First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden

Journal Pre-proof First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden Giulio Grandi, Lidia Chitimia-Dobler, Phimphanit Choklikitumnuey, Christina Strube, Andrea Springer, Ann Albihn, Thomas G.T. Jaenson, Anna Omazic

PII:

S1877-959X(19)30312-7

DOI:

https://doi.org/10.1016/j.ttbdis.2020.101403

Reference:

TTBDIS 101403

To appear in:

Ticks and Tick-borne Diseases

Received Date:

22 July 2019

Revised Date:

20 December 2019

Accepted Date:

27 January 2020

Please cite this article as: Grandi G, Chitimia-Dobler L, Choklikitumnuey P, Strube C, Springer A, Albihn A, Jaenson TGT, Omazic A, First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden, Ticks and Tick-borne Diseases (2020), doi: https://doi.org/10.1016/j.ttbdis.2020.101403

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First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden. Giulio Grandia,b*, Lidia Chitimia-Doblerc, Phimphanit Choklikitumnueya, Christina Strubed, Andrea Springerd, Ann Albihna,e, Thomas G.T. Jaensonf, Anna Omazice

Authors’ affiliations: a. Department of Biomedical Sciences and Veterinary Public Health (BVF), Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden ([email protected]; [email protected]) b. Department of Microbiology, National Veterinary Institute (SVA), Uppsala, Sweden

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c. Bundeswehr Institute of Microbiology, Munich, Germany; and Parasitology Unit, Institute of Zoology, University of Hohenheim, Stuttgart, Germany ([email protected]) d. Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany ([email protected]; [email protected])

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e. Department of Chemistry, Environment and Food Hygiene, National Veterinary Institute (SVA), Uppsala, Sweden ([email protected]; [email protected])

Giulio Grandi

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*Corresponding author:

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f. Medical Entomology Unit, Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden ([email protected])

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Swedish University of Agricultural Sciences (SLU) Department of Biomedical Sciences and Veterinary Public Health (BVF)

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Ulls väg 26, SE-757 56 Uppsala, Sweden Phone: +46 (0)18-67 23 98 Fax +46 (0)18-67 20 00 Email address: [email protected]

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Abstract From July 2018 to January 2019 we recorded 41 specimens of adult Hyalomma ticks, which had been found on horses, cattle or humans in 14 Swedish provinces. In 20 cases we received tick specimens, which were identified morphologically as adults of H. marginatum (n=11) or H. rufipes (n= 9). These are the first documented records in Sweden of adults of H. marginatum and H. rufipes. Molecular tests for Crimean-Congo haemorrhagic fever virus and piroplasms (Babesia spp. and Theileria spp.) proved negative; 12 out of 20 tested specimens were positive for rickettsiae (R. aeschlimannii was identified in 11 of the ticks). All ticks originated from people or animals that had not been abroad

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during the previous two months. These data suggest (i) that the adult Hyalomma ticks originated from immature ticks, which had been brought from the south by migratory birds arriving in Sweden during spring or early summer; and that (ii) due to the exceptionally warm summer of 2018 these immature

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ticks had been able to develop to the adult stage in the summer and/or autumn of the same year. The rapidly changing climate most likely now permits these two Hyalomma species to develop to the

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adult, reproductive stage in northern Europe. There is consequently a need to revise the risk maps on the potential geographic occurrence of relevant tick species and related tick-borne pathogens in

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Sweden and in the neighbouring countries.

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Introduction

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Keywords: Hyalomma, climate change, CCHFV, Rickettsia, Sweden

The tick species Hyalomma marginatum is often referred to as the Mediterranean Hyalomma and its

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close relative H. rufipes as the hairy Hyalomma or the coarse-legged Hyalomma (Estrada-Peña et al.2017). H. marginatum is mainly distributed in southern Europe, northern Africa and parts of Asia (Santos-Silva and Vatansever, 2017). H. rufipes inhabits parts of the Sahel and the drier areas south of the Sahara, and areas around the Red Sea (Vatansever, 2017). Both species are two-host ticks and can therefore be transported for a long distance on the same host individual, on which the tick engorges twice, leaving the host as a fed nymph after having stayed on the same host for two to five weeks

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(Balashov 1972; Hoogstraal 1979; Knight et al. 1978). In this way these ticks can infest the same bird migrating from Africa or southern Europe to reach northern Europe several days or a few weeks later. This phenomenon has been documented by several authors in Fennoscandia (Nuorteva and Hoogstraal, 1963; Mehl et al., 1984; Jaenson et al., 1994; Hasle, 2013; Labbé Sandelin et al., 2015). In order to complete development from the egg stage to reproducing adults these ticks require a warm climate, i.e. a high total temperature sum and a relatively dry atmosphere. The only occasional report of an adult Hyalomma tick found in northern Europe dates back to the 1930s: a male of H. marginatum was found in the vegetation on the Danish island of Bornholm in June 1939 (Johnsen,

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1943). Later, in Sweden in 2011, one H. marginatum adult tick was encountered on a horse imported from Portugal (Gittan Gröndahl, SVA and Ulrika Forshell, Bayer Animal Health, personal

communication). However, these records were regarded as rare and occasional introductions and no

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proof of a permanent presence of this tick species in Sweden. There are relatively recent previous

records of adult Hyalomma ticks from locations in Germany (Kampen et al., 2007; Chitimia-Dobler et

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al., 2016; Oehme et al., 2017) and Hungary (Hornok and Horváth, 2012). In the summer of 2018, there were many records (N=35) of adult Hyalomma ticks in Germany (Chitimia-Dobler et al., 2019)

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as well as an occurrence record of a male H. rufipes on a horse in the UK (Hansford et al., 2019). Additionally, three specimens of adult Hyalomma spp. were found in the Netherlands in 2019

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(ProMed, 2019) . These records confirm and even anticipate the outcome of the population models of Estrada-Peña et al. (2011, 2012, 2015). In one of them (Estrada-Peña et al. 2012), parts of Germany

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and the Netherlands were identified as areas where an occupancy by H. marginatum ticks could take place, while in the latest work only the potential for introduction but no further development of

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permanent populations was described for the same areas (Estrada-Peña et al. 2015). This emphasizes the need to assess the potential risk that these tick species will be able to transmit pathogens of humans and animals north of their previously known distributional areas. Both species are proven vectors of the Crimean-Congo haemorrhagic fever virus (CCHFV). The following potential pathogens of humans have also been detected in or associated with one or both of these Hyalomma species: West Nile virus; Dhori virus, Bahig virus, Alkhurma virus, Rickettsia spp., Coxiella burnetii, Anaplasma spp. and Borrelia burgdorferi s.l. Regarding domesticated animals, these tick species may possibly be 3

vectors of Babesia spp. and Theileria spp. (Santos-Silva and Vatansever, 2017; Vatansever, 2017; ECDC, 2018).

In the present study, we recorded in Sweden for the first time several adults of H.

marginatum and H. rufipes. In view of their important role as disease vectors there is an urgent need to assess the potential consequences for human and animal health due to such introduction events, which will most likely become more frequent whenever the climate will change as predicted by IPCC (IPCC, 2018). Material and Methods

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A programme, supported by the use of social media, was issued in Swedish mass media in order to collect ticks from the Sweden north of the River Dalälven within the frame of an international project (NordForsk-CLINF, https://clinf.org/). We asked people to send to the National Veterinary Institute

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(SVA) in Uppsala, Sweden any tick found on themselves, on animals or in the environment. The success of this campaign generated interest about ticks even among people living south River

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Dalälven. Thus, people started to contact SVA to report findings of “unusual” ticks from all over the country. Persons who contacted SVA for this purpose were asked to send photographs of “their

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unusual” ticks and if we were able to confirm the tick as a potentially interesting species, we contacted the “tick collector” to ask if the tick was still available – and if so to send it to SVA.

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After arrival at SVA the tick specimens were frozen at -20 °C, later examined with a stereomicroscope (Leica MZ16, Leica Microsystems, Stockholm, Sweden) and eventually identified

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using morphological keys (Apanaskevich and Horak, 2008). Total nucleic acids from all tick specimens were extracted using the MagNA Pure LC RNA/DNA Kit

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(Roche, Mannheim, Germany) in a MagNA Pure LC Instrument (Roche) according to the manufacturer’s instructions. The total nucleic acid was stored at -80°C until use. The tick RNA was tested for CCHFV using a published real-time reverse transcriptase Polymerase Chain Reaction (RTPCR) protocol (Atkinson et al., 2012), while the DNA was tested for Rickettsia spp. using a panRickettsia real-time PCR (Wölfel et al., 2008) and for piroplasms (Babesia/Theileria) with a

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conventional PCR (Casati et al., 2006). Moreover, a 23S-5S intergenic spacer region PCR was applied to identify the Rickettsia spp. in case of positive results (Chitimia-Dobler et al., 2019).

Results On 31 July 2018 a horse owner from Nyköping (latitude 59 °N), province of Södermanland, Sweden, contacted SVA in order to send a “strange tick”, which she had found under the tail of her horse. On 21–22 August 2018, three weeks after the first record, two other horse owners, one from Koppom

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(latitude 60°N), province of Värmland, and the other from Landskrona (latitude 56°N), province of Skåne, contacted SVA since each person had found “an exceptionally big tick with extremely

aggressive behaviour”. None of their horses had travelled during the previous two months. Soon after

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media coverage (TV, radio, newspapers) of these findings many reports of Hyalomma ticks came to SVA.

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A total of 41 reports of Hyalomma specimens were received from 31 July 2018 to 6 January

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2019 (Figure 1). In some cases (n=21) the person who reported the case could only provide a picture of the presumed Hyalomma specimen, but when the quality of the photograph was satisfactory it was possible to confirm that the tick was a Hyalomma species and even to identify the sex of the tick.

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Ticks identified by us, based on photographs, as adult Hyalomma ticks, are listed in Table 1. Twenty Hyalomma ticks were sent to SVA between 31 July and 29 October 2018. The results of the

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morphological identifications are shown in Table 2. The majority of these ticks were attached to the

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perineal region of horses. Based on the size of these ticks they had not been able to imbibe a full blood meal. Regarding animal health, none of these horses exhibited any signs or symptoms of illness after removal of the attached Hyalomma tick. None of the horses had more than one tick each. All ticks were negative for CCHFVs and piroplasms whereas 12 ticks were positive for Rickettsia spp. (Table 2). The Rickettsia was identified as R. aeschlimannii, with one exception. Its sequence was neither belonging to R. aeschlimannii nor to R. africae. Further investigations on the unidentified Rickettsia are ongoing, the results of which will be reported elsewhere. 5

Discussion To the authors’ knowledge, these are the only published records of adult Hyalomma ticks in Sweden and the first records of H. rufipes in Sweden. As mentioned before, the only previous findings of Hyalomma in Fennoscandia – excluding those of larvae and nymphs on migratory birds and those found on imported animals – occurred on the Danish island of Bornholm in 1939 (Johnsen, 1943). In addition, one male Hyalomma tick was collected at Askersund (Närke province, Sweden) from a horse that had not travelled abroad in the summer of 2017 (Anders Lindström, SVA, personal

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communication). H. marginatum and H. rufipes are two-host ticks. This means that the larva feeds and moults to the nymphal stage on the same host, usually a small mammal or a bird. The nymph then remains on the same host on which it feeds. The adult female then engorges on a second host, usually cattle or wild ungulates (Knight et al., 1978). The ability of the immature ticks to ingest the first two

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blood meals on the same avian host enables them to be transported by migratory birds to distant

locations. According to Balashov (1972) the time from the moment when the unfed larva attaches to a

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bird until the engorged nymph leaves the host and drops to the ground lasts from 12 to 27 days.

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Knight et al. (1978) studied the life cycle of H. rufipes under laboratory conditions at about 26 °C and 80 % relative humidity: the time from the beginning of the larval blood feeding period to the end of nymphal blood feeding, including the nymphal premolt period, was recorded to last 18-36 days on

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average. This exceeds the time required for many migratory birds to fly from Northern Africa to Northern Europe (Åkesson et al., 2012; Hedenström et al., 2013; Arlt et al., 2015) . The summer of

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2018 was the warmest ever recorded based on the records by the Swedish Meteorological and Hydrological Institute (SMHI), which in Sweden started in the eighteenth century (SMHI, 2018). In

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most parts of southern Sweden the mean temperature during the summer was 2– 4 ºC higher than the long-term mean temperature based on the standard period 1961 – 1990. This exceptionally warm and sunny summer is the most likely factor that explains the successful development in Sweden of immature Hyalomma to the adult stage. Similar observations have been reported from neighbouring regions (Hansford et al., 2019; Duscher et al., 2018; Chitimia-Dobler et al., 2019). Since such hot summers will become more frequent in the near future (IPCC 2018), the likelihood will increase that

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immature Hyalomma ticks, introduced by birds to Sweden, will be able to develop to the reproductive stage, which may attach and feed on large animals and humans. The importance of Hyalomma ticks as disease vectors has been recently reassessed as it has been demonstrated that H. rufipes ticks collected from migratory birds caught in the Mediterranean Basin can harbour CCHFV (Lindeborg et al., 2012) and Alkhurma virus (Hoffman et al., 2018), as well as potentially human-pathogenic bacteria (R. aeschlimannii, Ehrlichia spp., Coxiella burnetii, Borrelia burgdorferi s.l.; Vatansever, 2017). The absence of CCHFV in the specimens collected in the

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present study conforms to results of similar studies on adult Hyalomma ticks found in Germany (Chitimia-Dobler et al., 2019).

R. aeschlimannii was the only Rickettsia species identified so far from the Hyalomma

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specimens collected in Sweden. It is known to be one of the agents of Mediterranean spotted fever

(Raoult et al., 2002) but has also been described as a cause of acute hepatitis (Tosoni et al., 2016). The

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only Rickettsia species so far known to be permanently present in Sweden are R. helvetica and R. sibirica in Ixodes ricinus (Wallménius et al., 2012). In view of our present results it appears that

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Hyalomma ticks may be able to introduce “new” Rickettsia species into this country. It is not known if other tick species (e.g. I. ricinus) are competent vectors of these Hyalomma-transmitted rickettsiae,

present in Sweden.

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but it is important to realize, in view of public and animal health, that new Rickettsia species might be

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From the veterinary point of view, H. marginatum may be responsible for the introduction of protozoan parasites like B. caballi and T. equi, the agents of equine piroplasmosis, and T. annulata,

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the agent of tropical/Mediterranean theileriosis in cattle (Santos-Silva and Vatansever, 2017). Recent studies conducted on H. marginatum ticks removed from cattle and horses in Italy, showed that 9 % harboured different piroplasms (Iori et al., 2010). Yet, none of the Hyalomma specimens collected in the present study was positive for these parasites. The risk of introduction of these pathogens to Sweden with Hyalomma ticks may therefore be considered to be relatively low. However, in view of our small sample size, further monitoring of Hyalomma ticks in Sweden is warranted to better assess the risk of introduction of these pathogens. 7

Adult Hyalomma ticks prefer to feed on large mammals, particularly ungulates grazing in open areas. The large number of Hyalomma specimens from horses compared to the relatively few records of such ticks from cattle is likely due to the fact that horses are generally much more handled and more often carefully examined for ectoparasites, including ticks. A general, pro-active strategy for the country-wide surveillance of the potential introduction of exotic ticks needs to be implemented, hopefully as collaboration between Public Health and Veterinary authorities. There are examples of such tick surveillance initiatives in other countries, like

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the UK (Hansford et al., 2018) and the Netherlands (Jongejan et al., 2019). The present findings are in fact a demonstration of a fruitful and efficient co-operation among governmental staff members and their stakeholders.

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Author Statement

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This study was designed, directed and coordinated by Giulio Grandi and Anna Omazic, that were the principal investigators. They were also the major responsible for species identification (Giulio Grandi), for the georeferencing of records (Anna Omazic), for taking care of contacts with public and for writing the manuscript (both). Lidia Chitimia Dobler contributed to microbiological analyses of the collected material (CCHFV and rickettsiae) and to the editing of the manuscript. Christina Strube and Andrea Springer contributed to the microbiological analyses of the collected materials for piroplasms and and to the editing of the manuscript. Phimphanit Choklikitumnuey contributed to laboratory analysis of the collected materials (photographical documentation of the material, preliminary identification, preparation of material for analysis) and to editing of the manuscript. Thomas Jaenson and Ann Albihn contributed to writing and editing the manuscript.

Funding

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All the authors have read and approved the manuscript in its final form.

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The present study was performed within the project: NordForsk Climate-change effects on the epidemiology of infectious diseases and the impacts on Northern Societies (NordForsk-CLINF; www.clinf.org), which is funded by NordForsk [Grant no. 76413]. TGTJ’s research on the ecology of ticks and tick-borne infections is funded by Carl Tryggers stiftelse, Helge Ax:son Johnsons stiftelse, Längmanska kulturfonden and Magnus Bergvalls stiftelse, all in Stockholm, Sweden.

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None of the funding bodies played any role in the planning and design of the study, data collection, analyses, data interpretations, writing of the manuscript, and in the decision about when and where to submit the manuscript for publication.

Acknowledgments We are very grateful to Dmitry Apanaskevich, Georgia Southern University, Statesboro (GA, USA), for the confirmation of species identification of the male H. marginatum; to Mikael Propst, SVA, and the staff at the Communication Department at SVA, for taking care of the NordForsk-CLINF-related campaign; to Ann Högberg, SVA, for the taking care of tick samples; to Technician Sabine Schaper,

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Institute of Microbiology, Bundeswehr, Germany for taking care of the molecular analyses; to all

persons who responded to the NordForsk-CLINF-related campaign and our request to submit tick

specimens for our survey; and to all horse and cattle owners for their interest to collaborate and for providing important information. Special thanks to Gunnar Andersson, SVA, for assistance with

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graphical presentation of Hyalomma records in Sweden.

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References

Arlt, D., Olsson, P., Fox, J.W., Low, M., Pärt, T., 2015. Prolonged stopover duration characterises migration strategy and constraints of a longdistance migrant songbird. Anim. Migr. 2, 47–62.

na

Åkesson, S., Klaassen, R., Holmgren, J., Fox, J.W., Hedenström, A., 2012. Migration Routes and Strategies in a Highly Aerial Migrant, the Common Swift Apus apus, Revealed by Light-Level Geolocators. PLoS ONE 7(7): e41195. https://doi.org/10.1371/journal.pone.0041195

ur

Apanaskevich, D.A., Horak, I.G., 2008. The genus Hyalomma Koch, 1844: V. Re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species

Jo

(Acari: Ixodidae) with redescription of all parasitic stages and notes on biology. Int. J. Acarol. 34, 1342.

Atkinson, B., Chamberlain, J., Logue, C.H., Cook, N., Bruce, C., Dowall, S.D., Hewson, R., 2012. Development of a real-time RT-PCR assay for the detection of Crimean-Congo hemorrhagic fever virus. Vector Borne Zoonotic Dis. 12, 786-793. https://doi.org/10.1089/vbz.2011.0770. Balashov, Y.S., 1972. Bloodsucking ticks (Ixodoidea) – vectors of disease of man and animals. Misc. Publ. Entomol. Soc. America. 8, 163-176.

9

Casati, S., Sager, H., Gern, L., Piffaretti, J.C., 2006. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann. Agric. Environ. Med. 13, 65-70 Chitimia-Dobler, L., Schaper, S., Rieß, R., Bitterwolf, K., Frangoulidis, D., Bestehorn, M., Springer, A., Oehme, R., Drehmann, M., Lindau, A., Mackenstedt, U., Strube, C., Dobler, G., 2019. Imported Hyalomma ticks in Germany in 2018. Parasit Vectors 12:134 https://doi.org/10.1186/s13071-0193380-4. Chitimia-Dobler, L., Nava, S., Bestehorn, M., Dobler, G., Wölfel, S., 2016. First detection of Hyalomma rufipes in Germany. Ticks Tick Borne Dis. 7, 1135-1138. https://doi.org/10.1016/j.ttbdis.2016.08.008.

ro of

Duscher, G.G., Hodžić, A., Hufnagl, P., Wille-Piazzai, W., Schötta, A.M., Markowicz, M.A., EstradaPeña, A., Stanek, G., Allerberger, F., 2018. Adult Hyalomma marginatum tick positive for Rickettsia aeschlimannii in Austria, October 2018. Euro Surveill. 2018;23(48):pii=1800595. https://doi.org/10.2807/1560-7917.ES.2018.23.48.1800595

-p

ECDC, 2018. Hyalomma marginatum – Factsheet for experts. https://ecdc.europa.eu/en/diseasevectors/facts/tick-factsheets/hyalomma-marginatum (accessed 13th April, 2019).

re

Estrada-Peña, A., de la Fuente, J., Latapia, T., Ortega, C., 2015. The impact of climate trends on a tick affecting public health: a retrospective modelling approach for Hyalomma marginatum (Ixodidae).

lP

PLoS One.10(5), e0125760. https://doi.org/10.1371/journal.pone.0125760. Estrada-Peña, A., Martínez Avilés, M., Muñoz Reoyo, M.J., 2011. A population model to describe the distribution and seasonal dynamics of the tick Hyalomma marginatum in the Mediterranean Basin.

na

Transbound. Emerg. Dis. 58, 213-223. https://doi.org/10.1111/j.1865-1682.2010.01198.x. Estrada-Peña, A., Pfäffle, M.P., Petney, T.N. 2017. Genus Hyalomma Koch, 1844. Pp. 343-348. In: Estrada-Peña, A., Mihalca, A.D., Petney, T.N. Ticks of Europe and North Africa – A Guide to

ur

Species Identification, Springer International Publishing AG, Cham, Switzerland. Estrada-Peña, A., Sánchez, N., Estrada-Sánchez, A., 2012. An assessment of the distribution and

Jo

spread of the tick Hyalomma marginatum in the western Palearctic under different climate scenarios. Vector-Borne Zoonotic Dis. 12, 758-768. https://doi.org/10.1089/vbz.2011.0771. Hansford, K.M., Pietzsch, M.E., Cull, B., Gillingham, E.L., Medlock, J.M., 2018 Potential risk posed by the importation of ticks into the UK on animals: records from the Tick Surveillance Scheme. Vet Rec. 182(4):107. doi: 10.1136/vr.104263. Hansford, K.M., Carter, D., Gillingham, E.L., Hernandez-Triana, L.M., Chamberlain, J., Cull, B., McGinley, L., Phipps, L.P., Medlock, J.M., 2019. Hyalomma rufipes on an untraveled horse: Is this

10

the first evidence of Hyalomma nymphs successfully moulting in the United Kingdom? Ticks Tickborne Dis. 10, 704-708. https://doi.org/10.1016/j.ttbdis.2019.03.003. Hasle, G., 2013. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front. Cell. Infect. Microbiol. 3:48. https://doi.org/10.3389/fcimb.2013.00048. Hedenström, A., Klaassen, R.H.G., Åkesson, S., 2013. Migration of the Little Ringed Plover Charadrius dubius breeding in South Sweden tracked by geolocators, Bird Study. 60, 466-474. Hoffman, T., Lindeborg, M., Barboutis, C., Erciyas-Yavuz, K., Evander, M., Fransson, T., Figuerola, J., Jaenson, T.G.T., Kiat, Y., Lindgren, P.E., Lundkvist, Å., Mohamed, N., Moutailler, S., Nyström, F., Olsen, B., Salaneck, E., 2018. Alkhurma hemorrhagic fever virus RNA in Hyalomma rufipes Ticks

ro of

infesting migratory birds, Europe and Asia Minor. Emerg. Infect. Dis. 24, 879-882. https://doi.org/10.3201/eid2405.171369.

Hoogstraal, H., 1979. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J. Med. Entomol. 15, 307-417.

-p

Hornok, S. & Horváth, G. 2012. First report of adult Hyalomma marginatum

in Hungary. Parasit. Vectors. 2012, 5:170.

re

rufipes (vector of Crimean-Congo haemorrhagic fever virus) on cattle under a continental climate

lP

Iori, A., Gabrielli, S., Calderini, P., Moretti, A., Pietrobelli, M., Tampieri, M.P., Galuppi, R., Cancrini, C., 2010. Tick reservoirs for piroplasms in central and northern Italy. Vet. Parasitol. 170, 291-296. https://doi.org/10.1016/j.vetpar.2010.02.027.

na

Intergovernmental Panel on Climate Change (IPCC), 2018: Summary for Policymakers. In: Global warming of 1.5 °C. An IPCC Special Report on the impacts of global warming of 1.5 °C above preindustrial levels and related global greenhouse gas emission pathways, in the context of strengthening

ur

the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [V. Masson-Delmotte, P. Zhai, H. O. Pörtner, D. Roberts, J. Skea, P. R. Shukla,A. Pirani, W.

Jo

Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis,E. Lonnoy, T. Maycock, M. Tignor, T. Waterfield (eds.)]. World Meteorological Organization, Geneva, Switzerland,32 pp Jaenson, T.G.,T., Tälleklint, L., Lundqvist, L., Olsen, B., Chirico, J., Mejlon, H., 1994. Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J. Med. Entomol. 31, 240-256. Johnsen, P. 1943. Hyalomma marginatum Koch, a tick new to Denmark. Entomol. Medd. 22, 381-383 (in Danish).

11

Jongejan, F., de Jong, S., Voskuilen, T., van den Heuvel, L., Bouman, R., Heesen, H., Ijzermans, C., Berger, L., 2019. "Tekenscanner": a novel smartphone application for companion animal owners and veterinarians to engage in tick and tick-borne pathogen surveillance in the Netherlands. Parasit Vectors. 12(1):116. doi: 10.1186/s13071-019-3373-3. Kampen, H., Poltz, W., Hartelt, K., Wölfel, R., Faulde, M., 2007. Detection of a questing Hyalomma marginatum marginatum adult female (Acari, Ixodidae) in southern Germany. Exp. Appl. Acarol. 43, 227–231. https://doi.org/10.1007/s10493-007-9113-y. Knight, M.M., Norval, R.A.I., Rechav, Y., 1978. The life cycle of the tick Hyalomma marginatum rufipes Koch (Acarina: Ixodidae) under laboratory conditions. J. Parasitol. 64, 143-146.

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Labbé Sandelin, L., Tolf, C., Larsson, S., Wilhelmsson, P., Salaneck, E., Jaenson, T.G., Lindgren, P.E., Olsen, B., Waldenström, J. 2015. Candidatus Neoehrlichia mikurensis in ticks from migrating birds in Sweden. PLoS One. 10(7), e0133250. https://doi.org/10.1371/journal.pone.0133250. Lindeborg, M., Barboutis, C., Ehrenborg, C., Fransson, T., Jaenson, T.G.T., Lindgren, P.-E.,

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Lundkvist, A., Nyström, F., Salaneck, E., Waldenström, J., Olsen, B., 2012. Migratory birds, ticks, and Crimean-Congo hemorrhagic fever virus. Emerg. Infect. Dis. 18, 2095–2097.

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https://doi.org/10.3201/eid1812.120718.

Mehl, R., Michaelsen, J., Lid, G., 1984. Ticks (Acari, Ixodides) on migratory birds in Norway. Fauna

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Norvegica Ser. B. 31, 46-58.

Nuorteva, P., Hoogstraal, H., 1963. The incidence of ticks (Ixodoidea, Ixodidae) on migratory birds arriving in Finland during the spring of 1962. Ann. Med. Exp. Fenniae 4, 457–468.

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Oehme, R., Bestehorn, M., Wölfel, S., Chitimia-Dobler, L., 2017. Hyalomma marginatum in Tübingen, Germany. Syst. Appl. Acarol. 22, 1-6. https://doi.org/10.11158/saa.22.1.1

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ProMed, 2019. Invasive tick - Netherlands (02): (Gelderland). http://www.promedmail.org Date: Mon 23 Sep 2019, Archive number 20190924.6692320

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Raoult, D., Fournier, P.E., Abboud, P., Caron, F. 2002. First Documented Human Rickettsia aeschlimannii Infection. Emerg Infect Dis. 8, 748–749. Santos-Silva, M.M., Vatansever, Z., 2017. Hyalomma marginatum Koch, 1844, in: Estrada Peña, A., Mihalca, A.D., Petney, T. (Eds.), Ticks of Europe and North Africa –A Guide to Species Identification Springer International Publishing, Cham, pp. 349-354. SMHI - Swedish Meteorological and Hydrological Institute. [The summer 2018 – extremely warm and sunny]. [in Swedish]. https://www.smhi.se/klimat/klimatet-da-och-nu/arets-vader/sommaren2018-extremt-varm-och-solig-1.138134 (accessed 13 April 2019)

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Tosoni, A., Mirijello, A., Ciervo, A., Mancini, F., Rezza, G., Damiano, F., Cauda, R., Gasbarrini, A., Addolorato, G., 2016. Human Rickettsia aeschlimannii infection: first case with acute hepatitis and review of the literature. Eur Rev Med Pharmacol Sci 20, 2630-2633 Vatansever, Z., 2017. Hyalomma rufipes Koch, 1844, in Estrada-Peña, , A., Mihalca, A.D., Petney, T. (Eds.), Ticks of Europe and North Africa – A guide to species identification. Springer International Publishing, Cham, pp. 355-359. Wallménius, K., Pettersson, J.H., Jaenson, T.G., Nilsson, K. 2012 Prevalence of Rickettsia spp., Anaplasma phagocytophilum, and Coxiella burnetii in adult Ixodes ricinus ticks from 29 study areas in central and southern Sweden. Ticks Tick Borne Dis. 3, 100-106

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Wölfel, R., Essbauer, S., Dobler, G., 2008. Diagnostics of tick-borne rickettsioses in Germany: a

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modern concept for a neglected disease. Int. J. Med. Microbiol. 298(S1), 368–374.

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Figure 1. Hyalomma in Sweden. Map of Sweden showing records reported by e-mail and specimens collected during July 2018 – January 2019, denoted “Hyalomma marginatum” (■), “Hyalomma rufipes” (●) and “Hyalomma sp.” (either H. marginatum or H. rufipes) based on photographical records (▲) . Cartographer: Gunnar Andersson, SVA.

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Table 1. Records of Hyalomma ticks collected in Sweden during July 2018 – January 2019. Ticks were identified to genus level based on photographs submitted by the persons who encountered the ticks. No tick specimen was available for these identifications. Sex of tick

Host species

Locality

Province

20/08/2018

Female

Horse

Koppom

Värmland

21/08/2018

Female

Human

Karlstad

Värmland

27/08/2018

Male

Horse

Ale

Västergötland

28/08/2018 (coll. 06/08/2018)

Female

Horse

Senoren, Karlstad

Blekinge

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Date of report (date of collection if different)

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Male

Horse

Degerfors

Värmland

28/08/2018 (coll. 27/08/2018)

Female

Horse

Enköping

Uppsala

27/08/2018 (coll.summer 2018, 5 specimens)

Female

Horse

Härryda, Landvetter

Västergötland

28/08/2018

Male

Horse

Jämsunda, Karlskrona

Blekinge

29/08/2018 (coll. summer 2018)

Female

Horse

Västra Husby, Norrköping

Östergötland

29/08/2018 (coll. 27/08/2018)

Female

Horse

Karlsborg

Västergötland

31/08/2018

Female

Horse

Växjö

Småland

03/09/2018 (coll. 09/08/2018)

Female

Horse

Stora Forsa, Askersund

Närke

01/09/2018

Female

Horse

Ornö, Haninge

Stockholm

03/09/2018

Female

Horse

Västerhaninge

Stockholm

14/09/2018 (coll. 13/09/2018)

Male

Horse

Nyköping

Södermanland

17/09/2018

Male

Horse

Löddeköpping

Skåne

01/10/2018 (coll. 29/09/2018)

Male

Horse

Grängesberg

Dalarna

04/09/2018 (coll. 25/08/2018)

Female

Horse

Järvstabyn, Gävle

Gästrikland

11/09/2018 (coll. 10/09/2018)

Female

Horse

Broaryd/Bursery, Småland Gislaved

13/09/2018

Female

Horse

Boet, Ödeshög

Östergötland

06/01/2019

Male

Horse

Mörrum, Karlshamn

Blekinge

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28/08/2018 (coll. 23/08/2018)

Table 2. Adult specimens of Hyalomma ticks collected in Sweden during July–October 2018 and morphologically identified to species level Host species

Locality

Province

Hyalomma species

Sex of tick

Rickettsia aeschlimannii

31/07/2018

Horse

Nyköping

Södermanland

H. marginatum

M

Negative

21/08/2018

Horse

Landskrona

Skåne

H. marginatum

F

Positive

17/08/2018

Horse

Nävekvarn, Nyköping

Södermanland

H. marginatum

F

Negative

26/08/2018

Horse

Klintehamn

Gotland

H. rufipes

M

Positive

End of July, 2018

Horse

Örebro

Närke

H. rufipes

F

Positive

05/09/2018

Horse

Upplands Väsby

Stockholm

H. marginatum

F

Positive

11/09/2018

Horse

Mjölby

Östergötland

H. marginatum

F

Negative

14/09/2018

Horse

Slageryd, Korsberga

Småland

H.marginatum

F

Negative

17/09/2018

Horse

Färgelanda, Dalsland

Västergötland

H. marginatum

M

Negative

20/09/2018

Horse

Veberöd

Skåne

H. rufipes

M

Negative

21/09/2018

Man

Gävle

Gästrikland

H. marginatum

F

Negative

26/09/2018

Man

Älvnäs, Vålberg

Värmland

H. rufipes

M

Positive

27/09/2018

Horse

Tveta, Säffle

Värmland

H. rufipes

M

Negative

04/09/2018

Horse

Sölvesborg

Blekinge

H. rufipes

M

Positive

07/10/2018

Horse

Vreta kloster

Östergötland

H. rufipes

F

Positive

25/09/2018

Cattle

Funnarp, Hästveda, Hässleholm

Skåne

H. marginatum

M

Positive

18/09/2018

Horse

Örserum, Gränna

Småland

H. rufipes

M

Positive

11/10/2018

Horse

Katthammarsvik

Gotland

H. marginatum

F

Positive (Rickettsia sp.)

18/09/2018

Horse

Ovanåker

Hälsingland

H. marginatum

M

Positive

29/10/2018

Horse

Bjurbäcken

Värmland

H. rufipes

M

Positive

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Date of collection