Characteristics, immunological events, and diagnostics of Babesia spp. infection, with emphasis on Babesia canis

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Abstract

Vector-borne infection constitutes a significant health issue in dogs worldwide. Recent reports point to an increasing number of canine vector-borne disease cases in European countries, including Poland. Canine babesiosis caused by various Babesia species is a protozoal tick-borne disease with worldwide distribution and significant veterinary importance. The development and application of molecular methods have increased our knowledge about canine babesiosis, its prevalence, and clinical and pathological aspects of the infection. Parasitologists and veterinary surgeons need an accurate description of the species responsible for canine babesiosis to improve diagnostic and therapeutic methods, as well as predictions for the course of the disease. Therefore, we decided to summarise recent knowledge concerning Babesia species and B. canis.

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  • 1. Abrahamsen M.S. Templeton T.J. Enomoto S. Abrahante J.E. Zhu G. Lancto C.A. Deng M. Liu C. Widmer G. Tzipori S. Buck G.A. Xu P. Bankier A.T. Dear P.H. Konfortov B.A. Spriggs H.F. Iyer L. Anantharaman V. Aravind L. Kapur V.: Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science 2004 304 441-445.

  • 2. Adaszek L. Winiarczyk S.: Molecular characterization of Babesia canis canis isolates from naturally infected dogs in Poland. Vet Parasitol 2008 152 235-241.

  • 3. Adaszek L. Winiarczyk S. Skrzypczak M.: The clinical course of babesiosis in 76 dogs infected with protozoan parasites Babesia canis canis. Pol J Vet Sci 2009 12 81-87.

  • 4. Allred D.R. Al Khedery B.: Antigenic variation of cytoadhesion in Babesia bovis and Plasmodium falciparum: different logics achieve the same goal. Mol Biochem Parasitol 2004 134 27-35.

  • 5. Alonso M. Blandino T. Mendoza E. Savon L. Camacho M.: Development of a Babesia bovis live attenuated vaccine. Arch Med Res 1993 25 273-277.

  • 6. Baneth G. Florin-Christensen M. Cardoso L. Schnittger L.: Reclassification of Theileria annae as Babesia vulpes sp. nov. Parasite Vectors 2015 8 207.

  • 7. Brayton K.A. Lau A.O.T. Herndon D.R. Hannick L. Kappmeyer L.S. Berens S.J. Bidwell S.L. Brown W.C. Crabtree J. Fadrosh D. Feldblum T. Forberger H.A. Haas B.J. Howell J.M. Khouri H. Koo H. Mann D.J. Norimine J. Paulsen I.T. Radune D. Ren Q. Smith Jr. R.K. Suarez C.E. White O. Wortman J.R. Knowles Jr. D.P. McElwain T.F. Nene V.M.: Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 2007 3 1401-1413.

  • 8. Cacciò S. Cammà C. Onuma M. Severini C.: The β-tubulin gene of Babesia and Theileria parasites is an informative marker for species discrimination. Int J Parasitol 2000 30 1181-1185.

  • 9. Carcy B. Précigout E. Schetters T. Gorenflot A.: Genetic basis for GPI-anchor merozoite surface antigen polymorphism of Babesia and resulting antigenic diversity. Vet Parasitol 2006 138 33-49.

  • 10. Carcy B. Randazzo S. Depoix D. Adaszek L. Cardoso L. Baneth G. Gorenflot A. Schetters T.P.: Classification of Babesia canis strains in Europe based on polymorphism of the Bc28.1-gene from the Babesia canis Bc28 multigene family. Vet Parasitol 2015 doi:10.1016/j.vetpar.2015.05.028

  • 11. Carret C. Walas F. Carcy B. Grande N. Précigout E. Moubri K. Schetters T.P. Gorenflot A.: Babesia canis canis Babesia canis vogeli Babesia canis rossi: differentiation of the three subspecies by a restriction fragment length polymorphism analysis on amplified small subunit ribosomal RNA genes. J Eukaryot Microbiol 1999 46 293-303.

  • 12. Callow L.L. Dalgliesh R.J. De Vos A.J.: Development of effective living vaccines against bovine babesiosis-the longest field trial? Int J Parasitol 1997 27 747-767.

  • 13. Cornillot E. Hadj-Kaddour K. Dassouli A. Noel B. Ranwez V. Vacherie B. Augagneur Y. Brès V. Duclos A. Randazzo S. Carcy B. Debierre-Grockiego F. Delbecq S. Moubri-Ménage K. Shams-Eldin H. Usmani-Brown S. Bringaud F. Wincker P. Vivarès C.P. Schwarz R.T. Schetters T.P. Krause P.J. Gorenflot A. Berry V. Barbe V. Mamoun C.B.: Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Res 2012 40 9102-9114.

  • 14. Costa-Júnior L.M. Rabelo É.M.L. Martins O.A. Ribeiro M.F.B.: Comparison of different direct diagnostic methods to identify Babesia bovis and Babesia bigemina in animals vaccinated with live attenuated parasites. Vet Parasitol 2006 139 231-236.

  • 15. Cuesta I. González L.M. Estrada K. Grande R. Zaballos Á. Lobo C.A. Barrera J. Sanchez-Flores A. Montero E.: Highquality draft genome sequence of Babesia divergens the etiological agent of cattle and human babesiosis. Genome announcements 2014 2 e01194-14.

  • 16. Depoix D. Carcy B. Jumas-Bilak E. Pages M. Precigout E. Schetters T.P. Ravel C. Gorenflot A.: Chromosome number genome size and polymorphism of European and South-African isolates of large Babesia parasites that infect dogs. Parasitology 2002 125 16-20.

  • 17. De Waal D.T. Combrink M.P.: Live vaccines against bovine babesiosis. Vet Parasitol 2006 138 88-96.

  • 18. Ellis J. Hefford C. Baverstock P.R. Dalrymple B.P. Johnson A. M.: Ribosomal DNA sequence comparison of Babesia and Theileria. Mol Biochem Parasit 1992 54 87-95.

  • 19. Eugui E.M. Allison A.C.: Differences in susceptibility of various mouse strains to haemoprotozoan infections: possible correlation with natural killer activity. Parasitol Immunol 1980 2 277-292.

  • 20. Fichera M.E. Roos D.S.: A plastid organelle as a drug target in apicomplexan parasites. Nature 1997 390 407-409.

  • 21. Freyburger L. Lemaitre L. Medaille C. Oberli F. Fanchon L. Bergamo P.: Comparative safety study of two commercialised vaccines against canine babesiosis induced by Babesia canis. Parasite 2011 18 311-318.

  • 22. Fukumoto S. Xuan X. Inoue N. Igarashi I. Sugimoto C. Fujisaki K. Nagasawa H. Mikami T. Suzuki H.: Molecular characterization of a gene encoding a 29-kDa cytoplasmic protein of Babesia gibsoni and evaluation of its diagnostic potentiality. Mol Biochem Parasitol 2003 131 129-136.

  • 23. Furuta P.I. Oliveira T.M.F.D.S. Teixeira M.C.A. Rocha A.G. Machado R.Z. Tinucci-Costa M.: Comparison between a soluble antigen-based ELISA and IFAT in detecting antibodies against Babesia canis in dogs. Revista Brasil Parasitol Vet 2009 18 41-45.

  • 24. Gardner M.J. Bishop R. Shah T. de Villiers E.P. Carlton J.M. Hall N. Ren Q. Paulsen I.T. Pain A. Berriman M. Wilson R.J.M. Sato S. Ralph S.A. Mann D.J. Xiong Z. Shallom S.J. Weidman J. Jiang L. Lynn L.J. Weaver B. Shoaibi A. Domingo A.R. Wasawo D. Crabtree J. Wortman J.R. Haas B. Angiuoli S.V. Creasy T.H. Lu C. Suh B. Silva J.C. Utterback T.R. Feldblyum T.V. Pertea M. Allen J. Nierman W.C. Taracha E.L.N. Salzberg S.L. White O.R. Fitzhugh H.A. Morzaria S. Venter J.C. Fraser C.M. Nene V.: Genome sequence of Theileria parva a bovine pathogen that transforms lymphocytes. Science 2005 309 134-137.

  • 25. Gardner M.J. Hall N. Fung E. White O. Berriman M. Hyman R.W. Carlton J.M. Pain A. Nelson K.E. Bowman S. Paulsen I.T. James K. Eisen J.A. Rutherford K. Salzberg S.L. Craig A. Kyes S. Chan M. Nenel V. Shallom S.J. Suh B. Peterson J. Angiuoli S. Pertea M. Allen J. Selengut J. Haft D. Mather M.W. Vaidya A.B. Martin D.M.A. Fairlamb A.H. Fraunholz M.J. Roos D.S. Ralph S.A. McFadden G.I. Cummings L.M. Subramanian G.M. Mungall C. Venter J.C. Carucci D.J. Hoffman S.L. Newbold C. Davis R.W. Fraser C.M. Barrell B.: Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002 419 498-511.

  • 26. Goff W.L. McElwain T.F. Suarez C.E. Johnson W.C. Brown W.C. Norimine J. Knowles Jr. D.P.: Competitive enzyme-linked immunosorbent assay based on a rhoptryassociated protein 1 epitope specifically identifies Babesia bovisinfected cattle. Clin Diagn Lab Immunol 2003 10 38-43.

  • 27. Goodger B.V.: Preparation and preliminary assessment of purified antigens in the passive haemagglutination test for bovine babesiosis. Aust Vet J 1971 47 251-256.

  • 28. Gray J. Zintl A. Hildebrandt A. Hunfeld K.P. Weiss L.: Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis 2010 1 3-10.

  • 29. Homer M.J. Aguilar-Delfin I. Telford S.R. Krause P.J. Persing D.H.: Babesiosis. Clin Microbiol Rev 2000 13 451-469.

  • 30. Irwin P.J.: Canine babesiosis: from molecular taxonomy to control. Parasite Vectors 2009 2 Suppl. 1 S4.

  • 31. Jackson A.P. Otto T.D. Darby A. Ramaprasad A. Xia D. Echaide I.E. Farber M. Gahlot S. Gamble J. Gupta D. Gupta Y. Jackson L. Malandrin L. Malas T.B. Moussa E. Nair M. Reid A.J. Sanders M. Sharma J. Tracey A. Quail M.A. Weir W. Wastling J.M. Hall N. Willadsen P. Lingelbach K. Shiels B. Tait A. Berriman M. Allred D.R. and Pain A.: The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying hostparasite interaction. Nucleic Acids Res 2014 42 7113-7131.

  • 32. Kirtz G. Leschnik M. Hooijberg E. Tichy A. Leidinger E.: Inclinic laboratory diagnosis of canine babesiosis (Babesia canis canis) for veterinary practitioners in Central Europe. Tierärztliche Praxis Kleintiere 2012 40 87-94.

  • 33. Kjemtrup A.M. Conrad P.A.: A review of the small canine piroplasms from California: Babesia conradae in the literature. Vet Parasitol 2006 138 112-117.

  • 34. Knowles Jr. D.P. Kappmeyer L.S. Perryman L.E.: Specific immune responses are required to control parasitemia in Babesia equi infection. Infect Immun 1994 62 1909-1913.

  • 35. Kratzer I.: Die Brauchbarkeit der Babesia rodhaini Antigene zum Nachweis von Babesia Infektionen im ELISA. Dissertation. Veterinm T Faculty University of Munich Munich 1979.

  • 36. Kubelová M. Sedlák K. Panev A. Široký P.: Conflicting results of serological PCR and microscopic methods clarify the various risk levels of canine babesiosis in Slovakia: A complex approach to Babesia canis diagnostics. Vet Parasitol 2013 191 353-357.

  • 37. Lau A.O.T.: An overview of the Babesia Plasmodium and Theileria genomes: a comparative perspective. Mol Biochem Parasitol 2009 164 1-8.

  • 38. Levine N.D.: The protozoan phylum Apicomplexa. Volume I. Volume II. CRC Press Inc 1988.

  • 39. López G. Todorovic R.A.: Rapid latex agglutination (RLA) test for the diagnosis of Babesia argentina. Vet Parasitol 1978 4 1-9.

  • 40. Mahoney D.F.: Bovine babesiosis: diagnosis of infection by a complement fixation test. Aust Vet J 1962 38 48-52.

  • 41. Martin A.R. Dunstan R.H. Roberts T.K. Brown G.K.: Babesia canis vogeli: a novel PCR for its detection in dogs in Australia. Exp Parasitol 2006 112 63-65.

  • 42. Matijatko V. Torti M. Schetters T.P.: Canine babesiosis in Europe: how many diseases? Trends Parasitol 2012 28 99-105.

  • 43. Moreau E. Bonsergent C. Al Dybiat I. Gonzalez L.M. Lobo C.A. Montero E. Malandrin L.: Babesia divergens apical membrane antigen-1 (BdAMA-1): A poorly polymorphic protein that induces a weak and late immune response. Exp Parasitol 2015 155 40-45.

  • 44. Morrissette N.S. Sibley L.D.: Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 2002 66 21-38.

  • 45. Nascimento E.M. Nogueira N. Silva T. Braschler T. Demierre N. Renaud P. Oliva A.G.: Dielectrophoretic sorting on a microfabricated flow cytometer: label free separation of Babesia bovis infected erythrocytes. Bioelectrochemistry 2008 73 123-128.

  • 46. Pedroni M.J. Sondgeroth K.S. Gallego-Lopez G.M. Echaide I. Lau A.O.T.: Comparative transcriptome analysis of geographically distinct virulent and attenuated Babesia bovis strains reveals similar gene expression changes through attenuation. BMC Genomics 2013 14 763-776.

  • 47. Reid A.J. Vermont S.J. Cotton J.A. Harris D. Hill- Cawthorne G.A. Könen-Waisman S. Latham S.M. Mourier T. Norton R. Quail M.A. Sanders M. Shanmugam D. Sohal A. Wasmuth J.D. Brunk B. Grigg M. E. Howard J.C. Parkinson J. Roos D.S. Trees A.J. Berriman M. Pain A. Wastling J.M.: Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: coccidia differing in host range and transmission strategy. PLoS Pathog 2012 8 e1002567.

  • 48. Schetters T.: Vaccination against canine babesiosis. Trends Parasitol 2005 21 179-184.

  • 49. Schetters T.P. Kleuskens J.A.G.M. Van De Crommert J. De Leeuw P.W.J. Finizio A.L. Gorenflot A.: Systemic inflammatory responses in dogs experimentally infected with Babesia canis; a haematological study. Vet Parasitol 2009 162 7-15.

  • 50. Schnittger L. Rodriguez A.E. Florin-Christensen M. Morrison D.A.: Babesia: a world emerging. Infect Genet Evol 2012 12 1788-1809.

  • 51. Sibley L.D.: Intracellular parasite invasion strategies. Science 2004 304 248-253.

  • 52. Solano-Gallego L. Baneth G.: Babesiosis in dogs and catsexpanding parasitological and clinical spectra. Vet Parasitol 2011 181 48-60.

  • 53. Striepen B. Jordan C.N. Reiff S. Van Dooren G.G.: Building the perfect parasite: cell division in apicomplexa. PLoS Pathog 2007 3 e78.

  • 54. Sun Y. Li S.G. Jiang J.F. Wang X. Zhang Y. Wang H. Cao W.C.: Babesia venatorum infection in child China. Emerg Infect Dis 2014 20 896.

  • 55. Sunaga F. Arai S. Itoh S. Taharaguchi S.: Protective efficacy of Babesia gibsoni culture-derived exoantigens against the challenge infection in dogs. Parasitol Res 2014 113 1681-1686.

  • 56. Uilenberg G.: Babesia-a historical overview. Vet Parasitol 2006 138 3-10.

  • 57. Vercammen F. De Deken R. Maes L.: Clinical and serological observations on experimental infections with Babesia canis and its diagnosis using the IFAT. Parasite 1995 2 407-410.

  • 58. Verdida R.A. Xuan X. Fukumoto S. Huang X. Zhou J. Igarashi I. Claveria F.G. Nagasawa H.: Development of a practical immunochromatographic test with recombinant P50 for the diagnosis of Babesia gibsoni infection in dogs. Parasitology 2005 131 769-774.

  • 59. Wasmuth J. Daub J. Peregrín-Alvarez J. M. Finney C. A. Parkinson J.: The origins of apicomplexan sequence innovation. Genome Res 2009 19 1202-1213.

  • 60. Wilson R.I.: Progress with parasite plastids. J Mol Biol 2002 319 257-274.

  • 61. Wilson Denny P.W. Preiser P.R. Rangachari K. Roberts K. Roy A. Whyte A. Strath M. Moore D.J. Moore P.W. Williamson D.H.: Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 1996 261 155-172.

  • 62. Yamasaki M. Hwang S.J. Ohta H. Yamato O. Maede Y. Takiguchi M.: Flow cytometry to evaluate the level of Babesia gibsoni parasitemia in vivo and in vitro by using the fluorescent nucleic acid stain SYTO16. Jpn J Vet Res 2008 55 129-136.

  • 63. Yamasaki M. Inokuma H. Sugimoto C. Shaw S.E. Aktas M. Yabsley M.J. Yamato O. Maede Y.: Comparison and phylogenetic analysis of the heat shock protein 70 gene of Babesia parasites from dogs. Vet Parasitol 2007 145 217-227.

  • 64. Zhoua J. Jiaa H. Nishikawaa Y. Fujisakia K. Xuan X.: Babesia gibsoni rhoptry-associated protein 1 and its potential use as a diagnostic antigen. Vet Parasitol 2007 145 16-20.

  • 65. Zwart D. Brocklesby D.W.: Babesiosis: non-specific resistance immunological factors and pathogenesis. Adv Parasitol 1979 17 49-113.

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