Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
BBS/E/I/00007039
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
34115806
PubMed Central
PMC8221790
DOI
10.1371/journal.ppat.1009654
PII: PPATHOGENS-D-21-00226
Knihovny.cz E-zdroje
- MeSH
- Ceratopogonidae parazitologie MeSH
- hmyz - vektory parazitologie MeSH
- Leishmania * MeSH
- leishmanióza přenos MeSH
- myši MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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
Entomology Group The Pirbright Institute Pirbright Surrey United Kingdom
Equine Clinic University of Veterinary Sciences Brno Czech Republic
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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 Leishmania and Endotrypanum. Parasitology. 2016;145(Special Issue 4): 430–442. doi: 10.1017/S0031182016002092 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, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) Provides Support for a Gondwanan Origin of Dixenous Parasitism in the Leishmaniinae. PLoS Negl Trop Dis. 2017;11(1):1–26. doi: 10.1371/journal.pntd.0005215 PubMed DOI PMC
Jariyapan N, Daroontum T, Jaiwong K, Chanmol W, Intakhan N, Sor-suwan S, et al.. Leishmania (Mundinia) orientalis n. sp. (Trypanosomatidae), a parasite from Thailand responsible for localised cutaneous leishmaniasis. Parasit Vectors [Internet]. 2018;11(1): 351. Available from: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-018-2908-3 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. Leishmania (Leishmania) martiniquensis n. sp. (Kinetoplastida: Trypanosomatidae), description of the parasite responsible for cutaneous leishmaniasis in Martinique Island (French West Indies). Parasite [Internet]. 2014;21: 12. Available from: http://www.parasite-journal.org/10.1051/parasite/2014011 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 Leishmania responsible for human cutaneous leishmaniasis in Ghana and classification in the Leishmania enriettii complex. Int J Parasitol. 2015;45(11): 679–684. doi: 10.1016/j.ijpara.2015.05.001 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 Leishmania siamensis. Am J Trop Med Hyg. 2012;86(5): 821–824. doi: 10.4269/ajtmh.2012.11-0707 PubMed DOI PMC
Siripattanapipong S, Leelayoova S, Ninsaeng U, Mungthin M. Detection of DNA of Leishmania siamensis in Sergentomyia (Neophlebotomus) iyengari (Diptera: Psychodidae) and molecular identification of blood meals of sand flies in an affected area, Southern Thailand. J Med Entomol. 2018;55(5): 1277–1283. doi: 10.1093/jme/tjy069 PubMed DOI
Supsrisunjai C, Kootiratrakarn T, Puangpet P, Bunnag T, Chaowalit P, Wessagowit V. Case report: Disseminated autochthonous dermal leishmaniasis caused by Leishmania siamensis (PCM2 Trang) in a patient from central Thailand infected with human immunodeficiency virus. Am J Trop Med Hyg. 2017;96(5): 1160–1163. doi: 10.4269/ajtmh.16-0472 PubMed DOI PMC
Reuss SM, Dunbar MD, Calderwood Mays MB, Owen JL, Mallicote MF, Archer LL, et al.. Autochthonous Leishmania siamensis in horse, Florida, USA. Emerg Infect Dis. 2012;18(9): 1545–1547. doi: 10.3201/eid1809.120184 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 Leishmania sp. in cutaneous lesions of horses in Central Europe. Vet Parasitol. 2009;166(3–4): 346–351. doi: 10.1016/j.vetpar.2009.09.001 PubMed DOI
Pothirat T, Tantiworawit A, Chaiwarith R, Jariyapan N, Wannasan A, Siriyasatien P, et al.. First Isolation of Leishmania from Northern Thailand: Case Report, Identification as Leishmania martiniquensis and Phylogenetic Position within the Leishmania enriettii Complex. 2014;8(12): e3339. PubMed PMC
Jungudomjaroen S, Phumee A, Chusri S, Kraivichian K, Jariyapan N, Payungporn S, et al.. Detection of Leishmania martiniquensis DNA in various clinical samples by quantitative PCR. Trop Biomed. 2015;32(4): 736–744. 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 Leishmania martiniquensis. Am J Trop Med Hyg. 2015;92(2): 317–319. doi: 10.4269/ajtmh.14-0205 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 Arvicanthis neumanni, A. niloticus and Mastomys natalensis for Leishmania donovani from Ethiopia and L. (Mundinia) sp. from Ghana. Int J Parasitol Parasites Wildl. 2020; 11: 40–45. doi: 10.1016/j.ijppaw.2019.12.002 PubMed DOI PMC
Belehu A, Turk JL. Establishment of cutaneous Leishmania enriettii infection in hamsters. Infect Immun. 1976;13(4): 1235–1241. doi: 10.1128/iai.13.4.1235-1241.1976 PubMed DOI PMC
Thomaz-Soccol V, Pratlong F, Langue R, Castro E, Luz E, Dedet JP. New isolation of Leishmania enriettii Muniz and Medina, 1948 in Paraná State, Brazil, 50 years after the first description, and isoenzymatic polymorphism of the L. enriettii taxon. Ann Trop Med Parasitol. 1996. Jan;90(5): 491–495. doi: 10.1080/00034983.1996.11813074 PubMed DOI
Seblova V, Sadlova J, Vojtkova B, Votypka J, Carpenter S, Bates PA, et al.. The biting midge Culicoides sonorensis (Diptera: Ceratopogonidae) is capable of developing late stage infections of Leishmania enriettii. PLoS Negl Trop Dis. 2015;9(9): 1–15. doi: 10.1371/journal.pntd.0004060 PubMed DOI PMC
Paranaiba LF, Pinheiro LJ, Macedo DH, Menezes-Neto A, Torrecilhas AC, Tafuri WL, et al.. An overview on Leishmania (Mundinia) enriettii: biology, immunopathology, LRV and extracellular vesicles during the host–parasite interaction. Parasitology. 2018. Sep;145(10): 1265–1273. doi: 10.1017/S0031182017001810 PubMed DOI
Paraense WL. The Spread of Leishmania enriettii through the Body of the Guineapig. Trans R Soc Trop Med Hyg. 1953;47(6): 556–560. doi: 10.1016/s0035-9203(53)80008-8 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 Leishmania martiniquensis—infected BALB/c mice in different routes and time points. M. Sc. Thesis, Chulalongkorn University. 2016. Available from http://cuir.car.chula.ac.th/handle/123456789/60706
Intakhan N, Chanmol W, Kongkaew A, Somboon P, Bates MD, Bates PA, et al.. Experimental infection of Leishmania (Mundinia) martiniquensis in BALB/c mice and Syrian golden hamsters. Parasitol Res. 2020;119(9): 3041–3051. doi: 10.1007/s00436-020-06842-w PubMed DOI
Becvar T, Siriyasatien P, Bates P, Volf P, Sádlová J. Development of Leishmania (Mundinia) in guinea pigs. Parasites and Vectors. 2020;13: 181 Available from: doi: 10.1186/s13071-020-04039-9 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 Leishmania in Australia. Int J Parasitol [Internet]. 2011;41(5): 571–579. Available from: doi: 10.1016/j.ijpara.2010.12.008 PubMed DOI
Chanmol W, Jariyapan N, Somboon P, Bates MD, Bates PA. Development of Leishmania orientalis in the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) and the biting midge Culicoides soronensis (Diptera: Ceratopogonidae). Acta Trop. 2019;199 Available from: 10.1016/j.actatropica.2019.105157 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 Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). J Med Entomol. 2000;37(1): 134–140. doi: 10.1603/0022-2585-37.1.134 PubMed DOI
Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Filho SPB, et al.. Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasite Vector [Internet]. 2016;9(1):1–6. Available from: doi: 10.1186/s13071-016-1444-2 PubMed DOI PMC
Kanjanopas K, Siripattanapipong S, Ninsaeng U, Hitakarun A, Jitkaew S, Kaewtaphaya P, et al.. Sergentomyia (Neophlebotomus) gemmea, a potential vector of Leishmania siamensis in southern Thailand. BMC Infect Dis. 2013;13(1): 13–6. doi: 10.1186/1471-2334-13-333 PubMed DOI PMC
Seblova V, Sadlova J, Carpenter S, Volf P. Speculations on biting midges and other bloodsucking arthropods as alternative vectors of Leishmania. Parasite Vector. 2014;7(1): 222. doi: 10.1186/1756-3305-7-222 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 Culicoides vectors of BTV in the post-genomic era: Resources, bottlenecks to progress and future directions. Virus Res [Internet]. 2014;182: 43–9. Available from: doi: 10.1016/j.virusres.2013.12.009 PubMed DOI PMC
Carpenter S, Groschup MH, Garros C, Felippe-Bauer ML, Purse B V. Culicoides biting midges, arboviruses and public health in Europe. Antiviral Res [Internet]. 2013;100(1): 102–113. Available from: doi: 10.1016/j.antiviral.2013.07.020 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 Leishmania infantum infection in Migonemyia migonei (França, 1920) (Diptera:Psychodidae:Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco State, Brazil. Acta Trop. 2010;116(1): 108–110. doi: 10.1016/j.actatropica.2010.03.009 PubMed DOI
Lainson R, Rangel EF. Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil—a review. Mem Inst Oswaldo Cruz. 2005;100: 811–827. doi: 10.1590/s0074-02762005000800001 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 Sergentomyia from the region. Invertebr Syst. 1988;2(6): 755–804.
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 Leishmania infantum by two major vectors: A comparison between a viscerotropic and a dermotropic strain. PLoS Negl Trop Dis. 2011;5(6): e1181. doi: 10.1371/journal.pntd.0001181 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. Sergentomyia schwetzi is not a competent vector for Leishmania donovani and other Leishmania species pathogenic to humans. Parasit Vectors. 2013;6(1): 186. Available from: http://www.parasitesandvectors.com/content/6/1/186. doi: 10.1186/1756-3305-6-186 PubMed DOI PMC
Sadlova J, Homola M, Myskova J, Jancarova M, Volf P. Refractoriness of Sergentomyia schwetzi to Leishmania spp. is mediated by the peritrophic matrix. PLoS Negl Trop Dis. 2018;12(4): e0006382. doi: 10.1371/journal.pntd.0006382 PubMed DOI PMC
Maia C, Depaquit J. Can Sergentomyia (Diptera, Psychodidae) play a role in the transmission of mammal-infecting Leishmania? Parasite [Internet]. 2016;23:55. Available from: doi: 10.1051/parasite/2016062 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): Leishmania donovani development in Phlebotomus argentipes: comparison of promastigote- and amastigote-initiated infections. Parasitology. 2017;144(4): 403–410. doi: 10.1017/S0031182016002067 PubMed DOI PMC
Serafim TD, Coutinho-Abreu IV, Oliveira F., Meneses C, Kamhawi S, Valenzuela JG. Sequential blood meals promote Leishmania replication and reverse metacyclogenesis augmenting vector infectivity. 2018; Nat Microbiol 3: 548–555. doi: 10.1038/s41564-018-0125-7 PubMed DOI PMC
Bates PA. Revising Leishmania’s life cycle. Nat Microbiol. 2018; 3: 529–530. doi: 10.1038/s41564-018-0154-2 PubMed DOI
Seblova V, Sadlova J, Carpenter S, Volf P. Development of Leishmania parasites in Culicoides nubeculosus (Diptera: Ceratopogonidae) and implications for screening vector competence. J Med Entomol [Internet]. 2012;49(5):967–70. Available from: doi: 10.1603/me12053 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 Leishmania Population. PLoS Genet. 2014;10(1): e1004092. doi: 10.1371/journal.pgen.1004092 PubMed DOI PMC
Myskova J, Votypka J, Volf P. Leishmania in Sand Flies: Comparison of Quantitative Polymerase Chain Reaction with Other Techniques to Determine the Intensity of Infection. J Med Entomol. 2008;45(1): 133–1388. doi: 10.1603/0022-2585(2008)45[133:lisfco]2.0.co;2 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 Leishmania major in its sand fly vector, Phlebotomus papatasi. Cell Microbiol. 2010;12(12): 1765–1779. doi: 10.1111/j.1462-5822.2010.01507.x PubMed DOI PMC
Rodgers MR, Popper SJ, Wirth DF. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp Parasitol. 1990;71(3): 267–275. doi: 10.1016/0014-4894(90)90031-7 PubMed DOI
Leishmania spp. in equids and their potential vectors in endemic areas of canine leishmaniasis
Porcisia transmission by prediuresis of sand flies