Research Article

Endoparasitic Infections and the Associated Risk Factors in Trade Donkeys (Equus Asinus) in Ganawuri District Market, Riyom Local Government Area, Plateau State, North Central Nigeria

Bata Shalangwa Ishaku1, Batim Turdam1, Maimadu Abdullahi1, Waziri Ibrahim Anjili2 and Mayowa Olabode2

1Department of Animal Health, Federal College of Animal Health and Production Technology, Vom, Plateau State, Nigeria; 2National Veterinary Research Institute, Vom Plateau State, Nigeria.

Editor | Muhammad Abubakar, National Veterinary Laboratories, Park Road, Islamabad, Pakistan.

Received | February 08, 2019; Accepted | February 28, 2019; Published | April 10, 2019

*Correspondence | Bata Shalangwa Ishaku, Department of Animal Health, Federal College of Animal Health and Production Technology, National Veterinary Research Institute, Vom Plateau State Nigeria; Email: drsshalangwa2005@yahoo.co.uk

Citation | Ishaku, B.S., B. Turdam, M. Abdullahi, Waziri, I. Anjili and M. Olabode. 2019. Endoparasitic infections and the associated risk factors in trade donkeys (Equus Asinus) in Ganawuri district market, Riyom local Government area, plateau state, north central Nigeria. Veterinary Sciences: Research and Reviews, 5(1): 16-24.

DOI | http://dx.doi.org/10.17582/journal.vsrr/2019/5.1.16.24

Key words | Cross-sectional, Endoparasitic, Infection, Gastrointestinal, Hemoparasites

Introduction

Parasites have great potentials for reducing the efficiency and production success as they compete with the host for nutrient utilization. Endoparasites are usually protozoa and helminthes that live inside the body of their host and poses a serious threat to their health (Ademola et al., 2004). Donkeys (Equus asinus) are among the early members of the horse family-Equidae that lived in close association with man and have been a working animal for thousands of years (Saul et al., 1997). At present, report has shown that about 44million donkeys are distributed throughout the world (Starkey et al., 2004). The animal plays an important role in the transportation of people and goods in arid and semi-arid areas despite advancement in technology throughout the world (Pearson et al., 1999). In Africa, the population of donkeys has been estimated to be about 13 million. Nigeria an example of one of the semi-arid areas alone has an estimated population of 7 million donkeys with the majority owned by small-holder and low-income farmers who do have little or no access to veterinary care (Kyewalabye et al., 1988; Starkey et al., 2000).

In addition to being kept as working animals, the meat of donkeys is considered as a traditional delicacy in some parts of Nigeria and is seen to be of very high nutritional value due to its high levels of unsaturated fatty acids (Polidori et al., 2009). Many diseases, however, affect donkeys and reduce their viability, lower their ability to work and their carcass (meat) quality through the reduction in body weight or failure to gain weight or even increase the mortality in acute cases (Khalifa et al., 1988; Mezgebu et al., 2013).

A majority of farmers who keep donkey do practice an extensive management system. This practice exposes donkeys to many infectious disease agents which could be parasitic, bacterial, fungal, and or viral (Ibrahim et al., 2011). According to Getachew et al. (2010), the commonly reported parasitic diseases that usually lead to the death of donkeys are haemoparasite such as babesiosis, trypanosomiasis and gastrointestinal helminthosis. The economic losses caused by trypanosomiasis are due to a loss in productivity, cost of treatment and the dead of the animal. These losses along with the control measures caused by trypanosmiasis alone have been estimated to be over 4.2million USD annually.

Donkeys are a host to a variety of gastrointestinal tract parasite of the family strongylidae, commonly called strongyle nematodes (Ayana et al., 2012). The most common gastrointestinal parasites of donkeys include large and small Strongyles, Ascaris, Oxyuris equi, Gasterophilus, lungworms, fluke and tapeworms and are commonly encountered in the most veterinary parasitological examination (Atawalna et al., 2015). Some of the gastrointestinal tract parasites especially strongyles, are active bloodsuckers, the commonly encountered manifestation is anemia, weakness, emaciation and sometimes colic and diarrhea (Burden et al., 2010). These parasites usually deprive their host of sufficient nutrients resulting in retarded growth, impaired productivity, discomfort, pains and sometimes death (Mezgebu et al., 2013). The various degree of damage depends on factors such as the species affected, nutritional and immune status of the animals (Mezgebu et al., 2013).

The free grazing of donkeys exposes them directly to infective stages of parasites, or indirectly to disease-transmitting agents such as ticks, and flies. These to a great extent affect the productivity and performance of the animal. According to Zerihun et al. (2011), parasitic helminthes are one of the factors that affect the health and performance of donkeys worldwide. Most importantly, the lack of adequate attention given to the health of donkeys and in some cases, the highly under reporting of the disease condition has resulted in the decline of their general wellbeing (Taylor et al., 2007; Sugun et al., 2015; Ismail et al., 2016). This study was therefore undertaken to assess the health status and risk factors visa-vis parasitic infections in trade donkeys at Ganawuri district, Riyom Local Government Area, Plateau State.

Materials and Methods

Study area

The study was conducted in Ganawuri district, Riyom Local Government Area Plateau State, Nigeria (Figure 1). Its headquarters is in the town of Riyom to the north of the Area at 9o3800″N, 8o4600″E. It has an area of 807km2 and a population of 131,557 at the 2006 census, which is predominantly Berom. The Local Government Area has boundaries with Kaduna and Nasarawa state. Between 20 and 30 donkeys from mostly North-eastern part of Nigeria are presented to Ganawuri market for slaughter.

Detection of hemoparasites: Identification of blood parasites and determination of packed cell volume (PCV) were done using thin and thick blood smear, and hematocrit centrifuge as described by Woo, (1969), Murray et al. (1983) and Urquhart et al. (2003). Examination of blood was done by the dark ground buffy coat and of smear after Giemsa staining using a light microscope under oil immersion (×100). The Trypanosoma and Babesia species were classified based on the morphology as described by Uilenberg (1998) and Soulsby (1982) respectively.

Faecal sample analysis: Floatation and sedimentation techniques were carried out as described by Urquhart et al. (2003) and Soulsby (1982). At the end of 10-15 min, the various slides were observed under the microscope using a magnification of ×10 and ×40 objective lenses.

Data analysis: Data obtained were analyzed using a Statistical Package for Social Sciences version 23. For categorical data, the chi-square test was used to determine the association between the presence of endo-parasites and factors such as age, sex, management systems, location and body condition of donkeys at slaughter in Ganawuri district. Student t-test was used to determine the statistically significant difference in mean values of pack cell volume in hemoparasite infected and non-infected donkeys. The p-values less than 0.05 were considered statistically significant. The result was summarized in tables and figures.

Results and Discussion

This study was carried out to determine the prevalence of endoparasites in donkeys at Ganawuri market, Plateau State. Greater proportions of the donkeys sampled were from the North-eastern part of the country (Figure 1). Based on coprological examination conducted using flotation and sedimentation technique, 276 were positive for gastrointestinal nematodes giving a prevalence of 92.0% (Table1). The result showed that greater proportions of the gastrointestinal nematodes identified were Strongyles (70.7%) (Figure 2).

The result showed that there was no statistically significant difference in the prevalence of gastrointestinal nematodes based on sex, age and location (p= 0.57; 0.20; 0.50). (Table 2). The study showed that there was a statistically significant difference in the prevalence based on body condition (p=0.03) and the type of management system. The prevalence was higher (48.9%) in those managed extensively (Table 2).

Table 1: Prevalence of endoparasitic infection in trade donkeys at Ganawuri district market, Riyom Local Government, Plateau State.

Table 2: Prevalence and risk factors for gastrointestinal nematodes in trade donkeys at Ganawuri district market, Riyom Local Government, Plateau State.

One hundred and eight of the 300 blood samples collected from the donkeys at Ganawuri market were positive for hemoparasites giving an overall prevalence of 36.0% (Table 1). The hemoparasites identified were T. congolense, T. vivax, B. cabali and B. equi. The proportion of the hemoparasites was; Babesia (50.0%), Trypanosoma spp. (36.1%) and mixed infection (Trypanosoma and Babesia) (13.9%) (Figure 3). There was a statistically significant difference in prevalence of haemoparasites in donkeys based on sex, (p=0.006; OR=7.303), body condition (p=0.001; OR=23.1), age (p=0.008) and management system (p=0.041) (Table 3). The prevalence was higher (41.72)

in age 10-12 yr, than in 7-9 yr (27.5) (Table 3). Prevalence based on source did not show any statistically significant difference (p=0.06). Lower range (21%-29%) of packed cell volume was found in donkeys positive for hemoparasites with a mean value of 25.56± 2.63 than in those that were negative (38.44±5.80) (p<0.001).

Ganawuri district market, Riyom Local Government Area, Plateau State, North Central Nigeria always has an influx of donkeys from mostly the North-eastern and western part of the country for sale and or slaughter. Prevalence and risk factors for endoparasites infection in these animals from November 2017 to May 2018 were examined. The prevalence of gastrointestinal nematodes in donkeys in this study was found to be 92.0%. Comparatively, lower prevalence was reported by some authors in Ethiopia and South Sudan (Sawsan et al., 2008; Regassa and Yimer, 2013; Tesfu et al., 2014; Enigidaw et al., 2015). Studies conducted in some parts of Ethiopia however reported a high prevalence of gastrointestinal nematodes similar to that in this study (Yoseph et al., 2001; Ayele et al., 2006; Ibrahim et al., 2011; Mezgebu et al., 2013; Tsegaye and Chala, 2015). In the North eastern part of Nigeria, Jajere et al. (2016) reported a prevalence of 98.3%. Factors such as climatic conditions, management system and access to veterinary care have been shown to influence the distribution of gastrointestinal helminthes. The relative difference or similarity in the prevalence of gastrointestinal nematodes in donkeys observed in the different studies could be due to differences or similarities in climatic conditions, management system and access to veterinary care. Variation in the sample size and sampling time and or season may also explain the reason for the differences observed. Greater proportions of the donkeys screened in this study were sourced from the North-eastern region of Nigeria. This could explain the reason for the similarity in the high prevalence reported by Jajere et al., 2016.

Table 3: Prevalence and risk factors for haemoparasites in trade donkeys at Ganawuri district market, Riyom Local Government, Plateau State.

Strongyle species accounted for greater percentage of the nematodes identified in this study. Two studies by Enigidaw et al. (2015) and Jajere et al. (2016) also reported a high occurrence rate of Strongyle than other gastrointestinal tract nematodes. Strongyles have been reported to require a longer period to complete their life cycle and the worm population and burden are not influenced by different anthelmintic pressures. This may explain the reason for the high occurrence of Strongyles than other gastrointestinal tract nematodes.

Single infection with P. equorum was not found in this study. Yoseph et al. (2001) and Fikru et al. (2005) have reported a prevalence of Parascaris eggs in donkeys to be 15.7% and 17.3% respectively. Though mixed infection, this study has also revealed a prevalence of 14.0%. Gizachew et al. (2010) reported a prevalence of 33.0% of mixed infection of Parascaris and Strongyles in donkeys.

Table 4: Mean Packed Cell Volumes of infected and non-infected trade donkeys with haemoparasites in Ganawuri district market, Riyom Local Government, Plateau State Nigeria.

Factors such as sex, age and location were not significantly associated with gastrointestinal nematodes infections in donkeys in the study area. Previous studies have also shown that age and sex were not significant factors in the prevalence of gastrointestinal helminthes in donkeys (Tolossa and Ashenafi, 2013; Mezgebu et al., 2013; Jajere et al., 2016). This shows that the prevalence of gastrointestinal nematodes is not sex dependent particularly since both sexes have equal chances of being exposed to the parasitic stages of the nematodes. However, some studies have revealed significant association between gastrointestinal helmiths in donkeys and sex and age (Worku and Afera, 2012; Tesfu et al., 2014; Enigidaw et al., 2015). Most of the donkeys sampled were adults. Increase in age usually increases exposure of animals to parasitic infection in the environment. Since all of the donkeys are adult, it did not show any difference in the prevalence between the ages. Donkeys from the Northeastern part of the country accounted for the majority of animals screened in this study. Similarity in the agroclimatic conditions in this region and within the states could be the reason for the lack of variation based on location. The management system practiced by farmers has been reported to be a risk factor for gastrointestinal helminthes infection in donkeys in a study conducted in North eastern Nigeria (Jajere et al., 2016). The type of management system of the donkeys in this study was also found to be a risk factor for the gastrointestinal tract nematode infection in this study. Those managed extensively had a higher prevalence than those intensively managed. This could be due to the fact that animals that are allowed to graze freely are more likely to pick up infective stage of these gastrointestinal tract nematodes and so the high prevalence.

The overall prevalence of hemoparasites in donkeys in this study was comparably similar with the finding of Pam et al. (2013) who reported a prevalence of 36.1% in horses in Jos South Local Government Area, Plateau State, Nigeria. The occurrence of Babesia species was higher in this study followed by Trypanosoma species. Although Pam et al. (2013) did not identify Trypanosoma species in horses; their study reported a high occurrence of Babesia species. Studies in Central Ethiopia reported a low prevalence of Babesia in donkeys (Mekibib et al., 2009; Tefera et al., 2011). In a related study in some regions of Gambia, and Northwest Ethiopia, lower prevalence of trypanosomes was reported (Faye et al., 2001; Bedada and Dagnachew, 2012). Differences in ecological/environmental factors and tsetse and ticks abundance visa-vis available control measures may be the reason for the variation in the prevalence of hemoparasites in the different locations. The prevalence however did not vary significantly with respect to the source of the donkeys. Studies reported by Mekibib et al. (2009) also showed no significant variation in the prevalence of both Babesia spp and T. vivax infection between Adigudem and Kwiha districts of Tigray region Northern Ethiopia. As earlier stated, the donkeys in this study were sourced mostly from North eastern parts of the country with possibly similar climate, vegetation and management practice. This explains the reason for lack of variation in the prevalence of hemoparasites with respect to the source of donkeys. It has been established that in the absence of appropriate tsetse flies, some trypanosome species can be transmitted mechanically between infected and susceptible donkeys (Radostits et al., 2007). Therefore, the high prevalence of trypanosome species may not suggest tsetse fly abundance. The high prevalence of trypanosome in this study may suggest that donkeys may serve as an important reservoir in the transmission and maintenance of the parasite cycle. Trypanosomiasis has a direct impact on livestock productivity, reducing meat and milk production (Onyekwelu et al., 2017). This is likely due to the chronic nature usually associated with T. congolense and T. vivax infections. Therefore, donkeys in the study area may be experiencing a reduction in activity due to the impact of hemoparasitic infection. Blood parasites identified in the study are intraerythrocytic. They usually cause hemolysis of Red blood cells (RBCs) leading to anemia, loss of appetite etc. This may account for the association between hemoparasite infection and poor body condition observed in this study. It invariably implies that the animals’ body condition can be useful in identifying those that need immediate attention. This was also supported by the low range of PCV recorded among those with the hemoparasite infection as donkeys that are positive with hemoparasites had lower PCV values ranging from (21-29), than the negative donkeys (30-50). The low PCV in donkeys with parasitic infestations as opposed to their healthy counterparts could therefore be attributed to the effect of the parasites.

Conclusion

Donkeys at slaughter in Ganawuri district market have a high prevalence of gastrointestinal nematodes and a moderate occurrence of hemoparasites. The gastrointestinal and hemo-parasites identified were Strongyles, P. equorum, S. westeri, B. cabali, B. equi, T. congolense and T. vivax. Factors such as age, sex and location did not influence the prevalence with gastrointestinal nematode infection. Management system influences gastrointestinal nematode and haemoparasites infection. The prevalence of endoparasitic infections varies across body condition. Those with poor body condition had the highest prevalence. Lower range of PCV was found in donkeys with hemoparsite infection. Donkeys in the area may serve as reservoir of transmission of Trypanosoma species and in maintaining the cycle.

Recommendations

There is a need for further studies that will utilize a more sensitive technique such as PCR that picks up trypanosomes especially in chronic cases. Improved hygienic practices, routine strategic deworming and treatment of infected donkeys are recommended. To reduce environmental contamination, all newly introduced stock should be quarantined, screened and treated with anthelminthics and antiprotozoal.

Authors Contribution

The research was carried out in collaboration with all the authors. Bata, Ishaku Shalangwa and Batim Turdam conceived, designed and developed the project. Batim, Turdam contributed in the sample collection and laboratory analysis. Batim Turdam, Maimadu Abdullahi and Waziri Ibrahim Anjili produced the tables and figures. Batim Turdam, Maimadu Abdullahi and Waziri Ibrahim Anjili also wrote the first draft of the article. Mayowa Olabode and Bata, Ishaku Shalangwa proof read and wrote the final draft of the article. Bata, Ishaku Shalangwa carried out the data analysis using statistical package for social sciences version 21. All the authors read the final draft of the manuscript.

References

Acha, P.N. and B. Szyfres. 1987. Zoonoses and communicable diseases common to man and animals. 2nd ed. Pan american health organisation/ World Health Organ. Sci. Publ. No. 503: pp. 852−860.

Ademola, I.O., B.O. Fagbemi and S.O. Idowu. 2004. Evaluation of the anthelmintic activity of Khaya senegalensis extract against gastrointestinal nematodes of sheep: in-vtro and in-vivo studies. Vet. Parasitol. 122: 151–164. https://doi.org/10.1016/j.vetpar.2004.04.001

Atawalna, J., B.O. Emikpe, E.K. Sallah, W. Shaibu and R.O. Folitse. 2015. The health problems, gastrointestinal and blood parasites commonly associated with donkeys in the upper East region in Ghana, Africa. J. Biometrical Res. 18(1): 37−41.

Ayana, M., Z. Tesfaheywet and F. Getnet. 2012. A cross sectional study on the prevalence of bovine Trypanosomosis in Amhara region, Northwest Ethiopia. Liv. Res. Rural Dev. 24(8). Retrieved January 20, 2019, from http://www.lrrd.org/lrrd24/8/tesf24148.htm

Ayele, G.G., E. Feseha, Bojia and A. Joe. 2006. Prevalence of gastro-intestinal parasites of donekeys in Dugda Bora District, Tehiopia, Liv. Res. Rural Dev. 18(10): 2–6.

Bedada, H. and S. Dagnachew. 2012. Study on the prevalence of donkey trypanosomosis in Awi zone northwest Ethiopia. Ethiop. Vet. J. 6(2): 65–76. https://doi.org/10.4314/evj.v16i2.6

Burden, F.A., N. Du-Toit, M. Hernandez-Gil, O. Prado-Ortiz and A.F. Trawford. 2010. Selected health and management issues facing working donkeys presented for veterinary treatment in rural Mexico: some possible risk factors and potential intervention strategies, Trop. Anim. Health Prod. 42(4): 597–605. Labeled. https://doi.org/10.1007/s11250-009-9462-0

Enigidaw, S., A. Assefa, N. Mekonnen and S. Belete. 2015. Prevalence of gastrointestinal nematode parasitic infections of horses and donkeys in and around Kombolcha Town. Am-Eurasian J. Sci. Res. 10(4): 228 −234.

Faye, D., P. de-Almeida, B. Goossens, S. Osaer, M. Ndao, D. Bervens, N. Speybroeck, F. Nieberding and S. Geerts. 2001. Prevalence and incidences of trypanosomosis in horses and donkeys in the Gambia. Vet. Parasitol. 102 (2): 101−114. https://doi.org/10.1016/S0304-4017(01)00503-9

Fikru, R., D. Reta and M. Bizunesh. 2005. Prevalence of equine gastrointestinal parasites in western hgihlands of Oromia, Ethiopia. Bull. Anim Health Prod. Africa. 53(3): 161−166. https://doi.org/10.4314/bahpa.v53i3.32704

Getachew A.M., A.F. Trawford, G. Feseha, S.W.J. Reid. 2010. Gastrointestinal parasites of working donkeys in Ethiopia. Trop Anim Health Prod. 42:27–33.

Gizachew, A. and D. Ayana. 2010. Study on strongyles and arascaris parasites population in working donkeys of centeral Shoa, Ethiopia. Lives. Res. Rural Dev. 22: 1 −5.

Ibrahim, N., T. Berhanu, B. Deressa and T. Tolosa. 2011. Survey of prevalence of helminth parasites of donkeys in and around Hawassa Town, Souther Ethiopia. Glob. Vet. 6: 223 −227.

Ismail, A.A., N.K. Ahmed, A.E. Bashar, H.I. Seri, E.A. El-Tigani-Asil and A.D. Abakar. 2016. A survey of seasonal gastrointestinal parasitic infections in donkeys from a semiarid sub-Saharan region, Sudan. J. Pathog.

Jajere, S.M., J.R. Lawal, A.M. Bello, Y. Wakil, U.A. Turaki and I. Waziri. 2016. Risk factors associated with the occurrence of gastrointestinal helminths among indigenous donkeys (Equus asinus) in Northeastern Nigeria. Sci. Article ID 3735210,

Khalifa, R., M.E. Monib and A.M. Mandour. 1988. A study of parasites infecting equines in Assist Governorate. Assiat Vet. Med. J. 20(40): 68.

Kyewalabye, KE., H.D. Kwari, M.O. Ajayi and P. Shingu. 1988. Clinical parameters of donkeys before and after Trypanosoma vivax. Rev. Ele. Med. Vet. Pays. Trop. 41: 265 −267.

Mekibib, B., M. Manegerew, A. Tadesse, F. Abuna, B. Megersa, A. Regassa, S. Mekuria and R. Abebe. 2009. Prevalence of hemoparasites and associated risk factors in working donkeys in Adigudem and Kwiha districts of Tigray region, Northern Ethiopia. Int. J. Vet. Med. 8(1)

Mezgebu, T., K. Tafesse and F. Tamiru. 2013. Prevalence of gastrointestinal parasites of horses and donkeys in and around Gondar town, Ethiopia. Open J. Vet. Med. 3: 267 −272. https://doi.org/10.4236/ojvm.2013.36043

Murray, M., J.C.M. Trail, D.A. Turner and Y. Wissococq. 1983. Livestock productivity and trypanotolerance. Network training manual, ILCA Addis Ababa Ethiopia. pp. 4 −10.

Onyekwelu, K.C., F.E. Ejezie, A.A. Eze, J.E. Ikekpeazu, R.C. Ezeh and G.C. Edeh. Prevalence of trypanosome infection in tsetse flies from Oji River and Emene axis of Enugu State, Nigeria: a preliminary report. Trop Parasitol. 7(2): 98 −102.

Pam, V.A., K.I. Ogbu, C.P. Igeh, C.J. Bot and G. Vincent. 2013. Prevalence of endoparasites of horses in Jos North and Jos South Local Government areas of Plateau State Nigeria. J. Anim. Sci. Adv. 3(2): 103 −108. https://doi.org/10.5455/jasa.20130226011052

Pearson, R.A., E. Nemgomasha and R. Krecek. 1999. The challenges in using donkeys for work in Africa. In meeting the challenges of animal traction. A resource book of the animal traction network for eastern and Southern Africa (ATNESA), Harare, Zimbabwe. Int. Technol. Publ. London. p. 326.

Polidori, P., C. Carallucci, D. Beghellic and S. Vincenzetti. 2009. Physical and chemical characteristics of donkey meat from Martina Franca breed. Meat Sci. 82(4): 469 −471. https://doi.org/10.1016/j.meatsci.2009.03.001

Radostits, O.M., C.C. Gay, K.W. Hincnchiff and P.D. Constaple. 2007. Veterinary medicine, a text book of the disease of cattle, sheep pigs, goats and horses. 10th edition-W. B. Sounders company Ltd London UK.

Regassa, A. and E. Yimer. 2013. Gastrointestinal parasites of equines in South Wollo Zone, North Eastern Ethiopia. Glob. Vet. (11): 824 −830.

Saul, C.L., L. Siefert and I. Opuda-asibo. 1997. Disease and health problems of donkeys: a case Study from Eastern Uganda. Workshop on animal traction network for eastern and southern Africa (ATNESA) in Debre, Ethiopia.

Sawsan, M.A.I., T. Hassan, H.I. Seri and B.Z. Hidaia. 2008. Field investigation of gastro-intestinal nematodes in horses and donkeys in South Darfur State, Sudan. 13th Sci. Congr. pp. 723 −729.

Soulbby, E.J.L. 1982. Helminthes, arithropods and protozoa of domesticated animals. 7th edition- Bailliere Tindall, London, UK.

Starkey, P. and M. Starkey. 2004. Regional and world trends in donkeys’ populations. A resource book of the animal traction network for eastern and southern Africa. In: Starkey, P. and fielding, D. (eds.). ACD-EU technical centre- for agricultural and rural cooperation (CTA), Wageningen, -Netherlands. pp. 10 −21.

Sugun, M.Y., F. Bresibe, S. Mailafiya, M. Muhammad, I. Suleiman and A.S. Abechi. 2015. Prevalence of gastrointestinal parasites in donkeys in and around Maiduguri metropolis Borno State, Nigeria. Direct Res. J. Agric. Food Sci. 3(4): 70 −73.

Taylor, M.A., R.L. Coop and R.L. Wall. 2007. Veterinary parasitology third edition Wiley-Blackwell publishing company. pp. 259 −314.

Tefera M, A. Worku, T. Tolosa, and M. Bitew. 2011. Prevalence and risk factors for donkey babesiosis in and around Debre Zeit, Central Ethiopia. Vet. Res. 4:56–60.

Tesfu, N., B. Asrade, R. Abebe and S. Kasaye. 2014. Prevalence and risk factors of gastroinestinal nematode parasites of horse and donkeys in Hawassa Town, school of veterinary medicine Hawassa university. J. Vet. Sci. Technol. 5: 5.

Tolossa, H.Y. and H. Ashenafi. 2013. Epidemiological study on gastrointestinal helminths of horses in Arsi-bale highlands of Oromiya region, Ethiopia, Addis Ababa Univ. Coll. Vet. Med. Agric. Ethiop Vet. J. 17(2): 51 −62.

Tsegaye, B. and A. Chala. 2015. Prevalence of endoparasitic helminths of donkeys in and around Haramaya district, Eastern Ethiopia. J. Vet. Med. Anim. Health. 7(6): 221 −224. https://doi.org/10.5897/JVMAH2015.0383

Uilenberg, G. 1998. A field guide for the diagnosis, treatment and prevention of African animal trypanosomosis. Food Agric. Organ. UN (FAO), Rome, Italy.

Urquhart, G.M., J. Armour, A.M. Dunn and F.W. Jennings. 2003. Veterinary parasitology.3rd Blackwell science ltd: Univ. Glasgow, Scotland edition. pp: 4 −78.

Woo, P.T.K. 1969. The haematocrit centrifuge for the detection of trypanosomes in blood. Can. J. Zool. 47: 921-923

Worku, S. and B. Afera. 2012. Prevalence of equine nematodes in and around Kombolcha, South Wollo-Ethiopia. Rev. Elect. De. Vet. 13: 1 −13.

Yoseph, S., G. Feseha and W. Abebe. 2001. Survey on helinthosis of eqines in Wonchi, Ethiopia, J. Ethiop Vet. Assoc. 5: 47 −61.

Zerihun, A., K. Bersisa, E. Bojia, G. Ayele, M. Tesfaye and D. Elana. 2011. Endoparasites of donkeys in sululta and gefersa districts of central Oromia, Ethiopia. J. Anim. Vet. Adv. 10(14): 1850 −1854. https://doi.org/10.3923/javaa.2011.1850.1854