Analyze Diet
Parasitology2020; 147(13); 1411-1424; doi: 10.1017/S0031182020001407

Equine piroplasmosis: an insight into global exposure of equids from 1990 to 2019 by systematic review and meta-analysis.

Abstract: Equine piroplasmosis (EP) is a tick-borne disease of economic importance, relevant in the international movement of equids. The causative agents are at least two apicomplexan protozoan parasites Babesia caballi and Theileria equi. To date, there is no study that estimates global and regional exposure of equids to EP. We therefore conducted a systematic review and meta-analysis to estimate the pooled prevalence and heterogeneity of EP using random-effects model. Six electronic databases were searched for publications on EP and assessed according to Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines. A total of 66 eligible studies published between 1990 and 2019 and representing 24 041 equids were included. The overall pooled prevalence estimates (PPEs) of B. caballi was 22.3% (95% CI 21.7-22.8), while the overall PPE for T. equi was 29.4% (95% CI 28.7-30.0). The overall pooled prevalence due to co-infection with both parasites was 11.8% (95% CI 11.32-12.32). Also, subgroup analysis according to sex, age, diagnostic technique, equid species, region and publication years showed a substantial degree of heterogeneity across studies computed for both B. caballi and T. equi infections in equids. Awareness of the current status of EP globally will alert the relevant authorities and stakeholders where necessary on the need for better preventive and control strategies against the disease.
Publication Date: 2020-08-03 PubMed ID: 32741382PubMed Central: PMC10317785DOI: 10.1017/S0031182020001407Google 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
  • Meta-Analysis
  • Research Support
  • Non-U.S. Gov't
  • Systematic 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 revolves around understanding the prevalence of Equine piroplasmosis (EP), a tick-borne disease affecting equids, at a global level based on systematic review and meta-analysis of studies from 1990 to 2019.

Research Objectives and Methods

  • The authors aim to estimate the worldwide and regional exposure of equids, the family of mammals comprising horses, donkeys, and zebras, to Equine piroplasmosis (EP).
  • EP is caused by at least two different parasites (Babesia caballi and Theileria equi), and is challenging to control due to its spread through ticks.
  • The researchers conducted a systematic review and meta-analysis, where they analyzed data from existing studies to draw broader conclusions.
  • They picked out relevant studies from six electronic databases following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines, resulting in 66 eligible studies including information on a total of 24,041 equids.

Findings and Interpretation

  • The research determined pooled prevalence estimates (PPEs), which is an estimate of the overall percentage of equids infected by the parasites.
  • The PPE for Babesia caballi was found to be 22.3%, while for Theileria equi was higher at 29.4%. The prevalence of co-infection by both parasites was estimated at 11.8%.
  • Moreover, the subgroup analysis, which divided data according to factors like sex, age, diagnostic technique, region, and publication years, revealed a high degree of heterogeneity, or variation, in the incidence of both B. caballi and T. equi infections in equids.

Significance and Impact

  • This research provides a comprehensive examination of the global status of EP, filling the gap in existing knowledge and establishing its widespread prevalence.
  • These findings can alert relevant authorities about the high prevalence of EP, driving the development and implementation of better preventive and control strategies against the disease.
  • Interestingly, the notable variation in infection rates suggests that certain factors might significantly influence the disease’s spread, which can be useful for targeted disease control efforts.

Cite This Article

APA
Onyiche TE, Taioe MO, Molefe NI, Biu AA, Luka J, Omeh IJ, Yokoyama N, Thekisoe O. (2020). Equine piroplasmosis: an insight into global exposure of equids from 1990 to 2019 by systematic review and meta-analysis. Parasitology, 147(13), 1411-1424. https://doi.org/10.1017/S0031182020001407

Publication

ISSN: 1469-8161
NlmUniqueID: 0401121
Country: England
Language: English
Volume: 147
Issue: 13
Pages: 1411-1424

Researcher Affiliations

Onyiche, ThankGod E
  • Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom2520, South Africa.
  • Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria.
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido080-8555, Japan.
Taioe, Moeti O
  • National Zoological Gardens of South Africa, South African National Biodiversity Institute, PO Box 754, Pretoria0001, South Africa.
Molefe, Nthatisi I
  • Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom2520, South Africa.
Biu, Abdullahi A
  • Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria.
Luka, Joshua
  • Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria.
Omeh, Isaac J
  • Department of Veterinary Physiology and Biochemistry, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria.
Yokoyama, Naoaki
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido080-8555, Japan.
Thekisoe, Oriel
  • Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom2520, South Africa.

MeSH Terms

  • Animals
  • Babesia / physiology
  • Babesiosis / epidemiology
  • Babesiosis / parasitology
  • Coinfection / epidemiology
  • Coinfection / parasitology
  • Coinfection / veterinary
  • Equidae
  • Horse Diseases / epidemiology
  • Horse Diseases / parasitology
  • Horses
  • Prevalence
  • Risk Factors
  • Theileria / physiology
  • Theileriasis / epidemiology
  • Theileriasis / parasitology

Conflict of Interest Statement

No conflict of interest exists among the authors.

References

This article includes 88 references
  1. Abedi V, Razmi G, Seifi H, Naghibi A. Molecular and serological detection of Theileria equi and Babesia caballi infection in horses and ixodid ticks in Iran.. Ticks Tick Borne Dis 2014 Apr;5(3):239-44.
    pubmed: 24556274doi: 10.1016/j.ttbdis.2013.11.008google scholar: lookup
  2. Abedi V, Razmi G, Seifi H, Naghibi A. Molecular detection of equine piroplasms in donkeys (Equus asinus) in North Khorasan province, Iran.. Iran J Vet Res 2015 Spring;16(2):202-4.
    pmc: PMC4827686pubmed: 27175176
  3. Abutarbush SM, Alqawasmeh DM, Mukbel RM, Al-Majali AM. Equine babesiosis: seroprevalence, risk factors and comparison of different diagnostic methods in Jordan.. Transbound Emerg Dis 2012 Feb;59(1):72-8.
  4. Acici M, Umur S, Guvenc T, Arslan HH, Kurt M. Seroprevalence of equine babesiosis in the Black Sea region of Turkey.. Parasitol Int 2008 Jun;57(2):198-200.
    pubmed: 18234550doi: 10.1016/j.parint.2007.12.009google scholar: lookup
  5. Akkan HA, Karaca M, Tutuncu M, Deger S, Keles I, Agaoglu Z. Serologic and microscopic studies on babesiosis in horses in the eastern border of Turkey.. Journal of Equine Veterinary Science 5, 181–183.
  6. Al-Obaidi QT, Arshad MM, Al-Sultan II, Azlinda AB, Mohd-Azam KGK. Comparison between microscopic examination and competitive ELISA for diagnosis of equine piroplasmosis in Kelantan. Malaysia.. Malaysia Journal of Veterinary Research 7, 23–29.
  7. Alanazi AD, Alyousif MS, Hassieb MM. Seroprevalence study on Theileria equi and Babesia caballi antibodies in horses from central province of Saudi Arabia.. J Parasitol 2012 Oct;98(5):1015-7.
    pubmed: 22489955doi: 10.1645/ge-2997.1google scholar: lookup
  8. Asgarali Z, Coombs DK, Mohammed F, Campbell MD, Caesar E. A serological study of Babesia caballi and Theileria equi in Thoroughbreds in Trinidad.. Vet Parasitol 2007 Mar 15;144(1-2):167-71.
    pubmed: 17118557doi: 10.1016/j.vetpar.2006.09.015google scholar: lookup
  9. Avarzed A, De Waal DT, Igarashi I, Saito A, Oyamada T, Toyoda Y, Suzuki N. Prevalence of equine piroplasmosis in Central Mongolia.. Onderstepoort J Vet Res 1997 Jun;64(2):141-5.
    pubmed: 9352563
  10. Ayala-Valdovinos MA, Lemus-Flores C, Galindo-García J, Sánchez-Chipres D, Duifhuis-Rivera T, Anguiano-Estrella R, Bañuelos-Pineda J, Rodríguez-Carpena JG. Nested PCR detection of Theileria equi infection and frequency in horses imported into Mexico.. Journal of Animal Veterinary Advances 13, 859–863.
  11. Balkaya I, Utuk AE, Piskin FC. Prevalance of Theileria equi and Babesia caballi in donkeys from Eastern Turkey in winter season.. Pakistan Veterinary Journal 30, 245–246.
  12. Bartolomé Del Pino LE, Nardini R, Veneziano V, Iacoponi F, Cersini A, Autorino GL, Buono F, Scicluna M. Babesia caballi and Theileria equi infections in horses in Central-Southern Italy: Sero-molecular survey and associated risk factors.. Ticks Tick Borne Dis 2016 Apr;7(3):462-9.
    pubmed: 26847198doi: 10.1016/j.ttbdis.2016.01.011google scholar: lookup
  13. Bhoora R, Quan M, Zweygarth E, Guthrie AJ, Prinsloo SA, Collins NE. Sequence heterogeneity in the gene encoding the rhoptry-associated protein-1 (RAP-1) of Babesia caballi isolates from South Africa.. Vet Parasitol 2010 May 11;169(3-4):279-88.
    pubmed: 20138703doi: 10.1016/j.vetpar.2010.01.009google scholar: lookup
  14. Boldbaatar D, Xuan X, Battsetseg B, Igarashi I, Battur B, Batsukh Z, Bayambaa B, Fujisaki K. Epidemiological study of equine piroplasmosis in Mongolia.. Vet Parasitol 2005 Jan 4;127(1):29-32.
    pubmed: 15619372doi: 10.1016/j.vetpar.2004.08.021google scholar: lookup
  15. Böse R, Jorgensen WK, Dalgliesh RJ, Friedhoff KT, de Vos AJ. Current state and future trends in the diagnosis of babesiosis.. Vet Parasitol 1995 Mar;57(1-3):61-74.
    pubmed: 7597794doi: 10.1016/0304-4017(94)03111-9google scholar: lookup
  16. Butler CM, Sloet van Oldruitenborgh-Oosterbaan MM, Stout TA, van der Kolk JH, Wollenberg Lv, Nielen M, Jongejan F, Werners AH, Houwers DJ. Prevalence of the causative agents of equine piroplasmosis in the South West of The Netherlands and the identification of two autochthonous clinical Theileria equi infections.. Vet J 2012 Aug;193(2):381-5.
    pubmed: 22266019doi: 10.1016/j.tvjl.2011.12.014google scholar: lookup
  17. Camacho AT, Guitian FJ, Pallas E, Gestal JJ, Olmeda AS, Habela MA, Telford SR 3rd, Spielman A. Theileria (Babesia) equi and Babesia caballi infections in horses in Galicia, Spain.. Trop Anim Health Prod 2005 May;37(4):293-302.
    pubmed: 15934637doi: 10.1007/s11250-005-5691-zgoogle scholar: lookup
  18. Camino E, de la Cruz ML, Dominguez L, Carvajal KA, Fores P, de Juan L, Cruz-Lopez F. Epidemiological situation of the exposure to agents causing equine piroplasmosis in Spanish purebred horses in Spain: seroprevalence and associated risk factors.. Journal of Equine Veterinary Science 67, 81–86.
  19. Cantú-Martínez MA, Segura-Correa JC, Silva-Páez ML, Avalos-Ramírez R, Wagner GG. Prevalence of antibodies to Theileria equi and Babesia caballi in horses from northeastern Mexico.. J Parasitol 2012 Aug;98(4):869-70.
    pubmed: 22339765doi: 10.1645/ge-3064.1google scholar: lookup
  20. Chahan B, Zhang S, Seo JY, Nakamura C, Zhang G, Bannai H, Jian Z, Inokuma H, Tuchiya K, Sato Y, Kabeya H, Maruyama S, Mikami T, Xuan X. Seroepidemiological evidence for the possible presence of Babesia (Theileria) equi and Babesia caballi infections in donkeys in western Xinjiang, China.. J Vet Med Sci 2006 Jul;68(7):753-5.
    pubmed: 16891793doi: 10.1292/jvms.68.753google scholar: lookup
  21. Montes Cortés MG, Fernández-García JL, Habela Martínez-Estéllez MÁ. Seroprevalence of Theileria equi and Babesia caballi in horses in Spain.. Parasite 2017;24:14.
    pmc: PMC5432961pubmed: 28497743doi: 10.1051/parasite/2017015google scholar: lookup
  22. Cruz-Flores MJ, Bata M, Co B, Claveria FG, Verdida R, Xuan X, Igarashi I. Immunochromatographic assay of Babesia caballi and Babesia equi Laveran 1901 (Theileria equi Mehlhorn and Schein, 1998) (Phylum Apicomplexa) infection in Philippine horses correlated with parasite detection in blood smears.. Veterinarski Arhiv 80, 715–722.
  23. Díaz-Sánchez AA, Pires MS, Estrada CY, Cañizares EV, Del Castillo Domínguez SL, Cabezas-Cruz A, Rivero EL, da Fonseca AH, Massard CL, Corona-González B. First molecular evidence of Babesia caballi and Theileria equi infections in horses in Cuba.. Parasitol Res 2018 Oct;117(10):3109-3118.
    pubmed: 30033488doi: 10.1007/s00436-018-6005-5google scholar: lookup
  24. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test.. BMJ 1997 Sep 13;315(7109):629-34.
    pmc: PMC2127453pubmed: 9310563doi: 10.1136/bmj.315.7109.629google scholar: lookup
  25. Gallusová M, Qablan MA, D'Amico G, Oborník M, Petrželková KJ, Mihalca AD, Modrý D. Piroplasms in feral and domestic equines in rural areas of the Danube Delta, Romania, with survey of dogs as a possible reservoir.. Vet Parasitol 2014 Dec 15;206(3-4):287-92.
    pubmed: 25468026doi: 10.1016/j.vetpar.2014.10.018google scholar: lookup
  26. García-Bocanegra I, Arenas-Montes A, Hernández E, Adaszek L, Carbonero A, Almería S, Jaén-Téllez JA, Gutiérrez-Palomino P, Arenas A. Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infection in equids.. Vet J 2013 Feb;195(2):172-8.
    pubmed: 22784418doi: 10.1016/j.tvjl.2012.06.012google scholar: lookup
  27. Gizachew A, Schuster RK, Joseph S, Wernery R, Georgy NA, Elizabeth SK, Wernery U. Piroplasmosis in donkeys – a hematological and serological study in Central Ethiopia.. Journal of Equine Veterinary Science 33, 18–21.
  28. Grandi G, Molinari G, Tittarelli M, Sassera D, Kramer LH. Prevalence of Theileria equi and Babesia caballi infection in horses from northern Italy.. Vector Borne Zoonotic Dis 2011 Jul;11(7):955-6.
    pubmed: 21254835doi: 10.1089/vbz.2010.0193google scholar: lookup
  29. Guidi E, Pradier S, Lebert I, Leblond A. Piroplasmosis in an endemic area: analysis of the risk factors and their implications in the control of Theileriosis and Babesiosis in horses.. Parasitol Res 2015 Jan;114(1):71-83.
    pubmed: 25280516doi: 10.1007/s00436-014-4161-9google scholar: lookup
  30. Gummow B, de Wet CS, de Waal DT. A sero-epidemiological survey of equine piroplasmosis in the northern and eastern Cape Provinces of South Africa.. J S Afr Vet Assoc 1996 Dec;67(4):204-8.
    pubmed: 9284032
  31. Guven E, Avcioglu H, Deniz A, Balkaya İ, Abay U, Yavuz Ş, Akyüz M. Prevalence and molecular characterization of Theileria equi and Babesia caballi in jereed horses in Erzurum, Turkey.. Acta Parasitol 2017 Mar 1;62(1):207-213.
    pubmed: 28030350doi: 10.1515/ap-2017-0025google scholar: lookup
  32. Hawkins E, Kock R, McKeever D, Gakuya F, Musyoki C, Chege SM, Mutinda M, Kariuki E, Davidson Z, Low B, Skilton RA, Njahira MN, Wamalwa M, Maina E. Prevalence of Theileria equi and Babesia caballi as well as the identification of associated ticks in sympatric Grevy's zebras (Equus grevyi) and donkeys (Equus africanus asinus) in northern Kenya.. J Wildl Dis 2015 Jan;51(1):137-47.
    pubmed: 25380362doi: 10.7589/2013-11-316google scholar: lookup
  33. Hedges LV, Vevea JL. Fixed-and random-effects models in meta-analysis.. Psychological Methods 3, 486.
  34. Heim A, Passos LM, Ribeiro MF, Costa-Júnior LM, Bastos CV, Cabral DD, Hirzmann J, Pfister K. Detection and molecular characterization of Babesia caballi and Theileria equi isolates from endemic areas of Brazil.. Parasitol Res 2007 Dec;102(1):63-8.
    pubmed: 17828553doi: 10.1007/s00436-007-0726-1google scholar: lookup
  35. Heuchert CM, de Giulli V Jr, de Athaide DF, Böse R, Friedhoff KT. Seroepidemiologic studies on Babesia equi and Babesia caballi infections in Brazil.. Vet Parasitol 1999 Aug 16;85(1):1-11.
    pubmed: 10447188doi: 10.1016/s0304-4017(99)00108-9google scholar: lookup
  36. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis.. Stat Med 2002 Jun 15;21(11):1539-58.
    pubmed: 12111919doi: 10.1002/sim.1186google scholar: lookup
  37. Homer MJ, Aguilar-Delfin I, Telford SR 3rd, Krause PJ, Persing DH. Babesiosis.. Clin Microbiol Rev 2000 Jul;13(3):451-69.
    pmc: PMC88943pubmed: 10885987doi: 10.1128/cmr.13.3.451google scholar: lookup
  38. Hussain MH, Saqib M, Raza F, Muhammad G, Asi MN, Mansoor MK, Saleem M, Jabbar A. Seroprevalence of Babesia caballi and Theileria equi in five draught equine populated metropolises of Punjab, Pakistan.. Vet Parasitol 2014 May 28;202(3-4):248-56.
    pubmed: 24582524doi: 10.1016/j.vetpar.2014.01.026google scholar: lookup
  39. Sunday Idoko I, Tirosh-Levy S, Leszkowicz Mazuz M, Mohammed Adam B, Sikiti Garba B, Wesley Nafarnda D, Steinman A. Genetic Characterization of Piroplasms in Donkeys and Horses from Nigeria.. Animals (Basel) 2020 Feb 18;10(2).
    pmc: PMC7070495pubmed: 32085574doi: 10.3390/ani10020324google scholar: lookup
  40. Ikadai H, Nagai A, Xuan X, Igarashi I, Tsugihiko K, Tsuji N, Oyamada T, Suzuki N, Fujisaki K. Seroepidemiologic studies on Babesia caballi and Babesia equi infections in Japan.. J Vet Med Sci 2002 Apr;64(4):325-8.
    pubmed: 12014577doi: 10.1292/jvms.64.325google scholar: lookup
  41. Jaffer O, Abdishakur F, Hakimuddin F, Riya A, Wernery U, Schuster RK. A comparative study of serological tests and PCR for the diagnosis of equine piroplasmosis.. Parasitol Res 2010 Feb;106(3):709-13.
    pubmed: 19894063doi: 10.1007/s00436-009-1669-5google scholar: lookup
  42. Narimani B, Hoghooghi-Rad N, Shayan P, Rahbari S. Molecular and Microscopic Detection of Theileria spp. among Cattle and Buffaloes in West Azarbaijan, Iran.. Arch Razi Inst 2017 Sep;72(3):189-195.
    pubmed: 30341940doi: 10.22092/ari.2017.111605google scholar: lookup
  43. Kamyingkird K, Yangtara S, Desquesnes M, Cao S, Moumouni A, Jittapalapong S, Igarashi I. Seroprevalence of Babesia caballi and Theileria equi in horses and mules from Northern Thailand.. The Journal of Protozoology Research 24, 11–17.
  44. Karatepe B, Karatepe M, Cakmak A, Karaer Z, Ergün G. Investigation of seroprevalence of Theileria equi and Babesia caballi in horses in Nigde province, Turkey.. Trop Anim Health Prod 2009 Jan;41(1):109-13.
    pubmed: 19052908doi: 10.1007/s11250-008-9164-zgoogle scholar: lookup
  45. Kerber CE, Labruna MB, Ferreira F, De Waal DT, Knowles DP, Gennari SM. Prevalence of equine Piroplasmosis and its association with tick infestation in the State of São Paulo, Brazil.. Rev Bras Parasitol Vet 2009 Oct-Dec;18(4):1-8.
    pubmed: 20040201doi: 10.4322/rbpv.01804001google scholar: lookup
  46. Kizilarslan F, Yildirim A, Duzlu O, Inci A, Onder Z, Ciloglu A. Molecular detection and characterization of Theileria equi and Babesia caballi in horses (Equus ferus Caballus) in Turkey.. Journal of Equine Veterinary Science 35, 830–835.
  47. Kouam MK, Kantzoura V, Gajadhar AA, Theis JH, Papadopoulos E, Theodoropoulos G. Seroprevalence of equine piroplasms and host-related factors associated with infection in Greece.. Vet Parasitol 2010 May 11;169(3-4):273-8.
    pubmed: 20138434doi: 10.1016/j.vetpar.2010.01.011google scholar: lookup
  48. Levine ND. Apicomplexa: the piroplasms.. In Soulsby EJL (ed.), Veterinary Protozoology. Ames, IA: Iowa State Universty Press, pp. 291–328.
  49. Machado RZ, Toledo CZ, Teixeira MC, André MR, Freschi CR, Sampaio PH. Molecular and serological detection of Theileria equi and Babesia caballi in donkeys (Equus asinus) in Brazil.. Vet Parasitol 2012 May 25;186(3-4):461-5.
    pubmed: 22186194doi: 10.1016/j.vetpar.2011.11.069google scholar: lookup
  50. Mahmoud MS, El-Ezz NT, Abdel-Shafy S, Nassar SA, El Namaky AH, Khalil WK, Knowles D, Kappmeyer L, Silva MG, Suarez CE. Assessment of Theileria equi and Babesia caballi infections in equine populations in Egypt by molecular, serological and hematological approaches.. Parasit Vectors 2016 May 4;9:260.
    pmc: PMC4857240pubmed: 27146413doi: 10.1186/s13071-016-1539-9google scholar: lookup
  51. Malekifard F, Tavassoli M, Yakhchali M, Darvishzadeh R. Detection of Theileria equi and Babesia caballi using microscopic and molecular methods in horses in suburb of Urmia, Iran.. Vet Res Forum 2014 Spring;5(2):129-33.
    pmc: PMC4279624pubmed: 25568706
  52. Mans BJ, Pienaar R, Latif AA. A review of Theileria diagnostics and epidemiology.. Int J Parasitol Parasites Wildl 2015 Apr;4(1):104-18.
  53. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement.. Syst Rev 2015 Jan 1;4(1):1.
    pmc: PMC4320440pubmed: 25554246doi: 10.1186/2046-4053-4-1google scholar: lookup
  54. Moretti A, Mangili V, Salvatori R, Maresca C, Scoccia E, Torina A, Moretta I, Gabrielli S, Tampieri MP, Pietrobelli M. Prevalence and diagnosis of Babesia and Theileria infections in horses in Italy: a preliminary study.. Vet J 2010 Jun;184(3):346-50.
    pubmed: 19394253doi: 10.1016/j.tvjl.2009.03.021google scholar: lookup
  55. Motloang MY, Thekisoe OM, Alhassan A, Bakheit M, Motheo MP, Masangane FE, Thibedi ML, Inoue N, Igarashi I, Sugimoto C, Mbati PA. Prevalence of Theileria equi and Babesia caballi infections in horses belonging to resource-poor farmers in the north-eastern Free State Province, South Africa.. Onderstepoort J Vet Res 2008 Jun;75(2):141-6.
    pubmed: 18788207doi: 10.4102/ojvr.v75i2.12google scholar: lookup
  56. Mujica FF, Perrone T, Forlano M, Coronado A, Meléndez RD, Barrios N, Alvarez R, Granda F. Serological prevalence of Babesia caballi and Theileria equi in horses of Lara State, Venezuela.. Vet Parasitol 2011 May 31;178(1-2):180-3.
    pubmed: 21273001doi: 10.1016/j.vetpar.2010.12.036google scholar: lookup
  57. Munkhjargal T, Sivakumar T, Battsetseg B, Nyamjargal T, Aboulaila M, Purevtseren B, Bayarsaikhan D, Byambaa B, Terkawi MA, Yokoyama N, Igarashi I. Prevalence and genetic diversity of equine piroplasms in Tov province, Mongolia.. Infect Genet Evol 2013 Jun;16:178-85.
    pubmed: 23416256doi: 10.1016/j.meegid.2013.02.005google scholar: lookup
  58. Nugraha AB, Cahyaningsih U, Amrozi A, Ridwan Y, Agungpriyono S, Taher DM, Guswanto A, Gantuya S, Tayebwa DS, Tuvshintulga B, Sivakumar T, Yokoyama N, Igarashi I. Serological and molecular prevalence of equine piroplasmosis in Western Java, Indonesia.. Vet Parasitol Reg Stud Reports 2018 Dec;14:1-6.
    pubmed: 31014711doi: 10.1016/j.vprsr.2018.07.009google scholar: lookup
  59. Oduori DO, Onyango SC, Kimari JN, MacLeod ET. A field survey for the seroprevalence of Theileria equi and Babesia caballi in donkeys from Nuu Division, Kenya.. Ticks Tick Borne Dis 2015 Jul;6(5):683-8.
    pubmed: 26072000doi: 10.1016/j.ttbdis.2015.05.015google scholar: lookup
  60. OIE. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, ch. 2.5.6 Equine Piroplasmosis.. .
  61. OIE. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, ch. 3.5.8 Equine Piroplasmosis.. .
  62. Onyiche TE, 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 May 16;16(10).
    pmc: PMC6572709pubmed: 31100920doi: 10.3390/ijerph16101736google scholar: lookup
  63. Onyiche TE, Taioe MO, Ogo NI, Sivakumar T, Biu AA, Mbaya AW, Xuan X, Yokoyama N, Thekisoe O. Molecular evidence of Babesia caballi and Theileria equi in equines and ticks in Nigeria: prevalence and risk factors analysis.. Parasitology 2020 Sep;147(11):1238-1248.
    doi: 10.1017/S0031182020000992pmc: PMC10317755pubmed: 32605687google scholar: lookup
  64. Piantedosi D, D'Alessio N, Di Loria A, Di Prisco F, Mariani U, Neola B, Santoro M, Montagnaro S, Capelli G, Veneziano V. Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infections in donkeys from Southern Italy.. Vet J 2014 Dec;202(3):578-82.
    pubmed: 25457263doi: 10.1016/j.tvjl.2014.09.025google scholar: lookup
  65. Posada-Guzmán MF, Dolz G, Romero-Zúñiga JJ, Jiménez-Rocha AE. Detection of Babesia caballi and Theileria equi in Blood from Equines from Four Indigenous Communities in Costa Rica.. Vet Med Int 2015;2015:236278.
    doi: 10.1155/2015/236278pmc: PMC4663365pubmed: 26649225google scholar: lookup
  66. Qablan MA, Oborník M, Petrželková KJ, Sloboda M, Shudiefat MF, Hořín P, Lukeš J, Modrý D. Infections by Babesia caballi and Theileria equi in Jordanian equids: epidemiology and genetic diversity.. Parasitology 2013 Aug;140(9):1096-103.
    pubmed: 23673249doi: 10.1017/s0031182013000486google scholar: lookup
  67. Ramsay JD, Ueti MW, Johnson WC, Scoles GA, Knowles DP, Mealey RH. Lymphocytes and macrophages are infected by Theileria equi, but T cells and B cells are not required to establish infection in vivo.. PLoS One 2013;8(10):e76996.
  68. Rapoport A, Aharonson-Raz K, Berlin D, Tal S, Gottlieb Y, Klement E, Steinman A. Molecular characterization of the Babesia caballi rap-1 gene and epidemiological survey in horses in Israel.. Infect Genet Evol 2014 Apr;23:115-20.
    pubmed: 24524984doi: 10.1016/j.meegid.2014.01.033google scholar: lookup
  69. Ros-García A, M'ghirbi Y, Hurtado A, Bouattour A. Prevalence and genetic diversity of piroplasm species in horses and ticks from Tunisia.. Infect Genet Evol 2013 Jul;17:33-7.
    pubmed: 23542456doi: 10.1016/j.meegid.2013.03.038google scholar: lookup
  70. Rosales R, Rangel-Rivas A, Escalona A, Jordan LS, Gonzatti MI, Aso PM, Perrone T, Silva-Iturriza A, Mijares A. Detection of Theileria equi and Babesia caballi infections in Venezuelan horses using Competitive-Inhibition ELISA and PCR.. Vet Parasitol 2013 Sep 1;196(1-2):37-43.
    pubmed: 23582233doi: 10.1016/j.vetpar.2013.02.004google scholar: lookup
  71. Rothschild CM. Equine piroplasmosis.. Journal of Equine Veterinary Science 33, 497–508.
  72. Rüegg SR, Torgerson P, Deplazes P, Mathis A. Age-dependent dynamics of Theileria equi and Babesia caballi infections in southwest Mongolia based on IFAT and/or PCR prevalence data from domestic horses and ticks.. Parasitology 2007 Jul;134(Pt 7):939-47.
    pubmed: 17306055doi: 10.1017/s0031182007002405google scholar: lookup
  73. Salim BO, Hassan SM, Bakheit MA, Alhassan A, Igarashi I, Karanis P, Abdelrahman MB. Diagnosis of Babesia caballi and Theileria equi infections in horses in Sudan using ELISA and PCR.. Parasitol Res 2008 Oct;103(5):1145-50.
    pubmed: 18618143doi: 10.1007/s00436-008-1108-zgoogle scholar: lookup
  74. Salim B, Bakheit MA, Kamau J, Sugimoto C. Current status of equine piroplasmosis in the Sudan.. Infect Genet Evol 2013 Jun;16:191-9.
    pubmed: 23485745doi: 10.1016/j.meegid.2013.02.008google scholar: lookup
  75. Sanusi M, Ahmed IA, Tahir I, Mai HM, Kalla DJU, Shuaibu I. Survey of equine piroplasmosis in the Savanna areas, Bauchi state, North-eastern Nigeria.. Ippologia 25, 3–8.
  76. Scoles GA, Ueti MW. Vector ecology of equine piroplasmosis.. Annu Rev Entomol 2015 Jan 7;60:561-80.
  77. Seo MG, Yun SH, Choi SK, Cho GJ, Park YS, Kwon OD, Cho KH, Kim TH, Jeong KS, Park SJ, Kwon YS, Kwak D. Seroprevalence of equine piroplasms in the Republic of Korea.. Vet Parasitol 2011 Jun 30;179(1-3):224-6.
    pubmed: 21429670doi: 10.1016/j.vetpar.2011.02.020google scholar: lookup
  78. Sevinc F, Maden M, Kumas C, Sevinc M, Ekici OD. A comparative study on the prevalence of Theileria equi and Babesia caballi infections in horse sub-populations in Turkey.. Vet Parasitol 2008 Oct 1;156(3-4):173-7.
    pubmed: 18672330doi: 10.1016/j.vetpar.2008.06.006google scholar: lookup
  79. Sigg L, Gerber V, Gottstein B, Doherr MG, Frey CF. Seroprevalence of Babesia caballi and Theileria equi in the Swiss horse population.. Parasitol Int 2010 Sep;59(3):313-7.
    pubmed: 20178863doi: 10.1016/j.parint.2010.02.005google scholar: lookup
  80. Sumbria D, Das Singla L, Sharma A. Theileria equi and Babesia caballi infection of equids in Punjab, India: a serological and molecular survey.. Trop Anim Health Prod 2016 Jan;48(1):45-52.
    pubmed: 26387094doi: 10.1007/s11250-015-0917-1google scholar: lookup
  81. Turaki UA, Kumsha HA, Biu AA, Bokko PB. Prevalence of piroplasmosis amongst local horses in Northeastern Nigeria.. Journal of Agricultural and Veterinary Science 4, 27.
  82. Uilenberg G. Babesia--a historical overview.. Vet Parasitol 2006 May 31;138(1-2):3-10.
    pubmed: 16513280doi: 10.1016/j.vetpar.2006.01.035google scholar: lookup
  83. Vieira TS, Vieira RF, Finger MA, Nascimento DA, Sicupira PM, Dutra LH, Deconto I, Barros-Filho IR, Dornbusch PT, Biondo AW, Vidotto O. Seroepidemiological survey of Theileria equi and Babesia caballi in horses from a rural and from urban areas of Paraná State, southern Brazil.. Ticks Tick Borne Dis 2013 Dec;4(6):537-41.
    pubmed: 24209493doi: 10.1016/j.ttbdis.2013.07.005google scholar: lookup
  84. Vieira MIB, Costa MM, de Oliveira MT, Gonçalves LR, André MR, Machado RZ. Serological detection and molecular characterization of piroplasmids in equids in Brazil.. Acta Trop 2018 Mar;179:81-87.
  85. Wang M, Guo W, Igarashi I, Xuan X, Wang X, Xiang W, Jia H. Epidemiological investigation of equine piroplasmosis in China by enzyme-linked immunosorbent assays.. J Vet Med Sci 2014 Apr;76(4):549-52.
    pmc: PMC4064140pubmed: 24292247doi: 10.1292/jvms.13-0477google scholar: lookup
  86. Wise LN, Kappmeyer LS, Mealey RH, Knowles DP. Review of equine piroplasmosis.. J Vet Intern Med 2013 Nov-Dec;27(6):1334-46.
    pubmed: 24033559doi: 10.1111/jvim.12168google scholar: lookup
  87. Xu Y, Zhang S, Huang X, Bayin C, Xuan X, Igarashi I, Fujisaki K, Kabeya H, Maruyama S, Mikami T. Seroepidemiologic studies on Babesia equi and Babesia caballi infections in horses in Jilin province of China.. J Vet Med Sci 2003 Sep;65(9):1015-7.
    pubmed: 14532697doi: 10.1292/jvms.65.1015google scholar: lookup
  88. Ybañez AP, Ybañez RHD, Talle MG, Arreglo RMT, Geens MJC, Villas JGI 3rd, Villar SR, Laruga CL, Cao S, Moumouni FPA, Liu M, Igarashi I, Xuan X. Serological and molecular detection of Theileria equi and Babesia caballi in Philippine horses.. Ticks Tick Borne Dis 2018 Jul;9(5):1125-1128.
    pubmed: 29693550doi: 10.1016/j.ttbdis.2018.04.010google scholar: lookup

Citations

This article has been cited 2 times.
  1. Tirosh-Levy S, Mazuz ML, Savitsky I, Pinkas D, Gottlieb Y, Steinman A. Serological and Molecular Prevalence of Babesia caballi in Apparently Healthy Horses in Israel.. Pathogens 2021 Apr 8;10(4).
    doi: 10.3390/pathogens10040445pubmed: 33917822google scholar: lookup
  2. Dirks E, de Heus P, Joachim A, Cavalleri JV, Schwendenwein I, Melchert M, Fuehrer HP. First Case of Autochthonous Equine Theileriosis in Austria.. Pathogens 2021 Mar 4;10(3).
    doi: 10.3390/pathogens10030298pubmed: 33806575google scholar: lookup