Novel foci of Dermacentor reticulatus ticks infected with Babesia canis and Babesia caballi in the Netherlands and in Belgium

Particle and Fibre Toxicology

Maxime Madder³  Michiel Wijnveld¹  Marleen van Roessel²  Jesse Lenssen²  Reinier Kortekaas²  Stefan Burgers²  Laura Berger²  Michael Putting²  Moniek Ringenier²  Frans Jongejan³ 

[1] Current address: Institute for Hygiene and Applied Immunology, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Kinderspitalgasse 15, Vienna, 1090, Austria;Utrecht Centre for Tick-borne Diseases (UCTD), FAO Reference Centre for Ticks and Tick-borne Diseases, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, Utrecht, 3584 CL, The Netherlands;Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Pretoria 0110, Onderstepoort, South Africa

关键词: Babesia caballi;    Babesia canis;    Belgium;    Netherlands;    Dermacentor reticulatus;    Ticks;   

Others  :  1172230
DOI  :  10.1186/s13071-015-0841-2

 received in 2015-03-05, accepted in 2015-04-03,  发布年份 2015

【 摘 要 】

Background

Autochthonous populations of Dermacentor reticulatus ticks in the Netherlands were discovered after fatal cases of babesiosis occurred in resident dogs in 2004. The presence of D. reticulatus in the Netherlands has also linked with the emergence of piroplasmosis in the resident horse population. The aim of this study was to put together results of continued surveillance of field sites and hosts for this tick in the Netherlands and also in Belgium and determine their infection status for Babesia and Theileria species.

Methods

Ticks were collected from the vegetation at 11 locations between 2011 and 2013. D. reticulatus ticks were also collected from different hosts between 2007 and 2013. Ticks were screened by PCR and reverse line blot (RLB).

Results

A total of 1368 D. reticulatus ticks were collected from 4 previously known field locations and from 5 new locations in the Netherlands and from 2 sites in Belgium (one old and one new location). A total of 855 ticks collected from 8 locations in the Netherlands and 2 locations in Belgium were tested. Fourteen ticks (1,64%) collected at 4 field locations (Dintelse Gorzen, Rozenburg, Slikken van de Heen and St. Philipsland) were positive for Babesia canis, whereas two ticks were positive for Babesia caballi, one tick in the Dintelse Gorzen in the Netherlands and one tick was found positive in De Panne in Belgium.

A further 1092 D. reticulatus ticks were collected between 2007 and 2013 from 40 dogs (132 ticks), two ticks from two humans, 51 ticks from 15 horses, two ticks from two cats, one tick from a roe deer, whereas most ticks (904) were collected from cattle (n = 25). Ticks were found throughout the year on dogs in nearly all provinces of the Netherlands. None of the ticks collected from these hosts were infected.

Conclusions

D. reticulatus is continuing its spread into novel areas. The finding that some autochthonous ticks are infected with B. canis and B. caballi poses a threat to the resident dog and horse population and justifies year-round tick control measures.

【 授权许可】

   
2015 Jongejan et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E. Effects of climate change on ticks and tick-borne diseases in europe. Interdiscip Perspect Infect Dis. 2009; 2009:1-12.
• [2]Estrada-Peña A, Farkas R, Jaenson TGT, Koenen F, Madder M, Pascucci I et al.. Association of environmental traits with the geographic ranges of ticks (Acari: Ixodidae) of medical and veterinary importance in the western Palearctic. A digital data set. Exp Appl Acarol. 2013; 59:351-366.
• [3]Dautel H, Dippel C, Oehme R, Hartelt K, Schettler E. Evidence for an increased geographical distribution of Dermacentor reticulatus in Germany and detection of Rickettsia sp. RpA4. Int J Med Microbiol. 2006; 296 Supplement 1:149-156.
• [4]Kubelová M, Tkadlec E, Bednář M, Roubalová E, Široký P. West-to-east differences of Babesia canis canis prevalence in Dermacentor reticulatus ticks in Slovakia. Vet Parasitol. 2011; 180:191-196.
• [5]Cochez C, Lempereur L, Madder M, Claerebout E, Simons L, De Wilde N et al.. Foci report on indigenous Dermacentor reticulatus populations in Belgium and a preliminary study of associated babesiosis pathogens. Med Vet Entomol. 2012; 26:355-358.
• [6]Rubel F, Brugger K, Monazahian M, Habedank B, Dautel H, Leverenz S et al.. The first German map of georeferenced ixodid tick locations. Parasit Vectors. 2014; 7:477. BioMed Central Full Text
• [7]Karbowiak G. The occurrence of the Dermacentor reticulatus tick – its expansion to new areas and possible causes. Ann Parasitol. 2014; 60:37-47.
• [8]Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004; 129:S3-S14.
• [9]Wójcik-Fatla A, Bartosik K, Buczek A, Dutkiewicz J. Babesia microti in Adult Dermacentor reticulatus Ticks from Eastern Poland. Vector-Borne Zoonotic Dis. 2012; 12:841-843.
• [10]Wójcik-Fatla A, Cisak E, Zajac V, Zwoliński J, Dutkiewicz J. Prevalence of tick-borne encephalitis virus in Ixodes ricinus and Dermacentor reticulatus ticks collected from the Lublin region (eastern Poland). Ticks Tick Borne Dis. 2011; 2:16-19.
• [11]Biernat B, Karbowiak G, Werszko J, Stańczak J. Prevalence of tick-borne encephalitis virus (TBEV) RNA in Dermacentor reticulatus ticks from natural and urban environment, Poland. Exp Appl Acarol. 2014; 64:543-551.
• [12]Nijhof AM, Bodaan C, Postigo M, Nieuwenhuijs H, Opsteegh M, Franssen L et al.. Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector Borne Zoonotic Dis. 2007; 7:585-95.
• [13]Parola P, Rovery C, Rolain JM, Brouqui P, Davoust B, Raoult D. Rickettsia slovaca and R. raoultii in Tick-borne Rickettsioses. Emerg Infect Dis. 2009; 15:1105-1108.
• [14]Alberdi MP, Nijhof AM, Jongejan F, Bell-Sakyi L. Tick cell culture isolation and growth of Rickettsia raoultii from Dutch Dermacentor reticulatus ticks. Ticks Tick Borne Dis. 2012; 3:349-54.
• [15]Paulauskas A, Radzijevskaja J, Rosef O. Molecular detection and characterization of Anaplasma phagocytophilum strains. Comp Immunol Microbiol Infect Dis. 2012; 35:187-195.
• [16]Karbowiak G, Vichová B, Slivinska K, Werszko J, Didyk J, Peťko B et al.. The infection of questing Dermacentor reticulatus ticks with Babesia canis and Anaplasma phagocytophilum in the Chernobyl exclusion zone. Vet Parasitol. 2014; 204:372-375.
• [17]Wirtgen M, Nahayo A, Linden A, Garigliany M, Desmecht D. Detection of Anaplasma phagocytophilum in Dermacentor reticulatus ticks. Vet Rec. 2011; 168:195.
• [18]Zivkovic Z, Nijhof AM, de la Fuente J, Kocan KM, Jongejan F. Experimental transmission of Anaplasma marginale by male Dermacentor reticulatus. BMC Vet Res. 2007; 3:32. BioMed Central Full Text
• [19]Bonnet S, de la Fuente J, Nicollet P, Liu X, Madani N, Blanchard B et al.. Prevalence of tick-borne pathogens in adult dermacentor spp. ticks from nine collection sites in France. Vector Borne Zoonotic Dis. 2013; 13:226-36.
• [20]Matjila TP, Nijhof AM, Taoufik A, Houwers D, Teske E, Penzhorn BL et al.. Autochthonous canine babesiosis in The Netherlands. Vet Parasitol. 2005; 131:23-9.
• [21]Butler CM, van Oldruitenborgh-Oosterbaan MM S, Stout TAE, van der Kolk JH, Van Den WL, Nielen M et al.. Prevalence of the causative agents of equine piroplasmosis in the South West of The Netherlands and the identification of two autochthonous clinical Theileria equi infections. Vet J. 2012; 193:381-5.
• [22]Lenssen J, Wijnveld M, Conijn A, Luijten A, Jongejan F. The “tick busters” survey. Tijdschr Diergeneeskd. 2011; 136:508-511.
• [23]Estrada-peña A, Bouattour A, Camicas J-L, Walker AR: Ticks of Domestic Animals in the Mediterranean Region: A Guide to Identification of Species. 2004.
• [24]Dantas-Torres F, Lia RP, Capelli G, Otranto D. Efficiency of flagging and dragging for tick collection. Exp Appl Acarol. 2013; 61:119-127.
• [25]Georges K, Loria GR, Riili S, Greco A, Caracappa S, Jongejan F et al.. Detection of haemoparasites in cattle by reverse line blot hybridisation with a note on the distribution of ticks in Sicily. Vet Parasitol. 2001; 99:273-86.
• [26]Giangaspero A, Marangi M, Papini R, Paoletti B, Wijnveld M, Jongejan F. Theileria sp. OT3 and other tick-borne pathogens in sheep and ticks in Italy: Molecular characterization and phylogeny. Ticks Tick Borne Dis. 2015; 6:75-83.
• [27]Gubbels JM, De Vos AP, Van der Weide M, Viseras J, Schouls LM, De Vries E et al.. Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol. 1999; 37:1782-9.
• [28]Nijhof AM, Penzhorn BL, Lynen G, Mollel JO, Morkel P, Bekker CPJ et al.. Babesia bicornis sp. nov. and Theileria bicornis sp. nov.: Tick-Borne Parasites Associated with Mortality in the Black Rhinoceros (Diceros bicornis). J Clin Microbiol. 2003; 41(5):2249-2254.
• [29]Martinod S, Gilot B. Epidemiology of canine babesiosis in relation to the activity of Dermacentor reticulatus in southern Jura (France). Exp Appl Acarol. 1991; 11:215-222.
• [30]Claerebout E, Losson B, Cochez C, Casaert S, Dalemans A-C, De Cat A et al.. Ticks and associated pathogens collected from dogs and cats in Belgium. Parasit Vectors. 2013; 6:183. BioMed Central Full Text
• [31]Uilenberg G, Top PDJ, Arends PJ, Kool PJ, Van Dijk JE, Van Schieveen PBE et al.. Autochtone babesiose bij de hond in Nederland? Tijdschr Diergeneesk. 1985; 110:93-8.
• [32]Losson B, Mollet J, Avez F, Malaise F, Mignon B. Description de trois cas autochtones de babesiose canine (Babesia canis) en Belgique. Ann Med Vet. 1999; 143:119-124.
• [33]Øines Ø, Storli K, Brun-Hansen H. First case of babesiosis caused by Babesia canis canis in a dog from Norway. Vet Parasitol. 2010; 171:350-353.
• [34]Schaarschmidt D, Gilli U, Gottstein B, Marreros N, Kuhnert P, Daeppen JA et al.. Questing Dermacentor reticulatus harbouring Babesia canis DNA associated with outbreaks of canine babesiosis in the Swiss Midlands. Ticks Tick Borne Dis. 2013; 4:334-340.
• [35]Schreiber C, Krücken J, Beck S, Maaz D, Pachnicke S, Krieger K et al.. Pathogens in ticks collected from dogs in Berlin/Brandenburg. Germany. Parasit Vectors. 2014; 7:535. BioMed Central Full Text
• [36]Jongejan F, Fourie JJ, Chester ST, Manavella C, Mallouk Y, Pollmeier MG et al.. The prevention of transmission of Babesia canis canis by Dermacentor reticulatus ticks to dogs using a novel combination of fipronil, amitraz and (S)-methoprene. Vet Parasitol. 2011; 179:343-350.
• [37]Fourie JJ, Stanneck D, Jongejan F. Prevention of transmission of Babesia canis by Dermacentor reticulatus ticks to dogs treated with an imidacloprid/flumethrin collar. Vet Parasitol. 2013; 192:273-278.
• [38]Beugnet F, Halos L, Larsen D, Labuschagné M, Erasmus H, Fourie J. The ability of an oral formulation of afoxolaner to block the transmission of Babesia canis by Dermacentor reticulatus ticks to dogs. Parasit Vectors. 2014:283.
• [39]Beugnet F, Marié JL. Emerging arthropod-borne diseases of companion animals in Europe. Vet Parasitol. 2009; 163:298-305.
• [40]Švehlová A, Berthová L, Sallay B, Boldiš V, Sparagano OAE, Špitalská E et al.. Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and Rickettsia and Babesia species in Slovakia. Ticks Tick Borne Dis. 2014; 5:600-605.