Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions

Abstract Background Bovine ephemeral fever virus (Rhabdoviridae: Ephemerovirus) (BEFV) causes bovine ephemeral fever (BEF), an economically important disease of cattle and water buffalo. Outbreaks of BEF in Africa, Australia, Asia and the Middle East are characterized by high rates of morbidity and...

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Main Authors: Jessica E. Stokes, Karin E. Darpel, Simon Gubbins, Simon Carpenter, María del Mar Fernández de Marco, Luis M. Hernández-Triana, Anthony R. Fooks, Nicholas Johnson, Christopher Sanders
Format: Article
Language:English
Published: BMC 2020-11-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04485-5
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author Jessica E. Stokes
Karin E. Darpel
Simon Gubbins
Simon Carpenter
María del Mar Fernández de Marco
Luis M. Hernández-Triana
Anthony R. Fooks
Nicholas Johnson
Christopher Sanders
author_facet Jessica E. Stokes
Karin E. Darpel
Simon Gubbins
Simon Carpenter
María del Mar Fernández de Marco
Luis M. Hernández-Triana
Anthony R. Fooks
Nicholas Johnson
Christopher Sanders
author_sort Jessica E. Stokes
collection DOAJ
description Abstract Background Bovine ephemeral fever virus (Rhabdoviridae: Ephemerovirus) (BEFV) causes bovine ephemeral fever (BEF), an economically important disease of cattle and water buffalo. Outbreaks of BEF in Africa, Australia, Asia and the Middle East are characterized by high rates of morbidity and highly efficient transmission between cattle hosts. Despite this, the vectors of BEFV remain poorly defined. Methods Colony lines of biting midges (Culicoides sonorensis) and mosquitoes (Aedes aegypti, Culex pipiens and Culex quinquefasciatus) were infected with a strain of BEFV originating from Israel by feeding on blood–virus suspensions and by intrathoracic inoculation. In addition, in vivo transmission of BEFV was also assessed by allowing C. sonorensis inoculated by the intrathoracic route to feed on male 6 month-old Holstein-Friesian calves. Results There was no evidence of BEFV replication within mosquitoes fed on blood/virus suspensions for mosquitoes of any species tested for each of the three colony lines. In 170 C. sonorensis fed on the blood/virus suspension, BEFV RNA was detected in the bodies of 13 individuals and in the heads of two individuals, indicative of fully disseminated infections and an oral susceptibility rate of 1.2%. BEFV RNA replication was further demonstrated in all C. sonorensis that were inoculated by the intrathoracic route with virus after 5, 6 or 7 days post-infection. Despite this, transmission of BEFV could not be demonstrated when infected C. sonorensis were allowed to feed on calves. Conclusions No evidence for infection or dissemination of BEFV (bovine/Israel/2005-6) in mosquitoes of three different species was found. Evidence was found for infection of C. sonorensis by the oral route. However, attempts to transmit BEFV to calves from infected C. sonorensis failed. These results highlight the challenge of defining the natural vector of BEFV and of establishing an in vivo transmission model. The results are discussed with reference to the translation of laboratory-based studies to inference of vector competence in the field. Graphic abstract
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spelling doaj.art-b648541409df4817aa63cb4fcdbc602f2022-12-21T19:04:11ZengBMCParasites & Vectors1756-33052020-11-0113111110.1186/s13071-020-04485-5Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditionsJessica E. Stokes0Karin E. Darpel1Simon Gubbins2Simon Carpenter3María del Mar Fernández de Marco4Luis M. Hernández-Triana5Anthony R. Fooks6Nicholas Johnson7Christopher Sanders8The Pirbright InstituteThe Pirbright InstituteThe Pirbright InstituteThe Pirbright InstituteVirology Department, Animal and Plant Health AgencyVirology Department, Animal and Plant Health AgencyVirology Department, Animal and Plant Health AgencyVirology Department, Animal and Plant Health AgencyThe Pirbright InstituteAbstract Background Bovine ephemeral fever virus (Rhabdoviridae: Ephemerovirus) (BEFV) causes bovine ephemeral fever (BEF), an economically important disease of cattle and water buffalo. Outbreaks of BEF in Africa, Australia, Asia and the Middle East are characterized by high rates of morbidity and highly efficient transmission between cattle hosts. Despite this, the vectors of BEFV remain poorly defined. Methods Colony lines of biting midges (Culicoides sonorensis) and mosquitoes (Aedes aegypti, Culex pipiens and Culex quinquefasciatus) were infected with a strain of BEFV originating from Israel by feeding on blood–virus suspensions and by intrathoracic inoculation. In addition, in vivo transmission of BEFV was also assessed by allowing C. sonorensis inoculated by the intrathoracic route to feed on male 6 month-old Holstein-Friesian calves. Results There was no evidence of BEFV replication within mosquitoes fed on blood/virus suspensions for mosquitoes of any species tested for each of the three colony lines. In 170 C. sonorensis fed on the blood/virus suspension, BEFV RNA was detected in the bodies of 13 individuals and in the heads of two individuals, indicative of fully disseminated infections and an oral susceptibility rate of 1.2%. BEFV RNA replication was further demonstrated in all C. sonorensis that were inoculated by the intrathoracic route with virus after 5, 6 or 7 days post-infection. Despite this, transmission of BEFV could not be demonstrated when infected C. sonorensis were allowed to feed on calves. Conclusions No evidence for infection or dissemination of BEFV (bovine/Israel/2005-6) in mosquitoes of three different species was found. Evidence was found for infection of C. sonorensis by the oral route. However, attempts to transmit BEFV to calves from infected C. sonorensis failed. These results highlight the challenge of defining the natural vector of BEFV and of establishing an in vivo transmission model. The results are discussed with reference to the translation of laboratory-based studies to inference of vector competence in the field. Graphic abstracthttp://link.springer.com/article/10.1186/s13071-020-04485-5VectorArbovirusCalvesCulicoidesAedesCulex
spellingShingle Jessica E. Stokes
Karin E. Darpel
Simon Gubbins
Simon Carpenter
María del Mar Fernández de Marco
Luis M. Hernández-Triana
Anthony R. Fooks
Nicholas Johnson
Christopher Sanders
Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
Parasites & Vectors
Vector
Arbovirus
Calves
Culicoides
Aedes
Culex
title Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
title_full Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
title_fullStr Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
title_full_unstemmed Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
title_short Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
title_sort investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions
topic Vector
Arbovirus
Calves
Culicoides
Aedes
Culex
url http://link.springer.com/article/10.1186/s13071-020-04485-5
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