Host and environmental factors as determinants of equine piroplasmosis seroprevalence in Central Spain
Abstract
Aim of study: To estimate equine piroplasmosis seroprevalence, identify associated risk factors and assess infection recentness.
Area of study: Community of Madrid (Central Spain)
Material and methods: Sera from 139 horses and 40 donkeys were examined by cELISA to evaluate Babesia caballi and Theileria equi seroprevalences and examine potential risk factors. They included species, gender, age, breed, colour coat, dedication, external parasite treatments, access to pasture, contact with other species, new introduction, tick infestation, farm altitude, land cover, soil type and climatic zone. A bivariate analysis was performed and significant variables were included in a logistic regression model to examine their independent contribution. In positive samples ELISA inhibition percentiles (EIPs) were used to assess whether infections were old or recent.
Main results: True seroprevalence (95% CI), adjusted for test sensitivity and specificity was 19% (13-27) for T. equi and 1% (0-3) for B. caballi. In the bivariate analysis, T. equi seroprevalence varied significantly according to horse and farm-level explanatory variables; high seroprevalence groups generally had high EIPs suggesting recent infection. The multivariable analysis revealed that T. equi seroprevalence increased with age, it was higher in police horses compared to sporting, recreational and breeding animals and in those living in lower altitude where planosol soil type was predominant.
Research highlights: T. equi seroprevalence in the area was significantly higher than B. caballi seroprevalence and depends on animal management and environmental factors that affect vector abundance and diversity. Identified risk factors must be considered to improve tick and tick-borne disease control and prevention.Downloads
References
Abutarbush SM, Alqawasmeh DM, Mukbel, RM, Al-Majali AM, 2012. Equine babesiosis: seroprevalence, risk factors and comparison of different diagnostic methods in Jordan. Transbound Emerg Dis 59: 72-78. https://doi.org/10.1111/j.1865-1682.2011.01244.x
Aharonson-Raz K, Rapoport A, Hawari IM, Lensky IM, Berlin D, Zivotofsky D, Klement E, Steinman A, 2014. 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 5: 366-372. https://doi.org/10.1016/j.ttbdis.2014.01.002
Barandika JF, Olmeda SA, Casado-Nistal MA, Hurtado A, Juste RA, Valcárcel F, Anda P, García-Pérez A, 2011. Differences in questing tick species distribution between atlantic and continental climate regions in Spain. J Med Entomol 48: 13-19. https://doi.org/10.1603/ME10079
Bartolomé Del Pino LE, Nardini R, Veneziano V, Iacoponi F, Cersini A, Autorino GL, Buono F, Scicluna MT, 2016. Babesia caballi and Theileria equi infections in horses in Central-Southern Italy: Sero-molecular survey and associated risk factors. Ticks Tick Borne Dis 7: 462-469. https://doi.org/10.1016/j.ttbdis.2016.01.011
Camino E, de la Cruz M.L, Dominguez L, Carvajal KA, Fores P, de Juan L, Cruz-Lopez, F, 2018. Epidemiological situation of the exposure to agents causing equine piroplasmosis in Spanish purebred Horses in Spain: seroprevalence and associated risk factors. J Equine Vet Sci 67: 81-86. https://doi.org/10.1016/j.jevs.2018.03.012
Camino E, Pozo P, Dorrego A, Carvajal KA, Buendia A, Gonzalez S, de Juan L, Dominguez L, Cruz-Lopez F, 2020. Importance of equine piroplasmosis antibody presence in Spanish horses prior to export. Ticks Tick Borne Dis 11: 101329. https://doi.org/10.1016/j.ttbdis.2019.101329
De Waal DT, 1992. Equine piroplasmosis: A review. Br Vet J 148: 6-14. https://doi.org/10.1016/0007-1935(92)90061-5
Devleesschauwer B, Torgerson P, Charlier J, Levecke B, Praet N, Dorny P, Berkvens D, Speybroeck N, 2013. Prevalence: Tools for prevalence assessment studies. R package version 0.2.0. http://cran.r-project.org/package=prevalence
FAO, 2015. World Reference Base for Soil Resources 2014, Update 2015. World Soil Resources Reports 106, FAO, Rome. ISBN 978-92-5-108369-7
García-Bocanegra I, Arenas-Montes A, Hernández E, Adaszek Ł, Carbonero A, Almería S, Jaén-Téllez JA, Gutiérrez-Palomino P, Arenas A, 2013. Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infection in equids. Vet J 195: 172-178. https://doi.org/10.1016/j.tvjl.2012.06.012
Gizachew A, Schuster RK, Joseph S, Wernery R, Georgy NA, Elizabeth SK, Asfaw Y, Regassa F, Wernery U, 2013. Piroplasmosis in donkeys: a hematological and serological study in Central Ethiopia. J Equine Vet Sci 33: 18-21. https://doi.org/10.1016/j.jevs.2012.04.003
Kouam MK, Kantzoura V, Masuoka PM, Gajadhar A, Theodoropoulos G, 2010. Genetic diversity of equine piroplasms in Greece with a note on speciation within Theileria genotypes (T. equi and T. equi-like). Infect Genet Evol 10: 963-968. https://doi.org/10.1016/j.meegid.2010.06.008
Machado RZ, Toledo CZP, Teixeira MC, André MR, Freschi CR, Sampaio PH, 2012. Molecular and serological detection of Theileria equi and Babesia caballi in donkeys (Equus asinus) in Brazil Vet Parasitol 186: 461-465. https://doi.org/10.1016/j.vetpar.2011.11.069
MAPA, 2003. El libro blanco de la agricultura y el desarrollo rural. Tomo III. Ministry of Agriculture, Spain. https://www.mapa.gob.es/eu/ministerio/servicios/informacion/cap04_12_t3_tcm35-102688.pdf
MAPA, 2018. Equine census. Ministry of Agriculture, Spain. https://www.mapa.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/indicadoreseconomicossectorequino2018comentarios_tcm30-420793.pdf
Montes Cortés MG, Fernández-García JL, Habela Martínez-Estéllez MA, 2017. Seroprevalence of Theileria equi and Babesia caballi in horses in Spain. Parasite 24: 14. https://doi.org/10.1051/parasite/2017015
Oduori DO, Onyango SC, Kimari JN, MacLeod ET, 2015. A field survey for the seroprevalence of Theileria equi and Babesia caballi in donkeys from Nuu Division, Kenya. Ticks Tick Borne Dis 6: 683-688. https://doi.org/10.1016/j.ttbdis.2015.05.015
OIE, 2011. Terrestrial Animal Health Code, 20th edition,
Olmeda AS, Bösse R, Ndjeng P, Sanmartín H, Meana A, 2000. Babesiosis equina: serodetección por inmunofluorescencia en animales sintomáticos y clínicamente sanos V Simposium Ibérico sobre Ixodoidea y enfermedades Transmitidas, Madrid (Spain), Sept 27-29. pp: 79-80.
Pfäffle M, Littwin N, Muders S V, Petney TN, 2013. The ecology of tick-borne diseases. Int J Parasitol 43: 1059-1077. https://doi.org/10.1016/j.ijpara.2013.06.009
Piantedosi D, D'Alessio N, Di Lori, A, Di Prisco F, Mariani U, Neola B, Santoro M, Montagnaro S, Capelli G, Veneziano V, 2014. Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infections in donkeys from Southern Italy. Vet J 202: 578-582. https://doi.org/10.1016/j.tvjl.2014.09.025
Ribeiro AJ, Cardoso L, Maia JM, Coutinho T, Cotovio M, 2013. Prevalence of Theileria equi, Babesia caballi, and Anaplasma phagocytophilum in horses from the north of Portugal. Parasitol Res 112: 2611-2617. https://doi.org/10.1007/s00436-013-3429-9
Santos TM dos, Roier ECR, Santos HA, Pires MS, Vilela JAR, Moraes LM de B, Almeida FQ de, Baldani CD, Machado RZ, Massard CL, 2011. Factors associated to Theileria equi in equids of two microregions from Rio de Janeiro, Brazil. Rev Bras Parasitol Vet 20: 235-241. https://doi.org/10.1590/S1984-29612011000300011
Schwarz A, Maier WA, Kistemann T, Kampen H, 2009. Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information Systems. Int J Hyg Environ Health 212: 87-96. https://doi.org/10.1016/j.ijheh.2007.12.001
Scoles G, Ueti MW, 2015. Vector ecology of equine piroplasmosis. Annu Rev Entomol 60: 561-580. https://doi.org/10.1146/annurev-ento-010814-021110
Shchuchinova LD, Kozlova IV, Zlobin VI, 2015. Influence of altitude on tick-borne encephalitis infection risk in the natural foci of the Altai Republic, Southern Siberia. Ticks Tick Borne Dis 6: 322-329. https://doi.org/10.1016/j.ttbdis.2015.02.005
Steinman A, Zimmerman T, Klement E, Lensky IM, Berlin D, Gottlieb Y, Baneth G, 2012. Demographic and environmental risk factors for infection by Theileria equi in 590 horses in Israel. Vet Parasitol 187: 558-562. https://doi.org/10.1016/j.vetpar.2012.01.018
Sumbria D, Singla LD, Sharma A, Bal MS, Randhawa CS, 2017. Molecular survey in relation to risk factors and haemato-biochemical alteration in Theileria equi infection of equines in Punjab Province India. Vet Parasitol Reg Stud Rep 8: 43-50. https://doi.org/10.1016/j.vprsr.2017.01.009
Thrusfield M, 2007. Veterinary Epidemiology, 3rd Ed. Wiley-Blackwell, USA, 624 pp.
Vanwambeke SO, Sumilo D, Bormane A, Lambin EF, Randolph SE, 2010. Landscape predictors of tick-borne encephalitis in Latvia: land cover, land use, and land ownership Vector Borne Zoonotic Dis 10: 497-506. https://doi.org/10.1089/vbz.2009.0116
Wise LN, Kappmeyer LS, Mealey RH, Knowles DP, 2013. Review of equine piroplasmosis. J Vet Intern Med 27 (6): 1334-1346. https://doi.org/10.1111/jvim.12168
Zanet S, Bassano M, Trisciuoglio A, Taricco I, Ferroglio E, 2017. Horses infected by piroplasms different from Babesia caballi and Theileria equi: species identification and risk factors analysis in Italy. Vet Parasitol 236: 38-41. https://doi.org/10.1016/j.vetpar.2017.01.003
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
