Molecular detection of Leishmania donovani, Leishmania major, and Trypanosoma species in Sergentomyia squamipleuris sand flies from a visceral leishmaniasis focus in Merti sub-County, eastern Kenya

Abstract

Background Visceral leishmaniasis (VL) and zoonotic cutaneous leishmaniasis (ZCL) are of public health concern in Merti sub-County, Kenya, but epidemiological data on transmission, vector abundance, distribution, and reservoir hosts remain limited. To better understand the disease and inform control measures to reduce transmission, we investigated the abundance and distribution of sand fly species responsible for Leishmania transmission in the sub-County and their blood-meal hosts. Methods We conducted an entomological survey in five villages with reported cases of VL in Merti sub-County, Kenya, using CDC miniature light traps and castor oil sticky papers. Sand flies were dissected and identified to the species level using standard taxonomic keys and PCR analysis of the cytochrome c oxidase subunit 1 (cox1) gene. Leishmania parasites were detected and identified by PCR and sequencing of internal transcribed spacer 1 (ITS1) genes. Blood-meal sources of engorged females were identified by high-resolution melting analysis of vertebrate cytochrome b (cyt-b) gene PCR products. Results We sampled 526 sand flies consisting of 8 species, Phlebotomus orientalis (1.52%; n = 8), and 7 Sergentomyia spp. Sergentomyia squamipleuris was the most abundant sand fly species (78.71%; n = 414) followed by Sergentomyia clydei (10.46%; n = 55). Leishmania major, Leishmania donovani, and Trypanosoma DNA were detected in S. squamipleuris specimens. Humans were the main sources of sand fly blood meals. However, we also detected mixed blood meals; one S. squamipleuris specimen had fed on both human and mouse (Mus musculus) blood, while two Ph. orientalis specimens fed on human, hyrax (Procavia capensis), and mouse (Mus musculus) blood. Conclusions Our findings implicate the potential involvement of S. squamipleuris in the transmission of Leishmania and question the dogma that human leishmaniases in the Old World are exclusively transmitted by sand flies of the Phlebotomus genus. The presence of Trypanosoma spp. may indicate mechanical transmission, whose efficiency should be investigated. Host preference analysis revealed the possibility of zoonotic transmission of leishmaniasis and other pathogens in the sub-County. Leishmania major and L. donovani are known to cause ZCL and VL, respectively. However, the reservoir status of the parasites is not uniform. Further studies are needed to determine the reservoir hosts of Leishmania spp. in the area.

Discovery of the vector of visceral leishmaniasis, Phlebotomus (Artemievus) alexandri Sinton, 1928, in Kenya suggests complex transmission dynamics

“…alexandri . To our knowledge, no case of human CL has been reported from the region of study apart from reports of molecular detection of L. major DNA in S. squamipleuris from the neighboring County of Isiolo ( Owino et al, 2021 ). We also detected L. major DNA in S. squamipleuris , as well as in S. africanus and S. dreyfussi .…”

“…The intracellular protozoan parasites of the genus Leishmania (Family Trypanosomatidae) are transmitted during blood-feeding by female sand flies of the genera Phlebotomus Rondani & Berte and Lutzomyia França, in the Old World and New World, respectively ( Torres-Guerrero et al, 2017 ; Ngere et al, 2020 ). Although some members of the genus Sergentomyia Franca & Parrot, have been reported to mechanically spread Leishmania parasites during blood-meal acquisition process, they are not considered biological vectors of leishmaniasis, but rather flies of biting nuisance ( Anjili et al, 2011 ; Owino et al, 2021 ). Clinically, there are four forms of the disease: visceral leishmaniasis (VL; also commonly referred to as ‘kala-azar’), which is the most fatal form of the disease; cutaneous leishmaniasis (CL); mucocutaneous leishmaniasis (MCL); and a putative post-kala-azar dermal leishmaniasis ( Inceboz, 2019 ; WHO, 2021 ).…”

Short Communication: Tabanid and muscoid hematophagous flies as potential vectors of Surra Disease in Yogyakarta, Indonesia

“…The study areas were selected by considering a large number of cases in the areas (Owino et al 2021). The study was conducted in areas with repeated outbreaks of Surra disease or an increasing number of cases in cattle.…”

Epidemiological Aspects of Zoonotic Cutaneous Leishmaniasis (ZCL) in Iran, the Middle East, and Worldwide: A Comprehensive Systematic Review

“…Despite many efforts to control the disease, ZCL continues to pose a threat to of its complex transmission process involving vectors, hosts, and human activities. The endemic nature of ZCL in Iran, along with new outbreaks and fluctuating infection rates, highlight the urgent need to deeply understand its epidemiology to design effective control and prevention strategies (60–64,5, 97,17).…”

“…This geographical spread shows that ZCL is not only a problem in Iran but also poses a challenge across countries. This underscores the need for a coordinated international effort in research and control measures to address this issue effectively (16–17,22–25,34–35,88–89,90,97,4,13,20,38,54,57,59,66,64,69).…”