Skip to main content

Babesia in Domestic Ruminants

  • Chapter
  • First Online:

Abstract

Babesia spp. are intraerythrocytic tick-transmitted apicomplexan protozoans, considered to be the second most commonly found parasites in the blood of mammals after trypanosomes. Ever since the discovery of parasitic inclusions in erythrocytes of cattle by Victor Babes, a great number of Babesia species have been described, and thanks to the advances in microscopy, cell biology, and molecular biology techniques, our knowledge is continually expanding. Most Babesia species that affect domestic ruminants, including cattle, water buffalo, and small ruminants, are distributed in tropical and subtropical regions of the world. Acute Babesia infections of these animals are associated with fever, anemia, hemoglobinuria, and abortions and, in some cases, neurological symptoms, respiratory distress, and even death. Babesiosis outbreaks can be prevented by a combination of vaccination with living attenuated organisms and tick control programs. However, these control methods have numerous limitations, and, additionally, commercial live vaccines are only available for bovine babesiosis caused by B. bovis and B. bigemina. Our knowledge on relevant parasite molecules that act in the interface with the mammalian and tick hosts is rapidly increasing in the postgenomic era and will aid in the development of new and improvement of known immunotherapeutic interventions.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, Mc Court RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol. 2005;52:399–451.

    Article  PubMed  Google Scholar 

  • Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus H, Mitchell EA, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rueckert S, Shadwick RS, Schoch CL, Smirnov A, Spiegel FW. The revised classification of eukaryotes. J Eukaryot Microbiol. 2012;59:429–93.

    PubMed  PubMed Central  Google Scholar 

  • Aktaş M, Altay K, Dumanli N. Development of a polymerase chain reaction method for diagnosis of Babesia ovis infection in sheep and goats. Vet Parasitol. 2005;133(4):277–81.

    Article  PubMed  CAS  Google Scholar 

  • Aktas M, Altay K, Ozubek S, Dumanli N. A survey of ixodid ticks feeding on cattle and prevalence of tick-borne pathogens in the Black Sea region of Turkey. Vet Parasitol. 2012;187(3–4):567–71.

    Article  PubMed  Google Scholar 

  • Alvarez J, Lopez U, Rojas C, Borgonio VM, Sanchez V, Castañeda R, Vargas P, Figueroa JV. Immunization of Bos taurus steers with Babesia bovis recombinant antigens MSA-1, MSA-2c and 12D3. Transbound Emerg Dis. 2010;57(1–2):87–90.

    Article  Google Scholar 

  • Alzan HF, Lau AO, Knowles DP, Herndon DR, Ueti MW, Scoles GA, Kappmeyer LS, Suarez CE. Expression of 6-Cys gene superfamily defines Babesia bovis sexual stage development within Rhipicephalus microplus. PLoS One. 2016;11(9):e0163791.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Asada M, Goto Y, Yahata K, Yokoyama N, Kawai S, Inoue N, Kaneko O, Kawazu S. Gliding motility of Babesia bovis merozoites visualized by time-lapse video microscopy. PLoS One. 2012;7(4):e35227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babes V. Sur l’hemoglobinurie bacterienne du boeuf. Comptesren dus hebdomadaires des seances de l’Academie des Sciences Paris. 1888;107:692–4.

    Google Scholar 

  • Babes V. L’etiologie d’une enzootie des moutons, denommee Carceag en Roumanie. (the etiology of an enzootic disease of sheep, called Carceag, in Romania) (in French). CR Hebd Acad Sci. 1892;115:359–61.

    Google Scholar 

  • Baravalle ME, Thompson C, Valentini B, Ferreira M, Torioni de Echaide S, Christensen MF, Echaide I. Babesia bovis biological clones and the inter-strain allelic diversity of the Bv80 gene support subpopulation selection as a mechanism involved in the attenuation of two virulent isolates. Vet Parasitol. 2012;190(3–4):391–400.

    Article  CAS  PubMed  Google Scholar 

  • Bastos RG, Suarez CE, Laughery JM, Johnson WC, Ueti MW, Knowles DP. Differential expression of three members of the multidomain adhesion CCp family in Babesia bigemina, Babesia bovis and Theileria equi. PLoS One. 2013;8(7):e67765.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besteiro S, Dubremetz JF, Lebrun M. The moving junction of apicomplexan parasites: a key structure for invasion. Cell Microbiology. 2011;13:797–805.

    Article  CAS  Google Scholar 

  • Blackman MJ, Bannister LH. Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol Biochem Parasitol. 2001;117(1):11–25.

    Article  CAS  PubMed  Google Scholar 

  • Blouin EF, van Rensburg L. An ultrastructural study of the development of Babesia occultans in the salivary glands of adult Hyalomma marginatum rufipes. Onderstepoort J Vet Res. 1988;55(2):93–100.

    CAS  PubMed  Google Scholar 

  • Bock RE, de Vos AJ. Immunity following use of Australian tick fever vaccine: a review of the evidence. Aust Vet J. 2001;79(12):832–9.

    Article  CAS  PubMed  Google Scholar 

  • Bock R, Jackson L, de Vos A, Jorgensen W. Babesiosis of cattle. Parasitology. 2004;129(S):247–69.

    Article  Google Scholar 

  • Bono MF, Mangold AJ, Baravalle ME, Valentini BS, Thompson CS, Wilkowsky SE, Echaide IE, Farber MD, Torioni de Echaide SM. Efficiency of a recombinant MSA-2c-based ELISA to establish the persistence of antibodies in cattle vaccinated with Babesia bovis. Vet Parasitol. 2008;157(3–4):203–10.

    Article  CAS  PubMed  Google Scholar 

  • Boonchit S, Xuan X, Yokoyama N, Goff WL, Waghela SD, Wagner G, Igarashi I. Improved enzyme-linked immunosorbent assay using C-terminal truncated recombinant antigens of Babesia bovis rhoptry-associated protein-1 for detection of specific antibodies. J Clin Microbiol. 2004;42(4):1601–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boonchit S, Alhassan A, Chan B, Xuan X, Yokoyama N, Ooshiro M, Goff WL, Waghela SD, Wagner G, Igarashi I. Expression of C-terminal truncated and full-length Babesia bigemina rhoptry-associated protein 1 and their potential use in enzyme-linked immunosorbent assay. Vet Parasitol. 2006;137(1–2):28–35.

    Article  CAS  PubMed  Google Scholar 

  • Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog. 2007;3(10):1401–13.

    Article  CAS  PubMed  Google Scholar 

  • Brown WC, Suarez CE, Shoda LK, Estes DM. Modulation of host immune responses by protozoal DNA. Vet Immunol Immunopathol. 1999;72(1–2):87–94.

    Article  CAS  PubMed  Google Scholar 

  • Brown WC, Norimine J, Knowles DP, Goff WL. Immune control of Babesia bovis infection. Vet Parasitol. 2006;138:75–87.

    Article  CAS  PubMed  Google Scholar 

  • Buling A, Criado-Fornelio A, Asenzo G, Benitez D, Barba-Carretero JC, Florin-Christensen M. A quantitative PCR assay for the detection and quantification of Babesia bovis and B. bigemina. Vet Parasitol. 2007;147(1–2):16–25.

    Article  CAS  PubMed  Google Scholar 

  • Caballero MC, Pedroni MJ, Palmer GH, Suarez CE, Davitt C, Lau AO. Characterization of acyl carrier protein and LytB in Babesia bovis apicoplast. Mol Biochem Parasitol. 2012;181(2):125–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantu A, Ortega-S JA, Mosqueda J, Garcia-Vazquez Z, Henke SE, George JE. Immunologic and molecular identification of Babesia bovis and Babesia bigemina in free-ranging white-tailed deer in northern Mexico. J Wildl Dis. 2007;43(3):504–7.

    Article  PubMed  Google Scholar 

  • Carletti T, Barreto C, Mesplet M, Mira A, Weir W, Shiels B, Oliva AG, Schnittger L, Florin-Christensen M. Characterization of a papain-like cysteine protease essential for the survival of Babesia ovis merozoites. Ticks Tick Borne Dis. 2016;7(1):85–93.

    Article  PubMed  Google Scholar 

  • Chauvin A, Moreau E, Bonnet S, Plantard O, Malandrin L. Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet Res. 2009;40(2):37.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chung CJ, Suarez CE, Bandaranayaka-Mudiyanselage CL, Bandaranayaka-Mudiyanselage CB, Rzepka J, Heiniger TJ, Chung G, Lee SS, Adams E, Yun G, Waldron SJ. A novel modified-indirect ELISA based on spherical body protein 4 for detecting antibody during acute and long-term infections with diverse Babesia bovis strains. Parasit Vectors. 2017;10(1):77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Combrink MP, Troskie PC, Pienaar R, Latif AA, Mans BJ. Genotypic diversity in Babesia bovis field isolates and vaccine strains from South Africa. Vet Parasitol. 2014;199(3–4):144–52.

    Article  CAS  PubMed  Google Scholar 

  • Criado-Fornelio A, Gónzalez-del-Río MA, Buling-Saraña A, Barba-Carretero JC. The “expanding universe” of piroplasms. Vet Parasitol. 2004;119(4):337–45.

    Article  CAS  PubMed  Google Scholar 

  • Criado-Fornelio A, Buling A, Asenzo G, Benitez D, Florin-Christensen M, Gonzalez-Oliva A, Henriques G, Silva M, Alongi A, Agnone A, Torina A, Madruga CR. Development of fluorogenic probe-based PCR assays for the detection and quantification of bovine piroplasmids. Vet Parasitol. 2009;162(3–4):200–6.

    Article  CAS  PubMed  Google Scholar 

  • Cursino-Santos JR, Halverson G, Rodriguez M, Narla M, Lobo CA. Identification of binding domains on red blood cell glycophorins for Babesia divergens. Transfusion. 2014;54(4):982–9.

    Article  CAS  PubMed  Google Scholar 

  • da Silveira JA, Rabelo EM, Ribeiro MF. Detection of Theileria and Babesia in brown brocket deer (Mazamagoua zoubira) and marsh deer (Blastocerus Dichotomus) in the state of Minas Gerais, Brazil. Vet Parasitol. 2011;177(1–2):61–6.

    Article  PubMed  Google Scholar 

  • de la Fuente J. Vaccines for vector control: exciting possibilities for the future. Vet Journal. 2012;194:139–40.

    Article  Google Scholar 

  • de Waal DT, Combrink MP. Live vaccines against bovine babesiosis. Vet Parasitol. 2006;138(1–2):88–96.

    Article  PubMed  CAS  Google Scholar 

  • Decaro N, Larocca V, Parisi A, Losurdo M, Lia RP, Greco MF, Miccolis A, Ventrella G, Otranto D, Buonavoglia C. Clinical bovine piroplasmosis caused by Babesia occultans in Italy. J Clin Microbiol. 2013;51(7):2432–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delbecq S, Auguin D, Yang YS, Löhr F, Arold S, Schetters T, Précigout E, Gorenflot A, Roumestand C. The solution structure of the adhesion protein Bd37 from Babesia divergens reveals structural homology with eukaryotic proteins involved in membrane trafficking. J Mol Biol. 2008;375(2):409–24.

    Article  CAS  PubMed  Google Scholar 

  • Dominguez M, Echaide I, Echaide ST, Mosqueda J, Cetrá B, Suarez CE, Florin-Christensen M. In silico predicted conserved B-cell epitopes in the merozoite surface antigen-2 family of B. bovis are neutralization sensitive. Vet Parasitol. 2010;167(2–4):216–26.

    Article  CAS  PubMed  Google Scholar 

  • Dominguez M, Echaide I, de Echaide ST, Wilkowsky S, Zabal O, Mosqueda JJ, Schnittger L, Florin-Christensen M. Validation and field evaluation of a competitive enzyme-linked immunosorbent assay for diagnosis of Babesia bovis infections in Argentina. Clin Vaccine Immunol. 2012;19(6):924–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowling SC, Perryman LE, Jasmer DP. A Babesia bovis 225-kilodalton spherical-body protein: localization to the cytoplasmic face of infected erythrocytes after merozoite invasion. Infect Immun. 1996;64(7):2618–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duzgun A, Wright IG, Waltisbuhl DJ, Gale KR, Goodger BV, Dargie JD, Alabay M, Cerci H. An ELISA for the diagnosis of Babesia ovis infection utilizing a synthetic, Babesia bovis-derived antigen. Vet Parasitol. 1991;39(3–4):225–31.

    Article  CAS  PubMed  Google Scholar 

  • Erster O, Roth A, Wollkomirsky R, Leibovich B, Savitzky I, Zamir S, Molad T, Shkap V. Quantitative analysis of Babesia ovis infection in sheep and ticks. Vet Parasitol. 2016;221:39–45.

    Article  PubMed  Google Scholar 

  • Estrada-Peña A, Venzal JM, Nava S, Mangold A, Guglielmone AA, Labruna MB, de la Fuente J. Reinstatement of Rhipicephalus (Boophilus) australis (Acari: Ixodidae) with redescription of the adult and larval stages. J Med Entomol. 2012;49(4):794–802.

    Article  PubMed  Google Scholar 

  • Ferreri L, Benitez D, Dominguez M, Rodriguez A, Asenzo G, Mesplet M, Florin-Christensen M, Schnittger L. Water buffalos as carriers of Babesia bovis in Argentina. Ann N Y Acad Sci. 2008;1149:149–51.

    Article  PubMed  Google Scholar 

  • Figueroa JV, Chieves LP, Johnson GS, Buening GM. Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Vet Parasitol. 1993;50(1–2):69–81.

    Article  CAS  PubMed  Google Scholar 

  • Flores DA, Minichiello Y, Araujo FR, Shkap V, Benítez D, Echaide I, Rolls P, Mosqueda J, Pacheco GM, Petterson M, Florin-Christensen M, Schnittger L. Evidence for extensive genetic diversity and substructuring of the Babesia bovis metapopulation. Transbound Emerg Dis. 2013;60(Suppl 2):131–6.

    Article  PubMed  Google Scholar 

  • Florin-Christensen M, Schnittger L. Piroplasmids and ticks: a long-lasting intimate relationship. Front Biosci. 2009;14:3064–73.

    Article  CAS  Google Scholar 

  • Florin-Christensen M, Suarez CE, Hines SA, Palmer GH, Brown WC, McElwain TF. The Babesia bovis merozoite surface antigen 2 locus contains four tandemly arranged and expressed genes encoding immunologically distinct proteins. Infect Immun. 2002;70(7):3566–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florin-Christensen M, Suarez CE, Rodriguez AE, Flores DA, Schnittger L. Vaccines against bovine babesiosis: where we are now and possible roads ahead. Parasitology. 2014;141:1563–92.

    Article  Google Scholar 

  • Gabrielli S, Galuppi R, Marcer F, Marini C, Tampieri MP, Moretti A, Pietrobelli M, Cancrini G. Development of culture-based serological assays to diagnose Babesia divergens infections. Vector Borne Zoonotic Dis. 2012;12(2):106–10.

    Article  PubMed  Google Scholar 

  • Gaffar FR, Franssen FF, de Vries E. Babesia bovis merozoites invade human, ovine, equine, porcine and caprine erythrocytes by a sialic acid-dependent mechanism followed by developmental arrest after a single round of cell fission. Int J Parasitol. 2003;33(14):1595–603.

    Article  CAS  PubMed  Google Scholar 

  • Gaffar FR, Yatsuda AP, Franssen FF, de Vries E. Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infect Immun. 2004a;72:2947–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaffar FR, Yatsuda AP, Franssen FF, de Vries E. A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin-related anonymous protein (TRAP) present in Plasmodium sporozoites. Mol Biochem Parasitol. 2004b;136:25–34.

    Article  CAS  PubMed  Google Scholar 

  • Gimenez AM, Françoso KS, Ersching J, Icimoto MY, Oliveira V, Rodriguez AE, Schnittger L, Florin-Christensen M, Rodrigues MM, Soares IS. A recombinant multi-antigen vaccine formulation containing Babesia bovis merozoite surface antigens MSA-2a(1), MSA-2b and MSA-2c elicits invasion-inhibitory antibodies and IFN-γ producing cells. Parasit Vectors. 2016;9(1):577.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goff WL, Bastos RG, Brown WC, Johnson WC, Schneider DA. The bovine spleen: interactions among splenic cell populations in the innate immunologic control of hemoparasitic infections. Vet Immunol Immunopathol. 2010;138(1–2):1–14.

    Article  CAS  PubMed  Google Scholar 

  • Gohil S, Kats LM, Sturm A, Cooke BM. Recent insights into alteration of red blood cells by Babesia bovis: moovin’ forward. Trends Parasitol. 2010;26(12):591–9.

    Article  PubMed  Google Scholar 

  • Gohil S, Herrmann S, Günther S, Cooke BM. Bovine babesiosis in the 21st century: advances in biology and functional genomics. Int J Parasitol. 2013;43(2):125–32.

    Article  CAS  PubMed  Google Scholar 

  • Guan G, Chauvin A, Luo J, Inoue N, Moreau E, Liu Z, Gao J, Thekisoe OM, Ma M, Liu A, Dang Z, Liu J, Ren Q, Jin Y, Sugimoto C, Yin H. The development and evaluation of a loop-mediated isothermal amplification (LAMP) method for detection of Babesia spp. infective to sheep and goats in China. Exp Parasitol. 2008;120(1):39–44.

    Article  CAS  PubMed  Google Scholar 

  • Gubbels MJ, Duraisingh MT. Evolution of apicomplexan secretory organelles. Int J Parasitol. 2012;42(12):1071–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gubbels JM, de Vos AP, van der Weide M, Viseras J, Schouls LM, de Vries E, Jongejan F. Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol. 1999;37(6):1782–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guillemi E, Ruybal P, Lia V, González S, Farber M, Wilkowsky SE. Multi-locus typing scheme for Babesia bovis and Babesia bigemina reveals high levels of genetic variability in strains from northern Argentina. Infect Genet Evol. 2013;14:214–22.

    Article  PubMed  Google Scholar 

  • Guswanto A, Allamanda P, Mariamah ES, Munkjargal T, Tuvshintulga B, Takemae H, Sivakumar T, AbouLaila M, Terkawi MA, Ichikawa-Seki M, Nishikawa Y, Yokoyama N, Igarashi I. Evaluation of immunochromatographic test (ICT) strips for the serological detection of Babesia bovis and Babesia bigemina infection in cattle from western java, Indonesia. Vet Parasitol. 2017;239:76–9.

    Article  PubMed  Google Scholar 

  • Habela M, Reina D, Nieto C, Navarrete IK. Antibody response and duration of latent infection in sheep following experimental infection with Babesia ovis. Vet Parasitol. 1990;35:1–10.

    Article  CAS  PubMed  Google Scholar 

  • Hadj-Kaddour K, Carcy B, Vallet A, Randazzo S, Delbecq S, Kleuskens J, Schetters T, Gorenflot A, Precigout E. Recombinant protein Bd37 protected gerbils against heterologous challenges with isolates of Babesia divergens polymorphic for the bd37 gene. Parasitology. 2007;134(Pt 2):187–96.

    Article  CAS  PubMed  Google Scholar 

  • Haghi MM, Etemadifar F, Fakhar M, Teshnizi SH, Soosaraei M, Shokri A, Hajihasani A, Mashhadi H. Status of babesiosis among domestic herbivores in Iran: a systematic review and meta-analysis. Parasitol Res. 2017;116(4):1101–9.

    Article  PubMed  Google Scholar 

  • He L, Zhou YQ, Oosthuizen MC, Zhao JL. Loop-mediated isothermal amplification (LAMP) detection of Babesia orientalis in water buffalo (Bubalus babalis, Linnaeus, 1758) in China. Vet Parasitol. 2009;165(1–2):36–40.

    Article  PubMed  Google Scholar 

  • He L, Feng HH, Zhang QL, Zhang WJ, Khan MK, Hu M, Zhou YQ, Zhao JL. Development and evaluation of real-time PCR assay for the detection of Babesia orientalis in water buffalo (Bubalus Bubalis, Linnaeus, 1758). J Parasitol. 2011;97(6):1166–9.

    Article  CAS  PubMed  Google Scholar 

  • He L, Feng HH, Zhang WJ, Zhang QL, Fang R, Wang LX, Tu P, Zhou YQ, Zhao JL, Oosthuizen MC. Occurrence of Theileria and Babesia species in water buffalo (Bubalus babalis, Linnaeus, 1758) in the Hubei province, South China. Vet Parasitol. 2012;186(3–4):490–6.

    Article  PubMed  Google Scholar 

  • He L, Zhang Y, Zhang QL, Zhang WJ, Feng HH, Khan MK, Hu M, Zhou YQ, Zhao JL. Mitochondrial genome of Babesia orientalis, apicomplexan parasite of water buffalo (Bubalus Bubalis, Linnaeus, 1758) endemic in China. Parasit Vectors. 2014;7:82.

    Article  PubMed  PubMed Central  Google Scholar 

  • Holman PJ, Carroll JE, Pugh R, Davis DS. Molecular detection of Babesia bovis and Babesia bigemina in white-tailed deer (Odocoileus virginianus) from tom Green County in central Texas. Vet Parasitol. 2011;177(3–4):298–304.

    Article  CAS  PubMed  Google Scholar 

  • Homer MJ, Aguilar-Delfin I, Telford SR III, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13:451–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornok S, Takács N, Kontschán J, György Z, Micsutka A, Iceton S, Flaisz B, Farkas R, Hofmann-Lehmann R. Diversity of Haemaphysalis-associated piroplasms of ruminants in Central-Eastern Europe, Hungary. Parasit Vectors. 2015;8:627.

    Article  PubMed  PubMed Central  Google Scholar 

  • Horta S, Barreto MC, Pepe A, Campos J, Oliva A. Highly sensitive method for diagnosis of subclinical Babesia ovis infection. Ticks Tick Borne Dis. 2014;5(6):902–6.

    Article  PubMed  Google Scholar 

  • Huang Y, He L, Hu J, He P, He J, Yu L, Malobi N, Zhou Y, Shen B, Zhao J. Characterization and annotation of Babesia orientalis apicoplast genome. Parasit Vec. 2015;8:543.

    Article  CAS  Google Scholar 

  • Hurtado A. Reverse line blot hybridization with species-specific oligonucleotide probes: application to piroplasm detection. Methods Mol Biol. 2015;1247:183–92.

    Article  PubMed  Google Scholar 

  • Hurtado A, Barandika JF, Oporto B, Minguijón E, Povedano I, García-Pérez AL. Risks of suffering tick-borne diseases in sheep translocated to a tick infested area: a laboratory approach for the investigation of an outbreak. Ticks Tick Borne Dis. 2015;6(1):31–7.

    Article  PubMed  Google Scholar 

  • Hutchings CL, Li A, Fernandez KM, Fletcher T, Jackson LA, Molloy JB, Jorgensen WK, Lim CT, Cooke BM. New insights into the altered adhesive and mechanical properties of red blood cells parasitized by Babesia bovis. Mol Microbiol. 2007;65(4):1092–110.

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo Ortiz JM, Molinari MP, Gravisaco MJ, Paoletta MS, Montenegro VN, Wilkowsky SE. Evaluation of different heterologous prime-boost immunization strategies against Babesia bovis using viral vectored and protein-adjuvant vaccines based on a chimeric multi-antigen. Vaccine. 2016;34(33):3913–9.

    Article  CAS  PubMed  Google Scholar 

  • Kakoma I, Mehlhorn H. Babesia of domestic ruminants. In: Kreier JP, Baker JR, editors. Parasitic protozoa. 2nd ed. New York: Academic; 1994. p. 141–216.

    Google Scholar 

  • Kim CM, Blanco LB, Alhassan A, Iseki H, Yokoyama N, Xuan X, Igarashi I. Development of a rapid immunochromatographic test for simultaneous serodiagnosis of bovine babesioses caused by Babesia bovis and Babesia bigemina. Am J Trop Med Hyg. 2008;78(1):117–21.

    Article  CAS  PubMed  Google Scholar 

  • Klinger CM, Nisbet RE, Ouologuem DT, Roos DS, Dacks JB. Cryptic organelle homology in apicomplexan parasites: insights from evolutionary cell biology. Curr Opin Microbiol. 2013;16(4):424–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch R. Beitrage zur Entwicklungsgeschichte der Piroplasmen. Z Hyg Infekt-Kr. 1906;54:1–9.

    Article  Google Scholar 

  • Lau AO, Kalyanaraman A, Echaide I, Palmer GH, Bock R, Pedroni MJ, Rameshkumar M, Ferreira MB, Fletcher TI, McElwain TF. Attenuation of virulence in an apicomplexan hemoparasite results in reduced genome diversity at the population level. BMC Genomics. 2011;12:410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lempereur L, Beck R, Fonseca I, Marques C, Duarte A, Santos M, Zúquete S, Gomes J, Walder G, Domingos A, Antunes S, Baneth G, Silaghi C, Holman P, Zintl A. Guidelines for the detection of Babesia and Theileria parasites. Vector Borne Zoonotic Dis. 2017;17(1):51–65.

    Article  PubMed  Google Scholar 

  • Lew AE, Dluzewski AR, Johnson AM, Pinder JC. Myosins of Babesia bovis: molecular characterisation, erythrocyte invasion, and phylogeny. Cell Motil Cytoskeleton. 2002;52:202–20.

    Article  CAS  PubMed  Google Scholar 

  • Li H, Child MA, Bogyo M. Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochim Biophys Acta. 2012;1824(1):177–85.

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Zhao JL, Zhou YQ, Liu EY, Yao BA, Fu Y. Study on some molecular characterization of Babesia orientalis. Vet Parasitol. 2005;130(3–4):191–8.

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Zhou YQ, Zhou DN, Liu EY, Du K, Chen SG, Yao BA, Zhao JL. Semi-nested PCR detection of Babesia orientalis in its natural hosts Rhipicephalus haemaphysaloides and buffalo. Vet Parasitol. 2007a;143(3–4):260.

    Article  CAS  PubMed  Google Scholar 

  • Liu AH, Yin H, Guan GQ, Schnittger L, Liu ZJ, Ma ML, Dang ZS, Liu JL, Ren QY, Bai Q, Ahmed JS, Luo JX. At least two genetically distinct large Babesia species infective to sheep and goats in China. Vet Parasitol. 2007b;147(3–4):246–51.

    Article  CAS  PubMed  Google Scholar 

  • Lobo CA. Babesia divergens and Plasmodium falciparum use common receptors glycophorins a and B, to invade the human red blood cell. Infect Immun. 2005;73(1):649–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobo CA, Rodriguez M, Cursino-Santos JR. Babesia and red cell invasion. Curr Opin Hematol. 2012;19(3):170–5.

    Article  PubMed  Google Scholar 

  • Maharana BR, Tewari AK, Saravanan BC, Sudhakar NR. Important hemoprotozoan diseases of livestock: challenges in current diagnostics and therapeutics: an update. Vet World. 2016;9(5):487–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahoney DF. The application of epizootiological principals in the control of babesiosis in cattle. Bull Off Int Epizoot. 1974;81:123–38.

    Google Scholar 

  • Mangold AJ, Vanzini VR, Echaide IE, de Eschaide ST, Volpogni MM, Guglielmone AA. Viability after thawing and dilution of simultaneously cryopreserved vaccinal Babesia bovis and Babesia bigemina strains cultured in vitro. Vet Parasitol. 1996;61:345–8.

    Article  CAS  PubMed  Google Scholar 

  • Martins TM, do Rosário VE, Domingos A. Expression and characterization of the Babesia bigemina cysteine protease BbiCPL1. Acta Trop. 2012;121(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  • Mesplet M, Echaide I, Dominguez M, Mosqueda JJ, Suarez CE, Schnittger L, Florin-Christensen M. Bovipain-2, the falcipain-2 ortholog, is expressed in intraerythrocytic stages of the tick-transmitted hemoparasite Babesia bovis. Parasit Vectors. 2010;3:113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mesplet M, Palmer GH, Pedroni MJ, Echaide I, Florin-Christensen M, Schnittger L, Lau AO. Genome-wide analysis of peptidase content and expression in a virulent and attenuated Babesia bovis strain pair. Mol Biochem Parasitol. 2011;179(2):111–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M, Chirico J, van der Wal FJ, Sprong H, Boye Pihl TP, Klitgaard K, Bødker R, Fach P, Moutailler S. High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol. 2014;4:103.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mihalca AD. The quest for piroplasms: from babes to smith to molecules. Sci Parasitol. 2010;11:14–9.

    Google Scholar 

  • Mosqueda J, McElwain TF, Palmer GH. Babesia bovis merozoite surface antigen 2 proteins are expressed on the merozoite and sporozoite surface, and specific antibodies inhibit attachment and invasion of erythrocytes. Infect Immun. 2002;70(11):6448–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ. Current advances in detection and treatment of babesiosis. Curr Med Chem. 2012;19(10):1504–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu Q, Marchand J, Yang C, Bonsergent C, Guan G, Yin H, Malandrin L. Rhoptry-associated protein (rap-1) genes in the sheep pathogen Babesia sp. Xinjiang: multiple transcribed copies differing by 3′ end repeated sequences. Vet Parasitol. 2015;211(3–4):158–69.

    Article  CAS  PubMed  Google Scholar 

  • Niu Q, Liu Z, Yang J, Yu P, Pan Y, Zhai B, Luo J, Moreau E, Guan G, Yin H. Expression analysis and biological characterization of Babesia sp. BQ1 (Lintan) (Babesia motasi-like) rhoptry-associated protein 1 and its potential use in serodiagnosis via ELISA. Parasit Vectors. 2016a;9(1):313.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niu Q, Liu Z, Yang J, Yu P, Pan Y, Zhai B, Luo J, Yin H. Genetic diversity and molecular characterization of Babesia motasi-like in small ruminants and ixodid ticks from China. Infect Genet Evol. 2016b;41:8–15.

    Article  CAS  PubMed  Google Scholar 

  • Niu Q, Liu Z, Yang J, Gao S, Pan Y, Guan G, Luo J, Yin H. Genetic characterization and molecular survey of Babesia sp. Xinjiang infection in small ruminants and ixodid ticks in China. Infect Genet Evol. 2017;49:330–5.

    Article  CAS  PubMed  Google Scholar 

  • O’Connor RM, Allred DR. Selection of Babesia bovis infected erythrocytes for adhesion to endothelial cells co-selects for altered variant erythrocyte surface antigen isoforms. J Immunol. 2000;164:2037–45.

    Article  PubMed  Google Scholar 

  • OIE World Organization for Animal Health Terrestrial Manual. Bovine Babesiosis. Chapter 2.4.2; 2014. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.04.02_BOVINE_BABESIOSIS.pdf.

    Google Scholar 

  • Pedroni MJ, Sondgeroth KS, Gallego-Lopez GM, Echaide I, Lau AO. Comparative transcriptome analysis of geographically distinct virulent and attenuated Babesia bovis strains reveals similar gene expression changes through attenuation. BMC Genomics. 2013;14:763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez de León AA, Strickman DA, Knowles DP, Fish D, Thacker E, de la Fuente J, Krause PJ, Wikel SK, Miller RS, Wagner GG, Almazán C, Hillman R, Messenger MT, Ugstad PO, Duhaime RA, Teel PD, Ortega-Santos A, Hewitt DG, Bowers EJ, Bent SJ, Cochran MH, TF ME, Scoles GA, Suarez CE, Davey R, Howell Freeman JM, Lohmeyer K, Li AY, Guerrero FD, Kammlah DM, Phillips P, Pound JM, Group for Emerging Babesioses and One Health Research and Development in the U.S. One health approach to identify research needs in bovine and human babesioses: workshop report. Parasit Vectors. 2010;3(1):36.

    Article  PubMed  PubMed Central  Google Scholar 

  • Perez-Llaneza A, Caballero M, Baravalle E, Mesplet M, Mosqueda J, Suarez CE, Echaide I, Katzer F, Pacheco GM, Florin-Christensen M, Schnittger L. Development of a tandem repeat-based multilocus typing system distinguishing Babesia bovis geographic isolates. Vet Parasitol. 2010;167(2–4):196–204.

    Article  CAS  PubMed  Google Scholar 

  • Ramos CM, Cooper SM, Holman PJ. Molecular and serologic evidence for Babesia bovis-like parasites in white-tailed deer (Odocoileus virginianus) in south Texas. Vet Parasitol. 2010;172(3–4):214–20.

    Article  PubMed  Google Scholar 

  • Ramos CA, Araújo FR, Souza II, Bacanelli G, Luiz HL, Russi LS, Oliveira RH, Soares CO, Rosinha GM, Alves LC. Real-time polymerase chain reaction based on msa2c gene for detection of Babesia bovis. Vet Parasitol. 2011;176(1):79–83.

    Article  CAS  PubMed  Google Scholar 

  • Ranjbar-Bahadori S, Eckert B, Omidian Z, Shirazi NS, Shayan P. Babesia ovis as the main causative agent of sheep babesiosis in Iran. Parasitol Res. 2012;110(4):1531–6.

    Article  PubMed  Google Scholar 

  • Ribeiro MFB, Patarroyo JHS. Ultrastructure of Babesia bigemina gametes obtained in “in vitro” erythrocyte cultures. Vet Parasitol. 1998;76:19–25.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez AE, Couto A, Echaide I, Schnittger L, Florin-Christensen M. Babesia bovis contains an abundant parasite-specific protein-free glycerophosphatidylinositol and the genes predicted for its assembly. Vet Parasitol. 2010;167(2–4):227–35.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez AE, Schnittger L, Tomazic ML, Florin-Christensen M. Current and prospective tools for the control of cattle-infecting Babesia parasites. In: Castillo V, Harris R, editors. Protozoa: biology, classification and role in disease. Hauppauge, NY: Nova; 2013a. p. 1–44.

    Google Scholar 

  • Rodriguez AE, Zamorano P, Wilkowsky S, Torrá F, Ferreri L, Dominguez M, Florin-Christensen M. Delivery of recombinant vaccines against bovine herpes virus type 1 gD and Babesia bovis MSA-2c to mice using liposomes derived from egg yolk lipids. Vet J. 2013b;196(3):550–1.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez AE, Florin-Christensen M, Flores DA, Echaide I, Suarez CE, Schnittger L. The glycosylphosphatidylinositol-anchored protein repertoire of Babesia bovis and its significance for erythrocyte invasion. Ticks Tick Borne Dis. 2014;5(3):343–8.

    Article  PubMed  Google Scholar 

  • Romero-Salas D, Mira A, Mosqueda J, García-Vázquez Z, Hidalgo-Ruiz M, Vela NA, de León AA, Florin-Christensen M, Schnittger L. Molecular and serological detection of Babesia bovis- and Babesia bigemina-infection in bovines and water buffaloes raised jointly in an endemic field. Vet Parasitol. 2016;217:101–7.

    Article  CAS  PubMed  Google Scholar 

  • Ruef BJ, Dowling SC, Conley PG, Perryman LE, Brown WC, Jasmer DP, Rice-Ficht AC. A unique Babesia bovis spherical body protein is conserved among geographic isolates and localizes to the infected erythrocyte membrane. Mol Biochem Parasitol. 2000;105(1):1–12.

    Article  CAS  PubMed  Google Scholar 

  • Schnittger L, Yin H, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS. Phylogeny of sheep and goat Theileria and Babesia parasites. Parasitology Res. 2003;91:398–406.

    Article  Google Scholar 

  • Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS. Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. Parasitol Res. 2004;92(3):189–96.

    Article  PubMed  Google Scholar 

  • Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: a world emerging. Infect Genet Evol. 2012;12(8):1788–809.

    Article  PubMed  Google Scholar 

  • Schötta AM, Wijnveld M, Stockinger H, Stanek G. Reverse line blot-based detection approaches of microbial pathogens in Ixodes ricinus ticks collected in Austria and impact of the chosen method. Appl Environ Microbiol. 2017; pii: AEM.00489-17.

    Google Scholar 

  • Shoda LK, Palmer GH, Florin-Christensen J, Florin-Christensen M, Godson DL, Brown WC. Babesia bovis-stimulated macrophages express interleukin-1beta, interleukin-12, tumor necrosis factor alpha, and nitric oxide and inhibit parasite replication in vitro. Infect Immun. 2000;68:5139–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simuunza M, Bilgic H, Karagenc T, Syakalima M, Shiels B, Tait A, Weir W. Population genetic analysis and sub-structuring in Babesia bovis. Mol Biochem Parasitol. 2011;177(2):106–15.

    Article  CAS  PubMed  Google Scholar 

  • Sivakumar T, Igarashi I, Yokoyama N. Babesia ovata: taxonomy, phylogeny and epidemiology. Vet Parasitol. 2016;229:99–106.

    Article  PubMed  Google Scholar 

  • Smith T, Kilborne FL. Investigations into the nature, causation and prevention of southern cattle fever. In: Ninth annual report of the Bureau of Animal Industry for the year 1892. Washington, DC: Government Printing Office; 1893. p. 177–304.

    Google Scholar 

  • Suarez CE, Palmer GH, Hötzel I, McElwain TF. Structure, sequence, and transcriptional analysis of the Babesia bovis rap-1 multigene locus. Mol Biochem Parasitol. 1998;93(2):215–24.

    Article  CAS  PubMed  Google Scholar 

  • Suarez CE, Florin-Christensen M, Hines SA, Palmer GH, Brown WC, McElwain TF. Characterization of allelic variation in the Babesia bovis merozoite surface antigen 1 (MSA-1) locus and identification of a cross-reactive inhibition-sensitive MSA-1 epitope. Infect Immun. 2000;68(12):6865–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suarez CE, Palmer GH, Florin-Christensen M, Hines SA, Hötzel I, McElwain TF, Organization, transcription, and expression of rhoptry associated protein genes in the Babesia bigemina rap-1 locus. Mol Biochem Parasitol. 2003;127(2):101–12.

    Google Scholar 

  • Terkawi MA, Seuseu FJ, Eko-Wibowo P, Huyen NX, Minoda Y, Abou Laila M, Kawai S, Yokoyama N, Xuan X, Igarashi I. Secretion of a new spherical body protein of Babesia bovis into the cytoplasm of infected erythrocytes. Mol Biochem Parasitol. 2011;178(1–2):40–5.

    Article  CAS  PubMed  Google Scholar 

  • Ueti MW, Olafson PU, Freeman JM, Johnson WC, Scoles GA. A virulent Babesia bovis strain failed to infect white-tailed deer (Odocoileus virginianus). PLoS One. 2015;10(6):e0131018.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uilenberg G. Babesia—a historical overview. Vet Parasitol. 2006;138:3–10.

    Article  PubMed  Google Scholar 

  • Weber G, Friedhoff KT. Preliminary observations on the ultrastructure of supposed sexual stages of Babesia bigemina (Piroplasmea). Z Parasitenkund. 1977;53:83–92.

    Article  CAS  Google Scholar 

  • Weerasooriya G, Sivakumar T, Lan DT, Long PT, Takemae H, Igarashi I, Inoue N, Yokoyama N. Epidemiology of bovine hemoprotozoa parasites in cattle and water buffalo in Vietnam. J Vet Med Sci. 2016;78(8):1361–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilkowsky SE, Farber M, Echaide I, Torioni de Echaide S, Zamorano PI, Dominguez M, Suarez CE, Florin-Christensen M. Babesia bovis merozoite surface protein-2c (MSA-2c) contains highly immunogenic, conserved B-cell epitopes that elicit neutralization-sensitive antibodies in cattle. Mol Biochem Parasitol. 2003;127(2):133–41.

    Article  CAS  PubMed  Google Scholar 

  • Willadsen P. Tick control: thoughts on a research agenda. Vet Parasitol. 2006;138:161–8.

    Article  PubMed  Google Scholar 

  • Yang Y, Li Q, Wang S, Chen X, Du A. Rapid and sensitive detection of Babesia bovis and Babesia bigemina by loop-mediated isothermal amplification combined with a lateral flow dipstick. Vet Parasitol. 2016;219:71–6.

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama N, Suthisak B, Hirata H, Matsuo T, Inoue N, Sugimoto C, Igarashi I. Cellular localization of Babesia bovis merozoite rhoptry-associated protein 1 andits erythrocyte-binding activity. Infect Immun. 2002;70(10):5822–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoyama N, Okamura M, Igarashi I. Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Vet Parasitol. 2006;138(1–2):22–32.

    Article  CAS  PubMed  Google Scholar 

  • Zhou M, Cao S, Sevinc F, Sevinc M, Ceylan O, Ekici S, Jirapattharasate C, Moumouni PF, Liu M, Wang G, Iguchi A, Vudriko P, Suzuki H, Xuan X. Molecular detection and genetic characterization of Babesia, Theileria and Anaplasma amongst apparently healthy sheep and goats in the central region of Turkey. Ticks Tick Borne Dis. 2017;8(2):246–52.

    Article  PubMed  Google Scholar 

  • Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev. 2003;16(4):622–36.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zintl A, Gray JS, Skerrett HE, Mulcahy G. Possible mechanisms underlying age-related resistance to bovine babesiosis. Parasite Immunol. 2005;27:115–20.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mónica Florin-Christensen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ganzinelli, S., Rodriguez, A., Schnittger, L., Florin-Christensen, M. (2018). Babesia in Domestic Ruminants. In: Florin-Christensen, M., Schnittger, L. (eds) Parasitic Protozoa of Farm Animals and Pets. Springer, Cham. https://doi.org/10.1007/978-3-319-70132-5_9

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-70132-5_9

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-70131-8

  • Online ISBN: 978-3-319-70132-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics