Trends in Parasitology 28, 136–141.Google Scholar
Herrera, HM, Aquino, LPCT, Menezes, RF, Marques, LC, Moraes, MAV, Werther, K and Machado, RZ (2001) Trypanosoma evansi experimental infection in the South American coati (Nasua nasua): clinical, parasitological and humoral immune response. Veterinary Parasitology 102, 209–216.Google Scholar
Herrera, HM, Dávila, AMR, Norek, A, Abreu, UG, Souza, SS, D'Andrea, PS and Jansen, AM (2004) Enzootiology of Trypanosoma evansi in Pantanal, Brazil. Veterinary Parasitology 125, 263–275.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
Hooijmans, CR and Ritskes-Hoitinga, M (2013) Progress in using systematic reviews of animal studies to improve translational research. PLoS Medicine 10, e1001482.Google Scholar
Kaushansky, K and Shattil, SJ (2007) Bloodlines: the importance of mentoring for the future of hematology. Blood 109, 1353–1354.Google Scholar
Kennedy, PGE (2013) Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). The Lancet Neurology 12, 186–194.Google Scholar
Kierszenbaum, F (1981) On evasion of Trypanosoma cruzi from the host immune response. Lymphoproliferative responses to trypanosomal antigens during acute and chronic experimental Chagas’ disease. Immunology 44, 641–648.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
Kita, H (2011) Eosinophils: multifaceted biological properties and roles in health and disease. Immunological Reviews 242, 161–177.Google Scholar
Klein, RP and Camacho, AA (1997) Electrocardiographic evaluation of dogs experimentally infected with Trypanosoma cruzi during the acute and indeterminate chronic phases of infection. Brazilian Journal of Veterinary Research and Animal Science 34, 337–344.Google Scholar
Kook, H, Zeng, W, Guibin, C, Kirby, M, Young, NS and Maciejewski, JP (2001) Increased cytotoxic T cells with effector phenotype in aplastic anemia and myelodysplasia. Experimental Hematology 29, 1270–1277.Google Scholar
Lopes, PDS, Ramos, ELP, Gomez-Hernandez, C, Ferreira, GLS and Rezende-Oliveira, K (2015) Prevalence of Chagas disease among blood donor candidates in Triangulo Mineiro, Minas Gerais State, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 57, 461–465.Google Scholar
Malvezi, AD, Cecchini, R, de Souza, F, Tadokoro, CE, Rizzo, LV and Pinge-Filho, P (2004) Involvement of nitric oxide (NO) and TNF-alpha in the oxidative stress associated with anemia in experimental Trypanosoma cruzi infection. FEMS Immunology and Medical Microbiology 41, 69–77.Google Scholar
Marcondes, MC, Borelli, P, Yoshida, N and Russo, M (2000) Acute Trypanosoma cruzi infection is associated with anemia, thrombocytopenia, leukopenia, and bone marrow hypoplasia: reversal by nifurtimox treatment. Microbes and Infection 2, 347–352.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
Martins-Melo, FR, Ramos, AN, Alencar, CH and Heukelbach, J (2012) Mortality related to Chagas disease and HIV/AIDS coinfection in Brazil. Journal of Tropical Medicine 2012, 1–4.Google Scholar
Maya, JD, Orellana, M, Ferreira, J, Kemmerling, U, López-Muñoz, R and Morello, A (2010) Chagas disease: present status of pathogenic mechanisms and chemotherapy. Biological Research 43, 323–331.Google Scholar
Mayadas, TN, Cullere, X and Lowell, CA (2014) The multifaceted functions of neutrophils. Annual Review of Pathology: Mechanisms of Disease 9, 181–218.Google Scholar
Melo, RC (1999) Depletion of immune effector cells induces myocardial damage in the acute experimental Trypanosoma cruzi infection: ultrastructural study in rats. Tissue and Cell 31, 281–290.Google Scholar
Melo, RC and Machado, CR (2001) Trypanosoma cruzi: peripheral blood monocytes and heart macrophages in the resistance to acute experimental infection in rats. Experimental Parasitology 97, 15–23.Google Scholar
Melo, RC, Fabrino, DL, D’Ávila, H, Teixeira, HC and Ferreira, AP (2003 a) Production of hydrogen peroxide by peripheral blood monocytes and specific macrophages during experimental infection with Trypanosoma cruzi in vivo. Cell Biology International 27, 853–861.Google Scholar
Melo, RCN, D’Ávila, H, Fabrino, DL, Almeida, PE and Bozza, PT (2003 b) Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue and Cell 35, 59–67.Google Scholar
Mendonça, PHB, da Rocha, RFDB, de Braz Moraes, JB, LaRocque-de-Freitas, IF, Logullo, J, Morrot, A, Nunes, MP, Freire-de-Lima, CG and Decote-Ricardo, D (2017) Canine macrophage DH82 cell line as a model to study susceptibility to Trypanosoma cruzi infection. Frontiers in Immunology 2017, 604–615.Google Scholar
Minning, TA, Weatherly, DB, Atwood, J, Orlando, R and Tarleton, RL (2009) The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10, 1–15.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
Moreno, EA, Araujo, MA, Alarcon, ME, Lugo, A, Moreno, SC and Borges, R (2007) Hematological and blood glucose alterations in Wistar rats with acute Chagasic infection during gestation. Investigacion Clinica 48, 187–198.Google Scholar
Nakhle, MC, Menezes, MDCSD and Irulegui, I (1989) Eosinophil levels in the acute phase of experimental Chagas’ disease. Revista do Instituto de Medicina Tropical de São Paulo 31, 384–391.Google Scholar
Obata, K, Mukai, K, Tsujimura, Y, Ishiwata, K, Kawano, Y, Minegishi, Y and Karasuyama, H (2007) Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 110, 913–920.Google Scholar
Olifiers, N, Jansen, AM, Herrera, HM, De Cassia Bianchi, R, D'Andrea, PS, De Miranda Mourão, G and Gompper, ME (2015) Co-Infection and wild animal health: effects of trypanosomatids and gastrointestinal parasites on coatis of the Brazilian Pantanal. PLoS ONE 10, 1–19.Google Scholar
Pan American Health Organization (PAHO) (2006) Quantitative estimation of Chagas disease in the Americas. Montevideo. OPAS/HDM/CD/425-06.Google Scholar
Pan American Health Organization (PAHO) (2014) Available at http://new.paho.org/hq/index.php?option=com_content&view=article&id=2382&temid=3921&lang=fr (Accessed 20 March 2014).Google Scholar
Petersen, RM, Gürtler, RE, Cecere, MC, Rubel, DN, Lauricella, MA, Hansen, D and Carlomagno, MA (2001) Association between nutritional indicators and infectivity of dogs seroreactive for Trypanosoma cruzi in a rural area of northwestern Argentina. Parasitology Research 87, 208–214.Google Scholar
Prata, A (2001) Clinical and epidemiological aspects of Chagas disease. The Lancet Infectious Diseases 1, 92–100.Google Scholar
Pung, OJ, Hulsebos, LH and Kuhn, RE (1988) Experimental Chagas’ disease (Trypanosoma cruzi) in the Brazilian squirrel monkey (Saimiri sciureus): hematology, cardiology, cellular and humoral immune responses. International Journal for Parasitology 18, 115–120.Google Scholar
Rashid, A, Rasheed, K and Hussain, A (2008) Trypanosomiasis in dog; a case report. Journal of Arthropod-Borne Diseases 2, 48–51.Google Scholar
Rassi, AJ, Rassi, A and Marin-Neto, JA (2010) Chagas disease. The Lancet 375, 1388–1402.Google Scholar
Repka, D, Rangel, HA, Atta, AM, Gavino, VA and Piedrabuena, AE (1985) Experimental Chagas’ disease in mice infected with one LD50 of parasite. Revista Brasileira de Biologia 45, 309–316.Google Scholar
Rivera, I, Moreno, EA, González, N and de Yarbuh, AL (2000) Caracterización de aislados de Trypanosoma cruzi del occidente de Venezuela. Revista de Ecología Latinoamericana 7, 1–10.Google Scholar
Roberson, EL, Hanson, WL and Chapman, WL (1973) Trypanosoma cruzi: effects of anti-thymocyte serum in mice and neonatal thymectomy in rats. Experimental Parasitology 34, 168–180.Google Scholar
Roellig, DM, McMillan, K, Ellis, AE, Vandeberg, JL, Champagne, DE and Yabsley, MJ (2010) Experimental infection of two South American reservoirs with four distinct strains of Trypanosoma cruzi. Parasitology 137, 959–966.Google Scholar
Santana, LF, Gaspar, RC, Rossi, GAM, Nascentes, GAN, de Oliveira, GP, da Costa, AJ and Rodrigues, EA (2015) Alterações clínicas, hematológicas, seminais e parasitemia de caprinos machos experimentalmente infectados com Toxoplasma gondii. Ciência Animal Brasileira 16, 399–409.Google Scholar
Santana, VL, Souza, AP, Lima, DA, Araújo, AL, Justiniano, SV, Dantas, RP and Melo, MA (2012) Caracterização clínica e laboratorial de cães naturalmente infectados com Trypanosoma cruzi no semiárido nordestino. Pesquisa Veterinaria Brasileira 32, 536–541.Google Scholar
Santello, FH, Frare, EO, Santos, CD, Toldo, MPA, Kawasse, LM, Zucoloto, S and Prado, JC (2007) Melatonin treatment reduces the severity of experimental Trypanosoma cruzi infection. Journal of Pineal Research 42, 359–363.Google Scholar
Santos, CD, Levy, AMA, Toldo, MPA, Azevedo, AP and Júnior, JC (2007) Haematological and histopathological findings after ovariectomy in Trypanosoma cruzi infected mice. Veterinary Parasitology 143, 222–228.Google Scholar
Schoenborn, JR and Wilson, CB (2007) Regulation of interferon-γ during innate and adaptive immune responses. Advances in Immunology 96, 41–101.Google Scholar
Shaw, GL and Quadagno, D (1975) Trypanosoma lewisi and T. cruzi: effect of infection on gestation in the rat. Experimental Parasitology 37, 211–217.Google Scholar
Shaw, RJ, Cromwell, O and Kay, AB (1984) Preferential generation of leukotriene C4 by human eosinophils. Clinical and Experimental Immunology 56, 716–722.Google Scholar
Shi, HZ (2004) Eosinophils function as antigen-presenting cells. Journal of Leukocyte Biology 76, 520–527.Google Scholar
Shikanai-Yasuda, MA and Carvalho, NB (2012) Oral transmission of Chagas disease. Clinical Infectious Diseases 54, 845–852.Google Scholar
Silva, RAMS, Victório, AM, Ramirez, L, Dávila, AMR, Trajano, V and Jansen, AM (1999) Hematological and blood chemistry alterations in coatis (Nasua nasua) naturally infected by Trypanosoma evansi in the Pantanal, Brazil. Revue d Elevage et de Medicine Veterinaire des Pays Tropicaux 52, 119–122.Google Scholar
Stevens, JR, Noyes, HA, Dover, GA and Gibson, WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.Google Scholar
Stockham, SL and Scott, MA (2013) Fundamentals of Veterinary Clinical Pathology, 2nd Edn. Iowa, USA: John Wiley & Sons.Google Scholar
Tatakihara, VLH, Malvezi, AD, Panis, C, Cecchini, R, Zanluqui, NG, Yamauchi, LM and Martins-Pinge, MC (2015) Nitric oxide-releasing indomethacin enhances susceptibility to Trypanosoma cruzi infection acting in the cell invasion and oxidative stress associated with anemia. Chemico-Biological Interactions 227, 104–111.Google Scholar
Teske, E (2011) Neutrophil structure and biochemistry. In Weiss, DJ and Wardrop, KJ (eds), Schalm's Veterinary Hematology. Iowa, USA: John Wiley & Sons, pp. 263–267.Google Scholar
Thomsen, AR, Pisa, P, Bro-Jørgensen, K and Kiessling, R (1986) Mechanisms of lymphocytic choriomeningitis virus-induced hemopoietic dysfunction. Journal of Virology 59, 428–433.Google Scholar
Tribulatti, MV, Mucci, J, Van Rooijen, N, Leguizamón, MS and Campetella, O (2005) The trans-sialidase from Trypanosoma cruzi induces thrombocytopenia during acute Chagas’ disease by reducing the platelet sialic acid contents. Infection and Immunity 73, 201–207.Google Scholar
Tyler, KM and Engman, DM (2001) The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472–481.Google Scholar
Uman, LS (2011) Information management for the busy practitioner: systematic reviews and meta-analyses. Journal of the American Academy of Child and Adolescent Psychiatry 20, 57–59.Google Scholar
Van Hove, L, Schisano, T and Brace, L (2000) Anemia diagnosis, classification, and monitoring using Cell-Dyn technology reviewed for the new millennium. Laboratory Hematology 6, 93–108.Google Scholar
Van Luijk, J, Bakker, B, Rovers, MM, Ritskes-Hoitinga, M, de Vries, RB and Leenaars, M (2014) Systematic reviews of animal studies; missing link in translational research? PLoS ONE 9, e89981.Google Scholar
Vandamme, TF (2014) Use of rodents as models of human diseases. Journal of Pharmacy e Bioallied Sciences 6, 2–9.Google Scholar
Weiss, DJ and Souza, CD (2011) Monocytes and macrophages and their disorders. In Weiss, DJ and Wardrop, KJ (eds), Schalm's Veterinary Hematology. Iowa, USA: John Wiley & Sons. pp. 298–306.Google Scholar
Zhu, J, Yamane, H and Paul, WE (2009) Differentiation of effector CD4 T cell populations. Annual Review of Immunology 28, 445–489.Google Scholar
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