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Molecular evidence of Babesia caballi and Theileria equi in equines and ticks in Nigeria: prevalence and risk factors analysis

Published online by Cambridge University Press:  17 June 2020

ThankGod E. Onyiche Open the ORCID record for ThankGod E. Onyiche [Opens in a new window] ,
Moeti O. Taioe ,
Ndudim I. Ogo ,
Thillaiampalam Sivakumar ,
Abdullahi A. Biu ,
Albert W. Mbaya ,
Xuenan Xuan ,
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
Ndudim I. Ogo
Affiliation:
Parasitology Division, National Veterinary Research Institute, Vom, Plateau State, Nigeria
Thillaiampalam Sivakumar
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido080-8555, Japan
Abdullahi A. Biu
Affiliation:
Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria
Albert W. Mbaya
Affiliation:
Department of Veterinary Parasitology and Entomology, University of Maiduguri, P. M. B. 1069, Maiduguri600230, Nigeria
Xuenan Xuan
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido080-8555, Japan
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: et.onyiche@unimaid.edu.ng
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Abstract

Babesia caballi and Theileria equi are biological agents responsible for equine piroplasmosis (EP). We conducted a robust and extensive epidemiological study in Nigeria on the prevalence and risk factors of EP. Blood (468, both horses and donkeys) and ticks (201 pools) were screened using polymerase chain reaction (PCR). DNA of equine piroplasms was observed in tick pools with B. caballi amplified in Rhipicephalus evertsi evertsi only [minimum infection rate (MIR) of 7.6%] while T. equi was observed in R. e. evertsi (MIR, 61.6%), Hyalomma dromedarii (MIR, 23.7%) and H. truncatum (MIR, 50.0%). Overall results showed that 196/468 (41.9%) animals were positive for equine piroplasms (both B. caballi and T. equi). The prevalence for T. equi was 189/468 (40.4%) compared to 7/468 (1.5%) for B. caballi. In the horses and donkeys, respectively, the prevalence for T. equi was (39.9%; 112/281) and (41.2%; 77/187) compared with (1.4%; 4/281) and (1.6%; 3/187) due to B. caballi. Our analysis showed that location (Jigawa state), Talon breed, horses used for work and reproduction, unsatisfactory husbandry practices, contact with other mammals are risk factors that associated positivity to T. equi infection in horses, whilst horses kept on intensive management appeared to be less prone to infection. On the other hand, Jangora breed of donkeys and location (Jigawa state) are risk factors to infection with T. equi in donkeys. Findings suggest the persistence of EP in equids and ticks in Nigeria.

Keywords

Babesia caballiequinesNigeriarisk factorsTheileria equi
Type
Research Article
Information
Parasitology , Volume 147 , Issue 11 , September 2020 , pp. 1238 - 1248
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

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 Diseases 59, 72–78.CrossRefGoogle ScholarPubMed
Alexander, J and Stimson, WH (1988) Sex hormones and the course of parasitic infection. Parasitology Today 4, 189–193.CrossRefGoogle Scholar
Alhassan, A, Pumidonming, W, Okamura, M, Hirata, H, Battsetseg, B, Fujisaki, K, Yokoyama, N and Igarashi, I (2005) Development of a single-round and multiplex PCR method for the simultaneous detection of Babesia caballi and Babesia equi in horse blood. Veterinary Parasitology 129, 43–49.CrossRefGoogle ScholarPubMed
Apanaskevich, DA and Horak, IG (2005) The genus Hyalomma. II The taxonomic status of H. (Euhyalomma) anatolicum Koch 1844 and H. (Euhyalomma) excavatum Koch 1844 with the redescription of all stages. Acarina 13, 181–197.Google 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
Berggoetz, M, Schmid, M, Ston, D, Wyss, V, Chevillon, C, Pretorius, AM and Gern, L (2014) Protozoan and bacterial pathogens in tick salivary glands in wild and domestic animal environments in South Africa. Ticks and Tick-Borne Diseases 5, 176–185.CrossRefGoogle ScholarPubMed
Bhoora, RV, Collins, NE, Schnittger, L, Troskie, C, Marumo, R, Labuschagne, K, Smith, RM, Dalton, DL and Mbizeni, S (2020) Molecular genotyping and epidemiology of equine piroplasmids in South Africa. Ticks and Tick-borne Diseases 11(2), 101358.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(1), 29–32.CrossRefGoogle 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
Brüning, A (1996) Equine piroplasmosis an update on diagnosis, treatment and prevention. British Veterinary Journal 152, 139–151.CrossRefGoogle Scholar
Bursac, Z, Gauss, CH, Williams, DK and Hosmer, DW (2008) Purposeful selection of variables in logistic regression. Source Code for Biology and Medicine 3, 17.CrossRefGoogle ScholarPubMed
Chan, CX and Ragan, MA (2013) Next generation phylogenomics. Biology Direct 8, 3.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, 1–11.Google Scholar
Dahiya, R, Salar, RK, Mandal, KD, Kumar, R, Tripathi, BN, Pal, Y and Kumar, S (2018) Risk factor analysis associated with Theileria equi infected equines in semi-arid and sub-humid ecological enzootic zones of India. Veterinary Parasitology: Regional Studies and Reports 12, 17–21.Google ScholarPubMed
Del Pino, LE, Roberto, N, Vincenzo, V, Francesca, I, Antonella, C, Luca, AG, Francesco, B 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
De Waal, DT and Potgieter, FT (1987) The trans-stadial transmission of Babesia caballi by Rhipicephalus evertsi evertsi. Onderstepoort Journal of Veterinary Research 54, 655–656.Google Scholar
Food and Agriculture Organization of the United Nations (FAO) (2016) FOOSTAT. Available at http://www.fao.org/faostat/en/#data/QA (Accessed 26 April 2019).Google Scholar
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(3–4), 287–292.CrossRefGoogle ScholarPubMed
García-Bocanegra, I, Arenas-Montes, A, Hernández, E, Adaszek, Ł, Carbonero, A, Almería, S, Jaén-Téllez, JA, Gutiérrez-Palomino, P 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
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
Hassan, MR, Steenstra, FA and Udo, HMJ (2013) Benefits of donkeys in rural and urban areas in northwest Nigeria. African Journal of Agricultural Research 8, 6202–6212.Google Scholar
Hawkins, E, Kock, R, McKeever, D, Gakuya, F, Musyoki, C, Chege, SM, Mutinda, M, Kariuki, E, Davidson, Z, Low, B 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
Heim, A, Passos, LM, Ribeiro, MF, Costa-Júnior, LM, Bastos, CV, Cabral, DD, Hirzmann, J 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
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
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
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
Mahmoud, MS, El-Ezz, NT, Abdel-Shafy, S, Nassar, SA, El Namaky, AH, Khalil, WK, Knowles, D, Kappmeyer, L, Silva, MG 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
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
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
Mshelia, WP, Sambo, KW, Adamu, S, Edeh, ER and Onoja, II (2016) Persistence of equine piroplasmosis in horses in Nigeria. Journal of Equine Veterinary Science 39, S104–S105.CrossRefGoogle Scholar
Munkhjargal, T, Sivakumar, T, Battsetseg, B, Nyamjargal, T, Aboulaila, M, Purevtseren, B, Bayarsaikhan, D, Byambaa, B, Terkawi, MA, Yokoyama, N and Igarashi, I (2013) Prevalence and genetic diversity of equine piroplasms in Tov province, Mongolia. Infection, Genetics and Evolution 16, 178–185.CrossRefGoogle ScholarPubMed
National Population Commission (2006) Population and housing census of the Federal Republic of Nigeria. Priority Tables 1, 22–29.Google Scholar
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 (2014) Piroplasmosis equina. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 1, 963–972.Google Scholar
Oladipo, TA, Adekunle, OF, Okuneye, OJ, Adebayo, MD, Adeoye, AT and Banjoko, OJ (2015) Pre and post polo competition prevalence of equine babesiosis in stable horses in Ibadan, Oyo state, Nigeria. International Journal of Research 6, 6–9.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
Piantedosi, D, D'Alessio, N, Di Loria, A, Di Prisco, F, Mariani, U, Neola, B, Santoro, M, Montagnaro, S, Capelli, G 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
Qablan, MA, Obornik, M, Petrželková, KJ, Sloboda, M, Shudiefat, MF, Hořín, P, Lukeš, J and Modrý, D (2013) Infections by Babesia caballi and Theileria equi in Jordanian equids: epidemiology and genetic diversity. Parasitology 140, 1096–1103.CrossRefGoogle ScholarPubMed
Roberts, CW, Walker, W and Alexander, J (2001) Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476–488.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
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
Santos, TM, Roier, EC, Santos, HA, Pires, MS, Vilela, JA, Moraes, LM, Almeida, FQ, Baldani, CD, Machado, RZ and Massard, CL (2011) Fatores associados à Theileria equi em equídeos de duas microrregiões do Rio de Janeiro. Brasil. Revista Brasileira de Parasitologia Veterinária 20, 235–241.CrossRefGoogle Scholar
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
Shkap, V, Cohen, I, Leibovitz, B, Savitsky, PE, Avni, G, Giger, U, Kappmayer, I and Knowles, D (1998) Seroprevalence of Babesia equi among horses in Israel using competitive inhibition ELISA and IFA assays. Veterinary Parasitology 76, 251–259.CrossRefGoogle ScholarPubMed
Short, MA, Clark, CK, Harvey, JW, Wenzlow, N, Hawkins, IK, Allred, DR, Knowles, DP, Corn, JL, Grause, JF, Hennager, SG and Kitchen, DL (2012) Outbreak of equine piroplasmosis in Florida. Journal of the American Veterinary Medical Association 240, 588–595.CrossRefGoogle ScholarPubMed
Silaghi, C, Hamel, D, Thiel, C, Pfister, K and Pfeiffer, M (2011) Spotted fever group rickettsiae in ticks, Germany. Emerging Infectious Diseases 17, 890.CrossRefGoogle ScholarPubMed
Sumbria, D, Singla, LD, Kumar, S, Sharma, A, Dahiya, RK and Setia, R (2016) Spatial distribution, risk factors and haemato-biochemical alterations associated with Theileria equi infected equids of Punjab (India) diagnosed by indirect ELISA and nested PCR. Acta Tropica 155, 104–112.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
Ueti, MW and Knowles, DP (2018) Equine piroplasmids. In Florin-Christensen, M and Schnittger, L (eds), Parasitic Protozoa of Farm Animals and Pets. Heidelberg, Germany: Springer, pp. 259–269.CrossRefGoogle Scholar
Walker, AR, Bouattour, A, Camicas, JL, Estrada-Pena, A, Horak, IG, Latif, AA, Pegram, RG and Preston, PM (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports. Scotland: The University of Edinburgh.Google Scholar
Wise, LN, Kappmeyer, LS, Mealey, RH and Knowles, DP (2013) Review of equine piroplasmosis. Journal of Veterinary Internal Medicine 27, 1334–1346.CrossRefGoogle ScholarPubMed
Zobba, R, Ardu, M, Niccolini, S, Chessa, B, Manna, L, Cocco, R and Parpaglia, MLP (2008) Clinical and laboratory findings in equine piroplasmosis. Journal of Equine Veterinary Science 28, 301–308.CrossRefGoogle Scholar