Leishmania parasites, causative agents of leishmaniasis, are currently divided into four subgenera: Leishmania, Viannia, Sauroleishmania and Mundinia. The recently established subgenus Mundinia has a wide geographical distribution and contains five species, three of which have the potential to infect and cause disease in humans. While the other Leishmania subgenera are transmitted exclusively by phlebotomine sand flies (Diptera: Psychodidae), natural vectors of Mundinia remain uncertain. This study investigates the potential of sand flies and biting midges of the genus Culicoides (Diptera: Ceratopogonidae) to transmit Leishmania parasites of the subgenus Mundinia. Sand flies (Phlebotomus argentipes, P. duboscqi and Lutzomyia migonei) and Culicoides biting midges (Culicoides sonorensis) were exposed to five Mundinia species through a chicken skin membrane and dissected at specific time intervals post bloodmeal. Potentially infected insects were also allowed to feed on ear pinnae of anaesthetized BALB/c mice and the presence of Leishmania DNA was subsequently confirmed in the mice using polymerase chain reaction analyses. In C. sonorensis, all Mundinia species tested were able to establish infection at a high rate, successfully colonize the stomodeal valve and produce a higher proportion of metacyclic forms than in sand flies. Subsequently, three parasite species, L. martiniquensis, L. orientalis and L. sp. from Ghana, were transmitted to the host mouse ear by C. sonorensis bite. In contrast, transmission experiments entirely failed with P. argentipes, although colonisation of the stomodeal valve was observed for L. orientalis and L. martiniquensis and metacyclic forms of L. orientalis were recorded. This laboratory-based transmission of Mundinia species highlights that Culicoides are potential vectors of members of this ancestral subgenus of Leishmania and we suggest further studies in endemic areas to confirm their role in the lifecycles of neglected pathogens.

Biology Centre Institute of Parasitology Czech Academy of Sciences České Budějovice Czech Republic

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Parasitology Faculty of Science Charles University Prague Czech Republic

Department of Veterinary Sciences CINeZ Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Prague Czech Republic

Division of Biomedical and Life Sciences Faculty of Health and Medicine Lancaster University Lancaster United Kingdom

Entomology Group The Pirbright Institute Pirbright Surrey United Kingdom

Equine Clinic University of Veterinary Sciences Brno Czech Republic

Vector Biology and Vector Borne Disease Research Unit Department of Parasitology Faculty of Medicine Chulalongkorn University Bangkok Thailand

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Ashford RW. The leishmaniases as emerging and reemerging zoonoses. Int J Parasitol. 2000;30(12–13): 1269–1281. doi: 10.1016/s0020-7519(00)00136-3 PubMed DOI

WHO. Available from: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis. 2020.

Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as PubMed DOI

Muniz J, Medina H. Cutaneous Leishmaniasis in the Guineapig. Hospital (Rio J). 1948;33(1): 7–25. PubMed

Rose K, Curtis J, Baldwin T, Mathis A, Kumar B, Sakthianandeswaren A, et al. Cutaneous leishmaniasis in red kangaroos: isolation and characterisation of the causative organisms. Int J Parasitol. 2004;34(6): 655–664. doi: 10.1016/j.ijpara.2004.03.001 PubMed DOI

Barratt J, Kaufer A, Peters B, Craig D, Lawrence A, Roberts T, et al. Isolation of Novel Trypanosomatid, PubMed DOI PMC

Jariyapan N, Daroontum T, Jaiwong K, Chanmol W, Intakhan N, Sor-suwan S, et al. PubMed DOI PMC

Dedet JP, Roche B, Pratlong F, Caies-Quist D, Jouannelle J, Benichou JC, et al. Diffuse cutaneous infection caused by a presumed monoxenous trypanosomatid in a patient infected with HIV. Trans R Soc Trop Med Hyg. 1995;89(6): 644–646. doi: 10.1016/0035-9203(95)90427-1 PubMed DOI

Desbois N, Pratlong F, Quist D, Dedet J-P. PubMed DOI PMC

Kwakye-Nuako G, Mosore MT, Duplessis C, Bates MD, Puplampu N, Mensah-Attipoe I, et al. First isolation of a new species of PubMed DOI

Bualert L, Charungkiattikul W, Thongsuksai P, Mungthin M, Siripattanapipong S, Khositnithikul R, et al. Case report: Autochthonous disseminated dermal and visceral leishmaniasis in an AIDS patient, Southern Thailand, caused by PubMed DOI PMC

Siripattanapipong S, Leelayoova S, Ninsaeng U, Mungthin M. Detection of DNA of PubMed DOI

Supsrisunjai C, Kootiratrakarn T, Puangpet P, Bunnag T, Chaowalit P, Wessagowit V. Case report: Disseminated autochthonous dermal leishmaniasis caused by PubMed DOI PMC

Reuss SM, Dunbar MD, Calderwood Mays MB, Owen JL, Mallicote MF, Archer LL, et al. Autochthonous PubMed DOI PMC

Lobsiger L, Müller N, Schweizer T, Frey CF, Wiederkehr D, Zumkehr B, et al. An autochthonous case of cutaneous bovine leishmaniasis in Switzerland. Vet Parasitol. 2010;169(3–4): 408–414. doi: 10.1016/j.vetpar.2010.01.022 PubMed DOI

Müller N, Welle M, Lobsiger L, Stoffel MH, Boghenbor KK, Hilbe M, et al. Occurrence of PubMed DOI

Pothirat T, Tantiworawit A, Chaiwarith R, Jariyapan N, Wannasan A, Siriyasatien P, et al. First Isolation of PubMed PMC

Jungudomjaroen S, Phumee A, Chusri S, Kraivichian K, Jariyapan N, Payungporn S, et al. Detection of PubMed

Boisseau-Garsaud AM, Cales-Quist D, Desbois N, Jouannelle J, Jouannelle A, Pratlong F, et al. A new case of cutaneous infection by a presumed monoxenous trypanosomatid in the island of Martinique (French West Indies). Trans R Soc Trop Med Hyg. 2000;94: 51–52. doi: 10.1016/s0035-9203(00)90435-8 PubMed DOI

Liautaud B, Vignier N, Miossec C, Plumelle Y, Kone M, Delta D, et al. First case of visceral leishmaniasis caused by PubMed DOI PMC

Dougall A, Shilton C, Low Choy J, Alexander B, Walton S. New reports of Australian cutaneous leishmaniasis in Northern Australian macropods. Epidemiol Infect. 2009;137(10): 1516–1520. doi: 10.1017/S0950268809002313 PubMed DOI

Sadlova J, Vojtkova B, Becvar T, Lestinova T, Spitzova T, Bates P, et al. Host competence of the African rodents PubMed DOI PMC

Belehu A, Turk JL. Establishment of cutaneous PubMed DOI PMC

Thomaz-Soccol V, Pratlong F, Langue R, Castro E, Luz E, Dedet JP. New isolation of PubMed DOI

Seblova V, Sadlova J, Vojtkova B, Votypka J, Carpenter S, Bates PA, et al. The biting midge PubMed DOI PMC

Paranaiba LF, Pinheiro LJ, Macedo DH, Menezes-Neto A, Torrecilhas AC, Tafuri WL, et al. An overview on PubMed DOI

Paraense WL. The Spread of PubMed DOI

Garin YJF, Sulahian A, Méneceur P, Pratlong F, Prina E, Gangneux JP, et al. Experimental pathogenicity of a presumed monoxenous trypanosomatid isolated from humans in a murine model. J Eukaryot Microbiol. 2001;48(2): 170–176. doi: 10.1111/j.1550-7408.2001.tb00299.x PubMed DOI

Somboonpoonpol N. Parasite burden, distribution and imunopathology of

Intakhan N, Chanmol W, Kongkaew A, Somboon P, Bates MD, Bates PA, et al. Experimental infection of PubMed DOI

Becvar T, Siriyasatien P, Bates P, Volf P, Sádlová J. Development of PubMed DOI PMC

Killick-Kendrick R. Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 1990;4(1): 1–24. doi: 10.1111/j.1365-2915.1990.tb00255.x PubMed DOI

Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol. 2013;27(2): 123–147. doi: 10.1111/j.1365-2915.2012.01034.x PubMed DOI

Dougall AM, Alexander B, Holt DC, Harris T, Sultan AH, Bates PA, et al. Evidence incriminating midges (Diptera: Ceratopogonidae) as potential vectors of PubMed DOI

Chanmol W, Jariyapan N, Somboon P, Bates MD, Bates PA. Development of PubMed DOI

Killick-Kendrick R. The biology and control of Phlebotomine sand flies. Clin Dermatol. 1999;17(3): 279–289. doi: 10.1016/s0738-081x(99)00046-2 PubMed DOI

Kostygov AY, Yurchenko V. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol (Praha). 2017;64: 1–5. PubMed

Nieves E, Pimenta PFP. Development of PubMed DOI

Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Filho SPB, et al. PubMed DOI PMC

Kanjanopas K, Siripattanapipong S, Ninsaeng U, Hitakarun A, Jitkaew S, Kaewtaphaya P, et al. PubMed DOI PMC

Seblova V, Sadlova J, Carpenter S, Volf P. Speculations on biting midges and other bloodsucking arthropods as alternative vectors of PubMed DOI PMC

Borkent A, Dominiak P. Catalog of the Biting Midges of the World (Diptera: Ceratopogonidae). Zootaxa. 2020;4787(1): 001–377. PubMed

Nayduch D, Cohnstaedt LW, Saski C, Lawson D, Kersey P, Fife M, et al. Studying PubMed DOI PMC

Carpenter S, Groschup MH, Garros C, Felippe-Bauer ML, Purse B V. PubMed DOI

Rangel EF, Lainson R. Proven and putative vectors of American cutaneous leishmaniasis in Brazil: Aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz. 2009;104(7). Available from: doi: 10.1590/s0074-02762009000700001 PubMed DOI

de Carvalho MR, Valença HF, da Silva FJ, de Pita-Pereira D, de Araújo Pereira T, Britto C, et al. Natural PubMed DOI

Lainson R, Rangel EF. PubMed DOI

Kweku MA, Odoom S, Puplampu N, Desewu K, Nuako GK, Gyan B, et al. An outbreak of suspected cutaneous leishmaniasis in Ghana: lessons learnt and preparation for future outbreaks. Glob Health Action. 2011;4. Available from: doi: 10.3402/gha.v4i0.5527 PubMed DOI PMC

Lewis DJ, Dyce AL. Taxonomy of the australasian phlebotominae (Diptera: Psychodidae) with revision of genus

Lawyer P, Killick-Kendrick M, Rowland T, Rowton E, Volf P. Laboratory colonization and mass rearing of phlebotomine sand flies (Diptera, Psychodidae). Parasite. 2017; 24: 42. doi: 10.1051/parasite/2017041 PubMed DOI PMC

Maia C, Seblova V, Sadlova J, Votypka J, Volf P. Experimental transmission of PubMed DOI PMC

Ozbel Y, Sanjoba C, Alten B, Asada M, Depaquit J, Matsumoto Y, et al. Distribution and ecological aspects of sand fly (Diptera: Psychodidae) species in Sri Lanka. J Vector Ecol. 2011; 36(s1). Available from: doi: 10.1111/j.1948-7134.2011.00115.x PubMed DOI

Sadlova J, Dvorak V, Seblova V, Warburg A, Votypka J, Volf P. PubMed DOI PMC

Sadlova J, Homola M, Myskova J, Jancarova M, Volf P. Refractoriness of PubMed DOI PMC

Maia C, Depaquit J. Can PubMed DOI PMC

Lainson R, Shaw JJ. The Role of Animals in the Epidemiology of South American Leishmaniasis. In: Lumsden WHR, Ewans DA, editors. Biology of the Kinetoplastida Vol 2. London, New York: Academic Press; 1979. pp. 1–116.

Sadlova J, Myskova J, Lestinova T, Votypka J, Yeo M, Volf P. (2017): PubMed DOI PMC

Serafim TD, Coutinho-Abreu IV, Oliveira F., Meneses C, Kamhawi S, Valenzuela JG. Sequential blood meals promote PubMed DOI PMC

Bates PA. Revising PubMed DOI

Seblova V, Sadlova J, Carpenter S, Volf P. Development of PubMed DOI

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36: 1–9. doi: 10.1111/j.1948-7134.2011.00106.x PubMed DOI

Rogers MB, Downing T, Smith BA, Imamura H, Sanders M, Svobodova M, et al. Genomic Confirmation of Hybridisation and Recent Inbreeding in a Vector-Isolated PubMed DOI PMC

Myskova J, Votypka J, Volf P. PubMed DOI

Sádlová J, Price HP, Smith BA, Votýpka J, Volf P, Smith DF. The stage-regulated HASPB and SHERP proteins are essential for differentiation of the protozoan parasite PubMed DOI PMC

Rodgers MR, Popper SJ, Wirth DF. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of PubMed DOI

Emergence of Autochthonous Leishmania (Mundinia) martiniquensis Infections in Horses, Czech Republic and Austria, 2019-2023

The development of L. major, L. donovani and L. martiniquensis, Leishmania currently emerging in Europe, in the sand fly species Phlebotomus perniciosus and P. tobbi

Leishmania spp. in equids and their potential vectors in endemic areas of canine leishmaniasis

Steppe lemmings and Chinese hamsters as new potential animal models for the study of the Leishmania subgenus Mundinia (Kinetoplastida: Trypanosomatidae)

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

Porcisia transmission by prediuresis of sand flies

Leishmania guyanensis M4147 as a new LRV1-bearing model parasite: Phosphatidate phosphatase 2-like protein controls cell cycle progression and intracellular lipid content