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Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year

  • S. M. THUMBI (a1), B. M. de. C. BRONSVOORT (a2), E. J. POOLE (a3), H. KIARA (a3), P. TOYE (a3), M. NDILA (a3), I. CONRADIE (a4), A. JENNINGS (a2), I. G. HANDEL (a2), J. A. W. COETZER (a4), O. HANOTTE (a5) and M. E. J. WOOLHOUSE (a1)...


The co-occurrence of different pathogen species and their simultaneous infection of hosts are common, and may affect host health outcomes. Co-infecting pathogens may interact synergistically (harming the host more) or antagonistically (harming the host less) compared with single infections. Here we have tested associations of infections and their co-infections with variation in growth rate using a subset of 455 animals of the Infectious Diseases of East Africa Livestock (IDEAL) cohort study surviving to one year. Data on live body weight, infections with helminth parasites and haemoparasites were collected every 5 weeks during the first year of life. Growth of zebu cattle during the first year of life was best described by a linear growth function. A large variation in daily weight gain with a range of 0·03–0·34 kg, and a mean of 0·135 kg (0·124, 0·146; 95% CI) was observed. After controlling for other significant covariates in mixed effects statistical models, the results revealed synergistic interactions (lower growth rates) with Theileria parva and Anaplasma marginale co-infections, and antagonistic interactions (relatively higher growth rates) with T. parva and Theileria mutans co-infections, compared with infections with T. parva only. Additionally, helminth infections can have a strong negative effect on the growth rates but this is burden-dependent, accounting for up to 30% decrease in growth rate in heavily infected animals. These findings present evidence of pathogen–pathogen interactions affecting host growth, and we discuss possible mechanisms that may explain observed directions of interactions as well as possible modifications to disease control strategies when co-infections are present.

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The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution licence .

Corresponding author

*Corresponding author: Centre for Infectious Diseases, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK. E-mail:


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Blanco, J. L. and Garcia, M. E. (2008). Immune response to fungal infections. Veterinary Immunology and Immunopathology 125, 4770.
Boag, B., Lello, J., Fenton, A., Tompkins, D. M. and Hudson, P. J. (2001). Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 14211428.
Brocklesby, D. W., Sellwood, S. A. and Harness, E. (1972). Some characteristics of a strain of Theileria mutans (Theiler, 1906) isolated from cattle in the county of Kent, England, and maintained in splenectomized calves. International Journal for Parasitology 2, 265271.
Bronsvoort, B. M. D. C., Thumbi, S., Poole, J., Kiara, H., Tosas-Auguet, O., Handel, I., Jennings, A., Conradie, I., Toye, P., Hanotte, O., Coetzer, K. and Woolhouse, M. E. J. (in press). Design and Descriptive epidemiology of the Infectious Diseases of East African Livestock (IDEAL) project, a longitudinal calf cohort study in western Kenya. BMC Veterinary Research.
Coetzer, J. and Tustin, R. (ed.) (2004). Infectious Diseases of Livestock, 2nd Edn.Oxford University Press, Oxford, UK.
Conlan, J. V., Vongxay, K., Fenwick, S., Blacksell, S. D. and Thompson, R. C. A. (2009). Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia? Trends in Parasitology 25, 398403.
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl), S23S38.
Craig, B. H., Tempest, L. J., Pilkington, J. G. and Pemberton, J. M. (2008). Metazoan–protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433441.
Diggle, P. J., Heagerty, P. J., Liang, K. Y. and Zeger, S. L. (2003). Analysis of Longitudinal Data. Oxford University Press, Oxford, UK.
Food and Agriculture Organization (FAO). (2007). The State of the World's Animal Genetic Resources for Food and Agriculture (ed. Rischkowsky, B. and Pilling, D.). FAO, Rome, Italy.
Fenton, A. and Perkins, S. E. (2010). Applying predator–prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137, 10271038.
Gachohi, J. M., Ngumi, P. N., Kitala, P. M. and Skilton, R. A. (2010). Estimating seroprevalence and variation to four tick-borne infections and determination of associated risk factors in cattle under traditional mixed farming system in Mbeere District, Kenya. Preventive Veterinary Medicine 95, 208223.
Gitau, G. K., Mcdermott, J. J., McDermott, B. and Perry, B. D. (2001). The impact of Theileria parva infections and other factors on calf mean daily weight gains in smallholder dairy farms in Murang'a District, Kenya. Preventive Veterinary Medicine 51, 149160.
Graham, A. L. (2008). Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences USA 105, 566570.
Gröhn, Y. T., Mcdermott, J. J., Schukken, Y. H., Hertl, J. A. and Eicker, S. W. (1999). Analysis of correlated continuous repeated observations: modelling the effect of ketosis on milk yield in dairy cows. Preventive Veterinary Medicine 39, 137153.
Hansen, J. and Perry, B. (1994). The Epidemiology, Diagnosis and Control of Helminth Parasites of Ruminants, A Handbook, 2nd Edn. ILRAD, Nairobi, Kenya.
Heinrichs, A. and Radostits, O. (2001). Health and production management of dairy calves and replacement heifers. In Herd Health, Food Animal Production Medicine, 3rd Edn (ed. Radostits, O.), pp. 333395. W.B. Saunders, Philadelphia, PA, USA.
Katende, J., Morzaria, S., Toye, P., Skilton, R., Nene, V., Nkonge, C. and Musoke, A. (1998). An enzyme-linked immunosorbent assay for detection of Theileria parva antibodies in cattle using a recombinant polymorphic immunodominant molecule. Parasitology Research 84, 408416.
Kocan, K. M., De La Fuente, J., Blouin, E. F., Coetzee, J. F. and Ewing, S. A. (2010). The natural history of Anaplasma marginale. Veterinary Parasitology 167, 95107.
Kristjanson, P., Krishna, A., Radeny, M. and Nindo, W. (2004). Pathways out of Poverty in Western Kenya and the Role of Livestock. FAO, Rome, Italy.
Lafferty, K. D. (2010). Microbiology. Interacting parasites. Science (New York, NY) 330, 187188.
Latif, A., Rowlands, G. and Punyua, D. (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. Elsevier, Amsterdam, the Netherlands.
Lello, J. and Hussell, T. (2008). Functional group/guild modelling of inter-specific pathogen interactions: a potential tool for predicting the consequences of co-infection. Parasitology 135, 825839.
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840844.
McHardy, N. and Kiara, H. (1995). Super-infection with Theileria parva in calves previously infected with Babesia bigemina or Anaplasma marginale. In International Conference on Tick-borne Pathogens, Kruger National Park (South Africa), 28 August–1 September 1995.
Moll, G., Lohding, A., Young, A. S. and Leitch, B. L. (1986). Epidemiology of theileriosis in calves in an endemic area of Kenya. Veterinary Parasitology 19, 255273. Elsevier, Amsterdam, the Netherlands.
Morzaria, S. P., Katende, J., Musoke, A., Nene, V., Skilton, R. and Bishop, R. (1999). Development of sero-diagnostic and molecular tools for the control of important tick-borne pathogens of cattle in Africa. Parassitologia 41(Suppl 1), 7380.
Murray, M., Murray, P. K. and Mcintyre, W. I. (1977). An improved parasitological technique for the diagnosis of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 325326.
Musoke, A., Nantulya, V. and Rurangirwa, F. (1984). Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52, 231238.
Ndungu, S. G., Ngumi, P. N., Mbogo, S. K., Dolan, T. T., Mutugi, J. J. and Young, A. S. (2005). Some preliminary observations on the susceptibility and resistance of different cattle breeds to Theileria parva infection. Onderstepoort Journal of Veterinary Research 72, 711.
Ogden, N. H., Swai, E., Beauchamp, G., Karimuribo, E., Fitzpatrick, J. L., Bryant, M. J., Kambarage, D. and French, N. P. (2005). Risk factors for tick attachment to smallholder dairy cattle in Tanzania. Preventive Veterinary Medicine 67, 157170.
OIE. (2008). Manual of diagnostic tests And vaccines For terrestrial animals, 6th Edn., p. 1343. Office International des Epizooties, Paris, France.
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133139.
Perry, B. (2002). Investing in Animal Health Research to Alleviate Poverty. International Livestock Research Institute, Nairobi, Kenya.
Perry, B. (2007). Poverty reduction through animal health. Science (USA) 315, 333334.
Pinheiro, J. and Bates, D. (2000). Mixed Effects Models in S and S-Plus. Springer-Verlag, NewYork.
R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3900051070 URL
Stachurski, F., Musonge, E. N., Achu-Kwi, M. D. and Saliki, J. T. (1993). Impact of natural infestation of Amblyomma variegatum on the liveweight gain of male Gudali cattle in Adamawa (Cameroon). Veterinary Parasitology 49, 299311.
Swai, E. S., Karimuribo, E. D., Kambarage, D. M. and Moshy, W. E. (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.
Tarawali, S., Herrero, M., Descheemaeker, K., Grings, E. and Blümmel, M. (2011). Pathways for sustainable development of mixed crop livestock systems: taking a livestock and pro-poor approach. Livestock Science 139, 1121.
Tebele, N., Skilton, R. A., Katende, J., Wells, C. W., Nene, V., Mcelwain, T., Morzaria, S. P. and Musoke, A. J. (2000). Cloning, characterization, and expression of a 200-kilodalton diagnostic antigen of Babesia bigemina. Journal of Cinical Microbiology 38, 22402247.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science (New York, N.Y.) 330, 243246.
Tomley, F. M. and Shirley, M. W. (2009). Livestock infectious diseases and zoonoses. Philosophical Transactions of the Royal Society of London 364, 26372642.
Walker, A., Bouattour, A., Camicas, L., Estrada-Pena, A., Horak, I., Latif, A., Pegram, R. and Preston, P. (2003). Ticks of Domestic Animals in Africa: a Guide to Identification of Species. Bioscience Reports, Edinburgh, UK.
Weir, J. P. (2005). Quantifying test–retest reliability using the intraclass correlation coefficient and the SEM. Journal of Strength and Conditioning Research 19, 231240.
Willett, J. (1997). Measuring change: what individual growth modeling buys you. In Change and Development: Issues of Theory, Method and Application (ed. Amsel, E. and Renninger, K. A.), pp. 213243. Lawrence Erlbaum Associates, Mahwah, NJ, USA.
Woo, P. T. (1970). The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Tropica 27, 384386.


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