Guidelines for the Detection of Babesia and Theileria Parasites.

[en] The genera Babesia and Theileria (phylum Apicomplexa, order Piroplasmida) are mainly transmitted by Ixodid ticks in which the sexual part of their life cycle followed by sporogony takes place. They include protozoan parasites that infect erythrocytes of a variety of vertebrate hosts, including domestic and wild animals, with some Babesia spp. also infecting humans. Babesia sporozoites transmitted in the tick's saliva during the bloodmeal directly infect erythrocytes, where they asexually multiply to produce pear-shaped merozoites in the process of merogony; whereas a pre-erythrocytic schizogonic life stage in leukocytes is found in Theileria and precedes merogony in the erythrocytes. The wide spectrum of Babesia and Theileria species and their dissimilar characteristics with relation to disease severity, transmission, epidemiology, and drug susceptibility stress the importance of accurate detection of babesiosis and theileriosis and their causative agents. These guidelines review the main methods currently used for the detection of Babesia and Theileria spp. for diagnostic purposes as well as epidemiological studies involving their vertebrate hosts and arthropod vectors. Serological methods were not included once they did not indicate current infection but rather exposure.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Lempereur, Laetitia ; Université de Liège > Département des maladies infectieuses et parasitaires (DMI) > Parasitologie et pathologie des maladies parasitaires

Beck, Relja

Fonseca, Isabel

Marques, Catia

Duarte, Ana

Santos, Marcos

Zuquete, Sara

Gomes, Jacinto

Walder, Gernot

Domingos, Ana

More authors (5 more)

Language :

English

Title :

Guidelines for the Detection of Babesia and Theileria Parasites.

Publication date :

2017

Journal title :

Vector Borne and Zoonotic Diseases

ISSN :

1530-3667

eISSN :

1557-7759

Publisher :

Mary Ann Liebert, United States - New York

Volume :

Issue :

Pages :

51-65

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 January 2017

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Bibliography

Allsopp M, Allsopp B. Molecular sequence evidence for the reclassification of some Babesia species. Ann N Y Acad Sci 2006; 1081:509-517.
Avarzed A, Igarashi I, Kanemaru T, Hirumi K, et al. Improved in vitro cultivation of Babesia caballi. J Vet Med Sci 1997; 59:479-481.
Ayoob AL, Hackner SG, Prittie J. Clinical management of canine babesiosis. J Vet Emerg Crit Care 2010a; 20:77-89.
Ayoob AL, Prittie J, Hackner SG. Feline babesiosis. J Vet Emerg Crit Care 2010b; 20:90-97.
Baneth G, Florin-Christensen M, Cardoso L, Schnittger L. Reclassification of Theileria annae as Babesia vulpes sp. nov. Parasit Vectors 2015; 8:207.
Baneth G, Kenny MJ, Tasker S, Anug Y, et al. Infection with a proposed new subspecies of Babesia canis, Babesia canis subsp. presentii, in domestic cats. J Clin Microbiol 2004; 42: 99-105.
Bhoora R, Franssen L, Oosthuizen M, Guthrie A, et al. Sequence heterogeneity in the 18S rRNA gene within Theileria equi and Babesia caballi from horses in South Africa. Vet Parasitol 2009; 159:112-120.
Bock R, Jackson L, de Vos A, Jorgensen W. Babesiosis of cattle. Parasitology 2004; 129 Suppl:S247-S69.
Bonnet S, Michelet L, Moutailler S, Cheval J, et al. Identification of parasitic communities within European ticks using next-generation sequencing. PLoS Negl Trop Dis 2014; 8:e2753.
Boom R, Sol CJ, Salimans MM, Jansen CL, et al. Rapid and simple method for purification of nucleic-acids. J Clin Mi-crobiol 1990; 28:495-503.
Bosman AM, Oosthuizen MC, Venter EH, Steyl JC, et al. Ba-besia lengau associated with cerebral and haemolytic babe-siosis in two domestic cats. Parasit Vectors 2013; 6:128.
Brown CG. Theileriidae. In: Taylor AE, Baker JR, eds. In Vitro Methods for Parasite Cultivation. London: Academic Press, 1987:230-253.
Brown CG, Ilhan T, Kirvar E, Thomas M, et al. Theileria les-toquardi and T. annulata in cattle, sheep, and goats. In vitro and in vivo studies. Ann N Y Acad Sci 1998; 849:44-51.
Canning EU, Winger CM. Babesiidae. In: Taylor AE, Baker JR, eds. In Vitro Methods for Parasite Cultivation. London: Academic Press, 1987:199-229.
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.
Chae J, Lee J, Kwon O, Holman P, et al. Nucleotide sequence heterogeneity in the small subunit ribosomal RNA gene variable (V4) region among and within geographic isolates of Theileria from cattle, elk and white-tailed deer. Vet Parasitol 1998; 75:41-52.
Chapman W, Ward P. Babesia rodhaini: Requirement of complement for penetration of human erythrocytes. Science 1977; 196:67-70.
Conrad PA, Kjemtrup AM, Carreno RA, Thomford J, et al. Description of Babesia duncani n.sp. (Apicomplexa: Babe-siidae) from humans and its differentiation from other piro-plasms. Int J Parasitol 2006; 36:779-789.
Criado-Fornelio A, Gónzalez-del-Río MA, Buling-Saraña A, Barba-Carretero JC. The "expanding universe" of piro-plasms. Vet Parasitol 2004; 119:337-345.
Darghouth MA, Preston PM, Bouattour A, Kilani M. Theiler-iosis. In: Lefèvre P-C, Blancou J, Chermette R, Uilenberg G, eds. Infectious and Parasitic Diseases of Livestock. Paris: Editions TEC & Doc, 2010:1839-1866.
De Vos AJ, Potgieter FT. Bovine babesiosis. In: Coetzer JA, Thomson GR, Tustin RC, eds. Infectious Diseases of Livestock. Capetown, Southern Africa: Oxford University Press, 1994:278-294.
De Waal DT. Porcine babesiosis. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press, 2004:435-437.
De Waal DT, Van Heerden J. Equine piroplasmosis. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press, 2004:425-434.
Edwards KT, Goddard J, Varela-Stokes AS. Examination of the Internal Morphology of the Ixodid Tick, Amblyomma macu-latum Koch, (Acari: Ixodidae); a "How-to" Pictorial Dissection Guide. Midsouth Entomologist 2009; 2:28-39.
Entrican JH, Williams H, Cook IA, Lancaster WM, et al. Babe-siosis in man: a case from Scotland. Br Med J 1979; 2:474.
Figueroa JV, L'Hostis M, Camus E. Bovine babesiosis. In: Lefèvre P-C, Blancou J, Chermette R, Uilenberg G, eds. Infectious and Parasitic Diseases of Livestock, 2nd volume. Paris: Editions TEC & Doc, 2010:1819-1838.
Gharbi M, Latrach R, Sassi L, Darghouth MA. Evaluation of a simple Theileria annulata culture protocol from experimentally infected bovine whole blood. Parasite 2012; 19:281-283.
Grande N, Precigout E, Ancelin ML, Moubri K, et al. Continuous in vitro culture of Babesia divergens in a serum-free medium. Parasitology 1997; 115(Pt 1):81-89.
Gubbels JM, De Vos AP, Van Der Weide M, Viseras J, et al. Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol 1999; 37:1782-1789.
Halos L, Jamal T, Vial L, Maillard R, et al. Determination of an efficient and reliable method for DNA extraction from ticks. Vet Res 2004; 35:709-713.
Häselbarth K, Tenter AM, Brade V, Krieger G, et al. First case of human babesiosis in Germany-Clinical presentation and molecular characterisation of the pathogen. Int J Med Mi-crobiol 2007; 297:197-204.
Heim A, Passos LM, Ribeiro MF, Costa-Júnior LM, et al. Detection and molecular characterization of Babesia caballi and Theileria equi isolates from endemic areas of Brazil. Parasitol Res 2007; 102:63-68.
Herwaldt BL, Cacciò S, Gherlinzoni F, Aspöck H, et al. Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis 2003; 9:942-948.
Hildebrandt A, Hunfeld KP, Baier M, Krumbholz A, et al. First confirmed autochthonous case of human Babesia microti infection in Europe. Eur J Clin Microbiol Infect Dis 2007; 26: 595-601.
Hilpertshauser H, Deplazes P, Schnyder M, Gern L, et al. Ba-besia spp. identified by PCR in ticks collected from domestic and wild ruminants in Southern Switzerland. Appl Environ Microbiol 2006; 72:6503-6507.
Holman PJ, Becu T, Bakos E, Polledo G, et al. Babesia equi field isolates cultured from horse blood using a micro-centrifuge method. J Parasitol 1998; 84:696-699.
Holman PJ, Chieves L, Frerichs WM, Olson D, et al. Babesia equi erythrocytic stage continuously cultured in an enriched medium. J Parasitol 1994a; 80:232-236.
Holman PJ, Craig TM, Crider D, Petrini KR, et al. Culture isolation and partial characterisation of a Babesia sp. from a North American Elk (Cervus elaphus). JWildl Dis 1994b; 30:460-465.
Holman PJ, Frerichs WM, Chieves L, Wagner GG. Culture confirmation of the carrier status of Babesia caballi-infected horses. J Clin Microbiol 1993a; 31:698-701.
Holman PJ, Petrini K, Rhyan J, Wagner GG. In vitro isolation and cultivation of a Babesia from an American woodland caribou (Rangifer tarandus caribou). J Wildl Dis 1994c; 30:195-200.
Holman PJ, Waldrup KA, Droleskey RE, Corrier DE,et al. In vitro growth of Babesia bovis in white-tailed deer (Odocoileus vir-ginianus) erythrocytes. J Parasitol 1993b; 79:233-237.
Hooshmand-Rad P, Hawa NJ. Cultivation of Theileria hirci in sheep lymphoid cells. Trop Anim Health Prod 1975; 7:121-122.
Hooshmand-Rad P, Magnusson U, Uggla A. 1993. Some characteristics of ovine lymphoid cells infected in vivo by Theileria hirci. Parasitol Res1993; 79:195-199.
Hunfeld K, Hildebrandt A, Gray J. Babesiosis: Recent insights into an ancient disease. Int J Parasitol 2008; 38:1219-1237.
Hurtado A. Reverse line blot hybridization with species-specific oligonucleotide probes: Application to piroplasm detection. Methods Mol Biol 2015; 1247:183-192.
Jacobson LS. The South African form of severe and complicated canine babesiosis: Clinical advances 1994-2004. Vet Parasitol 2006; 138:126-139.
Jiang JF, Zheng YC, Jiang RR, Li H, et al. Epidemiological, clinical, and laboratory characteristics of 48 cases of "Ba-besia venatorum" infection in China: A descriptive study. Lancet Infect Dis 2015; 15:196-203.
Jongejan F, Perie NM, van de Scheur HC, Franssen FF, et al. Cultivation of Theileria. I. Attempts to complete the cycle of Theileria parva in vitro. Vet Q 1984; 6:37-40.
Katzer F, McKellar S, Ben Miled L, D'Oliveira C, et al. Selection for antigenic diversity of Tams1, the major merozoite antigen of Theileria annulata. Ann N Y Acad Sci 1998; 849: 96-108.
Katzer F, Ngugi D, Oura C, Bishop R, et al. Extensive genotypic diversity in a recombining population of the apicomplexan parasite Theileria parva. Infect Immun 2006; 74:5456-5464.
Kimbita EN, Silayo RS, Dolan TT. Theileria parva: In vitro studies on the effects of holding temperature, pH and medium on sporozoite infectivity. Trop Anim Health Prod 2004; 36: 341-351.
Kjemtrup AM, Conrad PA. Human babesiosis: An emerging tick-borne disease. Int J Parasitol 2000; 30:1323-1337.
Kjemtrup AM, Wainwright K, Miller M, Penzhorn BL, et al. Babesia conradae, sp. Nov., a small canine Babesia identified in California. Vet Parasitol 2006; 138:103-111.
Kurtti TJ, Munderloh UG, Irvin AD, Büscher G. Theileria parva: Early events in the development of bovine lympho-blastoid cell lines persistently infected with macroschizonts. Exp Parasitol 1981; 52:280-290.
Lawrence JA. Theileria buffeli/orientalis infection. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press, 2004a:500-501.
Lawrence JA. Theileriosis of sheep and goats. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press, 2004b: 498-499.
Lempereur L, De Cat A, Caron Y, Madder M, et al. First molecular evidence of potentially zoonotic Babesia microti and Babesia sp. EU1 in Ixodes ricinus ticks in Belgium. Vector Borne Zoonotic Dis 2011; 11:125-130.
Levy MG, Erp E, Ristic M. Cultivation of Babesia. In: Ristic M, Kreier JP, eds. Babesiosis. New York: Academic Press; 1981: 207-221.
Lewis D, Williams H. Infection of the Mongolian gerbil with the cattle piroplasm Babesia divergens. Nature 1979; 278:170-171.
Malandrin L, Jouglin M, Sun Y, Brisseau N, et al. 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.
Malandrin L, L'Hostis M, Chauvin A. Isolation of Babesia divergens from carrier cattle blood using in vitro culture. Vet Res 2004; 35:131-139.
Malmquist WA, Nyindo MB, Brown CD. East Coast Fever: Cultivation in vitro of bovine spleen cell lines infected and transformed by Theileria parva. Trop Animal Health Prod 1970; 2:139-145.
Marx RE, Stern D. Oral and Maxillofacial Pathology: A Rationale for Diagnosis and Treatment. Chicago, IL: Quintessence, 2003:684.
Mehlhorn H. Encyclopedia of Parasitology. Berlin, Germany: Springer-Verlag, 2008.
Michelet L, Delannoy S, Devillers E, Umhang G, et al. High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol 2014; 4:103.
Miranda JP, Nascimento EM, Cruz HJ, Yin H, et al. Establishment of optimal conditions for long-term culture of erythrocytic stages of Theileria uilenbergi. Am J Vet Res 2006; 67:1908-1913.
Morrison WI. The aetiology, pathogenesis and control of thei-leriosis in domestic animals. Rev Sci Tech 2015; 34:599-611.
Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ, et al. Current advances in detection and treatment of babesiosis. Curr Med Chem 2012; 19:1504-1518.
Palmer DA, Buening GM, Carson CA. Cryopreservation of Babesia bovis for in vitro cultivation. Parasitology 1982; 84(Pt 3):567-572.
Pipano E, Shkap V, 2004. Theileria annulata theileriosis. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press, 2004:486-497.
Purnell RE. Babesiosis in various hosts. In: Ristic M, Kreier JP, eds. Babesiosis. New York: Academic Press, 1981:25-64.
Rahikainen A, Palo J, de Leeuw W, Budowle B, et al. DNA quality and quantity from up to 16 years old post-mortem blood stored on FTA cards. Forensic Sci Int 2016; 261: 148-153.
Ristic M, Levy MG. A new era of research toward solution of bovine babesiosis. In: Ristic M, Kreier JP, eds. Babesiosis. New York: Academic Press, 1981:509-544.
Rodriguez SD, Buening GM, Green TJ, Carson CA. Cloning of Babesia bovis by in vitro cultivation. Infect Immun 1983; 42: 15-18.
Santos M, Soares R, Costa P, Amaro A, et al. Revisiting the Tams1-encoding gene as a species-specific target for the molecular datection of Theileria annulata in bovine blood samples. Ticks Tick Borne Dis 2013; 4:72-77.
Schetters TP, Moubri K, Précigout E, Kleuskens J, et al. Different Babesia canis isolates, different diseases. Parasitology 1997; 115(Pt 5):485-493.
Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: A world emerging. Infect Genet Evol 2012; 12: 1788-1809.
Schnittger L, Yin H, Qi B, Gubbels MJ, et al. Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. 2004; 92:189-196.
Sharma G, Sharma RD, Nichani AK. Successful long-term in vitro cultivation of Theileria annulata schizonts in media supplemented with homologous and heterologous sera. Vet Parasitol 1998; 79:135-141.
Shkap V, Frank M, Fish L, Pipano E. Theileria annulata: In vitro cultivation of schizont-infected bovine lymphocytes. Vet Parasitol 1996; 65:11-20.
Sibeko KP, Oosthuizen MC, Collins NE, Geysen D, et al. Development and evaluation of a real-time polymerase chain reaction test for the detection of Theileria parva infections in Cape buffalo (Syncerus caffer) and cattle. Vet Parasitol 2008; 155:37-48.
Smith RP, Jr., Elias SP, Borelli TJ, Missaghi B, et al. Human babesiosis, Maine, USA, 1995-2011. Emerg Infect Dis 2014; 20:1727-1730.
Solano-Gallego L, Baneth G. Babesiosis in dogs and cats-Expanding parasitological and clinical spectra. Vet Parasitol 2011; 181:48-60.
Stagg DA, Brown CG, Crawford JG, Kanhai GK, et al. In vitro cultivation of Theileria lawrencei-infected lymphoblastoid cell lines derived from a buffalo (Syncerus caffer). Res Vet Sci 1974; 16:125-127.
Stagg DA, Kanhai GK, Young AS, Brown CG. The establishment of Theileria-infected cell lines from an eland (Tauro-tragus oryx, Lydekker 1906). Res Vet Sci 1976; 20:122-126.
Sunaga F, Namikawa K, Kanno Y. Continuous in vitro culture of erythrocytic stages of Babesia gibsoni and virulence of the cultivated parasite. J Vet Med Sci 2002; 64:571-575.
Timms P, Dalgliesh RJ, Barry DN, Dimmock CK, et al. Babesia bovis: Comparison of culture-derived parasites, non-living antigen and conventional vaccine in the protection of cattle against heterologous challenge. Aust Vet J 1983; 60:75-77.
Trager W, Jensen JB. Human malaria in continuous culture. Science 1976; 193:673-675.
Tretina K, Gotia HT, Mann DJ, Silva JC. Theileria-transformed bovine leukocytes have cancer hallmarks. Trends Parasitol 2015; 31:306-314.
Ueti MW, Palmer GH, Kappmeyer LS, Scoles GA, et al. Expression of equi merozoite antigen 2 during development of Babesia equi in the midgut and salivary gland of the vector tick Boophilus microplus. J Clin Microbiol 2003; 41:5803-5809.
Uilenberg G. Babesia-A historical overview. Vet Parasitol 2006; 138:3-10.
Uilenberg G. Theilerial species of domestic livestock. In: Irvin AD, Cunningham MP, Young AS, eds. Advances in the Control of Theileriosis. The Hague, Netherlands: Martinus Nijhoff Publishers, 1981:4-37.
Urquhart GM, Armour J, Duncan JL, Dunn AM, et al. In: Veterinary Protozoology, 2nd edition. Oxford: Blackwell Science Ltd, 1996:239.
Vega CA, Buening GM, Green TJ, Carson CA. In vitro cultivation of Babesia bigemina. Am J Vet Res 1985; 46:416-420.
WangG,VillafuerteP,ZhugeJ,VisintainerP,etal. Comparison of a quantitative PCR assay with peripheral blood smear examination for detection and quantitation of Babesia microti infection in humans. Diagn Microbiol Infect Dis 2015; 82:109-113.
Wiegmann L, Silaghi C, Obiegala A, Karnath C, et al. Occurrence of Babesia species in captive reindeer (Rangifer tar-andus) in Germany. Vet Parasitol 2015; 211:16-22.
Wilson M, Glaser KC, Adams-Fish D, Boley M, et al. Development of droplet digital PCR for the detection of Babesia microti and Babesia duncani. Exp Parasitol 2015; 149:24-31.
Wise LN, Kappmeyer LS, Mealey RH, Knowles DP. Review of equine piroplasmosis. J Vet Intern Med 2013;27:1334-1346.
Yabsley MJ, Shock BC. Natural history of Zoonotic Babesia: Role of wildlife reservoirs. Int J Parasitol Parasites Wildl 2012;2:18-31.
Yeruham I, Hadani A. Ovine babesiosis. In: Coetzer JA, Tustin RC, eds. Infectious Diseases of Livestock, 2nd edition. Capetown, Southern Africa: Oxford University Press; 2004:438-445.
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.
Zintl A, Mulcahy G, Skerrett HE, Taylor SM, et al. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev 2003; 16:622-636.
Zintl A, Westbrook C, Mulcahy G, Skerrett HE, et al. Invasion, and short- and long-term survival of Babesia divergens (Phylum Apicomplexa) cultures in non-bovine sera and erythrocytes. Parasitology 2002; 124(Pt 6):583-588.
Zweygarth E, Benade J, Steyl J, Prozesky L, et al. In vitro cultivation of a Theileria species from a roan antelope (Hippotragus equinus). Parasitol Res 2009b; 105:1755-1757.
Zweygarth E, Just MC, de Waal DT. Continuous in vitro cultivation of erythrocytic stages of Babesia equi. Parasitol Res 1995; 81:355-358.
Zweygarth E, Koekemoer O, Josemans AI, Rambritch N, et al. Theileria-infected cell line from an African buffalo (Syncerus caffer). Parasitol Res 2009a; 105:579-581.
Zweygarth E, Lopez-Rebollar LM. Continuous in vitro cultivation of Babesia gibsoni. Parasitol Res 2000; 86:905-907.31.