Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway

Particle and Fibre Toxicology

Olav Rosef²  Algimantas Paulauskas¹  Jana Radzijevskaja¹  Øivind Øines³ 

[1] Department of Biology, Vytautas Magnus University, Vileikos str. 8, Kaunas, LT-44404, Lithuania;ATP-Innovation AS, 3800, Bø i Telemark, Norway;Norwegian Veterinary Institute, P.O. Box 750, Sentrum, 0106, Oslo, Norway

关键词: Sequencing;    Prevalence;    Realtime PCR;    Piroplasmosis;    Zoonosis;    Questing Ixodes ricinus;    Babesia spp;   

Others  :  1231741
DOI  :  10.1186/1756-3305-5-156

 received in 2012-06-20, accepted in 2012-07-25,  发布年份 2012

【 摘 要 】

Background

Ixodes ricinus ticks transmit Babesia species to vertebrate hosts. Using molecular tools we were able to detect the presence of this piroplasmid in its vector. The aims of this study were to investigate the prevalence and identity of Babesia species in questing ticks collected in various areas of Norway.

Methods

DNA from questing l. ricinus ticks were examined with a realtime PCR for the presence of Babesia. Positive samples of tick DNA were identified to species using PCR, and sequence analysis.

Results

From a total of 1908 questing l. ricinus ticks, 17 (0.9%) indicated the presence of Babesia spp. after realtime-PCR screening. Ixodes ricinus harbouring Babesia spp. was detected in 9 out of 22 localities. Further molecular analyses of DNA from these positive ticks indicate the presence of Babesia venatorum, B. divergens, B. capreoli and a currently undescribed Babesia in Norwegian ticks. The most prevalent was B. venatorum found in 71% of the positive ticks.

Conclusions

A total of 17 out of 1908 (0.9%) ticks were positive for Babesia. Our data confirm that there are several Babesia species in ticks in Norway. Babesia venatorum was the most prevalent. This species has a zoonotic potential and may cause human babesiosis following a tick bite.

【 授权许可】

   
2012 Øines et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Mehl R: The distribution and host relations of Norwegian ticks (Acari, Ixodides). Fauna Norvegica 1983, 30:46-50.
• [2]Jore S, Viljugrein H, Hofshagen M, Brun-Hansen H, Kristoffersen AB, Nygård K, Brun E, Ottesen P, Sævik BK, Ytrehus B: Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasit Vectors 2011, 4:84-95. BioMed Central Full Text
• [3]Skrabalo Z, Deanovic Z: Piroplasmosis in man; report of a case. Doc Med Geogr Trop 1957, 9:11-16.
• [4]Homer MJ, Anguilar-Delfin I, Telford SR, Krause PJ, Persing DH: Babesiosis. Clin Microbiol Rev 2000, 13:451-469.
• [5]Herwaldt BL, Caccio S, Gherlinzoni F, Aspock H, Slemenda SB, Piccaluga P, Martinelli G, Edelhofer R, Hollenstein U, Poletti G, Pampiglione S, Loschenberger K, Tura S, Pieniazek NJ: Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis 2003, 9:942-948.
• [6]Martinot M, Zadeh MM, Hansmann Y, Grawey I, Christmann D, Aguillon S, Jouglin M, Chauvin A, De Briel D: Babesiosis in immunocompetent patients, Europe. Emerg Infect Dis 2011, 17:114-116.
• [7]Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS: Babesia divergens a bovine blood parasite of veterinary and zoonotic importance. Clin Rev Microbiol 2003, 16:622-636.
• [8]Haapasalo K, Soumalainen P, Sukura A, Siikamaki H, Jokiranta TS: Fatal babesiosis in man, Finland, 2004. Emerg Infec Dis 2010, 16:1116-1118.
• [9]Hasle G, Bjune GA, Christensson D, Røed KH, Whist AC, Leinaas HP: Detection of Babesia divergens in sothern Norway by using an immunofluorescence antibody test in cow sera. Acta Vet Scand 2010, 52:55. BioMed Central Full Text
• [10]Wiger R: Seasonal and annual variations in the prevalence of blood parasites in cyclic species of small rodents in Norway with special reference to Clethrionomys glareolus. Holarctic Ecol 1979, 2:169-175.
• [11]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.
• [12]Hasle G, Leinaas HP, Røed KH, Øines Ø: Transport of Babesia venatorum-infected Ixodes ricinus to Norway by northward migrating passerine birds. Acta Vet Scand 2011, 53:41. BioMed Central Full Text
• [13]Hillyard R: Ticks of North-West Europe. In Synopsis of the British Fauna (New Series). Edited by Barnes RSK, Crothers JH. The Natural History Museum, London; 1996:178. 58
• [14]Rijpkema S, Golubic D, Molkenboer M, Verbeek-De Kruif N, Schellekens J: Identification of four genomic groups of B. burgdorferi sensu lato in I. ricinus ticks collected in a Lyme borreliosis endemic region of Northern Croatia. Exp Appl Acarol 1996, 20:23-30.
• [15]Stañczak J, Racewicz B, Kubica-Biernat W, Kruminis-Lozowska J, Dabrowski A, Markowska M: Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks (Acari, Ixodidae) in different Polish woodlands. Ann Agric Environ Med 1999, 6:127-132.
• [16]Filippova NA: Ixodid ticks of the subfamiliy Ixodinae. Fauna in the USSR. Arachnidea, Vol 4. Nauka, Leningrad; 1977.
• [17]Radzijevskaja J, Indriulytë R, Paulauskas A, Ambrasienë D, Turčinavičienë J: Genetic polymorphism study in Ixodes ricinus L ticks population of Lithuania using RAPD markers. Acta Zool Lith 2005, 15:341-348.
• [18]Radzijevskaja J, Paulauskas A, Rosef O: Prevalence of Anaplasma phagocytophilum and Babesia divergens in Ixodes ricinus ticks from Lithuania and Norway. Int J Med Microbiol 2008, 298S1:218-221.
• [19]Zintl A, Finnerty EJ, Murphy TM, Waal TM, Gray J: Babesias of red deer (Cervus elaphus) in Ireland. Vet Res 2011, 42:7. BioMed Central Full Text
• [20]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. http://www.megasoftware.net webcite
• [21]Saitou N, Nei M: The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
• [22]Jukes TH, Cantor CR: Evolution of protein molecules. In Mammalian Protein Metabolism. Edited by Munro HN. Academic Press, New York; 1969:21-132.
• [23]Cassini R, Bonoli C, Montarsi F, Tessarin C, Marcer F, Galuppi R: Detection of Babesia EU1 in Ixodes ricinus ticks in northern Italy. Vet Parasitol 2010, 171:151-154.
• [24]Katargina O, Geller J, Vasilenko V, Kuznetsova T, Järvekűlg L, Vene S, Lundkvist Å, Golovljova I: Detection and characterization of Babesia species in Ixodes ticks in Estonia. Vector Borne Zoonotic Dis 2011, 11:923-928.
• [25]Cieniuch S, Stańczak J, Ruczaj A: The first detection of Babesia EU1 and Babesia canis canis in Ixodes ricinus ticks (Acari, Ixodidae) collected in urban and rural areas in northern Poland. Polish J Microbiol 2009, 58:231-236.
• [26]Becker CA, Bouju-Albert A, Jouglin M, Chauvin A, Malandrin L: Natural transmission of zoonotic Babesia spp. by Ixodes ricinus ticks. Emerg Infect Dis 2009, 15:320-322.
• [27]Bonnet S, Jouglin M, Malandrin L, Becker C, Agoulon A, L’Hostis M, Chauvin A: Transstadial and transovarial persistence of Babesia divergens DNA in Ixodes ricinus ticks fed on infected blood in a new skin-feeding technique. Parasitology 2007, 134:197-207.
• [28]Donnelly J, Peirce MA: Experiments on the transmission of Babesia divergens to cattle by the tick Ixodes ricinus. Int J Parasitol 1975, 5:363-367.
• [29]Malandrin L, Joughlin M, Sun Y, Brisseau N, Chauvin A: Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): Isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. Int J Parasitol 2010, 40:277-284.
• [30]Hilpertshauser H, Deplazes P, Schnyder M, Gern L, Mathis A: Babesia spp. Identified by PCR in ticks collected from domestic and wild ruminants in Southern Switzerland. Appl Environ Microbiol 2006, 72:6503-6507.
• [31]Rosef O, Paulauskas A, Radzijevskaja J: Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus in relation to the density of wild cervids. Acta Veterinaria Scandinavia 2009, 51(47):1-8.
• [32]Kik M, Nijhof AM, Balk JA, Jongejan F: Babesia sp. EU1 infection in a forest reindeer, the Netherlands. Emerg Infect Dis 2011, 17(5):936-938.
• [33]Langton C, Gray JS, Waters PF, Holman PJ: Naturally acquired babesiosis in a reindeer (Rangifer tarandus tarandus) herd in Great Britain. Parasitol Res 2003, 89:194-198.
• [34]Bartlett SL, Abou-Madi N, Messick JB, Birkenheuer A, Kollias GV: Diagnosis and treatement of Babesia odocoilei in captive reindeer (Rangifer tarandus tarandus) and recognition of three novel host species. J Zoo Wildl Med 2009, 440:152-159.