Analyze Diet
Pathogens (Basel, Switzerland)2022; 11(2); doi: 10.3390/pathogens11020168

Babesiosis and Theileriosis in North America.

Abstract: Babesia and Theileria are apicomplexan parasites that cause established and emerging diseases in humans, domestic and wild animals. These protozoans are transmitted by Ixodid ticks causing babesiosis or theileriosis, both characterized by fever, hemolytic anemia, jaundice, and splenomegaly. In North America (NA), the most common species affecting humans is B. microti, which is distributed in the Northeastern and Upper Midwestern United States (US), where the tick vector Ixodes scapularis is established. In livestock, B. bovis and B. bigemina are the most important pathogens causing bovine babesiosis in tropical regions of Mexico. Despite efforts toward eradication of their tick vector, Rhipicephalus microplus, B. bovis and B. bigemina present a constant threat of being reintroduced into the southern US and represent a continuous concern for the US cattle industry. Occasional outbreaks of T. equi, and T. orientalis have occurred in horses and cattle, respectively, in the US, with significant economic implications for livestock including quarantine, production loss, and euthanasia of infected animals. In addition, a new species, T. haneyi, has been recently discovered in horses from the Mexico-US border. Domestic dogs are hosts to at least four species of Babesia in NA that may result in clinical disease that ranges from subclinical to acute, severe anemia. Herein we review the pathogenesis, diagnosis, and epidemiology of the most important diseases caused by Babesia and Theileria to humans, domestic and wild animals in Canada, the US, and Mexico.
Publication Date: 2022-01-27 PubMed ID: 35215111PubMed Central: PMC8874406DOI: 10.3390/pathogens11020168Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article focuses on the diseases babesiosis and theileriosis, caused by the parasites Babesia and Theileria, affecting humans and animals in North America and their transmission through ticks. It discusses the distribution, pathogenesis, diagnosis, and epidemiology of these diseases, their economic impact on livestock industries, and identifies new species involved.

Parasites and Diseases

  • The research studies the effects of two main parasites, Babesia and Theileria, which cause two diseases known as babesiosis and theileriosis in both humans and animals. It offers an overview of the pathogenesis – or development – of these diseases.
  • These diseases generally appear as fever, hemolytic anemia, jaundice and splenomegaly. They are transmitted through a type of ticks known as ixodid ticks.

Distribution and Epidemiology

  • In North America, Babesia microti is the most common species of the Babesia parasite affecting humans. The research identifies geographical areas of distribution, specifically the Northeastern and Upper Midwestern United States.
  • In livestock, Babesia bovis and Babesia bigemina are the significant threats. These are most prevalent in tropical regions of Mexico but represent a constant threat to the southern US too.
  • The article also mentions the occasional outbreaks of Theileria equi and Theileria orientalis in horses and cattle in the US, and highlights the economic impacts such as quarantine, production loss, and euthanasia of infected animals.
  • A new species, Theileria haneyi, is also identified, found in horses from the Mexico-US border.

Effects on Domestic Animals

  • The article offers consideration to domestic dogs, which can host at least four different species of Babesia in North America and can display a range of clinical diseases from subclinical to severe anemia.

Diagnosis and Eradication Efforts

  • Despite efforts towards the eradication of the tick vector Rhipicephalus (Boophilus) microplus, these parasites present a threat of reintroduction and continuous concern to the livestock industry.

Research Scope

  • This work helps update understanding of these diseases, their effects on both humans and animals, and their distribution across North America. Also, it reviews the current epidemiological landscape and draws attention to new species that have been discovered.

Cite This Article

APA
Almazán C, Scimeca RC, Reichard MV, Mosqueda J. (2022). Babesiosis and Theileriosis in North America. Pathogens, 11(2). https://doi.org/10.3390/pathogens11020168

Publication

ISSN: 2076-0817
NlmUniqueID: 101596317
Country: Switzerland
Language: English
Volume: 11
Issue: 2

Researcher Affiliations

Almazán, Consuelo
  • Immunology and Vaccines Laboratory, C. A. Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Carretera a Chichimequillas, Queretaro 76140, Mexico.
Scimeca, Ruth C
  • Department of Veterinary Pathobiology, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078, USA.
Reichard, Mason V
  • Department of Veterinary Pathobiology, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078, USA.
Mosqueda, Juan
  • Immunology and Vaccines Laboratory, C. A. Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Carretera a Chichimequillas, Queretaro 76140, Mexico.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 113 references
  1. Nicholson W.L., Sonenshine D.E., Noden B.H., Brown R.N.. Ticks (Ixodida). 2019;pp. 603–672.
  2. Sonenshine D.E.. Range Expansion of Tick Disease Vectors in North America: Implications for Spread of Tick-Borne Disease. Int. J. Environ. Res. Public Health 2018;15:478.
    doi: 10.3390/ijerph15030478pmc: PMC5877023pubmed: 29522469google scholar: lookup
  3. Guglielmone A.A., Robbins R.G.. Hard Ticks (Acari: Ixodida: Ixodidae) Parasitizing Humans. 2018;Volume 230.
  4. Bullard J.M., Ahsanuddin A.N., Perry A.M., Lindsay L.R., Iranpour M., Dibernardo A., Van Caeseele P.G.. The First Case of Locally Acquired Tick-Borne Babesia Microti Infection in Canada. Can. J. Infect. Dis. Med. Microbiol. 2014;25:e87–e89.
    doi: 10.1155/2014/209521pmc: PMC4277163pubmed: 25587297google scholar: lookup
  5. Adams D.A., Thomas K.R., Jajosky R.A., Foster L., Sharp P., Onweh D.H., Schley A.W., Anderson W.J.. Summary of Notifiable Infectious Diseases and Conditions—United States. MMWR 2014;63:54.
  6. Bishop A., Wang H.-H., Grant W.E.. Using Data Surveillance to Understand the Rising Incidence of Babesiosis in the United States, 2011–2018. Vector-Borne Zoonotic Dis. 2021;21:391–395.
    doi: 10.1089/vbz.2020.2754pubmed: 33739890google scholar: lookup
  7. Krause P.J., Spielman A., Telford S.R., Sikand V.K., McKay K., Christianson D., Pollack R.J., Brassard P., Magera J., Ryan R.. Persistent Parasitemia after Acute Babesiosis. N. Engl. J. Med. 1998;339:160–165.
    doi: 10.1056/NEJM199807163390304pubmed: 9664092google scholar: lookup
  8. Krause P.J.. Babesiosis Diagnosis and Treatment. Vector-Borne Zoonotic Dis. 2003;3:45–51.
    doi: 10.1089/153036603765627451pubmed: 12804380google scholar: lookup
  9. Vannier E., Krause P.J.. Update on Babesiosis. Interdiscip. Perspect. Infect. Dis. 2009;2009.
    doi: 10.1155/2009/984568pmc: PMC2734943pubmed: 19727410google scholar: lookup
  10. Swei A., O’Connor K.E., Couper L.I., Thekkiniath J., Conrad P.A., Padgett K.A., Burns J., Yoshimizu M.H., Gonzales B., Munk B.. Evidence for Transmission of the Zoonotic Apicomplexan Parasite Babesia Duncani by the Tick Dermacentor Albipictus. Int. J. Parasitol. 2019;49:95–103.
  11. Krause P.J.. Human Babesiosis. Int. J. Parasitol. 2019;49:165–174.
    doi: 10.1016/j.ijpara.2018.11.007pubmed: 30690090google scholar: lookup
  12. Almazan C., Tipacamu G.A., Rodriguez S., Mosqueda J., Perez de Leon A.. Immunological Control of Ticks and Tick-Borne Diseases That Impact Cattle Health and Production. Front. Biosci. 2018;23:1535–1551.
    doi: 10.2741/4659pubmed: 29293449google scholar: lookup
  13. de León A.P., Vannier E., Alamazán C., Krause P.J.. Tick-Borne Protozoa. 2014;Voloume 2;pp. 147–179.
  14. Alvarez J.A., Rojas C., Figueroa J.V.. Diagnostic Tools for the Identification of Babesia Sp. in Persistently Infected Cattle. Pathogens 2019;8:143.
    doi: 10.3390/pathogens8030143pmc: PMC6789608pubmed: 31505741google scholar: lookup
  15. Starkey L.A., Little S.E.. Canine Tick-Borne Diseases. Infection 2015;5:55–60.
  16. Kjemtrup A.M., Wainwright K., Miller M., Penzhorn B.L., Carreno R.A.. Babesia Conradae, Sp. Nov., a Small Canine Babesia Identified in California. Vet. Parasitol. 2006;138:103–111.
    doi: 10.1016/j.vetpar.2006.01.044pubmed: 16524663google scholar: lookup
  17. Barash N.R., Thomas B., Birkenheuer A.J., Breitschwerdt E.B., Lemler E., Qurollo B.A.. Prevalence of Babesia Spp. and Clinical Characteristics of Babesia Vulpes Infections in North American Dogs. J. Vet. Intern. Med. 2019;33:2075–2081.
    doi: 10.1111/jvim.15560pmc: PMC6766513pubmed: 31334887google scholar: lookup
  18. Scoles G., Ueti M.. Vector Ecology of Equine Piroplasmosis. Annu. Rev. Entomol. 2015;60:561–580.
  19. Osorno B.M., Solana P.. Aislamiento e Identificación de Babesia Equi y Babesia Caballi En Caballos de México. Rev. Mex. De Cienc. Pecu. 1972;20:39–41.
  20. Mathieu A., Pastor A.R., Berkvens C.N., Gara-Boivin C., Hébert M., Léveillé A.N., Barta J.R., Smith D.A.. Babesia Odocoilei as a Cause of Mortality in Captive Cervids in Canada. Can. Vet. J. 2018;59:52.
    pmc: PMC5731394pubmed: 29302103
  21. Knowles D.P., Kappmeyer L.S., Haney D., Herndon D.R., Fry L.M., Munro J.B., Sears K., Ueti M.W., Wise L.N., Silva M.. Discovery of a Novel Species, Theileria Haneyi n. Sp., Infective to Equids, Highlights Exceptional Genomic Diversity within the Genus Theileria: Implications for Apicomplexan Parasite Surveillance. Int. J. Parasitol. 2018;48:679–690.
    doi: 10.1016/j.ijpara.2018.03.010pubmed: 29885436google scholar: lookup
  22. Oakes V.J., Yabsley M.J., Schwartz D., LeRoith T., Bissett C., Broaddus C., Schlater J.L., Todd S.M., Boes K.M., Brookhart M.. Theileria Orientalis Ikeda Genotype in Cattle, Virginia, USA. Emerg. Infect. Dis. 2019;25:1653.
    doi: 10.3201/eid2509.190088pmc: PMC6711211pubmed: 31237835google scholar: lookup
  23. Wood J., Johnson E.M., Allen K.E., Campbell G.A., Rezabek G., Bradway D.S., Pittman L.L., Little S.E., Panciera R.J.. Merogonic Stages of Theileria Cervi in Mule Deer (Odocoileus Hemionus). J. Vet. Diagn. Investig. 2013;25:662–665.
    doi: 10.1177/1040638713501173pubmed: 24029405google scholar: lookup
  24. Chae J., Levy M., Hunt J., Jr., Schlater J., Snider G., Waghela S.D., Holman P.J., Wagner G.G.. Theileria Sp. Infections Associated with Bovine Fatalities in the United States Confirmed by Small-Subunit RRNA Gene Analyses of Blood and Tick Samples. J. Clin. Microbiol. 1999;37:3037–3040.
  25. Peniche-Lara G., Balmaceda L., Perez-Osorio C., Munoz-Zanzi C.. Human Babesiosis, Yucatán State, Mexico, 2015. Emerg. Infect. Dis. 2018;24:2061.
    doi: 10.3201/eid2411.170512pmc: PMC6199998pubmed: 30334701google scholar: lookup
  26. Rodríguez-Vivas R.I., Grisi L., Pérez de León A.A., Villela H.S., Torres-Acosta J.F.d.J., Fragoso Sánchez H., Romero Salas D., Rosario Cruz R., Saldierna F., García Carrasco D.. Potential Economic Impact Assessment for Cattle Parasites in Mexico. Review. Rev. Mex. De Cienc. Pecu. 2017;8:61–74.
    doi: 10.22319/rmcp.v8i1.4305google scholar: lookup
  27. Esteve-Gasent M.D., Rodríguez-Vivas R.I., Medina R.F., Ellis D., Schwartz A., Cortés Garcia B., Hunt C., Tietjen M., Bonilla D., Thomas D.. Research on Integrated Management for Cattle Fever Ticks and Bovine Babesiosis in the United States and Mexico: Current Status and Opportunities for Binational Coordination. Pathogens 2020;9:871.
    doi: 10.3390/pathogens9110871pmc: PMC7690670pubmed: 33114005google scholar: lookup
  28. Dear J.D., Owens S.D., Lindsay L.L., Biondo A.W., Chomel B.B., Marcondes M., Sykes J.E.. Babesia Conradae Infection in Coyote Hunting Dogs Infected with Multiple Blood-Borne Pathogens. J. Vet. Intern. Med. 2018;32:1609–1617.
    doi: 10.1111/jvim.15233pmc: PMC6189381pubmed: 30307638google scholar: lookup
  29. Schoelkopf L., Hutchinson C.E., Bendele K.G., Goff W.L., Willette M., Rasmussen J.M., Holman P.J.. New Ruminant Hosts and Wider Geographic Range Identified for Babesia Odocoilei (Emerson and Wright 1970). J. Wildl. Dis. 2005;41:683–690.
    doi: 10.7589/0090-3558-41.4.683pubmed: 16456156google scholar: lookup
  30. Short M.A., Clark C.K., Harvey J.W., Wenzlow N., Hawkins I.K., Allred D.R., Knowles D.P., Corn J.L., Grause J.F., Hennager S.G.. Outbreak of Equine Piroplasmosis in Florida. J. Am. Vet. Med. Assoc. 2012;240:588–595.
    doi: 10.2460/javma.240.5.588pubmed: 22332629google scholar: lookup
  31. Scoles G.A., Hutcheson H.J., Schlater J.L., Hennager S.G., Pelzel A.M., Knowles D.P.. Equine Piroplasmosis Associated with Amblyomma Cajennense Ticks, Texas, USA. Emerg. Infect. Dis. 2011;17:1903.
    doi: 10.3201/eid1710.101182pmc: PMC3310643pubmed: 22000367google scholar: lookup
  32. Waldrup K.A., Collisson E., Bentsen S.E., Winkler C.K., Wagner G.G.. Prevalence of Erythrocytic Protozoa and Serologic Reactivity to Selected Pathogens in Deer in Texas. Prev. Vet. Med. 1989;7:49–58.
  33. Pavón-Rocha A.J., Cárdenas-Flores A., Rábago-Castro J.L., Barrón-Vargas C.A., Mosqueda J.. First Molecular Evidence of Theileria Cervi Infection in White-Tailed Deer (Odocoileus Virginianus) in Mexico. Vet. Parasitol. Reg. Stud. Rep. 2020;22:100482.
    doi: 10.1016/j.vprsr.2020.100482pubmed: 33308731google scholar: lookup
  34. Kjemtrup A.M., Conrad P.A.. Human Babesiosis: An Emerging Tick-Borne Disease. Int. J. Parasitol. 2000;30:1323–1337.
    doi: 10.1016/S0020-7519(00)00137-5pubmed: 11113258google scholar: lookup
  35. Bock R., Jackson L., de Vos A., Jorgensen W.. Babesiosis of Cattle. Parasitology 2004;129((Suppl. Sl)):S247–S269.
    doi: 10.1017/S0031182004005190pubmed: 15938514google scholar: lookup
  36. Baneth G.. Antiprotozoal Treatment of Canine Babesiosis. Vet. Parasitol. 2018;254:58–63.
    doi: 10.1016/j.vetpar.2018.03.001pubmed: 29657012google scholar: lookup
  37. Laha R., Das M., Sen A.. Morphology, Epidemiology, and Phylogeny of Babesia: An Overview. Trop. Parasitol. 2015;5:94.
    doi: 10.4103/2229-5070.162490pmc: PMC4557164pubmed: 26629451google scholar: lookup
  38. Riek R.F.. The Life Cycle of Babesia Bigemina (Smith and Kilborne, 1893) in the Tick Vector Boophilus Microplus (Canestrini). Aust. J. Agric. Res. 1964;15:802–821.
    doi: 10.1071/AR9640802google scholar: lookup
  39. Gohil S., Kats L.M., Sturm A., Cooke B.M.. Recent Insights into Alteration of Red Blood Cells by Babesia Bovis: Moovin’forward. Trends Parasitol. 2010;26:591–599.
    doi: 10.1016/j.pt.2010.06.012pubmed: 20598944google scholar: lookup
  40. Gray E.B., Herwaldt B.L.. Babesiosis Surveillance—United States, 2011–2015. MMWR Surveill. Summ. 2019;68:1–11.
    doi: 10.15585/mmwr.ss6806a1pubmed: 31145719google scholar: lookup
  41. Madison-Antenucci S., Kramer L.D., Gebhardt L.L., Kauffman E.. Emerging Tick-Borne Diseases. Clin. Microbiol. Rev. 2020;33.
    doi: 10.1128/CMR.00083-18pmc: PMC6941843pubmed: 31896541google scholar: lookup
  42. Shah J.S., Caoili E., Patton M.F., Tamhankar S., Myint M.M., Poruri A., Mark O., Horowitz R.I., Ashbaugh A.D., Ramasamy R.. Combined Immunofluorescence (IFA) and Fluorescence In Situ Hybridization (FISH) Assays for Diagnosing Babesiosis in Patients from the USA, Europe and Australia. Diagnostics 2020;10:761.
    doi: 10.3390/diagnostics10100761pmc: PMC7650773pubmed: 32998244google scholar: lookup
  43. Jalovecka M., Sojka D., Ascencio M., Schnittger L.. Babesia Life Cycle–When Phylogeny Meets Biology. Trends Parasitol. 2019;35:356–368.
    doi: 10.1016/j.pt.2019.01.007pubmed: 30733093google scholar: lookup
  44. Osorno B.M., Ristic M.. Babesia Canis En Perros En México. Rev. Mex. De Cienc. Pecu. 1974;1:36.
  45. De Vos A.J., De Waal D.T., Jackson L.A.. Bovine Babesiosis. Infect. Dis. Livest. Vol. One. 2004;2:406–424.
  46. Mosqueda J., Olvera-Ramirez A., Aguilar-Tipacamu G., Canto G.J.. Current Advances in Detection and Treatment of Babesiosis. Curr. Med. Chem. 2012;19:1504–1518.
    doi: 10.2174/092986712799828355pmc: PMC3355466pubmed: 22360483google scholar: lookup
  47. Guerrero F.D., Bendele K.G., Davey R.B., George J.E.. Detection of Babesia Bigemina Infection in Strains of Rhipicephalus (Boophilus) Microplus Collected from Outbreaks in South Texas. Vet. Parasitol. 2007;145:156–163.
    doi: 10.1016/j.vetpar.2006.11.014pubmed: 17178440google scholar: lookup
  48. Ramos J.A., Alvarez J.A., Figueroa J.V., Solis J., Rodriguez R.I., Hernandez R., Buening G.M., Vega C.A.. Evaluation of a Colorimetric Babesia Bigemina-DNA Probe within an Epidemiological Survey. Mem. Do Inst. Oswaldo Cruz. 1992;87:213–217.
  49. Solorio-Rivera J.L., Rodríguez-Vivas R.I., Pérez-Gutierrez E., Wagner G.. Management Factors Associated with Babesia Bovis Seroprevalence in Cattle from Eastern Yucatan, Mexico. Prev. Vet. Med. 1999;40:261–269.
    doi: 10.1016/S0167-5877(99)00019-7pubmed: 10423779google scholar: lookup
  50. Teclaw R.F., Romo S., Garcia Z., Castaneda M., Wagner G.G.. A Seroepidemiologic Study of Bovine Babesiosis in the Mexican States of Nuevo Leon, Tamaulipas and Coahuila. Prev. Vet. Med. 1985;3:403–415.
  51. Romero-Salas D., Mira A., Mosqueda J., García-Vázquez Z., Hidalgo-Ruiz M., Vela N.A.O., de León A.A.P., 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;217:101–107.
    doi: 10.1016/j.vetpar.2015.12.030pubmed: 26827869google scholar: lookup
  52. Rodríguez-Vivas R.I., Cob-Galera L.A., Domínguez-Alpizar J.L.. Hemoparásitos En Bovinos, Caninos y Equinos Diagnosticados En El Laboratorio de Parasitología de La Facultad de Medicina Veterinaria y Zootecnia de La Universidad Autónoma de Yucatan (1984–1999). Rev. Biomédica 2000;11:277–282.
  53. Cantu-C A., Ortega-S J.A., García-Vázquez Z., Mosqueda J., Henke S.E., George J.E.. Epizootiology of Babesia Bovis and Babesia Bigemina in Free-Ranging White-Tailed Deer in Northeastern Mexico. J. Parasitol. 2009;95:536–542.
    doi: 10.1645/GE-1648.1pubmed: 19642800google scholar: lookup
  54. Ramos C.M., Cooper S.M., Holman P.J.. Molecular and Serologic Evidence for Babesia Bovis-like Parasites in White-Tailed Deer (Odocoileus Virginianus) in South Texas. Vet. Parasitol. 2010;172:214–220.
    doi: 10.1016/j.vetpar.2010.05.004pubmed: 20605333google scholar: lookup
  55. Holman P.J., Carroll J.E., Pugh R., Davis D.S.. Molecular Detection of Babesia Bovis and Babesia Bigemina in White-Tailed Deer (Odocoileus Virginianus) from Tom Green County in Central Texas. Vet. Parasitol. 2011;177:298–304.
    doi: 10.1016/j.vetpar.2010.11.052pubmed: 21194841google scholar: lookup
  56. Cárdenas-Canales E.M., Ortega-Santos J.A., Campbell T.A., García-Vázquez Z., Cantú-Covarrubias A., Figueroa-Millán J.V., DeYoung R.W., Hewitt D.G., Bryant F.C.. Nilgai Antelope in Northern Mexico as a Possible Carrier for Cattle Fever Ticks and Babesia Bovis and Babesia Bigemina. J. Wildl. Dis. 2011;47:777–779.
    doi: 10.7589/0090-3558-47.3.777pubmed: 21719852google scholar: lookup
  57. García-Vázquez Z., Ortega-S J.A., Cantu-Covarruvias A., Mosqueda J., Hewitt D.G., DeYoung R.W., Campbell T.A., Bryant F.C.. Tick-Borne Diseases in Syntopic Populations of Fallow Deer (Dama Dama) and Axis Deer (Axis Axis) in Northern Mexico. J. Wildl. Dis. 2015;51:527–529.
    doi: 10.7589/2014-07-183pubmed: 25647599google scholar: lookup
  58. Lira-Amaya J.J., Rojas-Martinez C., Alvarez A., Pelaezflores A., Martinez-Ibañez F., Rosa D.P., Figueroamillan J.V.. First Molecular Detection of Babesia Canis Vogeli in Dogs and Rhipicephalus Sanguineus from Mexico. Arch. Palliat. Care. 2017;2:2–5.
  59. Birkenheuer A.J., Correa M.T., Levy M.G., Breitschwerdt E.B.. Geographic Distribution of Babesiosis among Dogs in the United States and Association with Dog Bites: 150 Cases (2000–2003). J. Am. Vet. Med. Assoc. 2005;227:942–947.
    doi: 10.2460/javma.2005.227.942pubmed: 16190594google scholar: lookup
  60. Stayton E.M., Lineberry M., Thomas J., Bass T., Allen K., Chandrashekar R., Yost G., Reichard M., Miller C.. Emergence of Babesia Conradae Infection in Coyote-Hunting Greyhounds in Oklahoma, USA. Res. Sq. 2021.
    doi: 10.1186/s13071-021-04897-xpmc: PMC8364010pubmed: 34391445google scholar: lookup
  61. Allison R.W., Yeagley T.J., Levis K., Reichard M.V.. Babesia Canis Rossi Infection in a Texas Dog. Vet. Clin. Pathol. 2011;40:345–350.
  62. Medrano-Bugarini R.A., Figueroa-Millán J.V., Rivera-Chavira B.E., Lira-Amaya J.J., Rodríguez-Alarcón C.A., Beristain-Ruiz D.M., Adame-Gallegos J.R.. Detection of Theileria Equi, Babesia Caballi, and Anaplasma Phagocytophilum DNA in Soft Ticks and Horses at Ciudad Juarez, Mexico. Southwest. Entomol. 2019;44:647–658.
    doi: 10.3958/059.044.0310google scholar: lookup
  63. Cantú-Martínez M.A., Segura-Correa J.C., Silva-Páez M.L., Avalos-Ramírez R., Wagner G.G.. Prevalence of Antibodies to Theileria Equi and Babesia Caballi in Horses from Northeastern Mexico. J. Parasitol. 2012;98:869–870.
    doi: 10.1645/GE-3064.1pubmed: 22339765google scholar: lookup
  64. Scott J.D., Pascoe E.L., Sajid M.S., Foley J.E.. Detection of Babesia Odocoilei in Ixodes Scapularis Ticks Collected in Southern Ontario, Canada. Pathogens 2021;10:327.
    doi: 10.3390/pathogens10030327pmc: PMC7999371pubmed: 33802071google scholar: lookup
  65. Olafson P.U., Thomas D.B., May M.A., Buckmeier B.G., Duhaime R.A.. Tick Vector and Disease Pathogen Surveillance of Nilgai Antelope (Boselaphus Tragocamelus) in Southeastern Texas, USA. J. Wildl. Dis. 2018;54:734–744.
    doi: 10.7589/2017-09-239pubmed: 29863973google scholar: lookup
  66. Ueti M.W., Olafson P.U., Freeman J.M., Johnson W.C., Scoles G.A.. A Virulent Babesia Bovis Strain Failed to Infect White-Tailed Deer (Odocoileus Virginianus). PLoS ONE 2015;10:e0131018.
  67. Vishwakarma P., Nandini M.K.. Overview of Canine Babesiosis. 2019;p. 109.
  68. Boozer A.L., Macintire D.K.. Canine Babesiosis. Vet. Clin. Small Anim. Pract. 2003;33:885–904.
    doi: 10.1016/S0195-5616(03)00039-1pubmed: 12910748google scholar: lookup
  69. Solano-Gallego L., Sainz Á., Roura X., Estrada-Peña A., Miró G.. A Review of Canine Babesiosis: The European Perspective. Parasites Vectors 2016;9:1–18.
    doi: 10.1186/s13071-016-1596-0pmc: PMC4902949pubmed: 27289223google scholar: lookup
  70. Emerson H.R., Wright W.T.. The Isolation of a Babesia in White-Tailed Deer. Bull. Wildl. Dis. Assoc. 1968;4:142–143.
    doi: 10.7589/0090-3558-4.4.142pubmed: 5693839google scholar: lookup
  71. Tirosh-Levy S., Gottlieb Y., Fry L.M., Knowles D.P., Steinman A.. Twenty Years of Equine Piroplasmosis Research: Global Distribution, Molecular Diagnosis, and Phylogeny. Pathogens 2020;9:926.
    doi: 10.3390/pathogens9110926pmc: PMC7695325pubmed: 33171698google scholar: lookup
  72. Wise L.N., Kappmeyer L.S., Mealey R.H., Knowles D.P.. Review of Equine Piroplasmosis. J. Vet. Intern. Med. 2013;27:1334–1346.
    doi: 10.1111/jvim.12168pubmed: 24033559google scholar: lookup
  73. Onyiche T.E., Suganuma K., Igarashi I., Yokoyama N., Xuan X., Thekisoe O.. A Review on Equine Piroplasmosis: Epidemiology, Vector Ecology, Risk Factors, Host Immunity, Diagnosis and Control. Int. J. Environ. Res. Public Health 2019;16:1736.
    doi: 10.3390/ijerph16101736pmc: PMC6572709pubmed: 31100920google scholar: lookup
  74. Rothschild C.M.. Equine Piroplasmosis. J. Equine Vet. Sci. 2013;33:497–508.
  75. Sears K.P., Kappmeyer L.S., Wise L.N., Silva M., Ueti M.W., White S., Reif K.E., Knowles D.P.. Infection Dynamics of Theileria Equi and Theileria Haneyi, a Newly Discovered Apicomplexan of the Horse. Vet. Parasitol. 2019;271:68–75.
    doi: 10.1016/j.vetpar.2019.06.009pubmed: 31303207google scholar: lookup
  76. Sumbria D., Moudgil A.D., Singla L.D.. Equine Piroplasmosis: Current Status. Veterinaria 2014;1:9–14.
  77. Laus F., Spaterna A., Faillace V., Veronesi F., Ravagnan S., Beribé F., Cerquetella M., Meligrana M., Tesei B.. Clinical Investigation on Theileria Equi and Babesia Caballi Infections in Italian Donkeys. BMC Vet. Res. 2015;11:1–7.
    doi: 10.1186/s12917-015-0411-zpmc: PMC4410693pubmed: 25927984google scholar: lookup
  78. Kouam M.K., Kantzoura V., Gajadhar A.A., Theis J.H., Papadopoulos E., Theodoropoulos G.. Seroprevalence of Equine Piroplasms and Host-Related Factors Associated with Infection in Greece. Vet. Parasitol. 2010;169:273–278.
    doi: 10.1016/j.vetpar.2010.01.011pubmed: 20138434google scholar: lookup
  79. Mahoney D.F., Wright I.G., Frerichs W.M., Groenendyk S., O’Sullivan B.M., Roberts M.C., Waddell A.H.. The Identification of Babesia Equi in Australia. Aust. Vet. J. 1977;53:461–464.
  80. Zobba R., Ardu M., Niccolini S., Chessa B., Manna L., Cocco R., Parpaglia M.L.P.. Clinical and Laboratory Findings in Equine Piroplasmosis. J. Equine Vet. Sci. 2008;28:301–308.
  81. Mahmoud M.S., El-Ezz N.T.A., Abdel-Shafy S., Nassar S.A., El Namaky A.H., Khalil W.K., Knowles D., Kappmeyer L., Silva M.G., Suarez C.E.. Assessment of Theileria Equi and Babesia Caballi Infections in Equine Populations in Egypt by Molecular, Serological and Hematological Approaches. Parasites Vectors 2016;9:1–10.
    doi: 10.1186/s13071-016-1539-9pmc: PMC4857240pubmed: 27146413google scholar: lookup
  82. Friedhoff K.T., Tenter A.M., Müller I.. Haemoparasites of Equines: Impact on International Trade of Horses. Rev. Sci. Et Tech. (Int. Off. Epizoot.) 1990;9:1187–1194.
    pubmed: 2132711
  83. Brüning A.. Equine Piroplasmosis an Update on Diagnosis, Treatment and Prevention. Br. Vet. J. 1996;152:139–151.
    doi: 10.1016/S0007-1935(96)80070-4pubmed: 8680838google scholar: lookup
  84. Awinda P.O.. Serum Antibodies from Babesia Caballi Seropositive Horses in the United States Demonstrate a Protein Recognition Pattern That Is Not Consistent with Infection. 2013.
  85. Alhassan A., Govind Y., Tam N.T., Thekisoe O.M., Yokoyama N., Inoue N., Igarashi I.. Comparative Evaluation of the Sensitivity of LAMP, PCR and in Vitro Culture Methods for the Diagnosis of Equine Piroplasmosis. Parasitol. Res. 2007;100:1165–1168.
    doi: 10.1007/s00436-006-0430-6pubmed: 17216488google scholar: lookup
  86. Hirato K., Ninomiya M., Uwano Y., Kuth T.. Studies on the Complement Fixation Reaction for Equine Piroplasmosis. Jpn. J. Vet. Sci. 1945;7:197–205.
    doi: 10.1292/jvms1939.7.197google scholar: lookup
  87. Knowles D.P., Jr., Kappmeyer L.S., Stiller D., Hennager S.G., Perryman L.E.. Antibody to a Recombinant Merozoite Protein Epitope Identifies Horses Infected with Babesia Equi. J. Clin. Microbiol. 1992;30:3122–3126.
  88. Ayala-Valdovinos M.A., Lemus-Flores C., Galindo-García J., Bañuelos-Pineda J., Rodríguez-Carpena J.G., Sánchez-Chiprés D., Duifhuis-Rivera T.. Diagnosis and Prevalence of Theileria Equi Horses in Western Mexico by Nested PCR. Parasitol. Int. 2017;66:821–824.
    doi: 10.1016/j.parint.2016.09.011pubmed: 27671686google scholar: lookup
  89. Romero-Salas D., Solis-Cortés M., Zazueta-Islas H.M., Flores-Vásquez F., Cruz-Romero A., Aguilar-Domínguez M., Salguero-Romero J.L., de León A.P., Fernández-Figueroa E.A., Lammoglia-Villagómez M.Á.. Molecular Detection of Theileria Equi in Horses from Veracruz, Mexico. Ticks Tick-Borne Dis. 2021;12:101671.
    doi: 10.1016/j.ttbdis.2021.101671pubmed: 33545504google scholar: lookup
  90. Bryant J.E., Anderson J.B., Willers K.H.. Control of Equine Piroplasmosis in Florida. J. Am. Vet. Med. Assoc. 1969;154:1034–1036.
    pubmed: 5813490
  91. Stockham S.L., Kjemtrup A.M., Conrad P.A., Schmidt D.A., Scott M.A., Robinson T.W., Tyler J.W., Johnson G.C., Carson C.A., Cuddihee P.. Theileriosis in a Missouri Beef Herd Caused by Theileria Buffeli: Case Report, Herd Investigation, Ultrastructure, Phylogenetic Analysis, and Experimental Transmission. Vet. Pathol. 2000;37:11–21.
    doi: 10.1354/vp.37-1-11pubmed: 10643976google scholar: lookup
  92. Splitter E.J.. Theileria Mutans Associated with Bovine Anaplasmosis in the United States. J. Am. Vet. Med. Assoc. 1950;117:134–135.
    pubmed: 15428394
  93. Cossio-Bayugar R., Pillars R., Schlater J., Holman P.J.. Theileria Buffeli Infection of a Michigan Cow Confirmed by Small Subunit Ribosomal RNA Gene Analysis. Vet. Parasitol. 2002;105:105–110.
    doi: 10.1016/S0304-4017(02)00003-1pubmed: 11900924google scholar: lookup
  94. Robinson R.M., Kuttler K.L., Thomas J.W., Marburger R.G.. Theileriasis in Texas White-Tailed Deer. J. Wildl. Manag. 1967;31:455–459.
    doi: 10.2307/3798123google scholar: lookup
  95. Chae J., Waghela S.D., Craig T.M., Kocan A.A., Wagner G.G., Holman P.J.. Two Theileria Cervi SSU RRNA Gene Sequence Types Found in Isolates from White-Tailed Deer and Elk in North America. J. Wildl. Dis. 1999;35:458–465.
    doi: 10.7589/0090-3558-35.3.458pubmed: 10479079google scholar: lookup
  96. Yabsley M.J., Quick T.C., Little S.E.. Theileriosis in a White-Tailed Deer (Odocoileus Virginianus) Fawn. J. Wildl. Dis. 2005;41:806–809.
    doi: 10.7589/0090-3558-41.4.806pubmed: 16456174google scholar: lookup
  97. Cauvin A., Hood K., Shuman R., Orange J., Blackburn J.K., Sayler K.A., Wisely S.M.. The Impact of Vector Control on the Prevalence of Theileria Cervi in Farmed Florida White-Tailed Deer, Odocoileus Virginianus. Parasites Vectors 2019;12:1–9.
    doi: 10.1186/s13071-019-3344-8pmc: PMC6417225pubmed: 30867021google scholar: lookup
  98. Kjemtrup A.M., Robinson T., Conrad P.A.. Description and Epidemiology of Theileria Youngi n. Sp. from a Northern Californian Dusky-Footed Woodrat (Neotoma Fuscipes) Population. J. Parasitol. 2001;87:373–378.
  99. Camacho A.T., Guitián F.J., Pallas E., Gestal J.J., Olmeda A.S., Goethert H.K., Telford S.R.. Infection of Dogs in North-West Spain with a Babesia Microti-like Agent. Vet. Rec. 2001;149:552–555.
    doi: 10.1136/vr.149.18.552pubmed: 11720208google scholar: lookup
  100. Uilenberg G., Perie N.M., Spanjer A.A.M., Franssen F.F.J.. Theileria Orientalis, a Cosmopolitan Blood Parasite of Cattle: Demonstration of the Schizont Stage. Res. Vet. Sci. 1985;38:352–360.
    doi: 10.1016/S0034-5288(18)31808-3pubmed: 3925510google scholar: lookup
  101. McKeever D.J.. Bovine Immunity–a Driver for Diversity in Theileria Parasites?. Trends Parasitol. 2009;25:269–276.
    doi: 10.1016/j.pt.2009.03.005pubmed: 19423397google scholar: lookup
  102. Mans B.J., Pienaar R., Latif A.A.. A Review of Theileria Diagnostics and Epidemiology. Int. J. Parasitol. Parasites Wildl. 2015;4:104–118.
  103. Irvin A.D.. Characterization of Species and Strains of Theileria. Adv. Parasitol. 1987;26:145–197.
    pubmed: 3118658
  104. Bishop R., Musoke A., Morzaria S., Gardner M., Nene V.. Theileria: Intracellular Protozoan Parasites of Wild and Domestic Ruminants Transmitted by Ixodid Ticks. Parasitology 2004;129:S271–S283.
    doi: 10.1017/S0031182003004748pubmed: 15938515google scholar: lookup
  105. Aktas M., Altay K., Dumanli N.. A Molecular Survey of Bovine Theileria Parasites among Apparently Healthy Cattle and with a Note on the Distribution of Ticks in Eastern Turkey. Vet. Parasitol. 2006;138:179–185.
    doi: 10.1016/j.vetpar.2006.01.052pubmed: 16510248google scholar: lookup
  106. Kamau J., de Vos A.J., Playford M., Salim B., Kinyanjui P., Sugimoto C.. Emergence of New Types of Theileria Orientalis in Australian Cattle and Possible Cause of Theileriosis Outbreaks. Parasites Vectors 2011;4:1–10.
    doi: 10.1186/1756-3305-4-22pmc: PMC3050848pubmed: 21338493google scholar: lookup
  107. Perera P.K., Gasser R.B., Firestone S.M., Anderson G.A., Malmo J., Davis G., Beggs D.S., Jabbar A.. Oriental Theileriosis in Dairy Cows Causes a Significant Milk Production Loss. Parasites Vectors 2014;7:1–8.
    doi: 10.1186/1756-3305-7-73pmc: PMC3937217pubmed: 24552213google scholar: lookup
  108. Lawrence K.E., Forsyth S.F., Vaatstra B.L., McFadden A.M.J., Pulford D.J., Govindaraju K., Pomroy W.E.. Clinical Haematology and Biochemistry Profiles of Cattle Naturally Infected with Theileria Orientalis Ikeda Type in New Zealand. N. Z. Vet. J. 2018;66:21–29.
    doi: 10.1080/00480169.2017.1391142pubmed: 29020888google scholar: lookup
  109. McFadden A.M.J., Hart M., Bueno I.M., Ha H.J., Heath A.C.G., Pulford D.J.. Monitoring Theileria Orientalis (Ikeda)-Associated Bovine Anaemia in Affected Cattle over Time. Vet. Parasitol. 2017;245:29–33.
    doi: 10.1016/j.vetpar.2017.07.035pubmed: 28969833google scholar: lookup
  110. Swilks E., Fell S.A., Hammer J.F., Sales N., Krebs G.L., Jenkins C.. Transplacental Transmission of Theileria Orientalis Occurs at a Low Rate in Field-Affected Cattle: Infection in Utero Does Not Appear to Be a Major Cause of Abortion. Parasites Vectors 2017;10:1–9.
    doi: 10.1186/s13071-017-2166-9pmc: PMC5423014pubmed: 28482923google scholar: lookup
  111. Gebrekidan H., Perera P.K., Ghafar A., Abbas T., Gasser R.B., Jabbar A.. An Appraisal of Oriental Theileriosis and the Theileria Orientalis Complex, with an Emphasis on Diagnosis and Genetic Characterisation. Parasitol. Res. 2020;119:11–22.
    doi: 10.1007/s00436-019-06557-7pmc: PMC7223495pubmed: 31811422google scholar: lookup
  112. Watts J.G., Playford M.C., Hickey K.L.. Theileria Orientalis: A Review. N. Z. Vet. J. 2016;64:3–9.
    doi: 10.1080/00480169.2015.1064792pubmed: 26143684google scholar: lookup
  113. Charaya G., Rakha N.K., Maan S., Kumar A., Kumar T., Jhambh R.. Comparative Evaluation of Polymerase Chain Reaction Assay with Microscopy for Detection of Asymptomatic Carrier State of Theileriosis in a Herd of Crossbred Cattle. Vet. World 2016;9:1039.