Detection of Leishmania tarentolae in lizards, sand flies and dogs in southern Italy, where Leishmania infantum is endemic: hindrances and opportunities

Abstract

Background Leishmania tarentolae is a protozoan isolated from geckoes (Tarentola annularis, Tarentola mauritanica), which is considered non-pathogenic and is transmitted by herpetophilic Sergentomyia spp. sand flies. This species occurs in sympatry with Leishmania infantum in areas where canine leishmaniasis is endemic. In the present study, we investigated the circulation of L. tarentolae and L. infantum in sand flies, dogs and lizards in a dog shelter in southern Italy, where canine leishmaniasis by L. infantum is endemic. Methods Sheltered dogs (n = 100) negative for Leishmania spp. (March 2020) were screened by immunofluorescence antibody test (IFAT) using promastigotes of both species at two time points (June 2020 and March 2021). Whole blood from dogs, tissues of Podarcis siculus lizards (n = 28) and sand flies (n = 2306) were also sampled and tested by a duplex real-time PCR (dqPCR). Host blood meal was assessed in sand flies by PCR. Results Overall, 16 dogs became positive for L. infantum and/or L. tarentolae by IFAT at one or both sampling periods. One canine blood sample was positive for L. infantum, whilst two for L. tarentolae by dqPCR. At the cytology of lizard blood, Leishmania spp. amastigote-like forms were detected in erythrocytes. Twenty-two tissue samples, mostly lung (21.4%), scored molecularly positive for L. tarentolae, corresponding to 10 lizards (i.e., 35.7%). Of the female Sergentomyia minuta sampled (n = 1252), 158 scored positive for L. tarentolae, four for L. infantum, and one co-infected. Two Phlebotomus perniciosus (out of 29 females) were positive for L. tarentolae. Engorged S. minuta (n = 10) fed on humans, and one P. perniciosus, positive for L. tarentolae, on lagomorphs. Conclusions Dogs and lacertid lizards (Podarcis siculus) were herein found for the first time infected by L. tarentolae. The detection of both L. tarentolae and L. infantum in S. minuta and P. perniciosus suggests their sympatric circulation, with a potential overlap in vertebrate hosts. The interactions between L. tarentolae and L. infantum should be further investigated in both vectors and vertebrate hosts to understand the potential implications for the diagnosis and control of canine leishmaniasis in endemic areas. Graphical abstract

Leishmania tarentolae and Leishmania infantum in humans, dogs and cats in the Pelagie archipelago, southern Italy

“…tarentolae is commonly regarded infecting geckoes (i.e., Tarentola annularis and T . mauritanica ) and recently also lacertid lizards ( Podarcis siculus ) [ 16 ]. Nonetheless, some strain (i.e., LEM-125) of L .…”

“…perniciosus and Phlebotomus perfiliewi , which usually feed on mammals, as well as in S . minuta fed on humans [ 16 , 17 ], the epidemiology of this parasite requires careful and thorough evaluation.…”

“…infantum subclinical infection (10%) was also recorded along with a high abundance of S . minuta [ 16 ]. These findings along with the serological positivity to L .…”

“…tarentolae DNA in a human being was from bone marrow and intestines of a 300-year-old Brazilian mummy [ 18 ]. Only recently the parasite DNA has been detected in the blood of human donors [ 17 ] and in sheltered dogs [ 16 ] in central and southern Italy, respectively. In addition, experimental studies demonstrated that L .…”

“…A recent surveillance on phlebotomine sand flies conducted in Sicily reported a high abundance of Sergentomyia minuta and Phlebotomus perniciosus, both competent vectors of Leishmania tarentolae and L. infantum in reptiles and mammalian hosts, respectively [14]. Unexpectedly, an increasing number of scientific evidence suggests that S. minuta feed also on humans [14][15][16][17]. The first evidence of L. tarentolae DNA in a human being was from bone marrow and intestines of a 300-year-old Brazilian mummy [18].…”