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Mixed infection in the anteater Tamandua tetradactyla (Mammalia: Pilosa) from Pará State, Brazil: Trypanosoma cruzi, T. rangeli and Leishmania infantum

Published online by Cambridge University Press:  20 December 2012

VITOR ANTÔNIO L. DE ARAÚJO ,
MARIANA C. BOITÉ ,
ELISA CUPOLILLO ,
ANA MARIA JANSEN  and
ANDRÉ LUIZ R. ROQUE
VITOR ANTÔNIO L. DE ARAÚJO
Affiliation:
Laboratory of Trypanosomatid Biology, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil
MARIANA C. BOITÉ
Affiliation:
Laboratory of Leishmaniasis Research, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil
ELISA CUPOLILLO
Affiliation:
Laboratory of Leishmaniasis Research, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil
ANA MARIA JANSEN
Affiliation:
Laboratory of Trypanosomatid Biology, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil
ANDRÉ LUIZ R. ROQUE*
Affiliation:
Laboratory of Trypanosomatid Biology, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil
*
*Corresponding author: Laboratory of Trypanosomatid Biology, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil 4365, Zip Code 21040-360, Rio de Janeiro/RJ, Brazil. Tel: +55 21 2562 1416. Fax: +55 21 2562 1609. E-mail: roque@ioc.fiocruz.br
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Summary

Some Trypanosoma and Leishmania species are multi-host parasites whose distribution overlaps in several parts of the Brazilian Amazon basin. Despite being a common trait among wild mammals, mixed infections and their consequences for the host's health and parasite transmission are still a poorly known phenomenon. Here we describe a triple mixed infection – Trypanosoma cruzi, T. rangeli and Leishmania infantum – in a bone marrow sample from an anteater Tamandua tetradactyla captured in a house backyard from the endemic Abaetetuba municipality in the Amazon basin. T. cruzi was also isolated from blood samples. The mini-exon multiplex PCR characterization detected the infection by T. rangeli and T. cruzi (TcI genotype), while L. infantum infection was confirmed by an ITS-PCR followed by amplicon sequencing. This is the first description of T. rangeli isolation from bone marrow and the first report of L. infantum infection in xenarthrans. The implications of this finding are discussed considering the influence of mixed infections in the role of this mammal species as a putative reservoir host of these 3 trypanosomatid species.

Keywords

Tamandua tetradactylaTrypanosoma cruziTrypanosoma rangeliLeishmania infantumbone marrowreservoirs
Type
Research Article
Information
Parasitology , Volume 140 , Issue 4 , April 2013 , pp. 455 - 460
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.) S23–S38.CrossRefGoogle ScholarPubMed
Deane, L. M. and Damasceno, R. G. (1961). Trypanosomidae from mammals of the Amazon region. II. Trypanosomas from Macacas of the Salgado Zone state of Pará. Revista do Instituto de Medicina Tropical de São Paulo 3, 61–70.Google ScholarPubMed
Degrave, W., Fernandes, O., Thiemann, O., Wincker, P., Britto, C., Cardoso, A., Pereira, J. B., Bozza, M., Lopes, U. and Morel, C. (1994). Detection of Trypanosoma cruzi and Leishmania using the polymerase chain reaction. Memórias do Instituto Oswaldo Cruz 89, 367–368. doi: 10.1590/S0074-02761994000300013.CrossRefGoogle ScholarPubMed
Dias, F. B., Quartier, M., Romaña, C. A., Diotaiuti, L. and Harry, M. (2010). Tamandua tetradactyla Linnaeus, 1758 (Myrmecophagidae) and Rhodnius robustus Larrousse, 1927 (Triatominae) infection focus by Trypanosoma rangeli Tejera, 1920 (Trypanosomatidae) in Attalea phalerata Mart. ex Spreng (Arecaceae) palm tree in the Brazilian Amazon. Infection, Genetics and Evolution 10, 1278–1281. doi: 10.1016/j.meegid.2010.06.020.CrossRefGoogle ScholarPubMed
Eger-Mangrich, I., de Oliveira, M. A., Grisard, E. C., de Souza, W. and Steindel, M. (2001). Interaction of Trypanosoma rangeli Tejera, 1920 with different cell lines in vitro. Parasitology Research 87, 505–509. doi: 10.1007/s004360000356.CrossRefGoogle ScholarPubMed
Ferguson, M. A. (1997). The surface glycoconjugates of trypanosomatid parasites. Philosophical Transactions of the Royal Society of London, B 352, 1295–1302.CrossRefGoogle ScholarPubMed
Fernandes, O., Santos, S. S., Cupolillo, E., Mendonca, B., Derre, R., Junqueira, A. C., Santos, L. C., Sturm, N. R., Naiff, R. D., Barret, T. V., Campbell, D. A. and Coura, J. R. (2001). A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T. rangeli in the Brazilian Amazon. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 97–99.CrossRefGoogle Scholar
Gadelha, C., Holden, J. M., Allison, H. C. and Field, M. C. (2011). Specializations in a successful parasite: what makes the bloodstream-form African trypanosome so deadly? Molecular and Biochemical Parasitology 179, 51–58. doi: 10.1016/j.molbiopara.2011.06.006.CrossRefGoogle Scholar
Gramiccia, M. and Gradoni, L. (2005). The current status of zoonotic leishmaniases and approaches to disease control. International Journal for Parasitology 35, 1169–1180. doi: 10.1016/j.ijpara.2005.07.001.CrossRefGoogle ScholarPubMed
Guhl, F. and Vallejo, G. A. (2003). Trypanosoma (Herpetosoma) rangeli Tejera, 1920: an updated review. Memórias do Instituto Oswaldo Cruz 98, 435–442. doi: 10.1590/S0074-02762003000400001.CrossRefGoogle ScholarPubMed
Hayssen, V. (2011). Tamandua tetradactyla (Pilosa: Myrmecophagidae). Mammal Species 43, 64–74.CrossRefGoogle Scholar
Lainson, R. and Rangel, E. F. (2005). Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Memórias do Instituto Oswaldo Cruz 100, 811–827. doi: 10.1590/S0074-02762005000800001.CrossRefGoogle ScholarPubMed
Lainson, R., Shaw, J. J. and Povoa, M. (1981). The importance of edentates (sloths and anteaters) as primary reservoirs of Leishmania braziliensis guyanensis, causative agent of “pianbois” in north Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 611–612.CrossRefGoogle Scholar
de Lima, H., Rodríguez, N., Barrios, M. A., Avila, A., Cañizales, I. and Gutiérrez, S. (2008). Isolation and molecular identification of Leishmania chagasi from a bat (Carollia perspicillata) in northeastern Venezuela. Memórias do Instituto Oswaldo Cruz 103, 412–414. doi: 10.1590/S0074-02762008000400018.CrossRefGoogle ScholarPubMed
Maslov, D. A., Podlipaev, S. A. and Lukes, J. (2001). Phylogeny of the kinetoplastida: taxonomic problems and insights into the evolution of parasitism. Memórias do Instituto Oswaldo Cruz 96, 397–402. doi: 10.1590/S0074-02762001000300021.CrossRefGoogle ScholarPubMed
Medri, M., Mourão, G. M. and Rodrigues, F. (2006). Ordem Xenarthra. In Mamíferos do Brasil (ed. Reis, N. R., Perachi, A. L., Petro, W. A. and Lima, I. P.), pp. 71–99. Universidade Estadual de Londrina, Londrina, Brazil.Google Scholar
Miles, M. A., Arias, J. R., Valente, S. A., Naiff, R. D., de Souza, A. A., Povoa, M. M., Lima, J. A. and Cedillos, R. A. (1983). Vertebrate hosts and vectors of Trypanosoma rangeli in the Amazon Basin of Brazil. American Journal of Tropical Medicine and Hygiene 32, 1251–1259.CrossRefGoogle ScholarPubMed
Mimori, T., Grimaldi, G. Jr., Kreutzer, R. D., Gomez, E. A., McMahon-Pratt, D., Tesh, R. B. and Hashiguchi, Y. (1989). Identification, using isoenzyme electrophoresis and monoclonal antibodies, of Leishmania isolated from humans and wild animals of Ecuador. American Journal of Tropical Medicine and Hygiene 40, 154–158.CrossRefGoogle ScholarPubMed
Noireau, F., Diosque, P. and Jansen, A. M. (2009). Trypanosoma cruzi: adaptation to its vectors and its hosts. Veterinary Research 40, 26. doi: 10.1051/vetres/2009009.CrossRefGoogle ScholarPubMed
Quinnell, R. J. and Courtenay, O. (2009). Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology 136, 1915–1934. doi: 10.1017/S0031182009991156.CrossRefGoogle ScholarPubMed
Rodrigues, B. A. and Melo, G. B. (1942). Contribuição ao estudo da tripanossomíase americana. Memórias do Instituto Oswaldo Cruz 37, 77–90.CrossRefGoogle Scholar
Roque, A. L. R., Cupolillo, E., Marchevsky, R. S. and Jansen, A. M. (2010). Thrichomys laurentius (Rodentia; Echimyidae) as a putative reservoir of Leishmania infantum and L. braziliensis: patterns of experimental infection. PLoS Neglected Tropical Diseases 4, e589. doi: 10.1371/journal.pntd.0000589.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, USA.Google Scholar
el Tai, N. O., Osman, O. F., el Fari, M., Presber, W. and Schönian, G. (2000). Genetic heterogeneity of ribosomal internal transcribed spacer in clinical samples of Leishmania donovani spotted on filter paper as revealed by single-strand conformation polymorphisms and sequencing. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 575–579.CrossRefGoogle ScholarPubMed
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243–246. doi: 10.1126/science.1190333.CrossRefGoogle Scholar
Yeo, M., Acosta, N., Llewellyn, M., Sánchez, H., Adamson, S., Miles, G. A., López, E., González, N., Patterson, J. S., Gaunt, M. W., de Arias, A. R. 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. doi: 10.1016/j.ijpara.2004.10.024.CrossRefGoogle ScholarPubMed
Zingales, B., Andrade, S. G., Briones, M. R., 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. Memórias do Instituto Oswaldo Cruz 104, 1051–1054.CrossRefGoogle ScholarPubMed