Abstract

Leishmaniasis is a debilitating disease of the tropics, subtropics and southern Europe caused by Leishmania parasites that are transmitted during blood feeding by phlebotomine sand flies (Diptera: Psychodidae). Using non-invasive micro-computed tomography, we were able to visualize the impact of the laboratory model infection of Lutzomyia longipalpis with Leishmania mexicana and its response to a second blood meal. For the first time we were able to show in 3D the plug of promastigote secretory gel (PSG) and parasites in the distended midgut of whole infected sand flies and measure its volume in relation to that of the midgut. We were also able to measure the degree of opening of the stomodeal valve and demonstrate the extension of the PSG and parasites into the pharynx. Although our pilot study could only examine a few flies, it supports the hypothesis that a second, non-infected, blood meal enhances parasite transmission as we showed that the thoracic PSG-parasite plug in infected flies after a second blood meal was, on average, more than twice the volume of the plug in infected flies that did not have a second blood meal.

Highlights

  • Phlebotomine sand flies (Diptera: Psychodidae) are vectors of the Leishmania (Trypanosomatida: Trypanosomatidae) parasites of vertebrates, including humans

  • Leishmaniasis is a debilitating disease of the tropics, subtropics and southern Europe caused by Leishmania parasites that are transmitted during blood feeding by phlebotomine sand flies (Diptera: Psychodidae)

  • Leishmaniasis is a debilitating disease of the tropics, subtropics and southern Europe caused by protozoa of the genus Leishmania, that are transmitted by blood feeding sand flies

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Summary

Introduction

Phlebotomine sand flies (Diptera: Psychodidae) are vectors of the Leishmania (Trypanosomatida: Trypanosomatidae) parasites of vertebrates, including humans. Leishmaniasis is a neglected tropical disease (NTD) associated with poverty, causing a significant health, welfare and economic burden as well as delays to a wide range of development programmes in the tropics, with some 1.5–2.0 million new cases annually [1]. It is the vertebrate hosts that suffer as a consequence of infection as Leishmania can have a significant impact on the sand fly vector [2], with parasite production of a proteophosphoglycan-rich promastigote secretory gel (PSG) that can block the lumen of the anterior midgut [3]. It is the accumulation of PSG and a mass of parasites that obstructs the sand fly gut [8,9] ( described as the ‘PSG-parasite plug’), making it difficult for the fly to feed and, thereby, leading to more and longer feeding attempts, which increase the chances of parasite transmission–termed the “blocked fly hypothesis” [8,10]

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