Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T16:44:09.626Z Has data issue: false hasContentIssue false

Associations between monthly rainfall and mortality in cattle due to East Coast fever, anaplasmosis and babesiosis

Published online by Cambridge University Press:  10 September 2020

Richard Chepkwony*
Affiliation:
Kenya Wildlife Service, P.O. Box 40241-00100, Nairobi, Kenya Wageningen University, Wildlife Ecology and Conservation Group, P.O. Box 47, 6700 AA, Wageningen, The Netherlands Wageningen University, Strategic Communications Group, P.O. Box 8130, 6700 EW, Wageningen, The Netherlands
Carolina Castagna
Affiliation:
Wageningen University, Wildlife Ecology and Conservation Group, P.O. Box 47, 6700 AA, Wageningen, The Netherlands
Ignas Heitkönig
Affiliation:
Wageningen University, Wildlife Ecology and Conservation Group, P.O. Box 47, 6700 AA, Wageningen, The Netherlands
Severine van Bommel
Affiliation:
Wageningen University, Strategic Communications Group, P.O. Box 8130, 6700 EW, Wageningen, The Netherlands University of Queensland, School of Agriculture and Food Sciences, Gatton, QLD4343, Australia
Frank van Langevelde
Affiliation:
Wageningen University, Wildlife Ecology and Conservation Group, P.O. Box 47, 6700 AA, Wageningen, The Netherlands School of Life Sciences, Westville Campus, University of KwaZulu-Natal, Durban4000, South Africa
*
Author for correspondence: Richard Chepkwony, E-mail: [email protected]

Abstract

Weather conditions can impact infectious disease transmission, causing mortalities in humans, wild and domestic animals. Although rainfall in dry tropical regions is highly variable over the year, rainfall is thought to play an important role in the transmission of tick-borne diseases. Whether variation in rainfall affects disease-induced mortalities, is, however, poorly understood. Here, we use long-term data on monthly rainfall and Boran cattle mortality (1998–2017) to investigate associations between within-year variation in rainfall and cattle mortalities due to East Coast fever (ECF), anaplasmosis and babesiosis in Laikipia, Kenya, using ARIMAX modelling. Results show a negative correlation between monthly rainfall and cattle mortality for ECF and anaplasmosis, with a lag effect of 2 and 6 months, respectively. There was no association between babesiosis-induced mortalities and monthly rainfall. The results of this study suggest that control of the tick-borne diseases ECF and anaplasmosis to reduce mortalities should be intensified during rainy periods after the respective estimated time lags following dry periods.

Type
Research Article
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

Allan, BF, Tallis, H, Chaplin-Kramer, R, Huckett, S, Kowal, VA, Musengezi, J, Okanga, S, Ostfeld, RS, Schieltz, J and Warui, CM (2017) Can integrating wildlife and livestock enhance ecosystem services in central Kenya? Frontiers in Ecology and the Environment 15, 328335.CrossRefGoogle Scholar
Anyamba, A, Chretien, J-P, Small, J, Tucker, CJ, Formenty, PB, Richardson, JH, Britch, SC, Schnabel, DC, Erickson, RL and Linthicum, KJ (2009) Prediction of a Rift Valley fever outbreak. Proceedings of the National Academy of Sciences 106, 955959.CrossRefGoogle ScholarPubMed
Awa, D, Adakal, H, Luogbou, N, Wachong, K, Leinyuy, I and Achukwi, M (2015) Cattle ticks in Cameroon: is Rhipicephalus (Boophilus) microplus absent in Cameroon and the Central African region? Ticks and Tick-Borne Diseases 6, 117122.CrossRefGoogle ScholarPubMed
Bi, P, Zhang, Y and Parton, KA (2007) Weather variables and Japanese encephalitis in the metropolitan area of Jinan City, China. Journal of Infection 55, 551556.CrossRefGoogle ScholarPubMed
Brocklesby, D (1962) The febrile reaction in fatal East Coast fever – A review of 150 cases. Bulletin of Epizootic Diseases of Africa 10, 4954.Google Scholar
Brown, I, Mulatti, P, Smietanka, K, Staubach, C, Willeberg, P, Adlhoch, C, Candiani, D, Fabris, C, Zancanaro, G and Morgado, J (2017) Avian influenza overview October 2016–August 2017. EFSA Journal 15, e05018.Google ScholarPubMed
Chepkwony, R, Van Bommel, S and Van Langevelde, F (2018) Citizen science for development: potential role of mobile phones in information sharing on ticks and tick-borne diseases in Laikipia, Kenya. NJAS – Wageningen Journal of Life Sciences 86–87, 123135.CrossRefGoogle Scholar
Clement, EP (2014) Using normalized Bayesian information criterion (BIC) to improve box-Jenkins model building. American Journal of Mathematics and Statistics 4, 214221.Google Scholar
Cumming, GS (2002) Comparing climate and vegetation as limiting factors for species ranges of African ticks. Ecology 83, 255268.CrossRefGoogle Scholar
Dantas-Torres, F (2015) Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect. International Journal for Parasitology: Parasites and Wildlife 4, 452461.Google Scholar
de Sousa, R, Luz, T, Parreira, P, Santos-Silva, M and Bacellar, F (2006) Boutonneuse fever and climate variability. Annals of the New York Academy of Sciences 1078, 162169.CrossRefGoogle ScholarPubMed
Fischhoff, IR, Sundaresan, SR, Cordingley, J and Rubenstein, DI (2007) Habitat use and movements of plains zebra (Equus burchelli) in response to predation danger from lions. Behavioral Ecology 18, 725729.Google Scholar
Fouque, F and Reeder, JC (2019) Impact of past and on-going changes on climate and weather on vector-borne diseases transmission: a look at the evidence. Infectious Diseases of Poverty 8, 19.CrossRefGoogle Scholar
Fyumagwa, RD, Runyoro, V, Horak, IG and Hoare, R (2007) Ecology and control of ticks as disease vectors in wildlife of the Ngorongoro Crater, Tanzania. South African Journal of Wildlife Research 37, 7990.CrossRefGoogle Scholar
Gachohi, J, Skilton, R, Hansen, F, Ngumi, P and Kitala, P (2012) Epidemiology of East Coast fever (Theileria parva infection) in Kenya: past, present and the future. Parasites & Vectors 5, 194.Google ScholarPubMed
Gaur, AS and Gaur, SS (2006) Statistical Methods for Practice and Research: A Guide to Data Analysis Using SPSS. Newbury Park, California: Sage Publications Inc.Google Scholar
Geweke, J and Porter-Hudak, S (1983) The estimation and application of long memory time series models. Journal of Time Series Analysis 4, 221238.CrossRefGoogle Scholar
Government of Kenya (2016) Laikipia County Integrated Development Plan (CIDP). Available at https://africaopendata.org/dataset/2013-2017-laikipia-county-integrated-development-plan-cidp.Google Scholar
Gubler, DJ, Reiter, P, Ebi, KL, Yap, W, Nasci, R and Patz, JA (2001) Climate variability and change in the United States: potential impacts on vector-and rodent-borne diseases. Environmental health perspectives 109, 223233.Google ScholarPubMed
Hechemy, KE, Oteo, JA, Raoult, D, Silverman, DJ and Blanco, JR (2006) A century of rickettsiology: emerging, reemerging rickettsioses, clinical, epidemiologic, and molecular diagnostic aspects and emerging veterinary rickettsioses: an overview. Annals of the New York Academy of Sciences 1078, 114.CrossRefGoogle ScholarPubMed
Heuer, C, Boehle, W, Rutagwenda, T, Jongejan, F, Unger, F, Kivaria, FM and Okello-Onen, J (2004) Endemic stability for Theileria parva infections in Ankole calves of the Ankole ranching scheme, Uganda. Onderstepoort Journal of Veterinary Research 71, 189195.Google Scholar
Huang, S-J and Shih, K-R (2003) Short-term load forecasting via ARMA Model identification including non-Gaussian process considerations. IEEE Transactions on Power Systems 18, 673679.CrossRefGoogle Scholar
Jongejan, F and Uilenberg, G (2004) The global importance of ticks. Parasitology 129, S3.CrossRefGoogle ScholarPubMed
Kanyari, P and Kagira, J (2000) The role of parasitic diseases as causes of mortality in cattle in a high potential area of central Kenya: a quantitative analysis. The Onderstepoort Journal of Veterinary Research 67, 157161.Google Scholar
Keeling, MJ and Rohani, P (2008) Modeling infectious diseases in humans and animals. Clinical Infectious Diseases 47, 864865.CrossRefGoogle Scholar
Keesing, F, Allan, BF, Young, TP and Ostfeld, RS (2013) Effects of wildlife and cattle on tick abundance in central Kenya. Ecological Applications 23, 14101418.CrossRefGoogle ScholarPubMed
Kocan, KM, De la Fuente, J, Guglielmone, AA and Meléndez, RD (2003) Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clinical Microbiology Reviews 16, 698712.CrossRefGoogle ScholarPubMed
Kołodziej-Sobocińska, M (2019) Factors affecting the spread of parasites in populations of wild European terrestrial mammals. Mammal Research 64, 301318.CrossRefGoogle Scholar
Laisser, ELK, Chenyambuga, SW, Msalya, G, Kipanyula, MJ, Mdegela, RH, Karimuribo, ED, Mwilawa, AJ and Kusiluka, LJK (2015) Knowledge and perception on ticks, tick-borne diseases and indigenous cattle tolerance to East Coast fever in agro-pastoral communities of Lake Zone in Tanzania. Livestock Research for Rural Development 27, Article 64. Retrieved September 15, 2020, from http://www.lrrd.org/lrrd27/4/lais27064.htmGoogle Scholar
Latif, AA, Rowlands, GJ, Punyua, DK, Hassan, SM and Capstick, PB (1995) An epidemiological study of tick-borne diseases and their effects on productivity of zebu cattle under traditional management on Rusinga Island, western Kenya. Preventive Veterinary Medicine 22, 169181.CrossRefGoogle Scholar
Lwande, OW, Paul, GO, Chiyo, PI, Ng'ang’a, E, Otieno, V, Obanda, V and Evander, M (2015) Spatio-temporal variation in prevalence of Rift Valley fever: a post-epidemic serum survey in cattle and wildlife in Kenya. Infection Ecology & Epidemiology 5, 30106.CrossRefGoogle ScholarPubMed
Maloo, SH (1993) Epidemiological Studies of Vector-Borne Diseases with Consequent Development of Preventive Medicine Programmes for Small-Holder Dairy Farmers in Coastal Kenya (PhD thesis). The University of Glasgow.Google Scholar
McCulloch, B, Kalaye, WJ, Tungaraza, R and Mbasha, EMS (1968) A study of the life history of the tick Rhipicephalus appendiculatus the main vector of East Goast fever-with reference to its behaviour under field conditions and with regard to its control in Sukumaland, Tanzania. Bulletin of Epizootic Diseases of Africa 16, 477500.Google Scholar
Monamele, GC, Vernet, MA, Nsaibirni, R, Bigna, JJR, Kenmoe, S, Njankouo, MR and Njouom, R (2017) Associations between meteorological parameters and influenza activity in a subtropical country: Case of five sentinel sites in Yaounde-Cameroon. PloS one 12, e0186914.CrossRefGoogle Scholar
Mwamuye, MM, Kariuki, E, Omondi, D, Kabii, J, Odongo, D, Masiga, D and Villinger, J (2016) Occurrence of novel and emergent tick-borne pathogens in a Kenyan biodiversity hotspot. International Journal of Infectious Diseases 45, 350.CrossRefGoogle Scholar
Norval, RAI, Sutherst, RW, Kurki, J, Gibson, JD and Kerr, JD (1988) The effect of the brown ear-tick Rhipicephalus appendiculatus on the growth of Sanga and European breed cattle. Veterinary Parasitology 30, 149164.CrossRefGoogle ScholarPubMed
Odadi, WO, Karachi, MK, Abdulrazak, SA and Young, TP (2011) African wild ungulates compete with or facilitate cattle depending on season. Science 333, 17531755.CrossRefGoogle ScholarPubMed
Okello-Onen, J, Tukahirwa, EM, Perry, BD, Rowlands, GJ, Nagda, SM, Musisi, G, Bode, E, Heinonen, R, Mwayi, W and Opuda-Asibo, J (1999) Population dynamics of ticks on indigenous cattle in a pastoral dry to semi-arid rangeland zone of Uganda. Experimental & Applied Acarology 23, 7988.CrossRefGoogle Scholar
Pipano, E, Krigel, Y, Markovics, A and Shkap, V (1992) The effect of oxytetracycline treatment on immunity induced by Anaplasma centrale. Veterinary Microbiology 31, 8187.CrossRefGoogle ScholarPubMed
Potkanski, T (1994) Property Concepts, Herding Patterns and Management of Natural Resources among the Ngorongoro and Salei Maasai of Tanzania (No. 6; Pastoral Land Tenure Series). London: International Institute for Environment and Development.Google Scholar
Radley, D, Brown, C, Burridge, M, Cunningham, M, Peirce, M and Purnell, R (1974) East coast fever: quantitative studies of Theileria parva in cattle. Experimental Parasitology 36, 278287.CrossRefGoogle ScholarPubMed
Robson, J, Pedersen, V, Odeke, G, Kamya, E and Brown, C (1977) East coast fever immunisation trials in Uganda: field exposure of zebu cattle immunized with three isolates of Theileria parva. Tropical Animal Health and Production 9, 219231.CrossRefGoogle ScholarPubMed
Rogers, DJ and Randolph, SE (2006) Climate change and vector-borne diseases. Advances in Parasitology 62, 345381.CrossRefGoogle ScholarPubMed
Subak, S (2003) Effects of climate on variability in Lyme disease incidence in the Northeastern United States. American Journal of Epidemiology 157, 531538.CrossRefGoogle ScholarPubMed
Swai, ES, Mtui, PF, Mbise, AN, Kaaya, E, Sanka, P and Loomu, PM (2006) Prevalence of gastro intestinal parasite infections in Maasai cattle in Ngorongoro district, Tanzania. Livestock Research for Rural Development 18, 1827.Google Scholar
Swai, ES, Karimuribo, ED, Kambarage, DM and Moshy, WE (2009) A longitudinal study on morbidity and mortality in youngstock smallholder dairy cattle with special reference to tick borne infections in Tanga region, Tanzania. Veterinary Parasitology 160, 3442.CrossRefGoogle ScholarPubMed
Theiler, A (1911) Further Investigations Into Anaplasmosis of South African Cattle. Pretoria: Government Printer and Stationery Office.Google Scholar
VanderWaal, K, Gilbertson, M, Okanga, S, Allan, BF and Craft, ME (2017) Seasonality and pathogen transmission in pastoral cattle contact networks. Royal Society Open Science 4, 170808.CrossRefGoogle ScholarPubMed
Walker, AR (2011) Eradication and control of livestock ticks: biological, economic and social perspectives. Parasitology 138, 945959.CrossRefGoogle ScholarPubMed
Walker, JG, Klein, EY and Levin, SA (2014) Disease at the wildlife-livestock interface: Acaricide use on domestic cattle does not prevent transmission of a tick-borne pathogen with multiple hosts. Veterinary Parasitology 199, 206214.CrossRefGoogle Scholar
Wangdi, K, Singhasivanon, P, Silawan, T, Lawpoolsri, S, White, NJ and Kaewkungwal, J (2010) Development of temporal modelling for forecasting and prediction of malaria infections using time-series and ARIMAX analyses: a case study in endemic districts of Bhutan. Malaria Journal 9, 251.CrossRefGoogle ScholarPubMed
Wesonga, FD, Orinda, GO, Ngae, GN and Grootenhuis, J (2006) Comparative tick counts on game, cattle and sheep on a working game ranch in Kenya. Tropical Animal Health and Production 38, 3542.CrossRefGoogle ScholarPubMed
Zieger, U, Cauldwell, A and Horak, IG (1998) Dynamics of free-living ixodid ticks on a game ranch in the Central Province, Zambia. The Onderstepoort Journal of Veterinary Research 65, 4959.Google ScholarPubMed