Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-29T12:58:11.619Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  03 August 2020

ThankGod E. Onyiche Open the ORCID record for ThankGod E. Onyiche [Opens in a new window] ,
Moeti O. Taioe ,
Nthatisi I. Molefe ,
Abdullahi A. Biu ,
Joshua Luka ,
Isaac J. Omeh ,
Naoaki Yokoyama  and
Oriel Thekisoe
ThankGod E. Onyiche*
Affiliation:
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
Moeti O. Taioe
Affiliation:
National Zoological Gardens of South Africa, South African National Biodiversity Institute, PO Box 754, Pretoria0001, South Africa
Nthatisi I. Molefe
Affiliation:
Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom2520, South Africa
Abdullahi A. Biu
Affiliation:
Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria
Joshua Luka
Affiliation:
Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria
Isaac J. Omeh
Affiliation:
Department of Veterinary Physiology and Biochemistry, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria
Naoaki Yokoyama
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido080-8555, Japan
Oriel Thekisoe
Affiliation:
Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom2520, South Africa
*
Author for correspondence: ThankGod E. Onyiche, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Apicomplexadonkeysequine piroplasmosishorsesmeta-analysis
Type
Review Article
Information
Parasitology , Volume 147 , Issue 13 , November 2020 , pp. 1411 - 1424
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abedi, V, Razmi, G, Seifi, H and Naghibi, A (2014) Molecular and serological detection of Theileria equi and Babesia caballi infection in horses and ixodid ticks in Iran. Ticks and Tick-Borne Diseases 5, 239–244.CrossRefGoogle ScholarPubMed
Abedi, V, Razmi, G, Seifi, H and Naghibi, A (2015) Molecular detection of equine piroplasms in donkeys (Equus asinus) in North Khorasan province, Iran. Iranian Journal of Veterinary Research 16, 202.Google ScholarPubMed
Abutarbush, SM, Alqawasmeh, DM, Mukbel, RM and Al-Majali, AM (2012) Equine babesiosis: seroprevalence, risk factors and comparison of different diagnostic methods in Jordan. Transboundary and Emerging Disease 59, 72–78.Google ScholarPubMed
Acici, M, Umur, S, Guvenc, T, Arslan, HH and Kurt, M (2008) Seroprevalence of equine babesiosis in the Black Sea region of Turkey. Parasitology International 57, 198–200.CrossRefGoogle ScholarPubMed
Akkan, HA, Karaca, M, Tutuncu, M, Deger, S, Keles, I and Agaoglu, Z (2003) Serologic and microscopic studies on babesiosis in horses in the eastern border of Turkey. Journal of Equine Veterinary Science 5, 181–183.CrossRefGoogle Scholar
Al-Obaidi, QT, Arshad, MM, Al-Sultan, II, Azlinda, AB and Mohd-Azam, KGK (2016) Comparison between microscopic examination and competitive ELISA for diagnosis of equine piroplasmosis in Kelantan. Malaysia. Malaysia Journal of Veterinary Research 7, 23–29.Google Scholar
Alanazi, AD, Alyousif, MS and Hassieb, MM (2012) Seroprevalence study on Theileria equi and Babesia caballi antibodies in horses from central province of Saudi Arabia. Journal of Parasitology 98, 1015–1017.CrossRefGoogle Scholar
Asgarali, Z, Coombs, DK, Mohammed, F, Campbell, MD and Caesar, E (2007) A serological study of Babesia caballi and Theileria equi in thoroughbreds in Trinidad. Veterinary Parasitology 144, 167–171.CrossRefGoogle ScholarPubMed
Avarzed, A, De Waal, DT, Igarashi, I, Saito, A, Oyamada, T, Toyoda, Y and Suzuki, N (1997) Prevalence of equine piroplasmosis in Central Mongolia. Onderstepoort Journal of Veterinary Research 64, 141–145.Google ScholarPubMed
Ayala-Valdovinos, MA, Lemus-Flores, C, Galindo-García, J, Sánchez-Chipres, D, Duifhuis-Rivera, T, Anguiano-Estrella, R, Bañuelos-Pineda, J and Rodríguez-Carpena, JG (2014) Nested PCR detection of Theileria equi infection and frequency in horses imported into Mexico. Journal of Animal Veterinary Advances 13, 859–863.Google Scholar
Balkaya, I, Utuk, AE and Piskin, FC (2010) Prevalance of Theileria equi and Babesia caballi in donkeys from Eastern Turkey in winter season. Pakistan Veterinary Journal 30, 245–246.Google Scholar
Bartolome, LED, Roberto, N, Vincenzo, V, Francesca, I, Antonella, C, Luca, A and Teresa, SM (2016) Babesia caballi and Theileria equi infections in horses in Central-Southern Italy: Sero-molecular survey and associated risk factors. Ticks and Tick-Borne Diseases 7, 462–469.CrossRefGoogle Scholar
Bhoora, R, Quan, M, Zweygarth, E, Guthrie, AJ, Prinsloo, SA and Collins, NE (2010) Sequence heterogeneity in the gene encoding the rhoptry-associated protein-1 (RAP-1) of Babesia caballi isolates from South Africa. Veterinary Parasitology 169, 279–288.CrossRefGoogle ScholarPubMed
Boldbaatar, D, Xuan, X, Battsetseg, B, Igarashi, I, Battur, B, Batsukh, Z and Fujisaki, K (2005) Epidemiological study of equine piroplasmosis in Mongolia. Veterinary Parasitology 127, 29–32.Google ScholarPubMed
Böse, R, Jorgensen, WK, Dalgliesh, RJ, Friedhoff, KT and De Vos, AJ (1995) Current state and future trends in the diagnosis of babesiosis. Veterinary Parasitology 57, 61–74.CrossRefGoogle Scholar
Butler, CM, van Oldruitenborgh-Oosterbaan, MMS, Stout, TA, van der Kolk, JH, Van den Wollenberg, L, Nielen, M and Houwers, DJ (2012) 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. The Veterinary Journal 193, 381–385.CrossRefGoogle ScholarPubMed
Camacho, AT, Guitian, FJ, Pallas, E, Gestal, JJ, Olmeda, AS, Habela, MA and Spielman, A (2005) Theileria (Babesia) equi and Babesia caballi infections in horses in Galicia, Spain. Tropical Animal Health Production 37, 293–302.CrossRefGoogle ScholarPubMed
Camino, E, de la Cruz, ML, Dominguez, L, Carvajal, KA, Fores, P, de Juan, L and 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. Journal of Equine Veterinary Science 67, 81–86.CrossRefGoogle Scholar
Cantú-Martínez, MA, Segura-Correa, JC, Silva-Páez, ML, Avalos-Ramírez, R and Wagner, GG (2012) Prevalence of antibodies to Theileria equi and Babesia caballi in horses from northeastern Mexico. Journal of Parasitology 98, 869–871.CrossRefGoogle ScholarPubMed
Chahan, B, Zhang, S, Seo J, Y, Nakamura, C, Zhang, G, Bannai, H and Kabeya, H (2006) Seroepidemiological evidence for the possible presence of Babesia (Theileria) equi and Babesia caballi infections in donkeys in western Xinjiang, China. Journal of Veterinary Medical Science 68, 753–755.CrossRefGoogle ScholarPubMed
Cortés, MGM, Fernández-García, JL and Martínez-Estéllez, MÁH (2017) Seroprevalence of Theileria equi and Babesia caballi in horses in Spain. Parasite 24, 14.Google Scholar
Cruz-Flores, MJ, Bata, M, Co, B, Claveria, FG, Verdida, R, Xuan, X and Igarashi, I (2010) 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.Google Scholar
Díaz-Sánchez, AA, Pires, MS, Estrada, CY, Cañizares, EV, del Castillo Domínguez, SL, Cabezas-Cruz, A and Corona-González, B (2018) First molecular evidence of Babesia caballi and Theileria equi infections in horses in Cuba. Parasitology Research 117, 3109–3118.CrossRefGoogle ScholarPubMed
Egger, M, Smith, GD, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629–634.CrossRefGoogle ScholarPubMed
Gallusová, M, Qablan, MA, D'Amico, G, Oborník, M, Petrželková, KJ, Mihalca, AD and Modrý, D (2014) Piroplasms in feral and domestic equines in rural areas of the Danube Delta, Romania, with survey of dogs as a possible reservoir. Veterinary Parasitology 206, 287–292.CrossRefGoogle ScholarPubMed
García-Bocanegra, I, Arenas-Montes, A, Hernández, E, Adaszek, Ł, Carbonero, A, Almería, S and Arenas, A (2013) Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infection in equids. The Veterinary Journal 195, 172–178.CrossRefGoogle ScholarPubMed
Gizachew, A, Schuster, RK, Joseph, S, Wernery, R, Georgy, NA, Elizabeth, SK and Wernery, U (2013) Piroplasmosis in donkeys – a hematological and serological study in Central Ethiopia. Journal of Equine Veterinary Science 33, 18–21.CrossRefGoogle Scholar
Grandi, G, Molinari, G, Tittarelli, M, Sassera, D and Kramer, LH (2011) Prevalence of Theileria equi and Babesia caballi infection in horses from northern Italy. Vector-Borne and Zoonotic Diseases 11, 955–956.CrossRefGoogle ScholarPubMed
Guidi, E, Pradier, S, Lebert, I and Leblond, A (2015) Piroplasmosis in an endemic area: analysis of the risk factors and their implications in the control of theileriosis and babesiosis in horses. Parasitology Research 114, 71–83.CrossRefGoogle Scholar
Gummow, B, De Wet, CS and De Waal, DT (1996) A sero-epidemiological survey of equine piroplasmosis in the northern and eastern Cape Provinces of South Africa. Journal of the South African Veterinary Association 67, 204–208.Google Scholar
Guven, E, Avcioglu, H, Deniz, A, Balkaya, İ, Abay, U, Yavuz, Ş and Akyüz, M (2017) Prevalence and molecular characterization of Theileria equi and Babesia caballi in jereed horses in Erzurum, Turkey. Acta Parasitologica 62, 207–213.CrossRefGoogle ScholarPubMed
Hawkins, E, Kock, R, McKeever, D, Gakuya, F, Musyoki, C, Chege, SM and Skilton, RA (2015) 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. Journal of Wildlife Diseases 51, 137–147.CrossRefGoogle Scholar
Hedges, LV and Vevea, JL (1998) Fixed-and random-effects models in meta-analysis. Psychological Methods 3, 486.Google Scholar
Heim, A, Passos, LM, Ribeiro, MF, Costa-Júnior, LM, Bastos, CV, Cabral, DD and Pfister, K (2007) Detection and molecular characterization of Babesia caballi and Theileria equi isolates from endemic areas of Brazil. Parasitology Research 102, 63–68.CrossRefGoogle ScholarPubMed
Heuchert, CMS, de Giulli, V Jr, De Athaide, DF, Böse, R and Friedhoff, KT (1999) Seroepidemiologic studies on Babesia equi and Babesia caballi infections in Brazil. Veterinary Parasitology 85, 1–11.CrossRefGoogle ScholarPubMed
Higgins, JP and Thompson, SG (2002) Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 1539–1558.CrossRefGoogle ScholarPubMed
Homer, MJ, Aguilar-Delfin, I, Telford, SR, Krause, PJ and Persing, DH (2000) Babesiosis. Clinical Microbiology Reviews 13, 451–469.CrossRefGoogle ScholarPubMed
Hussain, MH, Saqib, M, Raza, F, Muhammad, G, Asi, MN, Mansoor, MK and Jabbar, A (2014) Seroprevalence of Babesia caballi and Theileria equi in five draught equine populated metropolises of Punjab, Pakistan. Veterinary Parasitology 202, 248–256.CrossRefGoogle ScholarPubMed
Idoko, SI, Tirosh-Levy, S, Leszkowicz Mazuz, M, Mohammed, AB, Sikiti Garba, B, Wesley, ND and Steinman, A (2020) Genetic characterization of piroplasms in donkeys and horses from Nigeria. Animals 10, 324.CrossRefGoogle Scholar
Ikadai, H, Nagai, A, Xuan, X, Igarashi, I, Kamio, T, Tsuji, N and Fujisaki, K (2002) Seroepidemiologic studies on Babesia caballi and Babesia equi infections in Japan. Journal of Veterinary Medical Science 64, 325–328.CrossRefGoogle ScholarPubMed
Jaffer, O, Abdishakur, F, Hakimuddin, F, Riya, A, Wernery, U and Schuster, RK (2010) A comparative study of serological tests and PCR for the diagnosis of equine piroplasmosis. Parasitology Research 106, 709–713.CrossRefGoogle Scholar
Kakekhani, S, Rahbari, S, Madani, R and Bokaei, S (2017) Molecular and microscopic detection of Theileria equi and Babesia caballi in horses in Kurdestan Province, Iran. Archives of Razi Institute 72, 51–55.Google Scholar
Kamyingkird, K, Yangtara, S, Desquesnes, M, Cao, S, Moumouni, A, Jittapalapong, S and Igarashi, I (2016) Seroprevalence of Babesia caballi and Theileria equi in horses and mules from Northern Thailand. The Journal of Protozoology Research 24, 11–17.Google Scholar
Karatepe, B, Karatepe, M, Çakmak, A, Karaer, Z and Ergün, G (2009) Investigation of seroprevalence of Theileria equi and Babesia caballi in horses in Nigde province, Turkey. Tropical Animal Health and Production 41, 109–113.CrossRefGoogle ScholarPubMed
Kerber, CE, Labruna, MB, Ferreira, F, De Waal, DT, Knowles, DP and Gennari, SM (2009) Prevalence of equine piroplasmosis and its association with tick infestation in the State of São Paulo, Brazil. Revista Brasileira de Parasitologia Veterinária 18, 1–8.CrossRefGoogle ScholarPubMed
Kizilarslan, F, Yildirim, A, Duzlu, O, Inci, A, Onder, Z and Ciloglu, A (2015) 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.CrossRefGoogle Scholar
Kouam, MK, Kantzoura, V, Gajadhar, AA, Theis, JH, Papadopoulos, E and Theodoropoulos, G (2010) Seroprevalence of equine piroplasms and host-related factors associated with infection in Greece. Veterinary Parasitology 169, 273–278.CrossRefGoogle Scholar
Levine, ND (1985) Apicomplexa: the piroplasms. In Soulsby, EJL (ed.), Veterinary Protozoology. Ames, IA: Iowa State Universty Press, pp. 291–328.Google Scholar
Machado, RZ, Toledo, CZP, Teixeira, MCA, André, MR, Freschi, CR and Sampaio, H (2012) Molecular and serological detection of Theileria equi and Babesia caballi in donkeys (Equus asinus) in Brazil. Veterinary Parasitology 186, 461–465.CrossRefGoogle ScholarPubMed
Mahmoud, MS, El-Ezz, NTA, Abdel-Shafy, S, Nassar, SA, El Namaky, AH, Khalil, WK and Suarez, CE (2016) Assessment of Theileria equi and Babesia caballi infections in equine populations in Egypt by molecular, serological and hematological approaches. Parasites and Vectors 9, 260.CrossRefGoogle ScholarPubMed
Malekifard, F, Tavassoli, M, Yakhchali, M and Darvishzadeh, R (2014) Detection of Theileria equi and Babesia caballi using microscopic and molecular methods in horses in suburb of Urmia, Iran. Veterinary Research Forum 5, 129–134.Google ScholarPubMed
Mans, BJ, Pienaar, R and Latif, AA (2015) A review of Theileria diagnostics and epidemiology. International Journal for Parasitology: Parasites and Wildlife 4, 104–118.Google ScholarPubMed
Moher, D, Shamseer, L, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M and Stewart, LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) statement. Systematic Reviews 4, 1.CrossRefGoogle ScholarPubMed
Moretti, A, Mangili, V, Salvatori, R, Maresca, C, Scoccia, E, Torina, A and Pietrobelli, M (2010) Prevalence and diagnosis of Babesia and Theileria infections in horses in Italy: a preliminary study. The Veterinary Journal 184, 346–350.CrossRefGoogle ScholarPubMed
Motloang, MY, Thekisoe, OMM, Alhassan, A, Bakheit, M, Motheo, MP, Masangane, FES and Mbati, PA (2008) 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 Journal of Veterinary Research 75, 141–146.CrossRefGoogle ScholarPubMed
Mujica, FF, Perrone, T, Forlano, M, Coronado, A, Meléndez, RD, Barrios, N and Granda, F (2011) Serological prevalence of Babesia caballi and Theileria equi in horses of Lara State, Venezuela. Veterinary Parasitology 178, 180–183.CrossRefGoogle ScholarPubMed
Munkhjargal, T, Sivakumar, T, Battsetseg, B, Nyamjargal, T, Aboulaila, M, Purevtseren, B and Igarashi, I (2013) Prevalence and genetic diversity of equine piroplasms in Tov province, Mongolia. Infection, Genetics and Evolution 16, 178–185.CrossRefGoogle ScholarPubMed
Nugraha, AB, Cahyaningsih, U, Amrozi, A, Ridwan, Y, Agungpriyono, S, Taher, DM and Sivakumar, T (2018) Serological and molecular prevalence of equine piroplasmosis in Western Java, Indonesia. Veterinary Parasitology: Regional Studies and Reports 14, 1–6.Google ScholarPubMed
Oduori, DO, Onyango, SC, Kimari, JN and MacLeod, ET (2015) A field survey for the seroprevalence of Theileria equi and Babesia caballi in donkeys from Nuu Division, Kenya. Ticks and Tick-Borne Diseases 6, 683–688.CrossRefGoogle ScholarPubMed
OIE (2005) Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, ch. 2.5.6 Equine Piroplasmosis. Available at http://www.oie.int.eng.normes/mmanual/A_00084.htm (accessed 25 January 2011).Google Scholar
OIE (2018) Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, ch. 3.5.8 Equine Piroplasmosis. Available at https://www.oie.int/standard-setting/terrestrial-manual/access-online/ (accessed 29 April 2020).Google Scholar
Onyiche, TE, Suganuma, K, Igarashi, I, Yokoyama, N, Xuan, X and Thekisoe, O (2019) A review on equine piroplasmosis: epidemiology, vector ecology, risk factors, host immunity, diagnosis and control. International Journal of Environmental Research and Public Health 16, 1736.CrossRefGoogle Scholar
Onyiche, T, Taioe, M, Ogo, N, Sivakumar, T, Biu, A, Mbaya, A, Xuan, X, Yokoyama, N and Thekisoe, O (2020) Molecular evidence of Babesia caballi and Theileria equi in equines and ticks in Nigeria: prevalence and risk factors analysis. Parasitology, 1–35. doi:10.1017/S0031182020000992.CrossRefGoogle ScholarPubMed
Piantedosi, D, D'Alessio, N, Di Loria, A, Di Prisco, F, Mariani, U, Neola, B and Veneziano, V (2014) Seroprevalence and risk factors associated with Babesia caballi and Theileria equi infections in donkeys from Southern Italy. The Veterinary Journal 202, 578–582.CrossRefGoogle ScholarPubMed
Posada-Guzmán, MF, Dolz, G, Romero-Zúñiga, JJ and Jiménez-Rocha, AE (2015) Detection of Babesia caballi and Theileria equi in blood from equines from four indigenous communities in Costa Rica. Veterinary Medicine International, http://dx.doi.org/10.1155/2015/236278.CrossRefGoogle ScholarPubMed
Qablan, MA, Obornik, M, Petrželková, KJ, Sloboda, M, Shudiefat, MF, Hořín, P and Modrý, D (2013) Infections by Babesia caballi and Theileria equi in Jordanian equids: epidemiology and genetic diversity. Parasitology 140, 1096–1103.Google ScholarPubMed
Ramsay, JD, Ueti, MW, Johnson, WC, Scoles, GA, Knowles, DP and Mealey, RH (2013) Lymphocytes and macrophages are infected by Theileria equi, but T cells and B cells are not required to establish infection in vivo. PLoS ONE 8, e76996.CrossRefGoogle Scholar
Rapoport, A, Aharonson-Raz, K, Berlin, D, Tal, S, Gottlieb, Y, Klement, E and Steinman, A (2014) Molecular characterization of the Babesia caballi rap-1 gene and epidemiological survey in horses in Israel. Infection, Genetics and Evolution 23, 115–120.CrossRefGoogle ScholarPubMed
Ros-García, A, M'ghirbi, Y, Hurtado, A and Bouattour, A (2013) Prevalence and genetic diversity of piroplasm species in horses and ticks from Tunisia. Infection, Genetics and Evolution 17, 33–37.CrossRefGoogle ScholarPubMed
Rosales, R, Rangel-Rivas, A, Escalona, A, Jordan, LS, Gonzatti, MI, Aso, PM and Mijares, A (2013) Detection of Theileria equi and Babesia caballi infections in Venezuelan horses using Competitive-Inhibition ELISA and PCR. Veterinary Parasitology 196, 37–43.CrossRefGoogle ScholarPubMed
Rothschild, CM (2013) Equine piroplasmosis. Journal of Equine Veterinary Science 33, 497–508.CrossRefGoogle Scholar
Rüegg, SR, Torgerson, P, Deplazes, P and Mathis, A (2007) 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 134, 939–947.CrossRefGoogle ScholarPubMed
Salim, BOM, Hassan, SM, Bakheit, MA, Alhassan, A, Igarashi, I, Karanis, P and Abdelrahman, MB (2008) Diagnosis of Babesia caballi and Theileria equi infections in horses in Sudan using ELISA and PCR. Parasitology Research 103, 1145.CrossRefGoogle ScholarPubMed
Salim, B, Bakheit, MA, Kamau, J and Sugimoto, C (2013) Current status of equine piroplasmosis in the Sudan. Infection, Genetics and Evolution 16, 191–199.CrossRefGoogle ScholarPubMed
Sanusi, M, Ahmed, IA, Tahir, I, Mai, HM, Kalla, DJU and Shuaibu, I (2014) Survey of equine piroplasmosis in the Savanna areas, Bauchi state, North-eastern Nigeria. Ippologia 25, 3–8.Google Scholar
Scoles, GA and Ueti, MW (2015) Vector ecology of equine piroplasmosis. Annual Review of Entomology 60, 561–580.CrossRefGoogle ScholarPubMed
Seo, MG, Yun, SH, Choi, SK, Cho, GJ, Park, YS, Kwon, OD and Kwon, YS (2011) Seroprevalence of equine piroplasms in the Republic of Korea. Veterinary Parasitology 179, 224–226.CrossRefGoogle ScholarPubMed
Sevinc, F, Maden, M, Kumas, C, Sevinc, M and Ekici, OD (2008) A comparative study on the prevalence of Theileria equi and Babesia caballi infections in horse sub-populations in Turkey. Veterinary Parasitology 156, 173–177.CrossRefGoogle ScholarPubMed
Sigg, L, Gerber, V, Gottstein, B, Doherr, MG and Frey, CF (2010) Seroprevalence of Babesia caballi and Theileria equi in the Swiss horse population. Parasitology International 59, 313–317.CrossRefGoogle ScholarPubMed
Sumbria, D, Singla, LD and Sharma, A (2016) Theileria equi and Babesia caballi infection of equids in Punjab, India: a serological and molecular survey. Tropical Animal Health and Production 48, 45–52.CrossRefGoogle ScholarPubMed
Turaki, UA, Kumsha, HA, Biu, AA and Bokko, PB (2014) Prevalence of piroplasmosis amongst local horses in Northeastern Nigeria. Journal of Agricultural and Veterinary Science 4, 27.Google Scholar
Uilenberg, G (2006) Babesia – a historical overview. Veterinary Parasitology 138, 3–10.CrossRefGoogle ScholarPubMed
Vieira, TS, Vieira, RF, Finger, MA, Nascimento, DA, Sicupira, PM, Dutra, LH and Vidotto, O (2013) Seroepidemiological survey of Theileria equi and Babesia caballi in horses from a rural and from urban areas of Paraná State, southern Brazil. Ticks and Tick-Borne Diseases 4, 537–541.CrossRefGoogle ScholarPubMed
Vieira, MIB, Costa, MM, de Oliveira, MT, Gonçalves, LR, André, MR and Machado, RZ (2018) Serological detection and molecular characterization of piroplasmids in equids in Brazil. Acta Tropica 179, 81–87.CrossRefGoogle ScholarPubMed
Wang, M, Guo, W, Igarashi, I, Xuan, X, Wang, X, Xiang, W and Jia, H (2014) Epidemiological investigation of equine piroplasmosis in China by enzyme-linked immunosorbent assays. Journal of Veterinary Medical Science 76, 549–552.CrossRefGoogle ScholarPubMed
Wise, LN, Kappmeyer, LS, Mealey, RH and Knowles, DP (2013) Review of equine piroplasmosis. Journal of Veterinary Internal Medicine 27, 1334–1346.CrossRefGoogle ScholarPubMed
Xu, Y, Zhang, S, Huang, X, Bayin, C, Xuan, X, Igarashi, I and Mikami, T (2003) Seroepidemiologic studies on Babesia equi and Babesia caballi infections in horses in Jilin province of China. Journal of Veterinary Medical Science 65, 1015–1017.CrossRefGoogle ScholarPubMed
Ybañez, AP, Ybañez, RHD, Talle, MG, Arreglo, RMT, Geens, MJC, Villas, JGI and Liu, M (2018) Serological and molecular detection of Theileria equi and Babesia caballi in Philippine horses. Ticks and Tick-Borne Diseases 9, 1125–1128.CrossRefGoogle ScholarPubMed
Supplementary material: File

Onyiche et al. supplementary material

Onyiche et al. supplementary material
Download Onyiche et al. supplementary material(File)
File 3.5 MB