The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies

This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domesti...

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Bibliographic Details
Published in:Antiviral research Vol. 144; no. C; pp. 93 - 119
Main Authors: Gargili, Aysen, Estrada-Peña, Agustin, Spengler, Jessica R., Lukashev, Alexander, Nuttall, Patricia A., Bente, Dennis A.
Format: Journal Article
Language:English
Published: Netherlands Elsevier B.V 01.08.2017
Elsevier
Subjects:
Animals
Arthropod Vectors - virology
Disease Reservoirs
Disease Transmission, Infectious
Hemorrhagic Fever Virus, Crimean-Congo - isolation & purification
Hemorrhagic Fever, Crimean - transmission
Ticks - virology
ISSN:0166-3542, 1872-9096, 1872-9096
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Abstract This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research. •Hyalomma ticks are necessary to support the circulation of the CCHFV in natural foci.•Detection of CCHFV in feeding ticks does not discern the vectorial capacity of the tick.•There are basic rules that must be adhered to for experimental demonstration of the vectorial ability of a tick.•Investigation of CCHFV emergence and re-emergence requires consideration of tick, host, and environmental factors.
AbstractList This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research. •Hyalomma ticks are necessary to support the circulation of the CCHFV in natural foci.•Detection of CCHFV in feeding ticks does not discern the vectorial capacity of the tick.•There are basic rules that must be adhered to for experimental demonstration of the vectorial ability of a tick.•Investigation of CCHFV emergence and re-emergence requires consideration of tick, host, and environmental factors.
This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research.This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research.
This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research.
Author Lukashev, Alexander
Estrada-Peña, Agustin
Gargili, Aysen
Nuttall, Patricia A.
Spengler, Jessica R.
Bente, Dennis A.
AuthorAffiliation c Faculty of Health Sciences, Marmara University, Istanbul, Turkey
b Galveston National Laboratory, University of Texas Medical Branch, Galveston, TX, USA
a Department of Microbiology & Immunology, University of Texas Medical Branch, Galveston, TX, USA
h Department of Zoology, Oxford University, UK
f Chumakov Institute for Poliomyelitis and Viral Encephalitides, Moscow, Russia
g Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, Russia
e Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, USA
d Veterinary Faculty, University of Zaragoza, Zaragoza, Spain
AuthorAffiliation_xml – name: a Department of Microbiology & Immunology, University of Texas Medical Branch, Galveston, TX, USA
– name: d Veterinary Faculty, University of Zaragoza, Zaragoza, Spain
– name: c Faculty of Health Sciences, Marmara University, Istanbul, Turkey
– name: f Chumakov Institute for Poliomyelitis and Viral Encephalitides, Moscow, Russia
– name: b Galveston National Laboratory, University of Texas Medical Branch, Galveston, TX, USA
– name: e Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, USA
– name: h Department of Zoology, Oxford University, UK
– name: g Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, Russia
Author_xml – sequence: 1
  givenname: Aysen
  surname: Gargili
  fullname: Gargili, Aysen
  organization: Department of Microbiology & Immunology, University of Texas Medical Branch, Galveston, TX, USA
– sequence: 2
  givenname: Agustin
  orcidid: 0000-0001-7483-046X
  surname: Estrada-Peña
  fullname: Estrada-Peña, Agustin
  organization: Veterinary Faculty, University of Zaragoza, Zaragoza, Spain
– sequence: 3
  givenname: Jessica R.
  orcidid: 0000-0002-5383-0513
  surname: Spengler
  fullname: Spengler, Jessica R.
  organization: Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, USA
– sequence: 4
  givenname: Alexander
  surname: Lukashev
  fullname: Lukashev, Alexander
  organization: Chumakov Institute for Poliomyelitis and Viral Encephalitides, Moscow, Russia
– sequence: 5
  givenname: Patricia A.
  orcidid: 0000-0002-0385-8294
  surname: Nuttall
  fullname: Nuttall, Patricia A.
  organization: Department of Zoology, Oxford University, UK
– sequence: 6
  givenname: Dennis A.
  surname: Bente
  fullname: Bente, Dennis A.
  email: dabente@utmb.edu
  organization: Department of Microbiology & Immunology, University of Texas Medical Branch, Galveston, TX, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28579441$$D View this record in MEDLINE/PubMed
https://www.osti.gov/biblio/1550126$$D View this record in Osti.gov
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Snippet This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF...
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SubjectTerms Animals
Arthropod Vectors - virology
Disease Reservoirs
Disease Transmission, Infectious
Hemorrhagic Fever Virus, Crimean-Congo - isolation & purification
Hemorrhagic Fever, Crimean - transmission
Ticks - virology
Title The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies
URI https://dx.doi.org/10.1016/j.antiviral.2017.05.010
https://www.ncbi.nlm.nih.gov/pubmed/28579441
https://www.proquest.com/docview/1906144986
https://www.osti.gov/biblio/1550126
https://pubmed.ncbi.nlm.nih.gov/PMC6047067
Volume 144
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