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A systematic review of the Trypanosoma cruzi genetic heterogeneity, host immune response and genetic factors as plausible drivers of chronic chagasic cardiomyopathy

Published online by Cambridge University Press:  13 September 2018

Paula Jiménez
Affiliation:
Grupo de Investigaciones Microbiológicas-UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia Escuela de Medicina y Ciencias de la Salud, Universidad del Rosario, Bogotá, Colombia
Jesús Jaimes
Affiliation:
Grupo de Investigaciones Microbiológicas-UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia Escuela de Medicina y Ciencias de la Salud, Universidad del Rosario, Bogotá, Colombia
Cristina Poveda
Affiliation:
Departments of Pediatrics and Molecular Virology and Microbiology, National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, USA
Juan David Ramírez*
Affiliation:
Grupo de Investigaciones Microbiológicas-UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia
*
Author for correspondence: Juan David Ramírez, E-mail: [email protected]

Abstract

Chagas disease is a complex tropical pathology caused by the kinetoplastid Trypanosoma cruzi. This parasite displays massive genetic diversity and has been classified by international consensus in at least six Discrete Typing Units (DTUs) that are broadly distributed in the American continent. The main clinical manifestation of the disease is the chronic chagasic cardiomyopathy (CCC) that is lethal in the infected individuals. However, one intriguing feature is that only 30–40% of the infected individuals will develop CCC. Some authors have suggested that the immune response, host genetic factors, virulence factors and even the massive genetic heterogeneity of T. cruzi are responsible of this clinical pattern. To date, no conclusive data support the reason why a few percentages of the infected individuals will develop CCC. Therefore, we decided to conduct a systematic review analysing the host genetic factors, immune response, cytokine production, virulence factors and the plausible association of the parasite DTUs and CCC. The epidemiological and clinical implications are herein discussed.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

Both authors contributed equally.

References

Andersson, B (2011) The Trypanosoma cruzi genome; conserved core genes and extremely variable surface molecule families. Research in Microbiology 162, 619625.Google Scholar
Angheben, A, Buonfrate, D, Gobbi, F, Bisoffi, Z, Boix, L, Pupella, S and Gandini, G (2015) Chagas disease and transfusion medicine: a perspective from non-endemic countries. Blood Transfusion 13, 540550.Google Scholar
Apt, W, Zulantay, I, Saavedra, M, Araya, E, Arriagada, K, Arribada, A, Solari, A, Ortiz, S and Rodríguez, J (2015) Trypanosoma cruzi burden, genotypes, and clinical evaluation of Chilean patients with chronic Chagas cardiopathy. Parasitology Research 114, 30073018.Google Scholar
Aridgides, D, Salvador, R and PereiraPerrin, M (2013) Trypanosoma cruzi highjacks TrkC to enter cardiomyocytes and cardiac fibroblasts while exploiting TrkA for cardioprotection against oxidative stress. Cellular Microbiology 15, 13571366.Google Scholar
Balouz, V, Melli, LJ, Volcovich, R, Moscatelli, G, Moroni, S, González, N, Ballering, G, Bisio, M, Ciocchini, A and Buscaglia, CA (2017) The Trypomastigote Small Surface Antigen from Trypanosoma cruzi improves treatment evaluation and diagnosis in pediatric Chagas disease. Journal of Clinical Microbiology 55, 13171317.Google Scholar
Belaunzaran, LM, Lammel, ME, Gimenez, G, Bott, E, Durante de Isola, EL, Wilkowsky, ES and Barbieri, MA (2013) Phospholipase A(1): a novel virulence factor in Trypanosoma cruzi. Molecular and Biochemical Parasitology 187, 7786.Google Scholar
Bern, C, Kjos, S, Yabseley, M and Montgomery, S (2011) Trypanosoma cruzi and Chagas disease in United States. Clinical Microbiology Reviews 24, 655681.Google Scholar
Bhattacharyya, T, Brooks, J, Yeo, M, Lewis, MD, Llewellyn, MS, Miles, MA and Carrasco, HJ (2010) Analysis of molecular diversity of the Trypanosoma cruzi trypomastigote small surface antigen reveals novel epitopes, evidence of positive selection and potential implications for lineage-specific serology. International Journal for Parasitology 40, 921928.Google Scholar
Bhattacharyya, T, Falconar, AK, Luquetti, AO, Costales, JA, Grijalva, MJ, Lewis, MD, Messenger, LA, Tran, TT, Ramirez, JD, Guhl, F, Carrasco, HJ, Diosque, P, Garcia, L, Litvinov, SV and Miles, MA (2014) Development of peptide-based lineage-specific serology for chronic Chagas disease: geographical and clinical distribution of epitope recognition. PLoS Neglected Tropical Diseases 8, 112.Google Scholar
Branquinha, M, Marinho, F, Sangenito, L, Oliveira, S, Goncalves, K, Ennes-Vidal, V, d'Avila-Levy, C and Santos, A (2013) Calpains: potential targets for alternative chemotherapeutic intervention against human pathogenic trypanosomatids. Current Medicinal Chemistry 20, 31743185.Google Scholar
Brenière, S, Barnabé, C and Waleckx, E (2016) Over six thousand Trypanosoma cruzi strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Neglected Tropical Diseases 10, 119.Google Scholar
Brown, S, Cornforth, D and Mideo, N (2012) Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends in Microbiology 20, 336342.Google Scholar
Burgos, JM, Bisio, M, Duffy, T, Levin, M, Schijman, A, Altcheh, J, Burgos Freilij, H, Valadares, H, Freitas, J, Macedo, A, Seidenstein, M, Macchi, L and Piccinali, R (2007) Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. International Journal for Parasitology 37, 13191327.Google Scholar
Burgos, JM, Diez, M, Vigliano, C, Bisio, M, Risso, M, Duffy, T, Cura, C, Brusses, B, Favaloro, L, Leguizamon, MS, Lucero, RH, Laguens, R, Levin, MJ, Favaloro, R and Schijman, AG (2010) Molecular identification of Trypanosoma cruzi discrete typing units in end-stage chronic Chagas heart disease and reactivation after heart transplantation. Clinical Infectious Diseases 51, 485495.Google Scholar
Burleigh, BA and Woolsey, AM (2002) Cell signalling and Trypanosoma cruzi invasion. Cellular Microbiology 4, 701711.Google Scholar
Burleigh, BA, Caler, E, Webster, P and Andrews, N (1997) A cytosolic serine endopeptidase from Trypanosoma cruzi is required for the generation of Ca2+ signaling in mammalian cells. Journal of Cell Biology 13, 609620.Google Scholar
Cámara, M, Cánepa, GE, Lantos, AB, Balouz, V, Yu, H, Chen, X, Campetella, O, Mucci, J and Buscaglia, CA (2017) The trypomastigote small surface antigen (TSSA) regulates Trypanosoma cruzi infectivity and differentiation. PLoS Neglected Tropical Diseases 11, 121.Google Scholar
Camargo, R, Faria, LO, Kloss, A, Favali, CBF, Kuckelkorn, U, Kloetzel, PM, de Sá, CM and Lima, BD (2014) Trypanosoma cruzi infection down-modulates the immunoproteasome biosynthesis and the MHC class I cell surface expression in HeLa cells. PLoS ONE 9, 112.Google Scholar
Carareto, C, Manoel-Caetano, FS, Aparecida, CM, Silva, AE, Borim, AA and Miyazaki, K (2008) kDNA gene signatures of Trypanosoma cruzi in blood and oesophageal mucosa from chronic chagasic patients. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 11021107.Google Scholar
Carranza, JC, Valadares, HMS, D’Ávila, DA, Baptista, RP, Moreno, M, Galvão, LMC, Chiari, E, Sturm, NR, Gontijo, ED, Macedo, AM and Zingales, B (2009) Trypanosoma cruzi maxicircle heterogeneity in Chagas disease patients from Brazil. International Journal for Parasitology 39, 963973.Google Scholar
Carrasco, HJ, Segovia, M, Llewellyn, MS, Morocoima, A, Urdaneta-Morales, S, Martínez, C, Garcia, C, Rodríguez, M, Espinosa, R, de Noya, BA, Díaz-Bello, Z, Herrera, L, Fitzpatrick, S, Yeo, M, Miles, MA and Feliciangeli, MD (2012) Geographical distribution of Trypanosoma cruzi genotypes in Venezuela. PLoS Neglected Tropical Diseases 6, 19.Google Scholar
Chuenkova, MV and PereiraPerrin, M (2009) Trypanosoma cruzi targets Akt in host cells as an intracellular antiapoptotic strategy. Science Signaling 2, 120.Google Scholar
Chuenkova, MV and PereiraPerrin, M (2011) Neurodegeneration and neuroregeneration in Chagas disease. Advances in Parasitology 76, 195233.Google Scholar
Coates, BM, Sullivan, DP, Makanji, MY, Du, NY, Olson, CL, Muller, WA, Engman, DM and Epting, CL (2013) Endothelial transmigration by Trypanosoma cruzi. PLoS ONE 8, 110.Google Scholar
Colorado, IA, Acquatella, H, Catalioti, F, Fernandez, MT and Layrisse, Z (2000) Original articles: HLA class II DRB1, DQB1, DPB1 polymorphism and cardiomyopathy due to Trypanosoma cruzi chronic infection. Human Immunology 61, 320325.Google Scholar
Corral, RS, Guerrero, NA, Cuervo, H, Girones, N and Fresno, M (2013) Trypanosoma cruzi infection and endothelin-1 cooperatively activate pathogenic inflammatory pathways in cardiomyocytes. PLoS Neglected Tropical Diseases 7, 112.Google Scholar
Costa, G, Moreira, PR, Menezes, CAS, Silva, M, Dutra, WO, Rocha, MO and Gollob, KJ (2009) Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. Journal of Infectious Diseases 199, 451454.Google Scholar
Cruz, MC, Souza-Melo, N, da Silva, CV, DaRocha, WD, Bahia, D, Araújo, PR, Teixeira, SR and Mortara, RA (2012) Trypanosoma cruzi: role of δ-amastin on extracellular amastigote cell invasion and differentiation. PLoS ONE 7, 111.Google Scholar
Cruz, J, Santos-Miranda, A, Monti-Rocha, R, Machado, F, Sales, P, Campos, P and Roman-Campos, D (2016) Altered cardiomyocyte function and Trypanosoma cruzi persistence in Chagas disease. American Journal of Tropical Medicine and Hygiene 94, 10281033.Google Scholar
Cunha-Neto, E and Chevillard, C (2014) Chagas disease cardiomyopathy: immunopathology and genetics. Mediators of Inflammation 2014, 111.Google Scholar
Cupello, MP, Souza, CF, Nogueira, NP, Laranja, GA, Sabino, KC, Coelho, MG, Oliveira, MM and Paes, MC (2014) Trypanosomatid essential metabolic pathway: new approaches about heme fate in Trypanosoma cruzi. Biochemical and Biophysical Research Communications 449, 216221.Google Scholar
Cura, C, Bisio, M, Duffy, T, Schijman, A, Lucero, RH, Formichelli, LB, Brusés, BL, Merino, DE, Oshiro, E, Sosa-Estani, S, Burgos, J, Lejona, S, Anchart, E, Hernández, DO, Severini, GV, Velazquez, E, Lattes, R, Altcheh, J, Freilij, H, Diez, M, Nagel, C, Vigliano, C, Favaloro, L and Favaloro, RR (2012) Trypanosoma cruzi discrete typing units in Chagas disease patients from endemic and non-endemic regions of Argentina. Parasitology 139, 516521.Google Scholar
Cura, CI, Duffy, T, Lucero, RH, Bisio, M, Péneau, J, Jimenez-Coello, M, Calabuig, E, Gimenez, MJ, Valencia, E, Kjos, SA, Santalla, J, Mahaney, SM, Cayo, NM, Nagel, C, Barcán, L, Málaga Machaca, ES, Acosta, KY, Brutus, L, Ocampo, SB and Aznar, C (2015) Multiplex real-time PCR assay using TaqMan probes for the identification of Trypanosoma cruzi DTUs in biological and clinical samples. PLoS Neglected Tropical Diseases 9, 118.Google Scholar
Dario, M, Rodrigues, M, Barros, J, Xavier, S, Roque, A, Jansen, A and D'Andrea, P (2016) Ecological scenario and Trypanosoma cruzi DTU characterization of a fatal acute Chagas disease case transmitted orally (Espírito Santo state, Brazil). Parasites and Vectors 9, 114.Google Scholar
de Souza, W, de Carvalho, TMU and Barrias, ES (2010) Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 1, 118.Google Scholar
Deghaide, NHS, Dantas, RO and Donadi, EA (1998) HLA class I and II profiles of patients presenting with Chagas’ disease. Digestive Diseases and Sciences 43, 246252.Google Scholar
del Puerto, R, Nishizawa, JE, Kikuchi, M, Iihoshi, N, Roca, Y, Avilas, C, Gianella, A, Lora, J, Velarde, F, Gutierrez, U, Renjel, LA, Miura, S, Higo, H, Komiya, N, Maemura, K and Hirayama, K (2010) Lineage analysis of circulating Trypanosoma cruzi parasites and their association with clinical forms of Chagas disease in Bolivia. PLoS Neglected Tropical Diseases 4. doi: 10.1371/journal.pntd.0000687.Google Scholar
Dias, JC, Ramos, AN, Gontijo, ED, Luquetti, A, Shikanai-Yasuda, MA, Coura, JR, Torres, RM, Melo, JR, Almeida, EA, Oliveira, WJ, Silveira, AC, Rezende, JM, Pinto, FS, Ferreira, AW, Rassi, A, Fragata, AA Filho, Sousa, AS, Correia, D, Jansen, AM, Andrade, GM, Britto, CF, Pinto, AY, Rassi, AJ, Campos, DE, Abad-Franch, F, Santos, SE, Chiari, E, Hasslocher-Moreno, AM, Moreira, EF, Marques, DS, Silva, EL, Marin-Neto, JA, Galvão, LM, Xavier, SS, Valente, SA, Carvalho, NB, Cardoso, AV, Silva, RA, Costa, VM, Vivaldini, SM, Oliveira, SM, Valente, VD, Lima, MM and Alves, RV (2016). 2nd Brazilian consensus on Chagas disease, 2015. Revista da Sociedade Brasileira de Medicina Tropical 49, 359.Google Scholar
Díaz, ML, Torres, R and González, CI (2011) Differential protein expression in developmental stages of Trypanosoma cruzi I isolated from a patient with chronic chagasic cardiomyopathy. Biomédica 31, 503513.Google Scholar
Drigo, SA, Cunha-Neto, E, Ianni, B, Faé, KC, Nunes, VL, Buck, P, Mady, C, Kalil, J, Goldberg, AC, Cardoso, MRA and Braga, PE (2006) TNF gene polymorphisms are associated with reduced survival in severe Chagas’ disease cardiomyopathy patients. Microbes and Infection 8, 598603.Google Scholar
Duffy, T, Bisio, M, Altcheh, J, Burgos, JM, Diez, M, Levin, MJ, Favaloro, RR, Freilij, H and Schijman, AG (2009) Accurate real-time PCR strategy for monitoring bloodstream parasitic loads in Chagas disease patients. PLoS Neglected Tropical Diseases 3, 110.Google Scholar
El-Sayed, NM, Bartholomeu, DC, Ghedin, E, Delcher, AL, Blandin, G, Westenberger, SJ, Caler, E, Cerqueira, GC, Haas, B, Crabtree, J, Feldblyum, T, Hou, L, Koo, H, Lacerda, D, Pai, G, Pop, M, Salzberg, SL, Shetty, J, Simpson, AJ, Van Aken, S, Wortman, J, White, O, Fraser, CM, Myler, PJ, Aggarwal, G, Worthey, EA, Anupama, A, Attipoe, P, Cadag, E, Fazelina, G, Huang, Y, Louie, T, Nelson, S, Parsons, M, Pentony, M, Rinta, J, Robertson, L, Seyler, A, Sisk, E, Vogt, C, Stuart, KD, Nilsson, D, Tran, AN, Branche, C, Arner, E, Bontempi, E, Darban, H, Edwards, K, Ferella, M, Kindlund, E, Kluge, S, McKenna, A, Mizuno, Y, Ochaya, S, Tammi, MT, Andersson, B, Campbell, DA, Machado, CR, Teixeira, S, Åslund, L, Pettersson, U, Bringaud, F, Burton, P, McCulloch, R, Mottram, JC, Ward, PN, Carrington, M, Sharma, R, Da Silveira, JF, De Jong, P, Osoegawa, K, Englund, PT, Frasch, AC, Sanchez, DO, Gull, K, Wickstead, B, Horn, D, Klingbeil, M, Levin, MJ, Lorenzi, H, Ramirez, JL and Tarleton, R (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of chagas disease. Science 309, 409415.Google Scholar
Esper, L, Utsch, L, Brant, F, Teixeira, MM, Vieira, LQ, Machado, FS, Soriani, FM, Arantes, RM, Campos, CF, Pinho, V, Souza, DG and Tanowitz, HB (2014) Regulatory effects of IL-18 on cytokine profiles and development of myocarditis during Trypanosoma cruzi infection. Microbes and Infection 16, 481490.Google Scholar
Fernández-Mestre, MT, Montagnani, S and Layrisse, Z (2004) Original article: is the CCR5-59029-G/G genotype a protective factor for cardiomyopathy in Chagas disease? Human Immunology 65, 725728.Google Scholar
Ferreira, ÉC, Portocarrero, AR, Brustolin, CF, Ciupa, L, Massini, PF, Aleixo, DL and de Araújo, SM (2017) Phosphorus protects cardiac tissue by modifying the immune response in rats infected by Trypanosoma cruzi. Cytokine 17, 102106.Google Scholar
Flórez, O, Zafra, G, Morillo, C, Martín, J and González, CI (2006) Interleukin-1 gene cluster polymorphism in chagas disease in a Colombian case-control study. Human Immunology 67, 741748.Google Scholar
Franzén, O, Ochaya, S, Sherwood, E, Andersson, B, Lewis, MD, Llewellyn, MS and Miles, MA (2011) Shotgun sequencing analysis of Trypanosoma cruzi i Sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Neglected Tropical Diseases 5, 19.Google Scholar
Freire-de-Lima, L, Fonseca, LM, Oeltmann, T, Mendonça-Previato, L and Previato, JO (2015) The trans-sialidase, the major Trypanosoma cruzi virulence factor: Three decades of studies. Glycobiology 25, 11421149.Google Scholar
Gaunt, MW, Yeo, M, Frame, IA, Stothard, JR, Carrasco, HJ, Taylor, MC, Mena, S, Solis, P, Miles, GAJ, Acosta, N, de Arias, AR and Miles, MA (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421, 936939.Google Scholar
Guedes, PMM, Gutierrez, FRS, Silva, GK, Dellalibera-Joviliano, R, Rodrigues, GJ, Bendhack, LM, Rassi, A, Schmidt, A, Maciel, BC, Marin- Neto, JA and Silva, JS (2012) Deficient regulatory T cell activity and low frequency of IL-17-producing T cells correlate with the extent of cardiomyopathy in human Chagas’ disease. PLoS Neglected Tropical Diseases 6, e1630.Google Scholar
Guhl, F (2013). Epidemiologia molecular de Trypanosoma cruzi 1:1, 1-8. Retrieved from Redalyc website. Available at http://www.redalyc.org/articulo.oa?id=17027695001.Google Scholar
Guhl, F and Ramírez, JD (2013) Retrospective molecular integrated epidemiology of Chagas disease in Colombia. Infection, Genetics and Evolution 20, 148154.Google Scholar
Guhl, F, Auderheide, A and Ramírez, JD (2014) From ancient to contemporary molecular eco-epidemiology of Chagas disease in the Americas. International Journal for Parasitology 44, 605612.Google Scholar
Hassan, G, Mukherjee, S, Nagajyothi, F, Weiss, L and Petkova, S (2006) Trypanosoma cruzi infection induces proliferation of vascular smooth muscle cells. Infection and Immunity 74, 152159.Google Scholar
Henrique, PM, Marques, T, da Silva, MV, de Oliveira, CF, Rodrigues, V, Gomez-Hernandez, C, Ramirez, LE, Ferreira, WS, Nogueira, GA and Norris, KA (2016) Correlation between the virulence of T. cruzi strains, complement regulatory protein expression levels, and the ability to elicit lytic antibody production. Experimental Parasitology 170, 6672.Google Scholar
Hernández, C, Cucunubá, Z, Parra, E, Toro, G, Zambrano, P and Ramírez, JD (2014) Chagas disease (Trypanosoma cruzi) and HIV co-infection in Colombia. International Journal of Infectious Diseases 26, 146148.Google Scholar
Hernández, C, Cucunubá, Z, Flórez, C, Olivera, M, Valencia, C, Zambrano, P, León, C and Ramírez, JD (2016) Molecular diagnosis of chagas disease in Colombia: parasitic loads and discrete typing units in patients from acute and chronic phases. PLoS Neglected Tropical Diseases 10, e0004997.Google Scholar
Higuera, SL, Guhl, F and Ramírez, JD (2013) Identification of Trypanosoma cruzi discrete typing units (DTUs) through the implementation of a high-resolution melting (HRM) genotyping assay. Parasites & Vectors 6, 16.Google Scholar
Jackson, AP (2010) The evolution of amastin surface glycoproteins in Trypanosomatid parasites. Molecular Biology and Evolution 27, 3345.Google Scholar
Jackson, Y, Pinto, A and Pett, S (2014) Chagas disease in Australia and New Zealand: risks and needs for public health interventions. Tropical Medicine & International Health 19, 212218.Google Scholar
Kuete, V (2013) Medicinal Plant Research in Africa: Pharmacology and Chemistry, 1st Edn. London, UK: Elsevier Insights.Google Scholar
Lasso, P, Beltrán, L, Guzmán, F, Rosas, F, Thomas, MC, López, MC, González, JM, Cuéllar, A and Puerta, C (2016) Promiscuous recognition of a Trypanosoma cruzi CD8+ T cell epitope among HLA-A2, HLA-A24 and HLA-A1 supertypes in chagasic patients. PLoS ONE 11, e0150996.Google Scholar
Lauthier, JJ, Tomasini, N, Rumi, MM, D'Amato, AMA, Ragone, PG, Diosque, P, Barnabé, C, Tibayrenc, M, Yeo, M, Lewis, MD, Llewellyn, MS, Miles, MA and Basombrío, MA (2012) Candidate targets for multilocus sequence typing of Trypanosoma cruzi: validation using parasite stocks from the Chaco Region and a set of reference strains. Infection, Genetics and Evolution 12, 350358.Google Scholar
Layrisse, Z, Fernandez, MT, Montagnani, S, Matos, M, Balbas, O, Herrera, F, Colorado, IA, Catalioti, F and Acquatella, H (2000) HLA-C*03 is a risk factor for cardiomyopathy in Chagas disease. Human Immunology 61, 925929.Google Scholar
Leiby, DA, Nguyen, ML, Proctor, MC, Townsend, RL and Stramer, SL (2017) Frequency of Trypanosoma cruzi parasitemia among infected blood donors with a potential association between parasite lineage and transfusion transmission. Transfusion 57, 14261432.Google Scholar
Leon, CM, Ramirez, JD, Montilla, M, Vanegas, R, Castillo, M and Parra, E (2017) Murine models susceptibility to distinct Trypanosoma cruzi I genotypes infection. Parasitology 144, 512519.Google Scholar
Leon Rodrigez, DA, Carmona, FD, Echeverría, LE, González, CI and Martin, J (2016) IL18 gene variants influence the susceptibility to chagas disease. PLoS Neglected Tropical Diseases 10, e0004583.Google Scholar
Lewis, MD, Yeo, M, Llewellyn, MS, Miles, MA, Ma, J and Carrasco, HJ (2009) Genotyping of Trypanosoma cruzi: systematic selection of assays allowing rapid and accurate discrimination of all known lineages. American Journal of Tropical Medicine and Hygiene 81, 10411049.Google Scholar
Lima, L, Espinosa-Álvarez, O, Ortiz, PA, Camargo, EP, Teixeira, MMG, Trejo-Varón, JA, Carranza, JC, Pinto, CM, Serrano, MG and Buck, GA (2015 a) Genetic diversity of Trypanosoma cruzi in bats, and multilocus phylogenetic and phylogeographical analyses supporting Tcbat as an independent DTU (discrete typing unit). Acta Tropica 151, 166177.Google Scholar
Lima, L, Espinosa-Álvarez, O, Pinto, CM, Cavazzana, M Jr, Pavan, AC, Carranza, JC, Lim, BK, Campaner, M, Takata, CSA, Camargo, EP, Hamilton, PB and Teixeira, MMG (2015 b) New insights into the evolution of the Trypanosoma cruzi clade provided by a new trypanosome species tightly linked to Neotropical Pteronotus bats and related to an Australian lineage of trypanosomes. Parasites & Vectors 8, 118.Google Scholar
Llewellyn, MS, Miles, MA, Carrasco, HJ, Lewis, MD, Yeo, M, Vargas, J, Torrico, F, Diosque, P, Valente, V, Valente, SA and Gaunt, MW (2009) Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathogens 5, e1000410.Google Scholar
Llewellyn, MS, Messenger, LA, Luquetti, AO, Garcia, L, Torrico, F, Tavares, SBN, Cheaib, B, Derome, N, Delepine, M, Baulard, C, Deleuze, JF, Sauer, S, Miles, and Michael, A (2015) Deep sequencing of the Trypanosoma cruzi GP63 surface proteases reveals diversity and diversifying selection among chronic and congenital Chagas disease patients. PLoS Neglected Tropical Diseases 9, 123.Google Scholar
Longhi, SA, Tasso, LM, Gomez, KA, Atienza, A, Bonato, R, Chiale, P, Perez, G, Buying, A, Pinilla, C, Judkowski, VA, Balouz, V, Buscaglia, CA and Santos, R (2014) Cytokine production but lack of proliferation in peripheral blood mononuclear cells from chronic Chagas’ disease cardiomyopathy patients in response to T. cruzi ribosomal P proteins. PLoS Neglected Tropical Diseases 8, e2906.Google Scholar
Luquetti, AO, Tavares, S, Siriano, L, Oliveira, R, Campos, DE, Morais, CA and Oliveira, EC (2015) Congenital transmission of Trypanosoma cruzi in central Brazil. A study of 1211 individuals born to infected mothers. Memórias do Instituto Oswaldo Cruz 110, 369376.Google Scholar
Macedo, AM and Segatto, M (2010). Implications of Trypanosoma Cruzi Intraspecific Diversity in the Pathogenesis of Chagas Disease, in American Trypanosomiasis Chagas Disease One Hundred Years of Research, 2nd Edn. Montpellier, France: Academic Press.Google Scholar
Macedo, AM, Machado, CR, Oliveira, RP and Pena, SDJ (2004) Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of Chagas disease. Memórias do Instituto Oswaldo Cruz 99, 112.Google Scholar
Magalhães, LM, Villani, FN, Nunes, MC, Gollob, KJ, Rocha, MO and Dutra, WO (2013) High interleukin 17 expression is correlated with better cardiac function in human Chagas disease. The Journal of Infectious Diseases 207, 661665.Google Scholar
Malvezi, AD, Da Silva, RV, De Freitas, RC, Lovo-Martins, MI, Tatakihara, VLH, Zanluqui, NG, Neto, EC, Goldenberg, S, Bordignon, J, Yamada-Ogatta, SF, Martin-Pinge, MC, Cecchini, R and Pinge-Filho, P (2014) Inhibition of cyclooxygenase-1 and cyclooxygenase-2 impairs Trypanosoma cruzi entry into cardiac cells and promotes differential modulation of the inflammatory response. Antimicrobial Agents and Chemotherapy 58, 61576164.Google Scholar
Mantilla, JC, Zafra, GA, Macedo, AM and González, CI (2010) Mixed infection of Trypanosoma cruzi I and II in a Colombian cardiomyopathic patient. Human Pathology 4, 610613.Google Scholar
Marin-Neto, AJ, Rassi, A Jr and Maciel, BC (2015). Chagas disease: Pathology and pathogenesis. UpToDate. Avalaible at https://www.uptodate.com/contents/chagas-disease-pathology-and-pathogenesis.Google Scholar
Margioto Teston, AP, de Abreu, AP, Abegg, CP, Gomes, ML and de Ornelas Toledo, MJ (2017) Outcome of oral infection in mice inoculated with Trypanosoma cruzi IV of the Western Brazilian Amazon. Acta Tropica. 166, 212217.Google Scholar
Meloni, M, Caporali, A, Graiani, G, Lagrasta, C, Katare, R, Van Linthout, S, Spillmann, F, Campesi, I, Madeddu, P, Quaini, F and Emanueli, C (2010) Nerve growth factor promotes cardiac repair following myocardial infarction. Circulation Research 106, 1275–U1230.Google Scholar
Messenger, LA, Llewellyn, MS, Bhattacharyya, T, Franzén, O, Lewis, MD, Ramírez, JD, Carrasco, HJ, Andersson, B and Miles, MA (2012) Multiple mitochondrial introgression events and heteroplasmy in Trypanosoma cruzi revealed by maxicircle MLST and next generation sequencing. PLoS Neglected Tropical Diseases 6, 112.Google Scholar
Messenger, LA, Ramirez, JD, Llewellyn, MS, Guhl, F and Miles, MA (2016) Importation of hybrid human-associated Trypanosoma cruzi strains of southern South American origin, Colombia. Emerging Infectious Diseases 22, 14521455.Google Scholar
Miles, MA, Póvoa, M, Prata, A, Cedillos, RA, De Souza, AA and Macedo, M (1981) Do radically dissimilar Trypanosoma cruzi strains (zymodemes) cause Venezuelan and Brazilian forms of chagas’ disease? The Lancet 317, 13381340.Google Scholar
Moncayo, A and Yanine, MIO (2006) An update on Chagas disease (human American trypanosomiasis). Annals of Tropical Medicine & Parasitology 100, 663677.Google Scholar
Monteiro, FA, Peretolchina, T, Lazoski, C, Harris, K, Dotson, EM, Abad-Franch, F, Tamayo, E, Pennington, PM, Monroy, C, Cordon-Rosales, C, Salazar-Schettino, PM, Gómez-Palacio, A, Grijalva, MJ, Beard, CB and Marcet, PL (2013a) Phylogeographic pattern and extensive mitochondrial DNA divergence disclose a species complex within the Chagas disease vector Triatoma dimidiata. PLoS ONE 8, 115.Google Scholar
Monteiro, WM, Margioto-Teston, AP, Gruendling, AP, dos Reis, D, Gomes, ML, de Araújo, SM, Bahia, MT, Magalhães, LK, de Oliveira-Guerra, JA, Silveira, H, Toledo, MJ and Vale-Barbosa, M (2013b). Trypanosoma cruzi I and IV stocks from Brazilian Amazon are divergent in terms of biological and medical properties in mice. PLoS Neglected Tropical Diseases 7. doi: 10.1371/journal.pntd.0002069.Google Scholar
Nagib, PRA, Dutra, WO, Chiari, E, Conceição, RS and Machado, CRS (2007) Trypanosoma cruzi: populations bearing opposite virulence induce differential expansion of circulating CD3+CD4−CD8− T cells and cytokine serum levels in young and adult rats. Experimental Parasitology 116, 366374.Google Scholar
Nogueira, LG, Santos, RH, Ianni, BMFiorelli, AI, Mairena, EC, Benvenuti, LA, Frade, , Donadi, E, Dias, F, Saba, B, Wang, HT, Fragata, A, Sampaio, M, Hirata, MH, Buck, P, Mady, C, Bocchi, EA, Stolf, NA, Kalil, J and Cunha-Neto, E (2012). Myocardial chemokine expression and intensity of myocarditis in Chagas cardiomyopathy are controlled by polymorphisms in CXCL9 and CXCL10. PLoS Neglected Tropical Diseases 6, 113.Google Scholar
Nogueira, LG, Frade, AF, Ianni, BM, Laugier, L, Pissetti, CW, Cabantous, S, Baron, M, Peixoto-Gde, L, Borges-Ade, M, Donadi, E, Marin-Neto, JA, Schmidt, A, Dias, F, Saba, B, Wang, HT, Fragata, A, Sampaio, M, Hirata, MH, Buck, P, Mady, C, Martinelli, M, Lensi, M, Siqueira, SF, Pereira, AC, Rodrigues, VJ, Kalil, J, Chevillard, C and Cunha-Neto, E (2015) Functional IL18 polymorphism and susceptibility to Chronic Chagas Disease. Cytokine 73, 7983.Google Scholar
Okura, M, Fang, J, Salto, ML, Singer, RS, Docampo, R and Moreno, SN (2005) A lipid-modified phosphoinositide-specific phospholipase C (TcPI-PLC) is involved in differentiation of trypomastigotes to amastigotes of Trypanosoma cruzi. Journal of Biological Chemistry 280, 1623516243.Google Scholar
Osorio, L, Rios, I, Gutierrez, B and Gonzalez, J (2012) Virulence factors of Trypanosoma cruzi: who is who? Microbes and Infection 14, 13901402.Google Scholar
Petkova, SB, Tanowitz, HB, Magazine, HI, Factor, SM, Chan, J, Pestell, RG, Bouzahzah, B, Douglas, SA, Shtutin, V, Morris, SA, Tsang, E, Weiss, LM, Christ, GJ, Wittner, M and Huang, H (2000) Myocardial expression of endothelin-1 in murine Trypanosoma cruzi infection. Cardiovascular Pathology 9, 257265.Google Scholar
Pinto, CM, Kalko, EK, Cottontail, VM, Cottontail, I and Wellinghausen, N (2012) Tcbat a bat-exclusive lineage of Trypanosoma cruzi in the Panama Canal Zone, with comments on its classification and the use of the 18S rRNA gene for lineage identification. Infection, Genetics and Evolution 12, 13281332.Google Scholar
Pinto, CM, Ocaña-Mayorga, S, Tapia, E, Lobos, S, Zurita, A, Aguirre-Villacís, , MacDonals, A, Villacis, AG, Lima, L, Teixeira, MM, Grijalva, MJ and Perkins, S (2015) Bats, trypanosomes, and triatomines in Ecuador: new insights into the diversity, transmission, and origins of Trypanosoma cruzi and Chagas disease. PLoS ONE 10, e0139999.Google Scholar
Pissetti, CW, Correia, D, de Oliveira, RF, Llaguno, MM, Balarin, MA, Silva-Grecco, RL and Rodrigues, JV (2011) Genetic and functional role of TNF-alpha in the development Trypanosoma cruzi infection. PLoS Neglected Tropical Diseases 5, 110.Google Scholar
Poveda, C, Fresno, M, Gironès, NA, Martins-Filho, O, Ramírez, JD, Santi-Rocca, J, Marín-Neto, JA, Morillo, CA, Rosas, and Guhl, F (2014) Cytokine profiling in Chagas disease: towards understanding the association with infecting Trypanosoma cruzi discrete typing units (a BENEFIT TRIAL sub-study). PLoS ONE 9.Google Scholar
Prata, A (2001) Clinical and epidemiological aspects of Chagas disease. Lancet Infectious Diseases 1, 92100.Google Scholar
Ramasawmy, R, Faé, KC, Cunha-Neto, E, Borba, SC, Ianni, B, Mady, C, Goldberg, AC and Kalil, J (2008) Variants in the promoter region of IKBL/NFKBIL1 gene may mark susceptibility to the development of chronic Chagas’ cardiomyopathy among Trypanosoma cruzi-infected individuals. Molecular Immunology 45, 283288.Google Scholar
Ramírez, JD and Hernández, C (2017) Trypanosoma cruzi I: towards the need of genetic subdivision?, Part II. Acta Tropica S0001-706X, 3025030254.Google Scholar
Ramírez, JD and Llewellyn, MS (2014) Reproductive clonality in protozoan pathogens-truth or artefact? Molecular Ecology 23, 41954202.Google Scholar
Ramírez, JD, Guhl, F, Umezawa, ES, Morillo, CA, Rosas, F, Marin-Neto, JA and Restrepo, S (2009) Evaluation of adult chronic Chagas’ heart disease diagnosis by molecular and serological methods. Journal of Clinical Microbiology 47, 39453951.Google Scholar
Ramírez, JD, Guhl, F, Rendón, LM, Rosas, F, Marin-Neto, JA and Morillo, C (2010) Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic chagasic patients. PLoS Neglected Tropical Diseases 4.Google Scholar
Ramírez, JD, Guhl, F, Messenger, LA, Lewis, MD, Montilla, M, Cucunuba, Z and Llewellyn, MS (2012) Contemporary cryptic sexuality in Trypanosoma cruzi. Molecular Ecology 21, 42164226.Google Scholar
Ramírez, JD, Montilla, M, Cucunubá, ZM, Floréz, AC, Zambrano, P and Guhl, F (2013) Molecular epidemiology of human oral chagas disease outbreaks in Colombia. PLoS Neglected Tropical Diseases 7, 17.Google Scholar
Ramírez, JD, Hernández, C, Cucunubá, ZM, Montilla, M, Flórez, AC, Zambrano, P and Parra, E (2014) First report of human Trypanosoma cruzi infection attributed to TcBat genotype. Zoonoses and Public Health 61, 477479.Google Scholar
Rassi, JA, Rassi, A and Marin-Neto, JA (2009) Chagas heart disease: pathophysiologic mechanisms, prognostic factors and risk stratification. Memórias do Instituto Oswaldo Cruz 104, 152158.Google Scholar
Rassi, JA, Rassi, A and Marin-Neto, JA (2010) Chagas disease. The Lancet 375, 13881402.Google Scholar
Rassi, JA, Rassi, A and Marcondes de Rezende, J (2012) American trypanosomiasis (Chagas disease). Infectious Disease Clinics of North America 2, 275291.Google Scholar
Rassi, JA, Rassi, A and Marin-Neto, JA (2015) Chagas disease. The Lancet 375, 4571.Google Scholar
Rassi, JA, Marin Neto, JA and Rassi, A (2017) Chronic Chagas cardiomyopathy: a review of the main pathogenic mechanisms and the efficacy of aetiological treatment following the BENznidazole Evaluation for Interrupting Trypanosomiasis (BENEFIT) trial. Memórias do Instituto Oswaldo Cruz 112, 224235.Google Scholar
Reis, DD, Jones, EM, Tostes, S Jr, Lopes, ER, Gazzinelli, G, Colley, DG and McCurley, TL (1993). Characterization of inflammatory infiltrates in chronic chagasic myocardial lesions: presence of tumor necrosis factor-alpha+ cells and dominance of granzyme A+, CD8+ lymphocytes. The American Journal of Tropical Medicine and Hygiene 48, 637644.Google Scholar
Reis, PG, Sakita, KM, de Moraes, AG, Aquino, JS, Macedo, LC, Mazini, PS, Sell, AM, de Oliveira, DS, Bulgarelli, R and Laguila, JE (2017) Genetic polymorphisms of IL17 and Chagas disease in the south and southeast of Brazil. Journal of Immunology Research 2017, 7.Google Scholar
Rodrigues, MM, Oliveira, AC and Bellio, M (2012) The immune response to Trypanosoma cruzi : role of toll-like receptors and perspectives for vaccine development. Journal of Parasitology Research 2012, 112.Google Scholar
Rodríguez, JA, Marigorta, UM and Navarro, A (2014) Integrating genomics into evolutionary medicine. Current Opinion in Genetics & Development 29, 97102.Google Scholar
Roggero, E, Rosa Perez, A, Pollachini, N, Raquel Villar, S, Wildmann, J, Besedovsky, H and del Rey, A (2016) The sympathetic nervous system affects the susceptibility and course of Trypanosoma cruzi infection. Brain Behavior and Immunity 58, 228236.Google Scholar
Rojas, MW, Anaya, JM, Gómez, LM, Aristizabal, BH, Cano, R, LE and Lopera, HD (2017) Inmunología de Rojas (W. R. M. Ed. 18 ed.). Medellin (Antioquia, Colombia): Corporación para Investigaciones Biologicas. CIB 2017.Google Scholar
Rozas, M, Doncker, SD, Adaui, V, Coronado, X, Barnabé, C, Tibyarenc, M and Dujardin, JC (2007) Multilocus polymerase chain reaction restriction fragment-length polymorphism genotyping of Trypanosoma cruzi (Chagas disease): taxonomic and clinical applications. The Journal of Infectious Diseases 195, 1381.Google Scholar
Salomone, O, Caeiro, T, Madoery, R, Amuchastegui, M, Omelinauk, M, Juri, D and Kaski, J (2001) High plasma immunoreactive endothelin levels in patients with Chagas’ cardiomyopathy. American Journal of Cardiology 87, 12171220.Google Scholar
San Francisco, J, Gutierrez, B, Neira, I, Munoz, C, Sagua, H, Araya, JE, Andrade, JC, Zailberger, A, Catalán, A, Remonsellez, F, Vega, JL and González, J (2017) Decreased cruzipain and gp85/trans-sialidase family protein expression contributes to loss of Trypanosoma cruzi trypomastigote virulence. Microbes and Infection 19, 5561.Google Scholar
Sanjabi, S, Zenewicz, LA, Kamanaka, M and Flavell, RA (2009) Anti-inflammatory and pro-inflammatory roles of TGF-β, IL-10, and IL-22 in immunity and autoimmunity. Current Opinion in Pharmacology 9, 447453.Google Scholar
Sanmarco, LM, Visconti, LM, Eberhardt, N, Ramello, MC, Ponce, NE, Spitale, NB, Vozza, ML, Bernardi, GA, Gea, S, Minguez, AR and Aoki, MP (2016) IL-6 improves the nitric oxide-induced cytotoxic CD8+ T cell dysfunction in human chagas disease. Frontiers in Immunology 7, 112.Google Scholar
Sanoja, C, Carbajosa, S, Fresno, M and Gironès, N (2013) Analysis of the dynamics of infiltrating CD4+ T cell subsets in the heart during experimental Trypanosoma cruzi infection. PLoS ONE 8, 111.Google Scholar
Santi-Rocca, J, Fernandez-Cortes, F, Chillon-Marinas, C, Gonzalez-Rubio, ML, Girones, N, Fresno, M and Martin, D (2017) A multi-parametric analysis of Trypanosoma cruzi infection: common pathophysiologic patterns beyond extreme heterogeneity of host responses. Scientific Reports 7, 12.Google Scholar
Savino, W (2017) Endocrine immunology of chagas disease. In Endocrine Immunology. Karger Publishers, 160175. https://www.karger.com/Article/Abstract/452914Google Scholar
Segovia, M, Carrasco, HJ, Martínez, CE, Messenger, LA, Nessi, A, Londoño, JC, Espinosa, R, Martínez, C, Mijares, A, Bonfante-Cabarcas, R, Lewis, MD, de Noya, BA, Miles, MA and Llewellyn, MS (2013) Molecular epidemiologic source tracking of orally transmitted Chagas disease, Venezuela. Emerging Infectious Diseases 19, 10981101.Google Scholar
Strasen, J, Williams, T, Ertl, G, Ritter, O, Zoller, T and Stich, A (2014) Epidemiology of Chagas disease in Europe: many calculations, little knowledge. Clinical Research in Cardiology 103, 110.Google Scholar
Sturm, NR, Vargas, NS, Westenberger, SJ, Zingales, B and Campbell, DA (2003) Evidence for multiple hybrid groups in Trypanosoma cruzi. International Journal for Parasitology 33, 269279.Google Scholar
Sánchez, LV and Ramírez, JD (2013) Congenital and oral transmission of American trypanosomiasis: an overview of physiopathogenic aspects. Parasitology 140, 147159.Google Scholar
Sánchez-Montalvá, A, Salvador, F, Rodríguez-Palomares, J, Sulleiro, E, Sao-Avilés, A, Roure, S, Valerio, L, Evangelista, A and Molina, I (2016). Chagas cardiomyopathy: usefulness of EKG and echocardiogram in a non-endemic country. PLoS ONE 11. doi: 10.1371/journal.pone.0157597.Google Scholar
Tarleton, RL (1991) Regulation of immunity in Trypanosoma cruzi infection. Experimental Parasitology 73, 106109.Google Scholar
Tarleton, RL (2003). Chagas disease: a role for autoimmunity? Trends in Parasitology 19, 447.Google Scholar
Tarleton, RL (2015) CD8 T cells in Trypanosoma cruzi infection. Seminars in Immunopathology 37, 233238.Google Scholar
Tarleton, RL and Zhang, L (1999) Chagas disease etiology: autoimmunity or parasite persistence? Parasitology Today 15, 9499.Google Scholar
Teixeira, RL, Hecht, MM, Guimaro, MC, Sousa, AO and Nitz, N (2011) Pathogenesis of Chagas’ disease: parasite persistence and autoimmunity. Clinical Microbiology Reviews 24, 592630.Google Scholar
Telleria, J, Biron, D, Brizard, JP, Demettre, E, Séveno, M, Barnabé, C, Ayala, FJ and Tibayrenc, M (2010) Phylogenetic character mapping of proteomic diversity shows high correlation with subspecific phylogenetic diversity in Trypanosoma cruzi. Proceedings of the National Academy of Sciences of the United States of America 107, 20411–6.Google Scholar
Vago, AR, Andrade, LO, Leite, AA, d'Avila-Reis, D, Macedo, AM, Adad, SJ, Tostes, SJ, Moreira, MC, 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. American Journal of Pathology 156, 18051809.Google Scholar
Valadares, HM, Pimenta, JR, de Freitas, JM, Duffy, T, Bartholomeu, DC, Oliveira, RP, Chiari, E, Moreira, MC, Filho, GB, Schijman, AG, Franco, GR, Machado, CR, Pena, SD and Macedo, AM (2008) Genetic profiling of Trypanosoma cruzi directly in infected tissues using nested PCR of polymorphic microsatellites. International Journal for Parasitology 38, 839850.Google Scholar
Venegas, J, Coñoepan, W, Pichuantes, S, Miranda, S, Apt, W, Arribada, A, Zulantay, I, Coronado, X, Rodriguez, J, Reyes, E, Solari, A and Sanchez, G (2009) Differential distribution of Trypanosoma cruzi clones in human chronic chagasic cardiopathic and non-cardiopathic individuals. Acta Tropica 109, 187193.Google Scholar
Vicco, MH, Ferini, F, Rodeles, L, Cardona, P, Bontempi, I, Lioi, S, Beloscar, J, Nara, T, Marcipar, I and Bottasso, OA (2013) Assessment of cross-reactive host-pathogen antibodies in patients with different stages of chronic chagas disease. Revista Espanola de Cardiologia 66, 791796.Google Scholar
Vitelli-Avellar, DM, Sathler-Avelar, R, Mattoso-Barbosa, AM, Gouin, N, Perdigao-de-Oliveira, M, Valério-dos-Reis, L, Peres, CR, Elói-Santos, SM, Souza, GM, Rodrigues-do-Amaral, L, Teixeira-Carvahlo, A, Martins-Fihlo, OA, Dick, JEJ, Hubbard, GB, Vandenberg, JF and VandeBerg, JL (2017) Cynomolgus macaques naturally infected with Trypanosoma cruzi-I exhibit an overall mixed pro-inflammatory/modulated cytokine signature characteristic of human Chagas disease. Neglected Tropical Diseases. 11, e0005233.Google Scholar
Westenberger, SJ, Campbell, DA, Sturm, NR and Barnabé, C (2005) Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171, 527543.Google Scholar
WHO (2017) Weekly epidemiological record. World Health Organization, Relevé Épidémiologique Hebdomadaire, 92, 357368.Google Scholar
Wong, VK, Baker, S, Pickard, DJ, Parkhill, J, Page, AJ, Feasey, NA, Kingsley, RA, Thomson, NR, Keane, JA, Weill, FX, Edwards, DJ, Hawkey, J, Harris, SR, Mather, AE, Cain, AK, Hadfield, J, Hart, PJ, Thieu, NT, Klemm, EJ, Glinos, DA, Breiman, RJ, Watson, CH, Kariuki, S, Gordon, MA, Heyderman, RS, Okoro, C, Jacobs, J, Lunguya, O, Edmunds, WJ, Msefula, C, Chabalgoity, JA, Kama, M, Jenkins, K, Dutta, S, Marks, F, Campos, J, Thompson, C, Obaro, S, MacLennan, CA, Dolecek, C, Keddy, KH, Smith, AM, Parry, CM, Karkey, A, Mulholland, EK, Campbell, JI, Dongol, S, Basnyat, B, Dufour, M, Bandaranayake, D, Naseri, TT, Singh, SP, Hatta, M, Newton, P, Onsare, RS, Isaia, L, Dance, D, Davong, V, Thwaites, G, Wijedoru, L, Crump, JA, De Pinna, E, Nair, S, Nilles, EJ, Thanh, DP, Turner, P, Soeng, S, Valcanis, M, Powling, J, Dimovski, K, Hogg, G, Farrar, J, Holt, KE and Dougan, G (2015) Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nature Genetics 47, 632639.Google Scholar
Yeo, M, Acosta, N, Llewellyn, M, Sánchez, H, Adamson, S, Miles, GA, López, E, González, N, Patterson, JS, Gaunt, MW, de 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, 225233.Google Scholar
Yeo, M, Mauricio, IL, Messenger, LA, Lewis, MD, Llewellyn, MS, Acosta, N, Bhattacharyya, T, Diosque, P, Carrasco, HJ and Miles, MA (2011) Multilocus sequence typing (MLST) for lineage assignment and high resolution diversity studies in Trypanosoma cruzi. PLoS Neglected Tropical Diseases 5, 113.Google Scholar
Yoshida, N (2006) Molecular basis of mammalian cell invasion by Trypanosoma cruzi. Anais da Academia Brasileira de Ciências 78, 87111.Google Scholar
Yoshida, N, Tyler, KM and Llewellyn, MS (2011) Invasion mechanisms among emerging food-borne protozoan parasites. Trends in Parasitology 27, 459466.Google Scholar
Zafra, G, Mantilla, JC, Jacome, J, Macedo, AM and Gonzalez, CI (2011) Direct analysis of genetic variability in Trypanosoma cruzi populations from tissues of Colombian chagasic patients. Human Pathology 42, 11591168.Google Scholar
Zingales, B (2017) Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Tropica. S0001-706X, 3042630426.Google Scholar
Zingales, B, Andrade, SG, Briones, MR, 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 7, 10511054.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 2, 240253.Google Scholar
Zumaya-Estrada, FA, Messenger, LA, Lopez-Ordonez, T, Lewis, MD, Flores-Lopez, CA, Martínez-Ibarra, AJ, Pennington, PM, Cordon-Rosales, C, Carrasco, HV, Segovia, M, Miles, MA and Llewellyn, MS (2012) North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasites & Vectors 5, 226234.Google Scholar