Experimental infection and transmission of Leishmania by Lutzomyia cruzi (Diptera: Psychodidae): Aspects of the ecology of parasite-vector interactions.

Everton Falcão de Oliveira,Wagner de Souza Fernandes,Márcio José de Medeiros,Alda Izabel Souza,Eunice Aparecida Bianchi Galati,Elisa Teruya Oshiro,Alessandra Gutierrez de Oliveira,Paula Guerra Murat,Paulo Filemon Pimenta

doi:10.1371/journal.pntd.0005401

Abstract

Several parameters should be addressed before incriminating a vector for Leishmania transmission. Those may include its ability to become infected by the same Leishmania species found in humans, the degree of attractiveness for reservoirs and humans and capacity to sustain parasite infection under laboratory conditions. This study evaluated the vectorial capacity of Lutzomyia cruzi for Leishmania infantum and gathered information on its ability to harbor L. amazonensis. Laboratory-reared Lu. cruzi were infected experimentally by feeding them on dogs infected naturally with L. infantum and hamsters infected with L. amazonensis. Sand fly attractiveness to dogs and humans was determined using wild caught insects. The expected daily survival of infected Lu. cruzi, the duration of the gonotrophic cycle, and the extrinsic incubation period were also investigated for both parasites. Vector competence was investigated for both Leishmania species. The mean proportion of female sand flies that fed on hosts was 0.40. For L. infantum and L. amazonensis, Lu. cruzi had experimental infection rates of 10.55% and 41.56%, respectively. The extrinsic incubation period was 3 days for both Leishmania species, regardless of the host. Survival expectancy of females infected with L. infantum and L. amazonensis after completing the gonotrophic cycle was 1.32 and 0.43, respectively. There was no association between L. infantum infection and sand fly longevity, but L. amazonensis–infected flies had significantly greater survival probabilities. Furthermore, egg-laying was significantly detrimental to survival. Lu. cruzi was found to be highly attracted to both dogs and humans. After a bloodmeal on experimentally infected hosts, both parasites were able to survive and develop late-stage infections in Lu. cruzi. However, transmission was demonstrated only for L. amazonensis–infected sand flies. In conclusion, Lu. cruzi fulfilled several of the requirements of vectorial capacity for L. infantum transmission. Moreover, it was also permissive to L. amazonensis.

Highlights

The parasite Leishmania infantum, the causative agent of visceral leishmaniasis (VL), is commonly transmitted by Lutzomyia longipalpis, which is widely distributed in Latin America [1,2]
The sand fly Lutzomyia longipalpis, which belongs to a species complex, had been solely incriminated in Latin American transmission of Leishmania infantum
Lutzomyia cruzi has been suspected of transmitting L. infantum in Corumbaand vicinity, and this study aimed to provide more accurate evidence of this phenomenon

Summary

Introduction

The parasite Leishmania infantum, the causative agent of visceral leishmaniasis (VL), is commonly transmitted by Lutzomyia longipalpis, which is widely distributed in Latin America [1,2]. The designation of a sand fly species as a vector of Leishmania must meet the criteria initially proposed by Killick-Kendrick [10], namely: (i) the existence of a substantial relationship with reservoirs and humans (demonstrating that the sand fly is anthropophilic and commonly feeds on the reservoir host(s)); (ii) the repeated isolation and identification, from female sand flies that have not recently fed, of the same species of Leishmania as is found in human cases of leishmaniasis; (iii) the presence of the sand fly in places where Leishmania and the disease it causes are found; (iv) the density and rate of natural infection by Leishmania; (v) the development of late-stage infections in specimens experimentally infected in the laboratory; and (vi). Mathematical modeling has recently been employed to demonstrate how vector abundance influences the incidence of the disease [11]

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