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

doi:10.1016/j.antiviral.2017.05.010

Antiviral Research

Volume 144, August 2017, Pages 93-119

https://doi.org/10.1016/j.antiviral.2017.05.010 Get rights and content

Highlights

•
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.

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.

Section snippets

Scope of this review

This manuscript is part of a series of reviews that aims to cover all published research on Crimean-Congo hemorrhagic fever (CCHF), a frequently severe disease produced by Crimean-Congo hemorrhagic fever virus (CCHFV; family Bunyaviridae, genus Nairovirus). Previous reviews have focused on epidemiology, molecular characterization, seroepidemiological studies, and the role of wild and domestic vertebrate animals in CCHFV maintenance and amplification of the infection (Bente et al., 2013,

Epidemiology of Crimean-Congo hemorrhagic fever

Among the tick-borne viruses, CCHFV is the most important cause of severe and fatal human hemorrhagic disease. CCHF has a variable case fatality rate of 3% to over 50%. However, based on improved diagnostic capabilities and data from cases in Turkey in the last decade, it is likely that the range is much smaller and the higher rates reflect a failure to recognize less severe infections in smaller outbreaks (Bente et al., 2013). No evidence of disease has been detected in animals naturally

Studies on the role of ticks in the maintenance and transmission of CCHFV

A variety of studies have investigated the role of ticks in the ecology of CCHFV. Data from these studies fall into three categories:

•
studies of unengorged ticks collected during questing, or using eggs laid by engorged females;
•
studies of ticks collected feeding on hosts; and
•
experimental tick infection studies in the laboratory.

Each approach presents limitations in our ability to interpret the data for formulating conclusions on reservoir and/or vector status of a tick species. Specifically,

Relative roles of tick species in maintenance and transmission

The geographic distribution of CCHFV overlaps well with the known distribution of the ticks of the genus Hyalomma, and suggests that several species of the genus are naturally involved in its circulation. While CCHFV has been detected and/or isolated in non-Hyalomma species, such as Rhipicephalus, Dermacentor, and Ixodes, there is still little evidence that these ticks circulate the virus in nature or support an active focus. Rather, non-Hyalomma species may feed on the same host(s) as CCHFV

Conclusions

During recent years, new foci of CCHFV have been recognized in several parts of the world, including the Balkan countries, southwest Russia, the Middle East, India, Turkey, and southwestern Europe. Furthermore, the distribution of known tick vectors and reservoirs is expanding. For example, H. marginatum has been introduced into the UK (Jameson et al., 2012), Germany (Kampen et al., 2007), and the Netherlands (Nijhof et al., 2007). Permanent populations of H. marginatum have yet to establish in

Basic rules to demonstrate vectorial ability

Researchers must adhere to a set of basic procedures to demonstrate the vectorial ability of a species of tick:

1.
ticks must be fed on infected natural hosts, and not exposed to virus through intracoelomic, immersion, or intra-anal inoculation;
2.
following feeding, virus must be detected in molted ticks from the feeding batch;
3.
infected ticks must then be allowed to feed on naive hosts that the particular tick species investigated would feed on in nature;
4.
virus must then be found in those hosts and;
5.

Financial support

This work was partially supported by UTMB's National Biocontainment Training Center Fellowship Program [to A.G.] and an appointment to the Research Participation Program at the Centers for Disease Control and Prevention administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U.S. Department of Energy and CDC, and by the National Institutes of Health Loan Repayment Award [to J.R.S.].

The findings and conclusions in this report are those of

Acknowledgements

The authors would like to acknowledge Elizabeth Ervin for assistance with figures and Tatyana Klimova for assistance editing the manuscript.

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

Highlights

Abstract

Section snippets

Scope of this review

Epidemiology of Crimean-Congo hemorrhagic fever

Studies on the role of ticks in the maintenance and transmission of CCHFV

Relative roles of tick species in maintenance and transmission

Conclusions

Basic rules to demonstrate vectorial ability

Financial support

Acknowledgements

Antivir. Res.

Curr. Opin. Virol.

Mol. Phylogenet. Evol.

Virology

Trends Microbiol.

Clin. Microbiol. Infect.

Lancet Infect. Dis.

Curr. Opin. Virol.

Antivir. Res.

Res. Virol.

Res. Virol.

Adv. Parasitol.

Ticks Tick. Borne Dis.

Crimean-Congo hemorrhagic fever virus in livestock ticks and animal handler seroprevalence at an abattoir in Ghana

BMC Infect. Dis.

Molecular detection of Crimean-Congo haemorrhagic fever virus (CCHFV) but not West Nile virus (WNV) in hard ticks from provinces in northern Turkey

Zoonoses Public Hlth

An antigenic investigation of Crimean-Congo hemorrhagic fever virus (CCHFV) in hard ticks from provinces in northern Turkey

Trop. Anim. Health Prod.

Serosurvey and molecular detection of Crimean-Congo hemorrhagic fever virus (CCHFV) in northern Turkey

Trop. Anim. Health Prod.

The genus Hyalomma: VII. Redescription of all parasitic stages of H. (Euhyalomma) dromedarii and H. (E.) schulzei (Acari: Ixodidae)

J. Med. Entomol.

Investigation of Crimean hemorrhagic fever natural foci in south-eastern Turkmenia

Sb. Tr. Ekol. Virus

Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model

J. Virol. Nov.

On the problem of natural hosts of Crimean hemorrhagic fever virus in Astrakhan Region

Tr. Inst. Polio. Virusn. Entsefalitov Akad. Med. Nauk. SSSR

Study of susceptibility to Crimean hemorrhagic fever (CHF) virus in European and long-eared hedgehogs

Tezisy Konf. Vop. Med. Virus

Species diversity of ixodid ticks feeding on humans in Amasya, Turkey: seasonal abundance and presence of Crimean-Congo hemorrhagic fever virus

J. Med. Entomol.

Molecular epidemiology of African and Asian Crimean-Congo haemorrhagic fever isolates

Epidemiol. Infect.

Expression of heat shock proteins and subolesin affects stress responses, Anaplasma phagocytophilum infection and questing behaviour in the tick, Ixodes scapularis

Med. Vet. Entomol.

Isolation of CHF virus from Rhipicephalus rossicus and Dermacentor marginatus ticks in Rostov Oblast and Krasnodar region. Viral hemorrhagic fevers Crime hemorrhagic fever, Omsk hemorrhagic fever, hemorrhagic fever with Ren Syndr Chumakov

MP Tr. Inst. Polio Virus Entsef Akad. Med. Nauk. SSSR

La Fievre hemorragique de Crimee-Congo au Senegal

Bull. Soc. Pathol. Exot.

Congo virus from domestic livestock, African hedgehog, and arthropods in Nigeria

Am. J. Trop. Med. Hyg.

Co-evolutionary patterns of variation in small and large RNA segments of Crimean-Congo hemorrhagic fever virus

J. Gen. Virol.

Crimean-Congo hemorrhagic fever in the one-humped camel (Camelus dromedarius) in East and Northeast of Iran

J. Arthropod Borne Dis.

Crimean-Congo hemorrhagic fever virus in ticks from imported livestock

Egypt. Emerg. Infect. Dis.

A short story of the investigation of the virus of Crimean hemorrhagic fever

Tr. Inst. Polio. Virusn. Entsefalitov Akad. Med. Nauk. SSSR

On the results of investigations of the etiology and epidemiology of Crimean hemorrhagic fever in the USSR

Contribution to 30 years of investigation of Crimean hemorrhagic fever

Isolation and identification of Crimean hemorrhagic fever and West Nile fever viruses from ticks collected in Moldavia

Tr. Imt. Polio. Virusn. Entsifalitov Akad. Med. Nauk. SSSR

Host distributions do not limit the species ranges of most African ticks (Acari: ixodida)

Bull. Ent. Res.

Crimean-Congo hemorrhagic fever virus genomics and global diversity

J. Virol.

Replication and tissue tropisms of Crimean-Congo hemorrhagic fever virus in experimentally infected adult Hyalomma truncatum (Acari: Ixodidae)

J. Med. Entomol.

Transmission of Crimean-Congo hemorrhagic fever virus by Hyalomma impeltatum (Acari:Ixodidae) after experimental infection

J. Med. Entomol.

Experimental vector incompetence of a soft tick, Ornithodoros sonrai (Acari: Argasidae), for Crimean-Congo hemorrhagic fever virus

J. Med. Entomol.

Short report: duration of tick attachment required for transmission of powassan virus by deer ticks

Am. J. Trop. Med. Hyg.

Rapid risk assessment: crimean-Congo haemorrhagic fever in Spain. 8 Sept 2016