Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T08:18:58.379Z Has data issue: false hasContentIssue false
  • English
  • Français

First finding of Trypanosoma cruzi II in vampire bats from a district free of domestic vector-borne transmission in Northeastern Argentina

Published online by Cambridge University Press:  25 May 2016

HERNÁN D. ARGIBAY ,
M. MARCELA OROZCO ,
M. VICTORIA CARDINAL ,
MIGUEL A. RINAS ,
MARÍA ARNAIZ ,
CARLOS MENA SEGURA  and
RICARDO E. GÜRTLER
HERNÁN D. ARGIBAY
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, UBA-IEGEBA CONICET, Buenos Aires, Argentina
M. MARCELA OROZCO
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, UBA-IEGEBA CONICET, Buenos Aires, Argentina
M. VICTORIA CARDINAL
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, UBA-IEGEBA CONICET, Buenos Aires, Argentina
MIGUEL A. RINAS
Affiliation:
Parque Ecológico El Puma, Ministerio de Ecología y Recursos Naturales Renovables, Provincia de Misiones, Argentina
MARÍA ARNAIZ
Affiliation:
Instituto Nacional de Parasitología Dr. Mario Fatala Chaben, ANLIS Malbrán, Buenos Aires, Argentina
CARLOS MENA SEGURA
Affiliation:
Instituto de Zoonosis Luis Pasteur, Gobierno de la Ciudad de Buenos Aires, Argentina
RICARDO E. GÜRTLER*
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, UBA-IEGEBA CONICET, Buenos Aires, Argentina
*
*Corresponding author: Intendente Güiraldes 2160, Ciudad Universitaria, CP: C1425EGA, Ciudad Autónoma de Buenos Aires, Argentina. Tel: +54-11-45763318. Fax: +54-11-45763318. E-mail: gurtler@ege.fcen.uba.ar
Get access Rights & Permissions [Opens in a new window]

Summary

Establishing the putative links between sylvatic and domestic transmission cycles of Trypanosoma cruzi, the etiological agent of Chagas disease, is of public health relevance. We conducted three surveys to assess T. cruzi infection in wild mammals from a rural and a preserved area in Misiones Province, Northeastern Argentina, which had recently been declared free of vector- and blood-borne transmission of human T. cruzi infection. A total of 200 wild mammals were examined by xenodiagnosis (XD) and/or polymerase chain reaction (PCR) amplification of the hyper-variable region of kinetoplast DNA minicircles of T. cruzi (kDNA-PCR). The overall prevalence of T. cruzi infection was 8%. Nine (16%) of 57 Didelphis albiventris opossums and two (7%) of 29 Desmodus rotundus vampire bats were positive by both XD and kDNA-PCR. Additionally, one D. rotundus positive for T. cruzi by kDNA-PCR tested positive by satellite-DNA-PCR (SAT-DNA-PCR). The T. cruzi-infected bats were captured indoors and in the yard of a vacant dwelling. All D. albiventris were infected with TcI and both XD-positive D. rotundus by TcII. Fifty-five opossum cubs within the marsupium were negative by XD. The mean infectiousness to the vector was 62% in D. albiventris and 50% in D. rotundus. Mice experimentally infected with a parasite isolate from a vampire bat displayed lesions typically caused by T. cruzi. Our study documents the presence of the genotype TcII in a sylvatic host for the first time in Argentina, and the occurrence of two transmission cycles of T. cruzi in a district free of domestic vector-borne transmission.

Keywords

Trypanosoma cruzidiscrete typing unitDesmodus rotundusDidelphis albiventris
Type
Research Article
Information
Parasitology , Volume 143 , Issue 11 , September 2016 , pp. 1358 - 1368
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abalos, J. W., de Mischis, C. C. and Kufner, M. B. (1980). Triatomismo domiciliario en la Provincia de Misiones. Revista Medicina 40, 217–221.Google Scholar
Alvarado-Otegui, J. A., Ceballos, L. A., Orozco, M. M., Enriquez, G. F., Cardinal, M. V., Cura, C., Schijman, A. G., Kitron, U. and Gürtler, R. E. (2012). The sylvatic transmission cycle of Trypanosoma cruzi in a rural area in the humid Chaco of Argentina. Acta Tropica 124, 79–86.CrossRefGoogle Scholar
Añez, N., Crisante, G. and Soriano, P. J. (2009). Trypanosoma cruzi congenital transmission in wild bats. Acta Tropica 109, 78–80.CrossRefGoogle ScholarPubMed
Bar, M. E., Mabel Alvarez, B., Oscherov, E. B., Damborsky, M. P. and Jörg, M. E. (1999). Contribución al conocimiento de los reservorios del Trypanosoma cruzi (Chagas,1909) en la Provincia de Corrientes, Argentina. Revista da Sociedade Brasileira de Medicina Tropical 32, 271–276.CrossRefGoogle Scholar
Ben Younés-Chennoufi, A., Hontebeyrie-Joskowicz, M., Tricottet, V., Eisen, H., Reynes, M. and Said, G. (1988). Persistence of Trypanosoma cruzi antigens in the inflammatory lesions of chronically infected mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 77–83.CrossRefGoogle ScholarPubMed
Brisse, S., Barnabé, C. and Tibayrenc, M. (2000). Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. International Journal for Parasitology 30, 35–44.CrossRefGoogle ScholarPubMed
Burgos, J. M., Begher, S. B., Freitas, J. M., Bisio, M., Duffy, T., Altcheh, J., Teijeiro, R., Lopez Alcoba, H., Deccarlini, F., Freilij, H., Levin, M. J., Levalle, J., Macedo, A. M. and Schijman, A. G. (2005). Molecular diagnosis and typing of Trypanosoma cruzi populations and lineages in cerebral Chagas disease in a patient with AIDS. The American Journal of Tropical Medicine and Hygiene 73, 1016–1018.Google Scholar
Burgos, J. M., Altcheh, J., Bisio, M., Duffy, T., Valadares, H. M. S., Seidenstein, M. E., Piccinali, R., Freitas, J. M., Levin, M. J., Macchi, L., Macedo, A. M., Freilij, H. and Schijman, A. G. (2007). Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. International Journal for Parasitology 37, 1319–1327.Google Scholar
Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V. and Schountz, T. (2006). Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19, 531–545.CrossRefGoogle ScholarPubMed
Carcavallo, R. U., Girón, I. G., Jurberg, J. and Lent, H. (1999). Atlas of Chagas’ disease vectors in the Americas. Volume III. Editora Fiocruz, Rio de Janeiro, Brazil.Google Scholar
Cardinal, M. V., Lauricella, M. A., Ceballos, L. A., Lanati, L., Marcet, P. L., Levin, M. J., Kitron, U., Gürtler, R. E. and Schijman, A. G. (2008). Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina. International Journal for Parasitology 38, 1533–1543.CrossRefGoogle ScholarPubMed
Cavazzana, M., Marcili, A., Lima, L., da Silva, F. M., Junqueira, Â. C. V., Veludo, H. H., Viola, L. B., Campaner, M., Nunes, V. L. B., Paiva, F., Coura, J. R., Camargo, E. P. and Teixeira, M. M. G. (2010). Phylogeographical, ecological and biological patterns shown by nuclear (ssrRNA and gGAPDH) and mitochondrial (Cyt b) genes of trypanosomes of the subgenus Schizotrypanum parasitic in Brazilian bats. International Journal for Parasitology 40, 345–355.Google Scholar
Ceballos, L. A., Piccinali, R. V., Berkunsky, I., Kitron, U. and Gürtler, R. E. (2009). First finding of melanic sylvatic Triatoma infestans (Hemiptera: Reduviidae) colonies in the Argentine Chaco. Journal of Medical Entomology 46, 1195–202.Google Scholar
Cura, C. I., Lucero, R. H., Bisio, M., Oshiro, E., Formichelli, L. B., Burgos, J. M., Lejona, S., Brusés, B. L., Hernández, D. O., Severini, G. V., Velazquez, E., Duffy, T., Anchart, E., Lattes, R., Altcheh, J., Freilij, H., Diez, M., Nagel, C., Vigliano, C., Favaloro, L., Favaloro, R. R., Merino, D. E., Sosa-Estani, S. and Schijman, A. G. (2012). Trypanosoma cruzi discrete typing units in Chagas disease patients from endemic and non-endemic regions of Argentina. Parasitology 139, 516–521.Google Scholar
Damborsky, M. P., Bar, M. E. and Oscherov, E. B. (2001). Detección de triatominos (Hemiptera: Reduviidae) en ambientes domésticos y extradomésticos. Corrientes, Argentina. Cadernos de Saúde Pública 17, 843–849.CrossRefGoogle ScholarPubMed
Desquesnes, M., Holzmuller, P., Lai, D.-H., Dargantes, A., Lun, Z.-R. and Jittaplapong, S. (2013). Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects. BioMed Research International 2013, 194176.CrossRefGoogle Scholar
García, L., Ortiz, S., Osorio, G., Torrico, M. C., Torrico, F. and Solari, A. (2012). Phylogenetic analysis of Bolivian bat trypanosomes of the subgenus schizotrypanum based on cytochrome b sequence and minicircle analyses. PLoS ONE 7, 1–7.Google Scholar
Greenhall, A. M., Joermann, G. and Schmidt, U. (1983). Desmodus rotundus . Mammalian Species 202, 1–6.Google Scholar
Gürtler, R. E. and Cardinal, M. V. (2015). Reservoir host competence and the role of domestic and commensal hosts in the transmission of Trypanosoma cruzi . Acta Tropica 151, 32–50. doi:10.1016/j.actatropica.2015.05.029.CrossRefGoogle ScholarPubMed
Gürtler, R. E., Cecere, M. C., Lauricella, M. A., Cardinal, M. V., Kitron, U. and Cohen, J. E. (2007). Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134, 69–82.Google Scholar
Hamilton, P. B., Teixeira, M. M. G. and Stevens, J. R. (2012). The evolution of Trypanosoma cruzi: The “bat seeding” hypothesis. Trends in Parasitology 28, 136–141.CrossRefGoogle ScholarPubMed
Jansen, A. M., Xavier, S. C. C. and Roque, A. L. R. (2015). The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Tropica 151, 1–15. doi:10.1016/j.actatropica.2015.07.018.Google Scholar
Lima, V. D. S., das C. Xavier, S. C., Maldonado, I. F. R., Roque, A. L. R., Vicente, A. C. P. and Jansen, A. M. (2014). Expanding the knowledge of the geographic distribution of Trypanosoma cruzi TcII and TcV/TcVI genotypes in the Brazilian Amazon. PLoS ONE 9, e116137.Google Scholar
Lima, L., Espinosa-Álvarez, O., Ortiz, P. A., Trejo-Varón, J. A., Carranza, J. C., Pinto, C. M., Serrano, M. G., Buck, G. A., Camargo, E. P. and Teixeira, M. M. G. (2015). 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, 166–177.CrossRefGoogle ScholarPubMed
Lisboa, C. V., Mangia, R. H., Rubião, E., De Lima, N. R. C., Das Chagas Xavier, S. C., Picinatti, A., Ferreira, L. F., Fernandes, O. and Jansen, A. M. (2004). Trypanosoma cruzi transmission in a captive primate unit, Rio de Janeiro, Brazil. Acta Tropica 90, 97–106.Google Scholar
Lisboa, C. V., Pinho, A. P., Herrera, H. M., Gerhardt, M., Cupolillo, E. and Jansen, A. M. (2008). Trypanosoma cruzi (kinetoplastida, Trypanosomatidae) genotypes in neotropical bats in Brazil. Veterinary Parasitology 156, 314–318.Google Scholar
Lisboa, C. V., Monteiro, R. V., Martins, A. F., Xavier, S. C. D. C., Lima, V. D. S. and Jansen, A. M. (2015). Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp.): an 11-year follow-up. Memórias do Instituto Oswaldo Cruz 110, 394–402. doi:10.1590/0074-02760140400.CrossRefGoogle Scholar
Litvoc, J., Goldbaum, M. and da. Silva, G. R. (1990). Determinants of the process of domiciliary infestation by Panstrongylus megistus: the role of housing and deforesting. Revista do Instituto de Medicina Tropical de Säo Paulo 32, 443–449.Google ScholarPubMed
Lopes, R. A., Ribeiro, R. D., Carvalho, T. L., de Albuquerque, S. and Watanabe, I. S. (1991). Presence of amastigotes in the Weber's lingual salivary gland of Trypanosoma cruzi-infected mice. Brazilian Dental Journal 2, 75–79.Google Scholar
Luis, A. D., Hayman, D. T. S., O'Shea, T. J., Cryan, P. M., Gilbert, A. T., Pulliam, J. R. C., Mills, J. N., Timonin, M. E., Willis, C. K. R., Cunningham, A. a, Fooks, A. R., Rupprecht, C. E., Wood, J. L. N. and Webb, C. T. (2013). A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Biological Sciences/The Royal Society 280, 20122753.Google Scholar
Marcili, A., Lima, L., Cavazzana, M., Junqueira, a C. V., Veludo, H. H., Maia Da Silva, F., Campaner, M., Paiva, F., Nunes, V. L. B. and Teixeira, M. M. G. (2009 a). A new genotype of Trypanosoma cruzi associated with bats evidenced by phylogenetic analyses using SSU rDNA, cytochrome b and Histone H2B genes and genotyping based on ITS1 rDNA. Parasitology 136, 641–655.Google Scholar
Marcili, A., Valente, V. C., Valente, S. a., Junqueira, A. C. V., Da Silva, F. M., Pinto, A. Y. D. N., Naiff, R. D., Campaner, M., Coura, J. R., Camargo, E. P., Miles, M. a. and Teixeira, M. M. G. (2009 b). Trypanosoma cruzi in Brazilian Amazonia: lineages TCI and TCIIa in wild primates, Rhodnius spp. and in humans with Chagas disease associated with oral transmission. International Journal for Parasitology 39, 615–623.Google Scholar
Marsden, P. D. and Hagstrom, J. W. (1966). Trypanosoma cruzi in the saliva of beagle puppies. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 189–191.Google Scholar
Martínez-Díaz, R. A., Escario, J. A., Nogal-Ruiz, J. J. and Gómez-Barrio, A. (2001). Biological characterization of Trypanosoma cruzi strains. Memórias do Instituto Oswaldo Cruz 96, 53–59.Google Scholar
Miles, M. A., Souza, A. A. and Póvoa, M. M. (1981). Mammal tracking and nest location in Brazilian forest with an improved spool-and-line device. Journal of Zoology (London) 195, 331–347.Google Scholar
Miles, M. a, Llewellyn, M. S., Lewis, M. D., Yeo, M., Baleela, R., Fitzpatrick, S., Gaunt, M. W. and Mauricio, I. L. (2009). The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology 136, 1509–1528.Google Scholar
Molyneux, D. H., Ostfeld, R. S., Bernstein, A. and Chivian, E. (2008). Ecosystem disturbance, biodiversity loss, and human infectious disease. In Sustaining Life: How Human Health Depends on Biodiversity (ed. Chivian, E. and Bernstein, A.), pp 293–294. Oxford University Press, Oxford, UK.Google Scholar
Noireau, F., Diosque, P. and Jansen, A. M. (2009). Trypanosoma cruzi: adaptation to its vectors and its hosts. Veterinary Research 40, 26.Google Scholar
Orozco, M. M., Enriquez, G. F., Alvarado-Otegui, J. a., Cardinal, M. V., Schijman, A. G., Kitron, U. and Gürtler, R. E. (2013). New sylvatic hosts of Trypanosoma cruzi and their reservoir competence in the humid Chaco of Argentina: a longitudinal study. American Journal of Tropical Medicine and Hygiene 88, 872–882.Google Scholar
Orozco, M. M., Piccinali, R. V., Mora, M. S., Enriquez, G. F., Cardinal, M. V. and Gürtler, R. E. (2014). The role of sigmodontine rodents as sylvatic hosts of Trypanosoma cruzi in the Argentinean Chaco. Infection, Genetics and Evolution 22, 12–22.Google Scholar
PAHO (2012). Organización Panamericana de la Salud. IIa Reunión Sudamericana de Iniciativas Subregionales de Prevención, Control y Atención de la Enfermedad de Chagas. Conclusiones, recomendaciones y resoluciones. 1–6. Pan American Health Organization, Buenos Aires, Argentina.Google Scholar
Ramírez, J. D., Tapia-Calle, G., Muñoz-Cruz, G., Poveda, C., Rendón, L. M., Hincapié, E. and Guhl, F. (2014). Trypanosome species in neo-tropical bats: biological, evolutionary and epidemiological implications. Infection, Genetics and Evolution 22, 250–256.CrossRefGoogle ScholarPubMed
Rocha, F. L., Roque, A. L. R., Arrais, R. C., Santos, J. P., Lima, V. D. S., Xavier, S. C. D. C., Cordeir-Estrela, P., D'Andrea, P. S. and Jansen, A. M. (2012). Trypanosoma cruzi TcI and TcII transmission among wild carnivores, small mammals and dogs in a conservation unit and surrounding areas, Brazil. Parasitology 140, 1–11. doi:10.1017/S0031182012001539.Google Scholar
Rocha, F. L., Roque, A. L. R., de Lima, J. S., Cheida, C. C., Lemos, F. G., de Azevedo, F. C., Arrais, R. C., Bilac, D., Herrera, H. M., Mourão, G. and Jansen, A. M. (2013). Trypanosoma cruzi infection in Neotropical wild carnivores (Mammalia: Carnivora): at the top of the T. cruzi transmission chain. PLoS ONE 8, e67463. doi:10.1371/journal.pone.0067463.Google Scholar
Roellig, D. M. and Yabsley, M. J. (2010). Short report: infectivity, pathogenicity, and virulence of Trypanosoma cruzi isolates from sylvatic animals and vectors, and domestic dogs from the United States in ICR strain mice and SD strain rats. American Journal of Tropical Medicine and Hygiene 83, 519–522.Google Scholar
Santos, J. Jr, Viola, M., Lorosa, E., Machado, E., Ruas Neto, A. and Corseui, E. (2013). Evaluation of natural foci of Panstrongylus megistus in a forest fragment Porto Alegre, State of Rio Grande do Sul, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 46, 575–583.Google Scholar
Schijman, A. G., Lauricella, M. A., Marcet, P. L., Duffy, T., Cardinal, M. V., Bisio, M., Levin, M. J., Kitron, U. and Gürtler, R. E. (2006). Differential detection of Blastocrithidia triatomae and Trypanosoma cruzi by amplification of 24salpha ribosomal RNA genes in faeces of sylvatic triatomine species from rural northwestern Argentina. Acta Tropica 99, 50–54.Google Scholar
Schweigmann, N. J., Pietrokovsky, S., Bottazzi, V., Conti, O., Bujas, M. A. and Wisnivesky-Colli, C. (1999). Estudio de la prevalencia de la infección por Trypanosoma cruzi en zarigüeyas (Didelphis albiventris) en Santiago del Estero, Argentina. Revista Panamericana de Salud Pública 6, 371–377.CrossRefGoogle Scholar
Sergeant, E. (2015). Epitools epidemiological calculators. AusVet Animal Health Services and Australian Biosecurity Cooperative Research Centre for Emerging Infectious Disease. http://epitools.ausvet.com.au Google Scholar
Sun, J. and Tarleton, R. L. (1993). Predominance of CD8+ T lymphocytes in the inflammatory lesions of mice with acute Trypanosoma cruzi infection. The American Journal of Tropical Medicine and Hygiene 48, 161–169.Google Scholar
Tarleton, R. L., Gürtler, R. E., Urbina, J. a., Ramsey, J. and Viotti, R. (2014). Chagas disease and the London declaration on neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e3219.Google Scholar
Thomas, M. E., Rasweiler, J. J. IV and D'Alessandro, A. (2007). Experimental transmission of the parasitic flagellates Trypanosoma cruzi and Trypanosoma rangeli between triatomine bugs or mice and captive neotropical bats. Memorias do Instituto Oswaldo Cruz 102, 559–565.Google Scholar
Tibayrenc, M. (2009). Modelling the transmission of Trypanosoma cruzi: the need for an Integrated Genetic Epidemiological and Population Genomics Approach. In Genetics and Evolution of Infectious Diseases (ed. Edwin, M. and Spear, R. C.), pp. 200–211. Landes Bioscience and Springer Science+Business Media, Massachusets, USA.Google Scholar
Vaz, V. C., D'Andrea, P. S. and Jansen, a. M. (2007). Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi . Parasitology 134, 1785–1793.Google Scholar
Viglizzo, E. F., Frank, F. C. and Carreño, L. (2006). Ecorregiones Pampa y Campos y Malezales. In La Situación Ambiental Argentina 2005 (ed. Brown, A., Martinez Ortiz, U., Acerbi, M. and Corcuera, J.), pp. 261–278. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina.Google Scholar
West, G., Heard, D. and Caulkett, N. (2007). Zoo Animal and Wildlife: Immobilization and Anesthesia. Blackwell Pub Professional, Iowa, USA.Google Scholar
Yeo, M., Acosta, N., Llewellyn, M., Sánchez, H., Adamson, S., Miles, G. A. J., López, E., González, N., Patterson, J. S., Gaunt, M. W., Rojas De Arias, A. and Miles, M. a. (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.CrossRefGoogle ScholarPubMed
Zingales, B., Andrade, S. G., Briones, M. R. S., Campbell, D. A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, a. M., Machado, C. R., Miles, M. A., Romanha, A. J., Sturm, N. R., Tibayrenc, M. and Schijman, A. G. (2009). A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memorias do Instituto Oswaldo Cruz 104, 1051–1054.Google Scholar
Zingales, B., Miles, M. A., Campbell, D. A., Tibayrenc, M., Macedo, A. M., Teixeira, M. M. G., Schijman, A. G., Llewellyn, M. S., Lages-Silva, E., Machado, C. R., Andrade, S. G. and Sturm, N. R. (2012). The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infection, Genetics and Evolution 12, 240–253.Google Scholar
Supplementary material: File

Argibay supplementary material

Table S1

Download Argibay supplementary material(File)
File 32.8 KB