Evaluation of an Italian Phlebotomus perfiliewi (Larroussius) wild population as a permissive vector species for Leishmania tropica and L. major transmission

TL;DR

This study shows that an Italian sand fly species can support the development of two Leishmania parasites, though less efficiently than known vectors.

Contribution

The study experimentally demonstrates that Phlebotomus perfiliewi can support the development of L. tropica and L. major in Italy.

Findings

P. perfiliewi supported L. tropica development with a 25.2% infection positivity rate.

P. perfiliewi supported L. major metacyclogenesis, though with a lower feeding rate than the control species.

Parasite migration to the stomodeal valve suggests potential for full developmental cycles in P. perfiliewi.

Abstract

Among pathogenic Leishmania species, L. major and L. tropica, occur mainly in North African and Middle Eastern countries, primarily transmitted by Phlebotomus papatasi and P. sergenti respectively. In Italy, P. perfiliewi is the second most abundant sand fly species involved in L. infantum transmission exhibiting opportunistic behaviour in rural and semi-urban settings. Experimental infections were conducted to assess the susceptibility of a wild Italian P. perfiliewi population to the development of L. tropica and L. major.

Experiments were performed with a wild P. perfiliewi population, collected in Magliano in Toscana (Tuscany, Italy). In separate experiments, females were artificially infected with a suspension of L. tropica or L. major (106 promastigotes/ml). Infection progression was monitored through microscopic midgut dissection and supported by molecular analyses.

Experimental infections with L. tropica yielded 5923 engorged females, with an average feeding rate of 25.7% and a survival rate of 70%. The infection positivity rate was 25.2%, significantly lower than that observed in the control species. Nonetheless, parasite migration to the stomodeal valve suggests that P. perfiliewi may support the full developmental cycle of L. tropica, although less efficiently than the control species. Infections with L. major showed a significantly lower mean feeding rate (p = 0.05) and a positivity rate of 46.6%, compared to 70.5% in P. perniciosus (p = 0.03). Still, P. perfiliewi appeared capable of supporting L. major metacyclogenesis, even under light to moderate parasite loads (p = 0.007).

These findings suggest that P. perfiliewi can support the development of both L. tropica and L. major under experimental conditions, with greater susceptibility observed for L. tropica. However, without in vivo confirmation or xenodiagnosis, its capacity for natural transmission remains unestablished. Nonetheless, implementing integrated One Health surveillance strategies would be advisable to monitor potential changes in the epidemiology of both exotic and endemic Leishmania species.

The online version contains supplementary material available at 10.1186/s13071-025-07170-7.

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