Experimental transmission of Leishmania (Mundinia) parasites by
biting midges (Diptera: Ceratopogonidae)

J 2021

Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)

BECVAR, Tomas, Barbora VOJTKOVA, Padet SIRIYASATIEN, Jan VOTYPKA, David MODRÝ et. al.

Basic information

Original name

Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)

Authors

BECVAR, Tomas, Barbora VOJTKOVA, Padet SIRIYASATIEN, Jan VOTYPKA, David MODRÝ (203 Czech Republic, belonging to the institution), Petr JAHN, Paul BATES, Simon CARPENTER, Petr VOLF and Jovana SADLOVA (guarantor)

Edition

PLoS Pathogens, San Francisco, Public Library of Science, 2021, 1553-7366

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10606 Microbiology

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 7.464

RIV identification code

RIV/00216224:14310/21:00123525

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1371/journal.ppat.1009654

UT WoS

000664722900002

Keywords in English

CUTANEOUS LEISHMANIASIS; VISCERAL LEISHMANIASIS; SAND FLIES; PUBLIC-HEALTH; INFECTION; VECTOR; SIAMENSIS; THAILAND; PATIENT; DNA

Abstract

V originále

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. Author summaryLeishmania parasites are causative agents of leishmaniasis, a disease affecting millions of humans worldwide. It is widely accepted that these flagellates are transmitted exclusively by phlebotomine sand flies (Diptera: Phlebotominae). Reservoir hosts and insect vectors for the newly established Leishmania subgenus Mundinia, however, remain poorly understood. Preliminary evidence from field-based studies discovered biting midges (Diptera: Ceratopogonidae) that were naturally infected by L. (Mundinia) macropodum in Australia. This surprising finding led us to carry out a detailed laboratory study aimed at comparison of the development of all currently known species of the subgenus Mundinia in both putative vector families. We found that all five Mundinia species developed successfully in C. sonorensis and the successful transmission of three Mundinia species from infected insects to mice was demonstrated for the first time. This is the first detailed in vivo evidence that biting midges can act as competent vectors of Leishmania parasites of the subgenus Mundinia and has considerable epidemiological implications for control of these neglected pathogens.

Citovat

BECVAR, Tomas, Barbora VOJTKOVA, Padet SIRIYASATIEN, Jan VOTYPKA, David MODRÝ, Petr JAHN, Paul BATES, Simon CARPENTER, Petr VOLF and Jovana SADLOVA. Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae). PLoS Pathogens. San Francisco: Public Library of Science, 2021, vol. 17, No 6, p. "e1009654", 18 pp. ISSN 1553-7366. Available from: https://dx.doi.org/10.1371/journal.ppat.1009654.

@article{1817121,
   author = {Becvar, Tomas and Vojtkova, Barbora and Siriyasatien, Padet and Votypka, Jan and Modrý, David and Jahn, Petr and Bates, Paul and Carpenter, Simon and Volf, Petr and Sadlova, Jovana},
   article_location = {San Francisco},
   article_number = {6},
   doi = {http://dx.doi.org/10.1371/journal.ppat.1009654},
   keywords = {CUTANEOUS LEISHMANIASIS; VISCERAL LEISHMANIASIS; SAND FLIES; PUBLIC-HEALTH; INFECTION; VECTOR; SIAMENSIS; THAILAND; PATIENT; DNA},
   language = {eng},
   issn = {1553-7366},
   journal = {PLoS Pathogens},
   title = {Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)},
   url = {https://doi.org/10.1371/journal.ppat.1009654},
   volume = {17},
   year = {2021}
}

TY  - JOUR
ID  - 1817121
AU  - Becvar, Tomas - Vojtkova, Barbora - Siriyasatien, Padet - Votypka, Jan - Modrý, David - Jahn, Petr - Bates, Paul - Carpenter, Simon - Volf, Petr - Sadlova, Jovana
PY  - 2021
TI  - Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)
JF  - PLoS Pathogens
VL  - 17
IS  - 6
SP  - "e1009654"
EP  - "e1009654"
PB  - Public Library of Science
SN  - 15537366
KW  - CUTANEOUS LEISHMANIASIS
KW  - VISCERAL LEISHMANIASIS
KW  - SAND FLIES
KW  - PUBLIC-HEALTH
KW  - INFECTION
KW  - VECTOR
KW  - SIAMENSIS
KW  - THAILAND
KW  - PATIENT
KW  - DNA
UR  - https://doi.org/10.1371/journal.ppat.1009654
N2  - 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. Author summaryLeishmania parasites are causative agents of leishmaniasis, a disease affecting millions of humans worldwide. It is widely accepted that these flagellates are transmitted exclusively by phlebotomine sand flies (Diptera: Phlebotominae). Reservoir hosts and insect vectors for the newly established Leishmania subgenus Mundinia, however, remain poorly understood. Preliminary evidence from field-based studies discovered biting midges (Diptera: Ceratopogonidae) that were naturally infected by L. (Mundinia) macropodum in Australia. This surprising finding led us to carry out a detailed laboratory study aimed at comparison of the development of all currently known species of the subgenus Mundinia in both putative vector families. We found that all five Mundinia species developed successfully in C. sonorensis and the successful transmission of three Mundinia species from infected insects to mice was demonstrated for the first time. This is the first detailed in vivo evidence that biting midges can act as competent vectors of Leishmania parasites of the subgenus Mundinia and has considerable epidemiological implications for control of these neglected pathogens.
ER  -

BECVAR, Tomas, Barbora VOJTKOVA, Padet SIRIYASATIEN, Jan VOTYPKA, David MODRÝ, Petr JAHN, Paul BATES, Simon CARPENTER, Petr VOLF and Jovana SADLOVA. Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae). \textit{PLoS Pathogens}. San Francisco: Public Library of Science, 2021, vol.~17, No~6, p.~''e1009654'', 18 pp. ISSN~1553-7366. Available from: https://dx.doi.org/10.1371/journal.ppat.1009654.

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