Geographic distribution of non-clinical Theileria parva infection among indigenous cattle populations in contrasting agro-ecological zones of Uganda: implications for control strategies

Particle and Fibre Toxicology

Riccardo Negrini²  Halid Kirunda¹  Vincent Muwanika³  Charles Masembe⁴  Fredrick Kabi¹ 

[1] National Livestock Resources Research Institute (NaLIRRI), P.O. Box 96 Tororo, Uganda;Istituto di Zootecnica, Università Cattolica del Sacro Cuore, Institute of Zootechnics, via Emilia Parmense 84, 29122 Piacenza, Italy;Department of Environmental Management, Molecular Genetics Laboratory, College of Agricultural and Environmental Sciences, Makerere University, P.O. Box 7062/7298 Kampala, Uganda;Department of Biological Sciences, College of Natural Sciences, Makerere University, Box 7062 Kampala, Uganda

关键词: Uganda;    Indigenous cattle;    Non-clinical T. parva AEZ gradient;    Endemic stability;    East Coast Fever;    Agro-ecological zones;   

Others  :  1150540
DOI  :  10.1186/1756-3305-7-414

 received in 2014-05-12, accepted in 2014-08-26,  发布年份 2014

【 摘 要 】

Background

Non-clinical Theileria parva infection among indigenous cattle occurs upon recovery from primary disease during the first year of life. Continuous exposure to infection through contaminated tick infestations with absence of clinical disease gives rise to endemic stability. Endemic stable populations may become sources of infection if contaminated tick vectors are shared with susceptible exotic cattle. This study aimed at establishing a nationwide distribution of non-clinical T. parva infection among indigenous cattle populations to inform novel control strategies.

Methods

The occurrence of non-clinical T. parva infection among apparently healthy 925 indigenous cattle from 209 herds spread out in 10 agro-ecological zones (AEZs) was determined using a nested PCR assay. The influence of AEZ, breed, sex, age and farmers’ ranking of ECF importance were interrogated for influence of non-clinical parasite occurrence.

Results

The overall prevalence of non-clinical T. parva infection was 30% (278/925). A gradual increase of non-clinical T. parva infection was observed ranging from 17% (95% CI: 0.03 – 0.23) to 43% (95% CI: 0.3 – 0.55) in the North Eastern Savannah Grasslands (NESG) to the Western Highland Ranges (WHR) respectively. A similarly associated 18% (95% CI: 0.07 – 0.28) and 35% (95% CI: 0.3 – 0.39) non-clinical parasite prevalence was observed among the East African shorthorn Zebu (EASZ) and Ankole cattle respectively. Average herd level non-clinical T. parva prevalence was 28%, ranging from zero to 100%. The likelihood of non-clinical T. parva infection was 35.5% greater in the western highlands compared to the northeastern semi-arid AEZs.

Conclusions

Non-clinical T. parva occurs countrywide, structured along patterns of AEZ and breed gradients. These findings may guide policy formulation, deployment of integrated control strategies and local cattle improvement programs.

【 授权许可】

   
2014 Kabi et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Norval RAI, Perry BD, Young AS, Lawrence JA, Mukhebi AW, Bishop R, McKeever D: The Epidemiology of Theileriosis in Africa. London, UK: Academic Press; 1992.
• [2]Jonsson NN, Bock RE, Jorgensen WK, Morton JM, Stear MJ: Is endemic stability of tick-borne disease in cattle a useful concept? Trends Parasitol 2012, 28(3):85-89.
• [3]Balikowa D: Dairy development in Uganda: A review of Uganda’s dairy industry, Dairy Development Authority (DDA), Uganda. 2011. http://www.fao.org/3/a-aq292e.pdf webcite. [Accessed: 20/2/2014]
• [4]Hanotte O, Bradley DG, Ochieng JW, Verjee Y, Hill EW, Rege JE: African pastoralism: genetic imprints of origins and migrations. Science 2002, 296:336-339.
• [5]Gachohi J, Skilton RA, Hansen F, Ngumi P, Kitala P: Epidemiology of East Coast fever (Theileria parva infection) in Kenya: past, present and the future. Parasit Vectors 2012, 5:194. BioMed Central Full Text
• [6]Lorusso V, Picozzi K, de Bronsvoort BMC, Majekodunmi A, Dongkum C, Balak G, Igweh A, Welburn SC: Ixodid ticks of traditionally managed cattle in central Nigeria: where Rhipicephalus (Boophilus) microplus does not dare (yet?). Parasit Vectors 2013, 6:171. BioMed Central Full Text
• [7]Delgado C: Rising consumption of meat and milk in developing countries has created a new food revolution. J Nutrition 2003, 133:3907S-3910S.
• [8]Fitzpatrick JL: Global food security: the impact of veterinary parasites and parasitologists. Vet Parasitol 2013, 195:233-248.
• [9]MAAIF: Agriculture for food and income security, agriculture sector development strategy and investment plan: 2010/11-2014/15. 2010. http://www.agriculture.go.ug/userfiles/AgriculturalSectorDevelopmentStrategyandInvestmentPlan29.pdf webcite. [Accessed 20/2/2014]
• [10]Minjauw B, McLeod A: Tick-borne diseases and poverty. The impact of ticks and tick-borne diseases on the livelihood of small-scale and marginal livestock owners in India and eastern and southern Africa. UK: Research report, DFID Animal Health Programme. University of Edinburgh: Centre for Tropical Veterinary Medicine; 2003.
• [11]Rubaire-Akiiki CM, Okello-Onen J, Musunga D, Kabagambe EK, Vaarst M, Okello D, Opolot C, Bisagaya A, Okori C, Bisagati C, Ongyera S, Mwayi MT: Effect of agro-ecological zone and grazing system on incidence of East Coast Fever in calves in Mbale and Sironko Districts of Eastern Uganda. Prev Vet Med 2006, 75(3–4):251-266.
• [12]Asiimwe BB, Weir W, Tait A, Lubega GW, Oura CAL: Haemoparasite infection kinetics and the population structure of Theileria parva on a single farm in Uganda. Vet Parasitol 2013, 193:8-4.
• [13]Olwoch JM, Reyers B, van Jaarsveld AS: Host-parasite distribution patterns under simulated climate:implications for tick-borne diseases. Int J Climatol 2009, 29:993-1000.
• [14]Magona JW, Walubengo J, Kabi F: Response of Nkedi Zebu and Ankole cattle to tick infestation and natural tick-borne, helminth and trypanosome infections in Uganda. Trop Anim Health Prod 2011, 43:1019-1033.
• [15]Mugabi K, McLoed A, Ocaido M: Socio-economic factors influencing the use of acaricides on livestock: a case study of the pastoralist communities of Nakasongola District, Central Uganda. Trop Anim Health Prod 2010, 42:131-136.
• [16]Magona JW, Walubengo J, Olaho-Mukani W, Jonsson NN, Welburn SC, Eisler MC: Spatial variation of tick abundance and seroconversion rates of indigenous cattle to Anaplasma marginale, Babesia bigemina and Theileria parva infections in Uganda. Exp Appl Acarol 2011, 55(2):203-213.
• [17]Magona JW, Walubengo J, Olaho-Mukani W, Jonsson NN, Welburn SC, Eisler MC: Clinical features associated with seroconversion to Anaplasma marginale, Babesia bigemina and Theileria parva infections in African cattle under natural tick challenge. Vet Parasitol 2008, 155(3–4):273-280.
• [18]Okello-Onen J, Tukahirwa EM, Perry BD, Rowlands GJ, Nagda SN, Musisi G, Bode E, Heinonen R, Mwayi W, Opuda-Asibo J: The impact of tick control on the productivity of indigenous cattle under ranch conditions in Uganda. Trop Anim Health Prod 2003, 35(3):237-247.
• [19]Mugisha A, McLeod A, Percy R: Socio-economic factors influencing control of vector-borne diseases in the pastoralist system of south-western Uganda. Trop Anim Health Prod 2008, 40:287-297.
• [20]Bardosh K, Waiswa C, Welburn SC: Conflict of interest: use of pyrethroids and amidines against tsetse and ticks in zoonotic sleeping sickness endemic areas of Uganda. Parasit Vectors 2013, 6:204. BioMed Central Full Text
• [21]Marcelino I, De Almeida M, Ventosa M, Pruneaus L, Meyer DF, Martinez D, Lefrancois T, Vachiery N, Coelho AV: Tick-borne diseases in cattle: applications of proteomics to develop new generation vaccines. J Proteom 2012, 75:4232-4250.
• [22]Rodriguez-Vivas RI, Trees AJ, Rosado-Aguilar JA, Villegas-Perez SL, Hodgkinson JE: Evolution of acaricide resistance: phenotypic and genotypic changes in field populations of Rhipicephalus (Boophilus) microplus in response to pyrethroid selection pressure. Int J Parasit 2011, 41:895-903.
• [23]Livestock keepers. Guardians of biodiversity. FAO Animal Production and Health Paper No. 167; 2009:59. ISBN: 978-92-5-106369-9. 2009, http://www.fao.org/docrep/012/i1034e/i1034e00.htm webcite [Accessed: 20/2/2014]
• [24]Ndumu DB, Baumung R, Wurzinger M, Drucker AG, Okeyo AM, Semambo D, Sölkner J: Performance and fitness traits versus phenotypic appearance in the African Ankole Longhorn cattle: A novel approach to identify selection criteria for indigenous breeds. Livest Sci 2008, 113:234-242.
• [25]Kugonza DR, Nabasirye M, Hanotte O, Mpairwe D, Okeyo AM: Pastoralists’ indigenous selection criteria and other breeding practices of the long-horned Ankole cattle in Uganda. Trop Anim Health Prod 2012, 44(3):557-565.
• [26]Hoffmann I: Livestock biodiversity and sustainability. Livest Sci 2011, 139:69-79.
• [27]LPP, LIFE Network, IUCN–WISP and FAO: Adding Value to Livestock Diversity- Marketing to promote local breeds and improve livelihoods. Rome: FAO Animal Production and Health Paper. No. 168; 2010:142. ISBN 978-92-5-106453-5. http://www.fao.org/docrep/012/i1283e/i1283e.pdf webcite. [Accessed: 20/2/2014]
• [28]Eisler MC, Lee MRF, Tarlton JF, Martin GB, Beddington J, Dungait JAJ, Greathead H, Liu J, Mathew S, Miller H, Misselbrook T, Murray P, Vinod KV, Van Saun R, Winter M: Agriculture: steps to sustainable livestock. Nature 2014, 507(7490):32-34.
• [29]Morzaria S, Nene V, Bishop R, Musoke A: Vaccines against Theileria parva. Ann NY Acad Sci 2000, 916:464-473.
• [30]Di Giulio G, Lynen G, Morzaria S, Oura C, Bishop R: Live immunization against East Coast fever - current status. Trends Parasitol 2009, 25:85-92.
• [31]Lathers CM: Role of veterinary medicine in public health: antibiotic use in food animals and humans and the effect on evolution of antibacterial resistance. J Clin Pharmacol 2001, 41:595-599.
• [32]Babiuk LA: Vaccination: a management tool in veterinary medicine. Vet J 2002, 164:188-201.
• [33]Vercruysse J, Schetters TPM, Knox DP, Willadsen P, Claerebout E: Control of parasitic disease using vaccines: an answer to drug resistance? Rev sci tech Off int Epiz 2007, 26(1):105-115.
• [34]Estrada-Peña A, Salman M: Current limitations in the control and spread of ticks that affect livestock. Agric 2013, 3:221-235.
• [35]Mondal DB, Sarma K, Saravanan M: Upcoming of the integrated tick control program of ruminants with special emphasis on livestock farming system in India. Ticks Tick Borne Dis 2013, 4:1-10.
• [36]Bazarusanga T, Vercruysse J, Marcotty T, Geysen D: Epidemiological studies on Theileriosis and the dynamics of Theileria parva infections in Rwanda. Vet Parasitol 2007, 143:214-221.
• [37]Van den Bossche P, Coetzer JA: Climate change and animal health in Africa. Rev sci tech Off int Epiz 2008, 27(2):551-562.
• [38]Githeko Andrew K, Lindsay Steve W, Confalonieri UE, Patz Jonathan A: Climate change and vector-borne diseases: a regional analysis. Bull World Health Org 2000, 78(9):1136-1147.
• [39]Odongo DO, Sunter JD, Kiara HK, Skilton RA, Bishop RP: A nested PCR assay exhibits enhanced sensitivity for detection of Theileria parva infections in bovine blood samples from carrier animals. Parasitol Res 2010, 106:357-365.
• [40]UBOS: Statistical Abstract. In Main Report. Kampala: Uganda Population and Housing Census; 2013.
• [41]Ministry of Agriculture, Animal Industry and Fisheries (MAAIF) and Ministry of Finance, Planning and Economic Development (MFPED). Increasing incomes through exports: a plan for zonal agricultural production, agro-processing and marketing. Entebbe, Uganda; 2004. http://www.foodnet.cgiar.org/scrip/docs%26databases/ifpristudies_ug_nonscrip/pdfs/Government_of_Uganda/Plan_for_zonal_ag_production_processing_and_marketing.pdf webcite [Accessed: 20/2/2014]
• [42]Thrusfield M: Veterinary Epidemiology. 3rd edition. Oxford: Blackwell Science; 2003.
• [43]NextGen: Next generation methods to preserve farm animal biodiversity by optimizing present and future breeding options. 2010. http://www.nextgen.epfl.ch/page-64067.html;jsessionid=D4367339C598E0F3A02E7C45F2D845E9 webcite [accessed 8/8/2014]
• [44]Muhanguzi D, Picozzi K, Hatendorf J, Thrusfield M, Welburn SC, Kabasa JD, Waiswa C: Prevalence and spatial distribution of Theileria parva in cattle under crop-livestock farming systems in Tororo District, Eastern Uganda. Parasit Vectors 2014, 7:91. BioMed Central Full Text
• [45]Ocaido M, Muwazi R, Opuda-Asibo J: Disease incidence in ranch and pastoral livestock herds around Lake Mburo National Park, in South Western Uganda. Trop Anim Health Prod 2009, 41:1299-1308.
• [46]Nalule S: Social Management of Rangelands and Settlement in Karamoja. FAO: Kampala; 2010.
• [47]Wurzinger M, Ndumu D, Baumung R, Drucker A, Okeyo AM, Semambo DK, Byamungu N, Sölkner J: Comparison of production systems and selection criteria of Ankole cattle by breeders in Burundi, Rwanda, Tanzania and Uganda. Trop Anim Health Prod 2006, 38:571-581.