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Assessment of the role of small mammals in the transmission cycle of tegumentary leishmaniasis and first report of natural infection with Leishmania braziliensis in two sigmodontines in northeastern Argentina

Abstract

To contribute to the knowledge of the role of small mammals in the transmission cycle of tegumentary leishmaniasis caused by Leishmania braziliensis, we studied the small mammal community and its temporal and spatial association with phlebotominae, as well as small mammal infection by Leishmania spp. by PCR-RFLP analyses in an endemic area of northeastern Argentina. Ten small mammal samplings were conducted (2007–2009, 7506 Sherman trap nights and 422 cage trap nights). In two of these samplings, 16 capture stations each one consisting of a CDC light trap to capture phlebotominae, two to four Sherman traps and two cage traps were placed. We found co-occurrence of phlebotominae and small mammal captures in four stations, which were all the stations with small mammal captures and yielded 97% (2295 specimens, including 21 gravid females) of the total phlebotominae captures, suggesting that small mammals may provide a potential source of blood for phlebotominae females. One Didelphis albiventris and two Rattus rattus were associated with high captures of Nyssomyia whitmani, vector of L. braziliensis in the study area. The PCR-RFLP analyses confirm the presence of L. braziliensis in two sigmodontine small mammals (Akodon sp. and Euryoryzomys russatus) for the first time in Argentina, to our knowledge.

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References

  1. Acardi SA, Liotta DJ, Santini MS, Romagosa CM, Salomón OD (2010) Detection of Leishmania infantum in naturally infected Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) and Canis familiaris in Misiones, Argentina: the first report of a PCR-RFLP and sequencing-based confirmation assay. Mem Inst Oswaldo Cruz 105(6):796–799. https://doi.org/10.1590/S0074-02762010000600011

  2. Acardi SA, Rago MV, Liotta DJ, Fernandez-Duque E, Salomón OD (2013) Leishmania (Viannia) DNA detection by PCR-RFLP and sequencing in free-ranging owl monkeys (Aotus azarai azarai) from Formosa, Argentina. Vet Parasitol 193(1-3):256–259. https://doi.org/10.1016/j.vetpar.2012.12.012

  3. Andrade MS, Courtenay O, Brito MEF, Carvalho FG, Carvalho AWS, Soares F, Carvalho SM, Costa Pietra L, Zampieri R, Floeter-Winter LM, Shaw JJ, Brandão-Filho SP (2015) Infectiousness of sylvatic and synanthropic small rodents implicates a multi-host reservoir of Leishmania (Viannia) braziliensis. PLoS Negl Trop Dis 9(10):e0004137. https://doi.org/10.1371/journal.pntd.0004137

  4. Chaves LF, Hernandez MJ, Dobson AP, Pascual M (2007) Sources and sinks: revisiting the criteria for identifying reservoirs for American cutaneous leishmaniasis. Trends Parasitol 23(7):311–316. https://doi.org/10.1016/j.pt.2007.05.003

  5. Cutolo AA, Teodoro AKM, Ovallos FG, Allegretti S, Galati EA (2014) Sandflies (Diptera: Psychodidae) associated with opossum nests at urban sites in southeastern Brazil: a risk factor for urban and periurban zoonotic Leishmania transmission? Mem Inst Oswaldo Cruz 109(3):391–393. https://doi.org/10.1590/0074-0276130511

  6. De Lima H, De Guglielmo Z, Rodriguez A, Convit J, Rodriguez N (2002) Cotton rats (Sigmodon hispidus) and black rats (Rattus rattus) as possible reservoirs of Leishmania spp. in Lara state, Venezuela. Mem Inst Oswaldo Cruz 97(2):169–174. https://doi.org/10.1590/S0074-02762002000200004

  7. Fernández MS, Lestani EA, Cavia R, Salomón OD (2012) Phlebotominae Fauna in a recent deforested area with American tegumentary leishmaniasis transmission (Puerto Iguazú, Misiones, Argentina): seasonal distribution in domestic and peridomestic environments. Acta Trop 122(1):16–23. https://doi.org/10.1016/j.actatropica.2011.11.006

  8. Ferreira EC, Cruz I, Cañavate C, de Melo LA, Pereira AAS, Madeira FAM, Valério SAN, Cunha HM, Paglia AP, Gontijo CMF (2015) Mixed infection of Leishmania infantum and Leishmania braziliensis in rodents from endemic urban area of the New World. BMC Vet Res 11(1):71. https://doi.org/10.1186/s12917-015-0392-y

  9. Fonteles RS, Vasconcelos GC, Azevedo PCB, Lopes GN, Moraes JLP, Lorosa ES, Kuppinger O, Rebelo JMM (2009) Preferencia alimentar sanguinea de Lutzomyia whitmani (Diptera, Psychodidae) em area de transmissao de leishmaniose cutanea americana, no Estado do Maranhao, Brasil. Rev Soc Bras Med Trop 42(6):647–650. https://doi.org/10.1590/S0037-86822009000600007

  10. Galati E (2003) Classificação de Phlebotominae. In: Rangel E, Lainson R (eds) Flebotomíneos do Brasil. Fiocruz, Rio do Janeiro, pp 23–51

  11. Geise L, Astua D, Sebastiao H (2005) Morphometric differentiation and distributional notes of three species of Akodon (Muridae, Sigmodontinae, Akodontini) in the Atlantic coastal area of Brazil. Arq Mus Nac 63:63–74

  12. Grimaldi G, Tesh RB (1993) Leishmaniases of the New World: current concepts and implications for future research. Clin Microbiol Rev 6(3):230–250. https://doi.org/10.1128/CMR.6.3.230

  13. Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Brandão Filho SP, Volf P (2016) Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasit Vectors 9:1

  14. Haydon DT, Cleaveland S, Taylor LH, Laurenson K (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis 3:1468–1472

  15. Marfurt J, Niederwieser I, Makia ND, Beck HP, Felger I (2003) Diagnostic genotyping of Old and New World Leishmania species by PCR-RFLP. Diagn Microbiol Infect Dis 46(2):115–124. https://doi.org/10.1016/S0732-8893(03)00040-3

  16. Martínez-Crovetto R (1963) Esquema fitogeográfico de la provincia de Misiones (República Argentina). Bonplandia 1:171–223

  17. Montalvo AM, Fraga J, Maes I, Dujardin JC, Van der Auwera G (2012) Three new sensitive and specific heat-shock protein 70 PCRs for global Leishmania species identification. Eur J Clin Microbiol Infect Dis 31(7):1453–1461. https://doi.org/10.1007/s10096-011-1463-z

  18. Moya SL, Giuliani MG, Manteca-Acosta M, Salomón OD, Liotta DJ (2015) First description of Migonemyia migonei (França) and Nyssomyia whitmani (Antunes & Coutinho) (Psychodidae: Phlebotominae) natural infected by Leishmania infantum in Argentina. Acta Trop 152:181–184. https://doi.org/10.1016/j.actatropica.2015.09.015

  19. Nuñez AC (2009) Las “DOSMIL”. Crónicas de una ciudadanía mediada por el conflicto: el territorio en disputa. Análisis de un caso sobre ocupación de tierras fiscales en el municipio de Puerto Iguazú, Misiones. [Tesis de grado]. Universidad Nacional de Misiones-Argentina

  20. Padula P, Martinez VP, Bellomo C, Maidana S, San Juan J, Tagliaferri P, Bargardi S, Vazquez C, Colucci N, Estévez J, Almiron M (2007) Pathogenic hantaviruses, northeastern Argentina and eastern Paraguay. Emerg Infect Dis 13(8):1211–1214. https://doi.org/10.3201/eid1308.061090

  21. Ready PD (2008) Leishmaniasis emergence and climate change. Rev sci tech Off int Epiz 27(2):399–412. https://doi.org/10.20506/rst.27.2.1803

  22. Rodriguez AF, Silva M (2012) Ecorregión Selva Paranaense. In: Ecorregiones y complejos ecosistémicos de Argentina. Orientación Gráfica Editora, 1ª ed, pp 225–245

  23. Roque ALR, Jansen AM (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl 3(3):251–262. https://doi.org/10.1016/j.ijppaw.2014.08.004

  24. Rusman F (2016) Evaluación de un ensayo de alta sensibilidad y especificidad para la detección de Leishmania sp. por Reacción en Cadena de la Polimerasa (PCR-RFLP) [Tesis de grado]. Universidad Nacional de Misiones-Argentina

  25. Salomón OD, Acardi SA, Liotta DJ, Fernández MS, Lestani E, López D, Mastrángelo AV, Figueroa M, Fattore G (2009) Epidemiological aspects of cutaneous leishmaniasis in the Iguazú falls area of Argentina. Acta Trop 109(1):5–11. https://doi.org/10.1016/j.actatropica.2008.08.002

  26. Salomón OD, Mastrángelo AV, Santini MS, Liotta DJ, Yadón ZE (2016) Retrospective eco-epidemiology as a tool for the surveillance of leishmaniasis in Misiones, Argentina, 1920–2014. Rev Panam Salud Pública 40(1):29–39

  27. Salomón OD, Quintana MG, Rosa JR (2008) Eco-epidemiologia de leishmaniasis cutánea en Argentina. Soc Iberoam Inf Científica (SIICSALUD) 16:514–520

  28. Salomón OD, Sosa-Estani S, Monzani AS, Studer C (2001) Brote epidémico de leishmaniosis tegumentaria en Puerto Esperanza, provincia de Misiones, 1998. Med (Buenos Aires) 61:385–390

  29. Vanasco NB, Sequeira MD, Sequeira G, Tarabla HD (2003) Associations between leptospiral infection and seropositivity in rodents and environmental characteristics in Argentina. Prev Vet Med 60(3):227–235. https://doi.org/10.1016/S0167-5877(03)00144-2

  30. WHO (2010) Control of the Leishmaniasis. Report of the meeting of the WHO experts committee on the control of Leishmaniasis, Geneva. WHO Technical report series 99

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Acknowledgements

We are grateful to the community involved in this study, to the local authorities, to the personnel of Parque Nacional Iguazú, and to the personnel of Ejército Argentino for providing support to carry out the study. A special thanks to Pablo Teta, David Flores, and Sergio Lucero from the Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” for their support with the systematic determination of rodents and marsupials, and to Victoria Vadell for his contribution in the fieldwork. Finally, we very much appreciate the logistic help from Fundación Mundo Sano throughout all the period of the study.

Funding

This research was supported by grants from the “Consejo Nacional de Investigaciones Científicas y Técnicas” and “Fundación Mundo Sano.”

Author information

Correspondence to María S. Fernández.

Ethics declarations

Individuals were humanely sacrificed following the procedures and protocols approved by the Argentine Law for Animal Care 14346 and Ethics Committee for Research on Laboratory Animals, Farm and Obtained from Natures of National Council of Science and Technical Research (CONICET; resolution 1047, section 2, annex II).

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Fernández, M.S., Fraschina, J., Acardi, S. et al. Assessment of the role of small mammals in the transmission cycle of tegumentary leishmaniasis and first report of natural infection with Leishmania braziliensis in two sigmodontines in northeastern Argentina. Parasitol Res 117, 405–412 (2018). https://doi.org/10.1007/s00436-017-5714-5

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Keywords

  • Small mammals
  • Nyssomyia whitmani
  • Co-occurrence
  • Leishmania braziliensis infection