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

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.

Author summary

Leishmaniasis is a vector-borne disease caused by the Leishmania parasite. It is transmitted by phlebotomine sand flies when infected females take a bloodmeal from a mammalian host. The transmission of Leishmania species involves complex ecological interactions between parasite–vector and vector–host. Until recently, the sand fly Lutzomyia longipalpis, which belongs to a species complex, had been solely incriminated in Latin American transmission of Leishmania infantum. However, there are still uncertainties concerning the L. infantum transmission, especially in an urban area endemic for visceral leishmaniasis in Brazil. Along the years, Lutzomyia cruzi has been suspected of transmitting L. infantum in Corumbá and vicinity, and this study aimed to provide more accurate evidence of this phenomenon. Laboratory-reared Lu. cruzi were infected experimentally by allowing them to feed on dogs naturally infected with L. infantum and on hamsters infected with L. amazonensis. Our results identified important life cycle parameters of Lu. cruzi infected by Leishmania in laboratory conditions. We identified the components related to vectorial capacity, and also the vector incrimination criteria of Lu. cruzi for L. infantum. Additionally, we demonstrated the experimental transmission of L. amazonensis by Lu. cruzi to a naïve host, and revealed strong evidence that supports Lu. cruzi as a vector of L. infantum and as a permissive vector for L. amazonensis.