Odour of domestic dogs infected with Leishmania infantum is attractive to female but not male sand flies: Evidence for parasite manipulation

Abstract

Globally visceral leishmaniasis (VL) causes thousands of human deaths every year. In South America, the etiologic agent, Leishmania infantum, is transmitted from an infected canine reservoir to human hosts by the bite of the sand fly vector; predominantly Lutzomyia longipalpis. Previous evidence from model rodent systems have suggested that the odour of infected hosts is altered by the parasite making them more attractive to the vector leading to an increased biting rate and improved transmission prospects for the pathogen. However, there has been no assessment of the effect of Le infantum infection on the attractiveness of dogs, which are the natural reservoirs for human infection. Hair collected from infected and uninfected dogs residing in a VL endemic city in Brazil was entrained to collect the volatile chemical odours present in the headspace. Female and male Lu. longipalpis sand flies were offered a choice of odour entrained from infected and uninfected dogs in a series of behavioural experiments. Odour of uninfected dogs was equally attractive to male or female Lu. longipalpis when compared to a solvent control. Female Lu. longipalpis were significantly more attracted to infected dog odour than uninfected dog odour in all 15 experimental replicates (average 45.7±0.87 females attracted to infected odour; 23.9±0.82 to uninfected odour; paired T-test, P = 0.000). Male Lu. longipalpis did not significantly prefer either infected or uninfected odour (average 36.1±0.4 males to infected odour; 35.7±0.6 to uninfected odour; paired T-test, P = 0.722). A significantly greater proportion of females chose the infected dog odour compared to the males (paired T-test, P = 0.000). The results showed that the odour of dogs infected with Le. infantum was significantly more attractive to blood-seeking female sand flies than it was to male sand flies. This is strong evidence for parasite manipulation of the host odour in a natural transmission system and indicates that infected dogs may have a disproportionate significance in maintaining infection in the canine and human population.

Insecticidal efficacy against Phlebotomus perniciosus in dogs treated orally with fluralaner in two different parallel-group, negative-control, random and masked trials

“…Recent published data show that Leishmania -infected dogs were significantly more attractive to P. perniciosus than uninfected dogs under both laboratory and field conditions [ 22 ] . A similar behavior was detected when L longipalpis was tested [ 23 ]. Therefore, treating Leishmania -positive dogs with fluralaner in endemic areas with an elevated incidence of human VL may represent a promising tool for reducing the infected P. perniciosus population and hence transmission.…”

Determination of the effect of collars containing 10% w/w imidacloprid and 4.5% w/w flumethrin (Seresto®) on the incidence of Leishmania and other canine vector-borne pathogen infections in Greece

“…This scenario is supported by the fact that insects identify potential host animals by combinations of visual, thermal, tactile and chemical (host odour) cues produced by the host, and are therefore found close to dog communities (this is more obvious for sand flies who have not a great ability to fly long distances) [ 26 ]. Moreover, it has been recently documented that the odour of L. infantum -infected dogs is more attractive to female sand flies than the odour of uninfected dogs, leading to enhanced infection and transmission opportunities for the parasite [ 27 ]. Our results suggest that the above-mentioned 16 dogs had some contact with Leishmania parasites due to the high infection pressure of the environment, but that the infection pressure was not sufficient high for the infection to be established.…”