First report on Babesia cf. microti infection of red foxes (Vulpes vulpes) from Hungary

Particle and Fibre Toxicology

Gad Baneth¹  Sándor Hornok³  Yaarit Nachum-Biala¹  Ákos Hornyák²  Nóra Takács³  Róbert Farkas³ 

[1] School of Veterinary Medicine, Hebrew University of Jerusalem, Jerusalem, Israel;Veterinary Diagnostic Directorate, National Food Chain Safety Office, Budapest, Hungary;Department of Parasitology and Zoology, Faculty of Veterinary Science, Szent István University, Budapest, Hungary

关键词: Hungary;    Babesia cf. microti;    Theileria annae;    Vulpes vulpes;    Red fox;   

Others  :  1147326
DOI  :  10.1186/s13071-015-0660-5

 received in 2014-11-12, accepted in 2015-01-13,  发布年份 2015

【 摘 要 】

Background

To date, only one report of a small Babesia infection based on microscopic observation which caused babesiosis in two dogs in Hungary has been published. Babesiosis due to Babesia canis - which is endemic in the local dogs - has only been detected in captive grey wolves. No information is available on babesial/theilerial infections in red foxes in Hungary. The aim of the study was to screen red foxes in Hungary for babesial parasites by PCR and to compare their partial 18S rRNA gene sequences to those parasites of domestic dogs and wild canids from other countries.

Methods

Blood samples of 404 red foxes originating from 316 locations representing all 19 Hungarian counties were screened in Hungary for babesial parasites by PCR and the partial 18S rRNA gene sequences were compared to those parasites of domestic dogs and wild canids from other countries.

Results

Altogether 81 red foxes out of 404 (20.0%; 95% CI: 16.4–24.2%) shot in 74 locations and in 17 of the 19 Hungarian counties were found to be infected with Babesia cf. microti by PCR.

Conclusions

This is the first report to demonstrate the occurrence of Babesia cf. microti in Hungary, and its widespread presence in the fox population throughout the country. Further studies are needed to identify the tick species involved in its transmission, and whether other mechanisms of transmission are involved in its spread in fox populations.

【 授权许可】

   
2015 Farkas et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Irwin P. Canine babesiosis: from molecular taxonomy to control. Parasites Vect. 2009; 2 Suppl 1:S4. BioMed Central Full Text
• [2]Boozer AL, Macintire DK. Canine babesiosis. Vet Clin North Am Small Anim Pract. 2003; 33:885-904.
• [3]Kjemtrup AM, Kocan AA, Whitworth L, Meinkoth J, Birkenheuer AJ, Cummings J, Boudreaux MK, Stockham SL, Irizarry-Rovira A, Conrad PA. There are at least three genetically distinct small piroplasms from dogs. Int J Parasitol. 2000; 30:1501-1505.
• [4]Criado-Fornelio A, Martinez-Marcos A, Bulin-Sarana A, Barba-Carretero JC. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I. Epizootiological aspects. Vet Parasitol. 2003; 113:189-201.
• [5]Matjila PT, Leisewitz AL, Oosthuizen MC, Jongejan F, Penzhorn BL. Detection of a Theileria species in dogs in South Africa. Vet Parasitol. 2008; 157:34-40.
• [6]Zahler M, Rinder H, Schein E, Gothe R. Detection of a new pathogenic Babesia microti-like species in dogs. Vet Parasitol. 2000; 89:241-248.
• [7]Yeagley TJ, Reichard MV, Hempstead JE, Allen KE, Parsons LM, White MA, Little SE, Meinkoth JH. Detection of Babesia gibsoni and the canine small Babesia ’Spanish isolate’ in blood samples obtained from dogs confiscated from dogfighting operations. J Am Vet Med Assoc. 2009; 235:535-539.
• [8]Camacho AT, Pallas E, Gestal JJ, Guitián FJ, Olmeda AS, Goethert HK, Telford SR. Infection of dogs in northwest Spain with a Babesia microti-like agent. Vet Rec. 2001; 149:552-555.
• [9]Guitián FJ, Camacho AT, Telford SR. Case–control study of canine infection by a newly recognised Babesia microti-like piroplasm. Prev Vet Med. 2003; 61:137-145.
• [10]Camacho AT, Guitian EJ, Pallas E, Gestal JJ, Olmeda AS, Goethert HK, Telford SR, Spielman A. Azotemia and mortality among Babesia microti-like infected dogs. J Vet Intern Med. 2004; 18:141-146.
• [11]Camacho-García AT. Piroplasma infection in dogs in northern Spain. Vet Parasitol. 2006; 138:97-102.
• [12]Beck R, Vojta L, Mrljak V, Marinculić A, Beck A, Živičnjak T, Cacciò SM. Diversity of Babesia and Theileria species in symptomatic and asymptomatic dogs in Croatia. Int J Parasitol. 2009; 39:843-848.
• [13]Simões PB, Cardoso L, Araújo M, Yisaschar-Mekuzas Y, Baneth G. Babesiosis due to the canine Babesia microti-like small piroplasm in dogs - first report from Portugal and possible vertical transmission. Parasites Vect. 2011; 4:50. BioMed Central Full Text
• [14]Criado-Fornelio A, Rey-Valeiron C, Buling A, Barba-Carretero JC, Jefferies R, Irwin P. New advances in molecular epizootiology of canine hematic protozoa from Venezuela, Thailand and Spain. Vet Parasitol. 2007; 144:261-269.
• [15]Gimenez C, Casado N, Criado-Fornelio A, de Miguel FA, Dominguez-Peñafiel G. Molecular survey of Piroplasmida and Hepatozoon isolated from domestic and wild animals in Burgos (northern Spain). Vet Parasitol. 2009; 162:47-50.
• [16]Lledó L, Giménez-Pardo C, Domínguez-Peñafiel G, Sousa R, Gegúndez MI, Casado N, Criado A. Molecular detection of hemoprotozoa and Rickettsia species in arthropods collected from wild animals in the Burgos Province, Spain. Vector Borne Zoonotic Dis. 2010; 10:735-738.
• [17]Pietrobelli M, Cancrini G, Moretti A, Tampieri MP. Animal babesiosis: an emerging zoonosis in Italy? Parassitologia. 2007; 49(S1):33-38.
• [18]Tampieri MP, Galuppi R, Bonoli C, Cancrini G, Moretti A, Pietrobelli M. Wild ungulates as Babesia hosts in northern and central Italy. Vector-Borne Zoonot. 2008; 8(5):667-674.
• [19]Zanet S, Trisciuoglio A, Bottero E, de Mera IG F, Gortazar C, Carpignano MG, Ferroglio E. Piroplasmosis in wildlife: Babesia and Theileria affecting free-ranging ungulates and carnivores in the Italian Alps. Parasites Vect. 2014; 7:70. BioMed Central Full Text
• [20]Dezdek D, Vojta L, Curković S, Lipej Z, Mihaljević Z, Cvetnić Z, Beck R. Molecular detection of Theileria annae and Hepatozoon canis in foxes (Vulpes vulpes) in Croatia. Vet Parasitol. 2010; 172:333-336.
• [21]Cardoso L, Cortes HC, Reis A, Rodrigues P, Simões M, Lopes AP, Vila-Viçosa MJ, Talmi-Frank D, Eyal O, Solano-Gallego L, Baneth G. Prevalence of Babesia microti-like infection in red foxes (Vulpes vulpes) from Portugal. Vet Parasitol. 2013; 196(1–2):90-95.
• [22]Najm NA, Meyer-Kayser E, Hoffmann L, Herb I, Fensterer V, Pfister K et al.. A molecular survey of Babesia spp. and Theileria spp. in red foxes (Vulpes vulpes) and their ticks from Thuringia, Germany. Ticks Tick Borne Dis. 2014; 5(4):386-391.
• [23]Duscher GG, Hans-Peter Fuehrer H, Kübber-Heiss A. Fox on the run – molecular surveillance of fox blood and tissue for the occurrence of tick-borne pathogens in Austria. Short Report. Parasites Vect. 2014; 7:521.
• [24]Goethert HK, Telford SR. What is Babesia microti? Parasitology. 2003; 127(Pt 4):301-309.
• [25]Clancey N, Horney B, Burton S, Birkenheuer A, McBurney S, Tefft K. Babesia (Theileria) annae in a red fox (Vulpes vulpes) from Prince Edward Island, Canada. J Wild Dis. 2010; 46(2):615-621.
• [26]Birkenheuer AJ, Horney B, Bailey M, Scott M, Sherbert B, Catto V, Marr HS, Camacho AT, Ballman AE. Babesia microti-like infections are prevalent in North American foxes. Vet Parasitol. 2010; 172:179-182.
• [27]Camacho AT, Pallas E, Gestal JJ, Guitián FJ, Olmeda AS, Telford SR, Spielman A. Ixodes hexagonus is the main candidate as vector of Theileria annae in northwest Spain. Vet Parasitol. 2003; 112:157-163.
• [28]Földvári G, Hell E, Farkas R. Babesia canis canis in dogs from Hungary: detection by PCR and sequencing. Vet Parasitol. 2005; 127:221-226.
• [29]Hornok S, Edelhofer R, Farkas R. Seroprevalence of canine babesiosis in Hungary suggesting breed predisposition. Parasitol Res. 2006; 99:638-642.
• [30]Farkas R, Földvári G, Fenyves B, Szilágyi A, Kótai I, Hegedűs GYT. First detection of small babesiae in dogs in Hungary. Vet Rec. 2004; 154:176-178.
• [31]Erdélyi K, Mezősi L, Vladov S, Földvári G. Fatal acute babesiosis in captive grey wolves (Canis lupus) due to Babesia canis. Ticks Tick Borne Dis. 2014; 5(3):281-283.
• [32]Casati S, Sager H, Gern L, Piffaretti JC. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med. 2006; 13:65-70.
• [33]Farkas R, Solymosi N, Takács N, Hornyák Á, Hornok S, Nachum-Biala Y, Baneth G. First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasites Vect. 2014; 7:303. BioMed Central Full Text
• [34]Hillyard PD. Ticks of North-West Europe. Backhuys Publishers, London. UK; 1996.
• [35]Babos S: Kullancsok – Ixodidea. Fauna Hungariae 77. XVIII. kötet, Arachnoidea 7. füzet. Akadémia Kiadó, Budapest 1965, 38 pp.
• [36]Sréter T, Széll Z, Varga I. Ectoparasite infestations of red foxes (Vulpes vulpes) in Hungary. Vet Parasitol. 2003; 115:349-354.
• [37]Cassini R, Zanutto S, Frangipane del Rogalbono A, Gabrielli S, Calderini P, Moretti A, Tampieri MP, Pietrobelli M. Canine piroplasmosis in Italy: epidemiological aspects in vertebrate and invertebrate hosts. Vet Parasitol. 2009; 165:30-35.
• [38]Iori A, Gabrielli S, Calderini P, Moretti A, Pietrobelli M, Tampieri MP, Galuppi R, Cancrini G. Tick reservoirs for piroplasms in central and northern Italy. Vet Parasitol. 2010; 170:291-296.
• [39]Falkenö U, Tasker S, Osterman-Lind E, Tvedten HW. Theileria annae in a young Swedish dog. Case report. Acta Vet Scand. 2013; 55:50. BioMed Central Full Text
• [40]Matsuu A, Kawabe A, Koshida Y, Ikadai H, Okano S, Higuchi S. Incidence of canine Babesia gibsoni infection and subclinical infection among Tosa dogs in Aomori Prefecture. Japan. J Vet Med Sci. 2004; 66:893-897.
• [41]Szabó L, Heltai M, Szűcs E, Lanszki J, Lehoczki R. Expansion range of the golden jackal in Hungary between 1997 and 2006. Mammalia. 2009; 73:307-311.
• [42]Schoop G, Dedié K. Uebertragung von Babesia canis auf Füchse. Deut Tierärtzl Wochschr. 1938; 46:88-90.
• [43]Gray J, Stedingk LV, Gürtelschmid M, Granström M. Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. J Clin Microbiol. 2002; 40(4):1259-1263.