Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds

Jameson, Lisa; Morgan, Peter J.; Medlock, Jolyon M.; Watola, George; Vaux, Alexander G.C.

doi:10.1016/j.ttbdis.2011.12.002

Cited by 127 publications

(92 citation statements)

References 21 publications

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“…Ticks of this species are found in Africa, southern Asia, and southern Europe (10,11); some specimens have been collected in northern European regions such as Germany or England (12,13). Birds are commonly parasitized by immature stages of H. marginatum, a 2-host tick that has the same host for larva and nymph stages.…”

Section: Discussionmentioning

confidence: 99%

“…A study conducted in England of CCHFV in ticks collected from migratory birds found negative real-time PCR results for CCHFV, although the parasitization rate of birds with H. marginatum ticks was low (13). In addition, a group of experts has reported that migratory birds may not be sufficient to establish new foci of CCHFV infection in Europe and may not represent a high risk for its implantation because adult ticks are necessary and immature specimens cannot find optimal climate conditions to molt in spring (10).…”

Section: Discussionmentioning

confidence: 99%

“…Autochthonous cases of CCHF have not been reported in southwestern Europe, and CCHFV has not been detected in ticks from migratory birds in Europe (13). However, some authors support the limited role of migratory birds harboring CCHFV-infected ticks for the establishment of the virus (10,15).…”

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Crimean-Congo Hemorrhagic Fever Virus in Ticks from Migratory Birds, Morocco1

Palomar¹,

Portillo²,

Santibáñez³

et al. 2013

Emerg. Infect. Dis.

125

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Crimean-Congo Hemorrhagic Fever Virus in Ticks from Migratory Birds, Morocco1

Palomar¹,

Portillo²,

Santibáñez³

et al. 2013

Emerg. Infect. Dis.

125

View full text Add to dashboard Cite

“…It has long been known that larvae and nymphs of ticks indigenous to the Mediterranean region and Africa can be found on birds returning to central and northern Europe from their winter migration. For example, investigators recently identified immature H. marginatum on several species of birds in the United Kingdom, and estimated that tens of thousands of such ticks arrive each spring (Jameson et al, 2012). Similarly, the African tick H. rufipes has been recovered from birds as far north as Norway (Hasle et al, 2009).…”

Section: Future Geographic Range and Incidence Of Cchfmentioning

confidence: 99%

Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity

et al. 2013

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Bente, Dennis A.; Forrester, Naomi L.; Watts, Douglas M.; McAuley, Alexander J.; Whitehouse, Chris A.; and Bray, Mike, "CrimeanCongo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity" (2013 b s t r a c tCrimean-Congo hemorrhagic fever (CCHF) is the most important tick-borne viral disease of humans, causing sporadic cases or outbreaks of severe illness across a huge geographic area, from western China to the Middle East and southeastern Europe and throughout most of Africa. CCHFV is maintained in vertical and horizontal transmission cycles involving ixodid ticks and a variety of wild and domestic vertebrates, which do not show signs of illness. The virus circulates in a number of tick genera, but Hyalomma ticks are the principal source of human infection, probably because both immature and adult forms actively seek hosts for the blood meals required at each stage of maturation. CCHF occurs most frequently among agricultural workers following the bite of an infected tick, and to a lesser extent among slaughterhouse workers exposed to the blood and tissues of infected livestock and medical personnel through contact with the body fluids of infected patients. CCHFV is the most genetically diverse of the arboviruses, with nucleotide sequence differences among isolates ranging from 20% for the viral S segment to 31% for the M segment. Viruses with diverse sequences can be found within the same geographic area, while closely related viruses have been isolated in far distant regions, suggesting that widespread dispersion of CCHFV has occurred at times in the past, possibly by ticks carried on migratory birds or through the international livestock trade. Reassortment among genome segments during co-infection of ticks or vertebrates appears to have played an important role in generating diversity, and represents a potential future source of novel viruses. In this article, we first review current knowledge of CCHFV, summarizing its molecular biology, maintenance and transmission, epidemiology and geographic range. We also include an extensive discussion of CCHFV genetic diversity, including maps of the range of the virus with superimposed phylogenetic trees. We then review the features of CCHF, including the clinical syndrome, diagnosis, treatment, pathogenesis, vaccine development and laboratory animal models of CCHF. The paper ends with a discussion of the possible future geographic range of the virus. For the benefit of researchers, we include a Supplementary Table listing all published reports of CCHF cases and outbreaks in the English-language literature, plus some principal articles in other languages, with total case numbers, case fatality rates and all CCHFV strains on GenBank.

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“…CCHFV has been isolated from H. marginatum and other Hyalomma ticks collected from migratory birds in Morocco and Turkey (3,4), and the ability of H. rufipes ticks to become infected from birds inoculated with the virus has been experimentally proven (24). Since Israel is situated at one of the largest migration routes in the world, where about 4% of the estimated 5 billion birds migrating from Africa to the Western Palearctic fly through every spring (25), it is suitable to identify which Hyalomma species are introduced into the country and determine their infection status, as was performed in other countries where yearly migratory events occur (26)(27)(28).…”

mentioning

confidence: 99%

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

Azagi

Klement

Perlman

et al. 2017

Appl Environ Microbiol

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Hyalomma ticks (Acari: Ixodidae) are hosts for Francisella-like endosymbionts (FLE) and may serve as vectors of zoonotic disease agents. This study aimed to provide an initial characterization of the interaction between Hyalomma and FLE and to determine the prevalence of pathogenic Rickettsia in these ticks. Hyalomma marginatum, Hyalomma rufipes, Hyalomma dromedarii, Hyalomma aegyptium, and Hyalomma excavatum ticks, identified morphologically and molecularly, were collected from different hosts and locations representing the distribution of the genus Hyalomma in Israel, as well as from migratory birds. A high prevalence of FLE was found in all Hyalomma species (90.6%), as well as efficient maternal transmission of FLE (91.8%), and the localization of FLE in Malpighian tubules, ovaries, and salivary glands in H. marginatum. Furthermore, we demonstrated strong cophylogeny between FLE and their host species. Contrary to FLE, the prevalence of Rickettsia ranged from 2.4% to 81.3% and was significantly different between Hyalomma species, with a higher prevalence in ticks collected from migratory birds. Using ompA gene sequences, most of the Rickettsia spp. were similar to Rickettsia aeschlimannii, while a few were similar to Rickettsia africae of the spotted fever group (SFG). Given their zoonotic importance, 249 ticks were tested for Crimean Congo hemorrhagic fever virus infection, and all were negative. The results imply that Hyalomma and FLE have obligatory symbiotic interactions, indicating a potential SFG Rickettsia zoonosis risk. A further understanding of the possible influence of FLE on Hyalomma development, as well as on its infection with Rickettsia pathogens, may lead to novel ways to control tick-borne zoonoses.IMPORTANCE This study shows that Francisella-like endosymbionts were ubiquitous in Hyalomma, were maternally transmitted, and cospeciated with their hosts. These findings imply that the interaction between FLE and Hyalomma is of an obligatory nature. It provides an example of an integrative taxonomy approach to simply differentiate among species infesting the same host and to identify nymphal and larval stages to be used in further studies. In addition, it shows the potential of imported Hyalomma ticks to serve as a vector for spotted fever group rickettsiae. The information gathered in this study can be further implemented in the development of symbiont-based disease control strategies for the benefit of human health.

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Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds

Cited by 127 publications

References 21 publications

Crimean-Congo Hemorrhagic Fever Virus in Ticks from Migratory Birds, Morocco1

Crimean-Congo Hemorrhagic Fever Virus in Ticks from Migratory Birds, Morocco1

Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

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