Analyze Diet
Pathogens (Basel, Switzerland)2021; 10(4); doi: 10.3390/pathogens10040445

Serological and Molecular Prevalence of Babesia caballi in Apparently Healthy Horses in Israel.

Abstract: Babesia caballi is a tick-borne hemoparasite of equines and one of the causative agents of equine piroplasmosis, which poses a great concern for the equine industry regarding animal welfare and international horse movement. The parasite is endemic in Israel; however, its seroprevalence in the area was never evaluated due to antigenic heterogenicity in the gene used in the commercially available kit. Blood samples were collected from 257 horses at 19 farms throughout the country and screened for the presence of anti-B. caballi antibodies via an indirect immunofluorescent antibody test (IFAT) and for the presence of parasite DNA by nested PCR. The seroprevalence of B. caballi was 69.6% and its molecular prevalence was 9.7%. The geographical area, horse's sex, breed, housing, exposure to ticks, and specifically to Hyalomma marginatum, and co-infection with Theileria equi were found to be significantly associated with serologic exposure in univariable analysis, while the geographical area and horses' sex remained significant in the multivariable analysis. The results of this study demonstrate a high level of exposure to B. caballi and identify important risk factors for infection. The difference between the serological and molecular prevalence, probably related to parasite clearance, is also highlighted.
Publication Date: 2021-04-08 PubMed ID: 33917822PubMed Central: PMC8068206DOI: 10.3390/pathogens10040445Google 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

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 study investigates the prevalence of the parasite Babesia caballi in horses in Israel using both serological (antibody presence) and molecular (DNA) testing. The research found a high rate of exposure and identified key risk factors for the parasite’s presence.

Introduction to Babesia caballi

  • Babesia caballi is a parasite that is transmitted by ticks and lives in the blood of horses
  • It is one of the agents responsible for equine piroplasmosis, a disease that seriously affects the health of horses and the horse industry
  • The disease poses major challenges for horse welfare and international transportation of horses
  • While it is already known that the parasite is widespread in Israel, the specific prevalence has not been previously researched because of antigenic heterogeneity, which refers to variations in the genes used in commercially available testing kits

Methodology of the Study

  • Researchers collected blood samples from 257 horses from 19 farms around Israel
  • All samples were screened for both the presence of anti-Babesia caballi antibodies (using an Indirect Immunofluorescent Antibody Test (IFAT)) and for the incidence of the parasite’s DNA via a nested PCR test

Results of the Research

  • Out of all horses, 69.6% were found to have antibodies, suggesting previous exposure to the parasite
  • The molecular prevalence, indicating a current infection, was observed to be significantly lower at 9.7%
    • Factor Analysis

      • The study sought to identify variables that had a significant impact on a horse’s exposure to Babesia caballi
      • The following factors were found to be significant: geographical area, horse’s sex, breed, type of housing, exposure to ticks (particularly to the specific ticks that spread Babesia caballi), and co-infection with other organisms
      • However, when multiple variables were considered at once, only the geographical area where the horse lived and the horse’s sex remained significant predictors of infection

      Conclusion and Implications

      • The study revealed a high level of previous exposure to Babesia caballi among the horses tested in Israel
      • The discrepancy between the serological and molecular prevalence may be due to the horses’ immune systems clearing the parasite over time
      • Identifying the principal risk factors of infection helps us understand the epidemiology of the disease and could assist in creating intervention measures to control its spread

Cite This Article

APA
Tirosh-Levy S, Mazuz ML, Savitsky I, Pinkas D, Gottlieb Y, Steinman A. (2021). Serological and Molecular Prevalence of Babesia caballi in Apparently Healthy Horses in Israel. Pathogens, 10(4). https://doi.org/10.3390/pathogens10040445

Publication

ISSN: 2076-0817
NlmUniqueID: 101596317
Country: Switzerland
Language: English
Volume: 10
Issue: 4

Researcher Affiliations

Tirosh-Levy, Sharon
  • Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
  • Division of Parasitology, Kimron Veterinary Institute, Beit Dagan 50250, Israel.
Mazuz, Monica L
  • Division of Parasitology, Kimron Veterinary Institute, Beit Dagan 50250, Israel.
Savitsky, Igor
  • Division of Parasitology, Kimron Veterinary Institute, Beit Dagan 50250, Israel.
Pinkas, Dana
  • Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
Gottlieb, Yuval
  • Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.
Steinman, Amir
  • Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot 7610001, Israel.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 36 references
  1. Rothschild CM. Equine piroplasmosis.. J. Equine Vet. Sci. 2013;23:115–120.
  2. Tirosh-Levy S, Gottlieb Y, Fry LM, Knowles DP, 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
  3. Wise LN, Kappmeyer LS, Mealey RH, Knowles DP. Review of equine piroplasmosis.. J. Vet. Int. Med. 2013;27:1334–1346.
    doi: 10.1111/jvim.12168pubmed: 24033559google scholar: lookup
  4. Friedhoff KT, Tenter AM, Muller I. Haemoparasites of equines: Impact on international trade of horses.. Rev. Sci. Tech. 1990;9:1187–1194.
    pubmed: 2132711
  5. Scoles GA, Ueti MW. Vector ecology of equine piroplasmosis.. Ann. Rev. Entomol. 2015;60:561–580.
  6. De Waal D. Equine piroplasmosis: A review.. Brit. Vet. J. 1992;148:6–14.
    doi: 10.1016/0007-1935(92)90061-5pubmed: 1551016google scholar: lookup
  7. Kappmeyer LS, Perryman LE, Hines SA, Baszler TV, Katz JB, Hennager SG, Knowles DP. Detection of equine antibodies to babesia caballi by recombinant B. caballi rhoptry-associated protein 1 in a competitive-inhibition enzyme-linked immunosorbent assay.. J. Clin. Microbiol. 1999;37:2285–2290.
  8. 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;169:279–288.
    doi: 10.1016/j.vetpar.2010.01.009pubmed: 20138703google scholar: lookup
  9. 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;9:260.
    doi: 10.1186/s13071-016-1539-9pmc: PMC4857240pubmed: 27146413google scholar: lookup
  10. 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;23:115–120.
    doi: 10.1016/j.meegid.2014.01.033pubmed: 24524984google scholar: lookup
  11. Aharonson-Raz K, Rapoport A, Hawari IM, Lensky IM, Berlin D, Zivotofsky D, Klement E, Steinman A. Novel description of force of infection and risk factors associated with Theileria equi in horses in Israel and in The Palestinian Authority.. Ticks Tick-Borne Dis. 2014;5:366–372.
    doi: 10.1016/j.ttbdis.2014.01.002pubmed: 24703834google scholar: lookup
  12. Ketter-Ratzon D, Tirosh-Levy S, Nachum-Biala Y, Saar T, Qura’n L, Zivotofsky D, Abdeen Z, Baneth G, Steinman A. Characterization of Theileria equi genotypes in horses in Israel, the Palestinian Authority and Jordan.. Ticks Tick-Borne Dis. 2017;8:499–505.
    doi: 10.1016/j.ttbdis.2017.02.010pubmed: 28286144google scholar: lookup
  13. Shkap V, Cohen I, Leibovitz B, Savitsky, Pipano E, Avni G, Shofer S, Giger U, Kappmeyer L, Knowles D. Seroprevalence of Babesia equi among horses in Israel using competitive inhibition ELISA and IFA assays.. Vet. Parasitol. 1998;76:251–259.
    doi: 10.1016/S0304-4017(97)00228-8pubmed: 9650862google scholar: lookup
  14. Steinman A, Zimmerman T, Klement E, Lensky IM, Berlin D, Gottlieb Y, Baneth G. Demographic and environmental risk factors for infection by Theileria equi in 590 horses in Israel.. Vet. Parasitol. 2012;187:558–562.
    doi: 10.1016/j.vetpar.2012.01.018pubmed: 22293151google scholar: lookup
  15. Tirosh-Levy S, Gottlieb Y, Arieli O, Mazuz ML, King R, Horowitz I, Steinman A. Genetic characteristics of Theileria equi in zebras, wild and domestic donkeys in Israel and the Palestinian Authority.. Ticks Tick Borne Dis. 2020;11:101286.
    doi: 10.1016/j.ttbdis.2019.101286pubmed: 31537490google scholar: lookup
  16. Tirosh-Levy S, Steinman A, Levy H, Katz Y, Shtilman M, Gottlieb Y. Parasite load and genotype are associated with clinical outcome of piroplasm-infected equines in Israel.. Parasit Vectors 2020;13:267.
    doi: 10.1186/s13071-020-04133-ypmc: PMC7240905pubmed: 32434550google scholar: lookup
  17. Tirosh-Levy S, Gottlieb Y, Mazuz ML, Savitsky I, Steinman A. Infection dynamics of Theileria equi in carrier horses is associated with management and tick exposure.. Ticks Tick Borne Dis. 2020;11:101508.
    doi: 10.1016/j.ttbdis.2020.101508pubmed: 32993928google scholar: lookup
  18. 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;59:72–78.
  19. Qablan MA, Obornik M, Petrzelkova KJ, Sloboda M, Shudiefat MF, Horin P, Lukes J, Modry D. Infections by Babesia caballi and Theileria equi in Jordanian equids: Epidemiology and genetic diversity.. Parasitology 2013;140:1096–1103.
    doi: 10.1017/S0031182013000486pubmed: 23673249google scholar: lookup
  20. Onyiche TE, Taioe MO, Molefe NI, Biu AA, Luka J, Omeh IJ, Yokoyama N, Thekisoe O. Equine piroplasmosis: An insight into global exposure of equids from 1990 to 2019 by systematic review and meta-analysis.. Parasitology 2020;147:1411–1424.
    doi: 10.1017/S0031182020001407pmc: PMC10317785pubmed: 32741382google scholar: lookup
  21. Ruegg SR, Heinzmann D, Barbour AD, Torgerson PR. Estimation of the transmission dynamics of Theileria equi and Babesia caballi in horses.. Parasitology 2008;135:555–565.
    doi: 10.1017/S0031182008004204pubmed: 18302805google scholar: lookup
  22. Ruegg 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;134:939–947.
    doi: 10.1017/S0031182007002405pubmed: 17306055google scholar: lookup
  23. 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 Sao Paulo, Brazil.. Rev. Bras. Parasitol. Vet. 2009;18:1–8.
    doi: 10.4322/rbpv.01804001pubmed: 20040201google scholar: lookup
  24. Wang J, Liu J, Yang J, Wang X, Li Z, Jianlin X, Li X, Xiang Q, Li Y, Liu Z. The first molecular detection and genetic diversity of Babesia caballi and Theileria equi in horses of Gansu province, China.. Ticks Tick Borne Dis. 2019;10:528–532.
    doi: 10.1016/j.ttbdis.2019.01.003pubmed: 30670354google scholar: lookup
  25. Xuan X, Nagai A, Battsetseg B, Fukumoto S, Makala LH, Inoue N, Igarashi I, Mikami T, Fujisaki K. Diagnosis of equine piroplasmosis in Brazil by serodiagnostic methods with recombinant antigens.. J. Vet. Med. Sci. 2001;63:1159–1160.
    doi: 10.1292/jvms.63.1159pubmed: 11714038google scholar: lookup
  26. Nugraha AB, Cahyaningsih U, Amrozi A, Ridwan Y, Agungpriyono S, Taher DM, Guswanto A, Gantuya S, Tayebwa DS, Tuvshintulga B. Serological and molecular prevalence of equine piroplasmosis in Western Java, Indonesia.. Vet. Parasitol. Reg. Stud. Rep. 2018;14:1–6.
    doi: 10.1016/j.vprsr.2018.07.009pubmed: 31014711google scholar: lookup
  27. 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;184:346–350.
    doi: 10.1016/j.tvjl.2009.03.021pubmed: 19394253google scholar: lookup
  28. 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;64:325–328.
    doi: 10.1292/jvms.64.325pubmed: 12014577google scholar: lookup
  29. Al-Obaidi Q, Arshad M, Al-Sultan I, Azlinda A, Mohd-Azam K. Comparison between microscopic examination and competitive ELISA for diagnosis of equine piroplasmosis in Kelantan, Malaysia.. Malays. J. Vet. Res. 2016;7:23–29.
  30. Munkhjargal T, Sivakumar T, Battsetseg B, Nyamjargal T, Aboulaila M, Purevtseren B, Bayarsaikhan D, Byambaa B, Terkawi MA, Yokoyama N. Prevalence and genetic diversity of equine piroplasms in Tov province, Mongolia.. Infect. Genet. Evol. 2013;16:178–185.
    doi: 10.1016/j.meegid.2013.02.005pubmed: 23416256google scholar: lookup
  31. 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;144:167–171.
    doi: 10.1016/j.vetpar.2006.09.015pubmed: 17118557google scholar: lookup
  32. Acici M, Umur S, Guvenc T, Arslan HH, Kurt M. Seroprevalence of equine babesiosis in the Black Sea region of Turkey.. Parasitol. Int. 2008;57:198–200.
    doi: 10.1016/j.parint.2007.12.009pubmed: 18234550google scholar: lookup
  33. Mujica FF, Perrone T, Forlano M, Coronado A, Melendez RD, Barrios N, Alvarez R, Granda F. Serological prevalence of Babesia caballi and Theileria equi in horses of Lara State, Venezuela.. Vet. Parasitol. 2011;178:180–183.
    doi: 10.1016/j.vetpar.2010.12.036pubmed: 21273001google scholar: lookup
  34. 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;196:37–43.
    doi: 10.1016/j.vetpar.2013.02.004pubmed: 23582233google scholar: lookup
  35. Tirosh-Levy S, Gottlieb Y, Apanaskevich DA, Mumcuoglu KY, Steinman A. Species distribution and seasonal dynamics of equine tick infestation in two Mediterranean climate niches in Israel.. Parasit Vectors 2018;11:546.
    doi: 10.1186/s13071-018-3093-0pmc: PMC6192331pubmed: 30326955google scholar: lookup
  36. Tirosh-Levy S, Gottlieb Y, Mimoun L, Mazuz ML, Steinman A. Transplacental Transmission of Theileria equi Is Not a Common Cause of Abortions and Infection of Foals in Israel.. Animals 2020;10:341.
    doi: 10.3390/ani10020341pmc: PMC7070885pubmed: 32098113google scholar: lookup