Hyalomma marginatum - Factsheet for experts

Factsheet
Hyalomma marginatum. Credit: Adam Cuerden

SPECIES NAME/ CLASSIFICATION: Hyalomma marginatum Koch, 1844

COMMON NAME/ SYNONYMS: Mediterranean Hyalomma;

OTHER NAMES IN USE: Hyalomma plumbeum Panzer, 1795 (mainly used in former Soviet countries) [3,18].

Hazard associated with tick species

Current issues 

Upsurge in Türkiye and parts of Russia

Prior to 2005 the proportion of Hyalomma marginatum ticks collected from previous studies in Türkiye did not exceed 5%. However in 2005, 74% of cattle were found infested with ticks, and 85% of ticks collected were Hyalomma marginatum [1]. 

Importation via migratory birds

Hyalomma marginatum is a common ectoparasite of passerine birds. Immatures remain attached for up to 26 days which enables their passive transport across continents [2-4] . Although it is likely that ticks on long-distance migrants are unable to establish, infested birds migrating short distances have a better chance of establishing new local populations (Vatansever, personal communication). 

Importation via livestock

Livestock are at particularly high risk of importing Hyalomma marginatum as they can support large infestations. It is not uncommon for up to 100 Hyalomma ticks to be found on one animal [5]. Tick control on imported livestock is rarely, if ever, performed. 

Ecological plasticity

Hyalomma marginatum ticks have a great capacity to support a wide range of temperature and humidity conditions [6]. The tick’s ability to adapt to a wide range of conditions and a variety of habitats including arid open, marsh and scrub make it extremely difficult to eradicate on a large scale [7]. 

Disease risk

Hyalomma marginatum is the main vector of Crimean-Congo haemorrhagic fever virus in Europe [8].

 

Geographical distribution

Current spread

Africa and Asia 

Hyalomma marginatum is widely distributed across North Africa and Asia where it is reported from Algeria, Armenia, Azerbaijan, Egypt, Ethiopia, Georgia, Iran, Iraq, Israel, Morocco, Sudan, Syria, Tunisia and Türkiye [3,7,9] .

Europe: Hyalomma marginatum is present in southern and eastern Europe, having been recorded in Albania, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, France, Greece, Italy, Kosovo, the former Yugoslav Republic of Macedonia, Moldova, Montenegro, Portugal, Romania, Russia, Serbia, Spain and Ukraine [3,7,9-11] .

Several sporadic records have also been reported for imported animals, humans, and migratory birds in Germany [12], Hungary [13], Russia [14], Finland [9], Netherlands [15] and the UK [4,16] but these do not represent established populations.

Potential for future spread 

Ectoparasites such as ticks have relatively little mobility by themselves, even Hyalomma marginatum. However, they can be transported over vast distances by their vertebrate hosts, in particular migratory birds and ungulates. Once attached to the skin of a host they may feed for a period of up to thirty days. It is the duration of attachment which enhances their ability for dispersal. Livestock in particular are at particularly high risk of importing ticks as they can support large infestations and it is not uncommon for up to 100 Hyalomma marginatum ticks to be found on one animal [5]. A study of ticks infesting migratory birds entering the UK found that 21% of ticks collected were Hyalomma marginatum [4]. The bird species most commonly infested with Hyalomma marginatum were Northern wheatear (Oenanthe oenanthe) and Whitethroat (Sylvia communis), with each positive bird harbouring 2‒5 nymphs. Hyalomma marginatum nymphs were also found singly on Sedge warbler (Acrocephalus schoenobaenus) and Common redstart (Phoenicurus phoenicurus).

Degradation of agricultural land leading to scrub encroachment has been identified as a risk factor for population explosions of Hyalomma marginatum, particularly when the land was previously cattle pasture [3].

Populations in the Mediterranean basin (southern Europe and North Africa) are currently considered to be regulated by rainfall and evapo-transpiration in summer. A decrease in both of these would be likely to have an impact on the available habitat for the tick and facilitate its spread towards northern latitudes. In contrast, populations in eastern Europe and the Caucasus are regulated by the minimum temperatures in late autumn. The low temperatures in late autumn force nymphs to overwinter engorged, with a subsequent high mortality rate. However, in regions where they currently survive, warmer autumns are allowing for the moulting of nymphs to adults, decreasing the mortality of the population and enabling gradual spread into suitable neighbouring territories [9]. Models of the distribution of Hyalomma marginatum under climate warming scenarios predict that these ticks would be supported in some sites where they are currently absent, although some areas where the tick is now present would become unsuitable habitat under the same scenarios [35]. The regions that showed the greatest probability of colonisation were Italy, south of the Alps, the Balkans, Romania, Ukraine, Moldova, wide areas of southern Russia and some areas of Germany and the Netherlands [35].

Livestock from the Balkans have previously been highlighted as a risk factor for importing Hyalomma marginatum into western Europe [9].

Entomology

SPECIES NAME/CLASSIFICATION: Hyalomma marginatum Koch, 1844

Under the genus Hyalomma Koch, 1844, Hyalomma (Euhyalomma) marginatum Koch 1844 was previously considered to be a complex grouping four subspecies: Hyalomma (E.) marginatum marginatum Koch, 1844; Hyalomma (E.) marginatum rufipes Koch 1844; Hyalomma (E.) marginatum turanicum Pomerantzev, 1946 and Hyalomma (E.) marginatum isaaci Sharif, 1928 [17].

In 2008, Apanaskevich & Horak re-evaluated this taxonomic classification leading to the re-establishment of Hyalomma rufipes, H. turanicum and H. isaaci as full species and H. marginatum no longer being referred to as H. m. marginatum.

COMMON NAME/SYNONYMS: Mediterranean Hyalomma;

OTHER NAMES IN USE: Hyalomma plumbeum Panzer, 1795 (mainly used in former Soviet countries) [3,18].

SUGGESTED IDENTIFICATION KEYS: A recent comprehensive taxonomic re-evaluation of the ‘marginatum’ group of Hyalomma ticks was published by Apanaskevich and Horak [3,18]. Useful information can also be found in [10,19-21]

 

Morphological characteristics/similar species

Hyalomma rufipes (distinguishable by dense punctuations, dense circumspiracular setae, and shape of the spiracular plate); Hyalomma turanicum (distinguishable by moderately dense punctuations, circumspiracular setae, and shape of the spiracular plate). 

 

Biology

Life cycle 

Hyalomma marginatum is a ditropic tick, meaning that engorged larvae remain on the same host to moult and feed again as nymphs. Adults seek and feed on a second host individual following a period of diapause [21]. All stages are generally most active in the summer months [3,22] .

Immatures

Active between June and October with peak numbers in July and August [23,24]. After feeding, the immatures either i) detach in early summer, moult to adults during the same season and overwinter as an adult or ii) those that feed in late summer detach in September/October and overwinter as nymphs, moulting to adults the following spring. However, the former is more common. 

Adults

Adult ticks become active in spring when average monthly temperatures reach 10.5°C. They actively seek/wait for a host when average daily temperatures are 22‒27°C and humidity is 75‒100%. When air temperature increases above 30°C and soil temperature above 45°C, ticks prefer to hide or even bury themselves in the soil [23,25]. Males and females mate on the host, with one male mating with many females over several weeks. Engorged females drop off the host, lay up to 7 000 eggs in soil and die. Larvae hatch after 20‒40 days [22,26] .

Voltinism

Usually there is a maximum of one generation per year [3,19,22] .

Host preferences

Host seeking

In contrast to Ixodes spp. that passively wait for a passing host at an elevated location in vegetation, Hyalomma sp. actively seek their hosts [3,23,27] .

Adults

Adults of Hyalomma ticks prefer to feed on large animals (Artyodactyla and Perissodactyla). Adult Hyalomma ticks hide on the ground and actively run toward an animal host when they sense certain signals including vibration, visual objects, carbon dioxide, ammonia or body temperature heat. They can visually recognise the host from 3‒4 metres up to 9 metres [7,27]. Adults of Hyalomma asiaticum can follow the host for ten minutes or more and during that time they walk/run a distance of up to 100 metres [27,28] . Similar observations have also been recorded for Hyalomma marginatum (Vatansever, personal communication).

Immatures

Immature stages preferably feed on small mammals such as Lagomorpha (Leporidae) and Insectivora (Erinaceidae) and ground-foraging birds, especially in the orders Passeriformes (Alaudidae and Corvidae) and Galliformes (Phasianidae) [23,24,29] They do not like to feed on rodents [22,26] . The immatures feed for two to three weeks with a resting period of three weeks to several months if they overwinter [3,19].

Feeding sites

On birds and small-medium-sized wild mammals Hyalomma marginatum ticks congregate around the head, in particular in and around the ears [3]. On hares, larvae first attach to the margins of the ears and after moulting to nymphs they migrate towards the face, neck and around the eyes (Z Vatansever, personal communication). As well as attaching to humans, adults are especially common on cattle and other ungulates including horses, sheep, goats, camels, deer and wild boar feeding for one to two weeks and mating on the host. On ruminants Hyalomma marginatum ticks congregate around the hind quarters, in particular the udder, scrotum, inguinal area and perineum [30].

Habitat

Hyalomma marginatum ticks prefer the Mediterranean climate of North Africa and southern Europe with low to moderate levels of humidity and a long dry season during the summer months. Both immature and adult stages are characteristically found in steppe, savannah and scrubland hill and valley biotypes [3,9,10,19] . They are absent from contemporary and former European deciduous and mixed forest biotypes where they are replaced chiefly by Ixodes ricinus, and Dermacentor marginatus [3].

 

Environmental thresholds/constraints/development criteria

Environmental/climatic thresholds

Adults are active at temperatures of >12°C [31,32] and larvae between 14‒16°C. Established populations are currently only maintained when the yearly accumulation of temperatures falls between 3 000‒4 000°C and water vapour deficit is below an average of 15 hPa [32]. Cuticle hardening: larva-nymph five days, nymph-adult eigh8 days [23,32,33] . Feeding period: larva/nymph 26 days, adults 14 days [32].

Overwintering

Engorged nymphs and unfed adults are capable of overwintering, however mortality rates are increased for engorged nymphs compared to unfed adults [22-24,26] . Populations are reported as surviving at temperatures down to -20°C in Russia. Below this, population crashes have been reported [3].

Dispersal range

Hyalomma ticks have well-developed eyes which are the main receptor for finding hosts and hiding places. In contrast to ambushing ticks such as Ixodes spp., they can migrate long distances horizontally. For example, Hyalomma asiaticum can migrate up to 500 metres in a month, but usually they disperse in a 80‒100m radius [34].

 

Epidemiology and transmission of pathogens

Vector status 

Hyalomma marginatum is considered to be the most important vector of Crimean-Congo haemorrhagic fever virus in Eurasia [3,8]. Rickettsia aeschlimannii has been isolated from Hyalomma marginatum ticks imported into Germany, Hungary and Russia on migratory birds [13,14,36] . This bacterium has also been detected in Hyalomma marginatum collected in Cyprus [37], and on the Italian island of Pianosa, an important stopping site for migratory birds [38]. Dhori virus [39], Bahig virus [40] and Matruh virus [41] have also been isolated from this tick species; however, its vectorial capacity is yet to be determined.

Crimean-Congo haemorrhagic fever virus

Role

Main vector and reservoir. Crimean-Congo haemorrhagic fever virus is maintained in the tick population by trans-stadial and trans-ovarial transmission with co-feeding and venereal transmission demonstrated for other Hyalomma spp. [42].

Clinical features

Infection in animals, other than suckling mice, is asymptomatic whereas in humans CCHFV is able to induce a severe multisystem syndrome associated with fever, shock and haemorrhage [43]. Typically, the clinical course follows four distinct phases: incubation, pre-haemorrhagic, haemorrhagic and convalescence.

Confirmed disease risk

Crimean-Congo haemorrhagic fever virus is considered to be an emerging pathogen in Europe and the distribution of known tick vector species currently far exceeds that of the virus. The seasonality of human cases corresponds with the main tick activity period (spring to summer). The risk of migratory birds importing CCHFV via ticks is predicted to be very low [44]. In the last decade Crimean-Congo haemorrhagic fever virus has been recognised as a growing problem in Eurasia, affecting several eastern European countries (Albania, Bulgaria, Kosovo and Russia), including the emergence of human clinical cases in Türkiye (2002), Greece (2008), Georgia (2009) and most recently in 2010, India. Seroprevalence studies have also found evidence for virus circulation in Hungary [45], Portugal [46] and most recently Romania [47]. Crimean-Congo haemorrhagic fever virus has been directly detected in Hyalomma marginatum collected in Türkiye [48-50] , Bulgaria [51] and Spain [52].

 

Public health (surveillance and control)

Collection techniques
 

Traditional flagging or dragging techniques suitable for many other ixodid ticks are less effective for hunter ticks such as Hyalomma marginatum. Instead, ticks can be collected directly from hosts while feeding or while seeking a host (collected from the ground).

Control methods

To reduce contact with human populations clearing areas where ticks may survive and rest (i.e. haystacks, brush piles, leaf litter, etc.) has some benefits [9]. However, Hyalomma marginatum ticks are particularly widespread in open lands, crop fields and scrub, which makes the use of area-wide acaricides unfeasible. It seems that the most effective way to control Hyalomma marginatum populations is periodical use of acaricides on ruminants.

The main groups of acaricides used for tick control (mainly targeted at livestock or livestock housing) are: pyrethroids, benzol-phenyl ureas, macrocyclic lactones, spinosad and fipronil [9]. Options for use include dipping tanks, spray races or hand-held sprays, pour-ons, spot-ons and grease formulas for targeted application [7].

Humans can take measures for general tick avoidance, including wearing protective clothing and using chemical tick repellent such as permethrin or deltamethrin. It should be kept in mind that preparations that are effective against other ticks (Ixodes) are less effective against Hyalomma ticks. Sometimes they can stimulate attachment response in Hyalomma ticks [53] Z. Vatansever, personal communication) [54].

Current areas of uncertainty

There is little research on the level of resistance of Hyalomma marginatum populations to regularly used acaricides.

There is some evidence to suggest that subpopulations of this tick species have adapted to individual climate niches [9] - further research is required to explore whether such variations will affect future spread.

The reason or combination of reasons which led to such a large population increase in Türkiye in the late 1990s/early 2000s are still being debated. We know that in places where Crimean-Congo haemorrhagic fever occurs there is an increase in Hyalomma marginatum population and therefore human-tick contact. However, the reasons for this increase are still unknown and at the present time we can only speculate. These scenarios include:

  1. Increase in wild animal population: personal observations support the fact that hare and wild boar populations have increased in Crimean-Congo haemorrhagic fever areas. Local predator-prey cycle imbalance has also been suggested as raising the risk of transmission [55].
  2. Agricultural practice and migration: Focused in areas where agriculture is still practised with primitive tools and mostly based on human efforts (e.g. where the whole family is engaged in harvesting). Similarly, in places where there has been a migration towards the main urban centres, leaving abandoned land suitable for wildlife and scrub formation. This can also be affected by changes in land use resulting from changes in crop importation levels, thus reducing the need for locally grown crops, with the land subsequently returning to tick-suitable grassland [55].
  3. Changes in animal husbandry and environmental regulations: In Türkiye, the sheep population in the area has decreased by about 60-70% since 1990. Ministry of Environment regulations now strictly prohibit grazing of sheep and goat in bush and forests.
    1. Decrease in sheep population may influence the increase in hare and ground-feeding bird population [56,57] [57].
    2. Decrease in sheep population may have led to changes in tick composition (e.g. shift from Rhipicephalus to Hyalomma)

References

1. Vatansever Z, Uzun R, Estrada-Peña A, Ergonul O. Crimean-Congo haemorrhagic fever in Turkey. In: Ergonul O, Whitehouse CA, editors. Crimean-Congo hemorrhagic fever: A global perspective Dordrecht: Springer; 2007.

2. Kaiser MN, Hoogstraal H, Watson GE. Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bull Entomol Res. 1974;64:97-110.

3. Hoogstraal H. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 1979 May 22;15(4):307-417.

4. Jameson LJ, Morgan PJ, Medlock JM, Watola G, Vaux AG. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks Tick Borne Dis. 2012 Apr;3(2):95-9.

5. Estrada-Pena A, Jameson L, Medlock J, Vatansever Z, Tishkova F. Unraveling the ecological complexities of tick-associated Crimean-Congo hemorrhagic fever virus transmission: a gap analysis for the western Palearctic. Vector Borne Zoonotic Dis. 2012 Sep;12(9):743-52.

6. Bouattour A, Darghouth MA, Daoud A. Distribution and ecology of ticks (Acari: Ixodidae) infesting livestock in Tunisia: an overview of eighth years field collections. Parassitologia. 1999 Sep;41 Suppl 1:5-10.

7. Latif AA, Walker AR. An introduction to the biology and control of ticks in Africa. International Consortium on ticks and tick borne diseases, 2004.

8. Ergonul O, Whitehouse CA. Crimean-Congo hemorrhagic fever: A global perspective. Dordrecht: Springer; 2007.

9. EFSA. Scientific opinion on the role of tick vectors in the epidemiology of Crimean-Congo hemorrhagic fever and African swine fever in Eurasia. . EFSA J. 2010;8(8):1703.
10. Estrada-Peña A, Bouattour A, Camicas JL, Walker AR. Ticks of domestic animals in the Mediterranean region. A guide to the Identification of species. . International Consortium on ticks and tick borne diseases (ICTTD-2). INCO-DEV Programme, European Union, 2004.

11. ECDC. Vector distribution maps Stockholm: European Centre for Disease Prevention and Control; 2013. Available from: http://www.ecdc.europa.eu/en/healthtopics/vectors/vector-maps/Pages/VBORNET-maps-tick-species.aspx.

12. Kampen H, Poltz W, Hartelt K, Wolfel R, Faulde M. Detection of a questing Hyalomma marginatum marginatum adult female (Acari, Ixodidae) in southern Germany. Exp Appl Acarol. 2007;43(3):227-31.

13. Hornok S, Csorgo T, de la Fuente J, Gyuranecz M, Privigyei C, Meli ML, et al. Synanthropic birds associated with high prevalence of tick-borne rickettsiae and with the first detection of Rickettsia aeschlimannii in Hungary. Vector Borne Zoonotic Dis. 2013 Feb;13(2):77-83.

14. Movila A, Alekseev AN, Dubinina HV, Toderas I. Detection of tick-borne pathogens in ticks from migratory birds in the Baltic region of Russia. Med Vet Entomol. 2013 Mar;27(1):113-7.

15. ICTTD. Newsletter on ticks and tick-borne diseases of livestock in the tropics, October. No. 37: ICTTD; 2008.

16. Jameson LJ, Medlock JM. Tick surveillance in Great Britain. Vector Borne Zoonotic Dis. 2011 Apr;11(4):403-12.

17. Horak IG, Camicas JL, Keirans JE. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. Exp Appl Acarol. 2002;28(1-4):27-54.
18. Apanaskevich DA, Horak IG. The genus Hyalomma Koch, 1844: V. re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species (Acari : Ixodidae) with redescription of all parasitic stages and notes on biology. Int J Acarol. 2008 Mar;34(1):13-42.

19. Pomerantzev BI. Ixodid ticks (Ixodidae). . In: Anastos G, editor. Fauna of USSR volume IV, no 2. Washington: The American Institute of Biological Sciences; 1959.
20. Feldman-Muhsam B. Revision of the genus Hyalomma. I. Description of Koch's types. . Bull Res Council Israel. 1954;4:150-70.

21. Walker A, Bouattour A, Camicas JL, Estrada-Pena A, Horak IG, Latif AA. Ticks of domestic animals in Africa. A guide to the identification of species. International Consortium on ticks and tick borne diseases (ICTTD-2). INCO-DEV Programme, European Union, 2003.

22. Kotti BK, Shaposhnikova LI, Evchenko Iu M, Levchenko BI, Surkhaev DB, Korzhov PN, et al. [Hyalomma marginatum Koch in Stavropol' region]. Zh Mikrobiol Epidemiol Immunobiol. 2001 Nov-Dec(6 Suppl):105-8.

23. Emelianova IN. [Ecology of the tick genus Hyalomma Koch 1844 (Acarina: Ixodidae) in Central Caucasus and adjacent territories]. Stavropol2006.

24. Emelianova IN. Hyalomma Koch, 1844 (ACARI: IXODIDAE) ticks of Central Precaucasia and surrounding territories. (Distribution, ecology, role in the natural foci of Crimean-Congo heamorrhagic fever) [MSc]. Stavropol: State University of Stavropol; 2006.

25. Tokhov Iu M. [Faunistic complex of Ixodidae in Stavropol Region: Dissemination, epizootic and epidemiologic value, control measures] Stavropol: Anti-plaque Institute, 2009.

26. Kotti BK, Shaposhnikova LI, Evchenko Iu M, Levchenko BI, Surkhaev DB, Korzhov PN, et al. [Hyalomma marginatum Koch in Stavropol' region]. Zh Mikrobiol Epidemiol Immunobiol. 2001 Nov-Dec(6 Suppl):105-8.

27. Romanenko VN. [Visual potentialities of the tick Hyalomma asiaticum asiaticum (Ixodidae)]. Parazitologiia. 2005 May-Jun;39(3):186-90.

28. Romanenko VN. Ecological bases of ethology of pasture ticks (Parasitiformes, Ixodidae) in finding and attacking hosts (Экологические основы этологии пастбищных иксодовых клещей (Parasitiformes, Ixodidae) при поиске и нападении на прокормителей). (In Russian). Bulletin of Tomsk State University (Вестник Томского государственного университета). 2007 (298):224-8.

29. Apanaskevich DA. [Host-parasite relationships of the genus Hyalomma Koch, 1844 (Acari, Ixodidae) and their connection with microevolutionary process]. Parazitologiia. 2004 Nov-Dec;38(6):515-23.

30. Papadopoulos B, Morel PC, Aeschlimann A. Ticks of domestic animals in the Macedonia region of Greece. Vet Parasitol. 1996 May;63(1-2):25-40.

31. Enigk K, Grittner I. [The rearing and biology of ticks]. Z Parasitenkd. 1953;16(1):56-83.

32. Estrada-Pena A, Martinez Aviles M, Munoz Reoyo MJ. A population model to describe the distribution and seasonal dynamics of the tick Hyalomma marginatum in the Mediterranean Basin. Transbound Emerg Dis. 2011 Jun;58(3):213-23.

33. Hueli LE. Estudio del ciclo biologico de Hyalomma marginatum marginatum Koch. 1844 (Acarina:Ixodidae) bajo, condiciones estandar de laboratorio. Rev Iber Parasitol. 1979;39:143-52.

34. Romanenko VN. Ecological bases of ethology of pasture ticks (Parasitiformes, Ixodidae) in finding and attacking hosts Bull Tomsk State Univ. 2007:224-8.

35. Estrada-Pena A, Sanchez N, Estrada-Sanchez A. An assessment of the distribution and spread of the tick Hyalomma marginatum in the western Palearctic under different climate scenarios. Vector Borne Zoonotic Dis. 2012 Sep;12(9):758-68.

36. Rumer L, Graser E, Hillebrand T, Talaska T, Dautel H, Mediannikov O, et al. Rickettsia aeschlimannii in Hyalomma marginatum ticks, Germany. Emerg Infect Dis. 2011 Feb;17(2):325-6.

37. Chochlakis D, Ioannou I, Sandalakis V, Dimitriou T, Kassinis N, Papadopoulos B, et al. Spotted fever group Rickettsiae in ticks in Cyprus. Microb Ecol. 2012 Feb;63(2):314-23.

38. Tomassone L, Grego E, Auricchio D, Iori A, Giannini F, Rambozzi L. Lyme borreliosis spirochetes and spotted fever group rickettsiae in ixodid ticks from Pianosa island, Tuscany Archipelago, Italy. Vector Borne Zoonotic Dis. 2013 Feb;13(2):84-91.

39. Filipe AR, Casals J. Isolation of Dhori virus from Hyalomma marginatum ticks in Portugal. Intervirology. 1979;11(2):124-7.

40. Converse JD, Hoogstraal H, Moussa MI, Stek M, Jr., Kaiser MN. Bahig virus (Tete group) in naturally- and transovarially-infected Hyalomma marginatum ticks from Egypt and Italy. Arch Gesamte Virusforsch. 1974;46(1-2):29-35.

41. Moussa MI, Imam IZ, Converse JD, El-Karamany RM. Isolation of Matruh virus from Hyalomma marginatum ticks in Egypt. J Egypt Public Health Assoc. 1974;49(6):341-8.

42. Turell MJ. Role of ticks in transmission of Crimean-Congo haemorrhagic fever virus. . In: Ergonul O, Whitehouse CA, editors. Crimean-Congo hemorrhagic fever: A global perspective. Dordrecht: Springer; 2007.

43. Beeching NJ, Fletcher TE, Hill DR, Thomson GL. Travellers and viral haemorrhagic fevers: what are the risks? Int J Antimicrob Agents. 2010 Nov;36 Suppl 1:S26-35.

44. Gale P, Stephenson B, Brouwer A, Martinez M, de la Torre A, Bosch J, et al. Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds. J Appl Microbiol. 2012 Feb;112(2):246-57.

45. Horvath LB. Precipitating antibodies to Crimean haemorrhagic fever virus in human sera collected in Hungary. Acta Microbiol Acad Sci Hung. 1976;23(4):331-5.

46. Filipe AR, Calisher CH, Lazuick J. Antibodies to Congo-Crimean haemorrhagic fever, Dhori, Thogoto and Bhanja viruses in southern Portugal. Acta Virol. 1985 Jul;29(4):324-8.

47. Ceianu SC, Raluca P, Daniel C, Lonut C, Aurelia I, Cristian I, et al., editors. Serological evidence for the circulation of the Crimean-Congo haemorrhagic fever virus in Romania. Annual meeting ArboZooNet; 2009; St Raphael, France.

48. Hekimoglu O, Ozer N, Ergunay K, Ozkul A. Species distribution and detection of Crimean Congo Hemorrhagic Fever Virus (CCHFV) in field-collected ticks in Ankara Province, Central Anatolia, Turkey. Exp Appl Acarol. 2012 Jan;56(1):75-84.

49. Tekin S, Bursali A, Mutluay N, Keskin A, Dundar E. Crimean-Congo hemorrhagic fever virus in various ixodid tick species from a highly endemic area. Vet Parasitol. 2012 May 25;186(3-4):546-52.

50. Yesilbag K, Aydin L, Dincer E, Alpay G, Girisgin AO, Tuncer P, et al. Tick survey and detection of Crimean-Congo hemorrhagic fever virus in tick species from a non-endemic area, South Marmara region, Turkey. Exp Appl Acarol. 2013 Jun;60(2):253-61.

51. Gergova I, Kunchev M, Kamarinchev B. Crimean-Congo hemorrhagic fever virus-tick survey in endemic areas in Bulgaria. J Med Virol. 2012 Apr;84(4):608-14.

52. Estrada-Pena A, Palomar AM, Santibanez P, Sanchez N, Habela MA, Portillo A, et al. Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010. Emerg Infect Dis. 2012 Jan;18(1):179-80.

53. Fryauff DJ, Shoukry MA, Schreck CE. Stimulation of attachment in a camel tick, Hyalomma dromedarii (Acari: Ixodidae): the unintended result of sublethal exposure to permethrin-impregnated fabric. J Med Entomol. 1994 Jan;31(1):23-9.

54. Fryauff DJ, Shoukry MA, Schreck CE. Stimulation of attachment in a camel tick, Hyalomma dromedarii (Acari: Ixodidae): the unintended result of sublethal exposure to permethrin-impregnated fabric. J Med Entomol. 1994 Jan;31(1):23-9.

55. Jameson LJ, Ramadani N, Medlock JM. Possible drivers of Crimean-Congo hemorrhagic fever virus transmission in Kosova. Vector Borne Zoonotic Dis. 2012 Sep;12(9):753-7.

56. Fuller RJ, Gough SJ. Changes in sheep numbers in Britain: implications for bird populations. Biol Conserv. 1999 Nov;91(1):73-89.

57. Smith RK, Jennings NV, Robinson A, Harris S. Conservation of European hares Lepus europaeus in Britain: is increasing habitat heterogeneity in farmland the answer? J Appl Ecol. 2004 Dec;41(6):1092-102.