BACKGROUND: Leishmania infantum is the most widespread etiological agent of visceral leishmaniasis (VL) in the world, with significant mortality rates in human cases. In Latin America, this parasite is primarily transmitted by Lutzomyia longipalpis, but the role of Lutzomyia migonei as a potential vector for this protozoan has been discussed. Laboratory and field investigations have contributed to this hypothesis; however, proof of the vector competence of L. migonei has not yet been provided. In this study, we evaluate for the first time the susceptibility of L. migonei to L. infantum. METHODS: Females of laboratory-reared L. migonei were fed through a chick-skin membrane on rabbit blood containing L. infantum promastigotes, dissected at 1, 5 and 8 days post-infection (PI) and checked microscopically for the presence, intensity and localisation of Leishmania infections. In addition, morphometric analysis of L. infantum promastigotes was performed. RESULTS: High infection rates of both L. infantum strains tested were observed in L. migonei, with colonisation of the stomodeal valve already on day 5 PI. At the late-stage infection, most L. migonei females had their cardia and stomodeal valve colonised by high numbers of parasites, and no significant differences were found compared to the development in L. longipalpis. Metacyclic forms were found in all parasite-vector combinations since day 5 PI. CONCLUSIONS: We propose that Lutzomyia migonei belongs to sand fly species permissive to various Leishmania spp. Here we demonstrate that L. migonei is highly susceptible to the development of L. infantum. This, together with its known anthropophily, abundance in VL foci and natural infection by L. infantum, constitute important evidence that L. migonei is another vector of this parasite in Latin America.

Department of Immunology Centro de Pesquisas Aggeu Magalhães Fundação Oswaldo Cruz Recife Pernambuco Brazil

Department of Parasitology Faculty of Science Charles University Prague Czech Republic

See more in PubMed

Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol. 2013;27:127–47. doi: 10.1111/j.1365-2915.2012.01034.x. PubMed DOI

Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7:e3567. doi: 10.1371/journal.pone.0035671. PubMed DOI PMC

Romero GA, Boelaert M. Control of visceral leishmaniasis in Latin America - a systematic review. PLoS Negl Trop Dis. 2010;4:e584. doi: 10.1371/journal.pntd.0000584. PubMed DOI PMC

Lainson R, Rangel EF. Lutzomyialongipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Mem Inst Oswaldo Cruz. 2005;100:811–27. doi: 10.1590/S0074-02762005000800001. PubMed DOI

Killick-Kendrick R. Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 1990;4:1–24. doi: 10.1111/j.1365-2915.1990.tb00255.x. PubMed DOI

Souza MB, Marzochi MC, Carvalho RW, Ribeiro PC, Pontes CS, Caetano JM, et al. Ausência de Lutzomyia longipalpis em algumas áreas de ocorrência de leishmaniose visceral no município do Rio de Janeiro. Cad Saude Publica. 2003;19:109–18. PubMed

Carvalho MR, Lima BS, Marinho-Júnior JF, Silva FJ, Valença HF, Almeida FA, et al. Phlebotomine sandfly species from an American visceral leishmaniasis area in the Northern Rainforest Region of Pernambuco State. Brazil Cad Saude Publica. 2007;23:1227–32. doi: 10.1590/S0102-311X2007000500024. PubMed DOI

Carvalho MR, Valença HF, Silva FJ, Pita-Pereira D, Araújo Pereira T, Britto C, et al. Natural Leishmania infantum infection in Migonemyia migonei (Franca, 1920) (Diptera: Psychodidae: Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco State, Brazil. Acta Trop. 2010;116:108–10. doi: 10.1016/j.actatropica.2010.03.009. PubMed DOI

Salomon OD, Quintana MG, Bezzi G, Morán ML, Betbeder E, Valdéz DV. Lutzomyia migonei as putative vector of visceral leishmaniasis in La Banda, Argentina. Acta Trop. 2010;113:84–7. doi: 10.1016/j.actatropica.2009.08.024. PubMed DOI

Moya SL, Giuliani MG, Manteca MA, Salomón OD, Liotta DJ. First description of Migonemyia migonei (França) and Nyssomyia whitmani (Antunes & Coutinho) (Psychodidae: Phlebotominae) natural infected by Leishmania infantum in Argentina. Acta Trop. 2015;152:181–4. PubMed

Rangel EF, Lainson R. Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz. 2009;104:937–54. doi: 10.1590/S0074-02762009000700001. PubMed DOI

Guimarães VCFV, Costa PL, Silva FJ, Silva KT, Silva KG, Araújo AI, et al. Phlebotomine sand flies (Diptera: Psychodidae) in São Vicente Férrer, a sympatric area to cutaneous and visceral leishmaniasis in Pernambuco, Brazil. Rev Soc Bras Med Trop. 2012;45:66–70. doi: 10.1590/S0037-86822012000100013. PubMed DOI

Aguiar GM, Vilela ML, Lima RB. Ecology of the sandflies of Itaguai, an area of cutaneous leishmaniasis in State of Rio de Janeiro. Food preferences (Diptera, Psychodidae, Phlebotominae) Mem Inst Oswaldo Cruz. 1987;82:583–4. doi: 10.1590/S0074-02761987000400020. PubMed DOI

Carvalho BM, Maximo M, Costa WA, Santana AL, Costa SM, Costa Rego TA, et al. Leishmaniasis transmission in an ecotourism area: potential vectors in Ilha Grande, Rio de Janeiro State, Brazil. Parasit Vectors. 2013;6:325. doi: 10.1186/1756-3305-6-325. PubMed DOI PMC

Guimarães VCFV, Costa PL, Silva FJ, Melo FL, Dantas-Torres F, Rodrigues EH, et al. Molecular detection of Leishmania in phlebotomine sand flies in a cutaneous and visceral leishmaniasis endemic area in northeastern Brazil. Rev Inst Med Trop Sao Paulo. 2014;56:357–60. doi: 10.1590/S0036-46652014000400015. PubMed DOI PMC

Maia C, Seblova V, Sadlova J, Votypka J, Volf P. Experimental transmission of Leishmania infantum by two major vectors: a comparison between a viscerotropic and a dermotropic strain. PLoS Negl Trop Dis. 2011;5:e1181. doi: 10.1371/journal.pntd.0001181. PubMed DOI PMC

Sadlova J, Dvorak V, Seblova V, Warburg A, Votypka J, Volf P. Sergentomyia schwetzi is not a competent vector for Leishmania donovani and other Leishmania species pathogenic to humans. Parasit Vectors. 2013;6:186. doi: 10.1186/1756-3305-6-186. PubMed DOI PMC

Seblova V, Myskova J, Hlavacova J, Votypka J, Antoniou M, Volf P. Natural hybrid of Leishmania infantum/L.donovani: development in Phlebotomus tobbi, P. perniciosus and Lutzomyia longipalpis and comparison with nonhybrid strains differing in tissue tropism. Parasit Vectors. 2015;8:605. doi: 10.1186/s13071-015-1217-3. PubMed DOI PMC

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36(Suppl 1):S1–9. doi: 10.1111/j.1948-7134.2011.00106.x. PubMed DOI

Noyes H, Chance M, Ponce C, Ponce E, Maingon R. Leishmania chagasi: Genotypically similar parasites from Honduras cause both visceral and cutaneous leishmaniasis in humans. Exp Parasitol. 1997;85:264–73. doi: 10.1006/expr.1996.4133. PubMed DOI

Svobodova M, Alten B, Zidkova L, Dvorak V, Hlavackova J, Myskova J, et al. Cutaneous leishmaniasis caused by Leishmania infantum transmitted by Phlebotomus tobbi. Int J Parasitol. 2009;39:251–56. doi: 10.1016/j.ijpara.2008.06.016. PubMed DOI

Myskova J, Votypka J, Volf P. Leishmania in sand flies: Comparison of quantitative polymerase chain reaction with other techniques to determine the intensity of infection. J Med Entomol. 2008;45:133–8. doi: 10.1093/jmedent/45.1.133. PubMed DOI

Walters LL. Leishmania differentiation in natural and unnatural sand fly hosts. J Eukaryot Microbiol. 1993;40:196–206. doi: 10.1111/j.1550-7408.1993.tb04904.x. PubMed DOI

Cihakova J, Volf P. Development of different Leishmania major strains in the vector sandflies Phlebotomus papatasi and P. duboscqi. Ann Trop Med Parasitol. 1997;91:267–79. doi: 10.1080/00034989761120. PubMed DOI

Lainson R, Shaw JJ. Observations on the development of Leishmania (L.) chagasi Cunha and Chagas in the midgut of the sandfly vector Lutzomyia longipalpis (Lutz and Neiva) Ann Parasitol Hum Comp. 1988;63:134–45. PubMed

Rogers ME, Bates PA. Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog. 2007;3:e91. doi: 10.1371/journal.ppat.0030091. PubMed DOI PMC

Kamhawi S. Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol. 2006;22:439–445. doi: 10.1016/j.pt.2006.06.012. PubMed DOI

Dostalova A, Volf P. Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5:276. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC

Elnaiem DA, Ward RD, Young PE. Development of Leishmania chagasi (Kinetoplastida: Trypanosomatidae) in the second blood-meal of its vector Lutzomyia longipalpis (Diptera: Psychodidae) Parasitol Res. 1994;80:414–9. doi: 10.1007/BF00932379. PubMed DOI

Freitas VC, Parreiras KP, Duarte AP, Secundino NF, Pimenta PF. Development of Leishmania (Leishmania) infantum chagasi in its natural sandfly vector Lutzomyialongipalpis. Am J Trop Med Hyg. 2012;86:606–12. doi: 10.4269/ajtmh.2012.11-0386. PubMed DOI PMC

Volf P, Myskova J. Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol. 2007;23:91–92. doi: 10.1016/j.pt.2006.12.010. PubMed DOI PMC

Nieves E, Pimenta PF. Development of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae) J Med Entomol. 2000;37:134–40. doi: 10.1603/0022-2585-37.1.134. PubMed DOI

Stability and suitability of housekeeping genes in phlebotomine sand flies

Porcisia transmission by prediuresis of sand flies

Examination of the interior of sand fly (Diptera: Psychodidae) abdomen reveals novel cuticular structures involved in pheromone release: Discovering the manifold

Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)

Development of Leishmania (Mundinia) in guinea pigs

Experimental infections and co-infections with Leishmania braziliensis and Leishmania infantum in two sand fly species, Lutzomyia migonei and Lutzomyia longipalpis

Lipophosphoglycan polymorphisms do not affect Leishmania amazonensis development in the permissive vectors Lutzomyia migonei and Lutzomyia longipalpis