Co-infections determine patterns of mortality in a population exposed to parasite infection

Science Advances

Volumn 1, Issue 2, 2015, Pages

  Woolhouse, Mark E J ^a   Thumbi, Samuel M ^a,b   Jennings, Amy ^c,d   Chase Topping, Margo ^a   Callaby, Rebecca ^a,e   Kiara, Henry ^f   Oosthuizen, Marinda C ^g   Mbole Kariuki, Mary N ^f,h   Conradie, Ilana ^g   Handel, Ian G ^c,d   Poole, E Jane ^f   Njiiri, Evalyne ^f   Collins, Nicola E ^g   Murray, Gemma ^a,l   Tapio, Miika ⁱ   Auguet, Olga Tosas ^a   Weir, Willie ^j   Morrison, W Ivan ^c,d   Kruuk, Loeske E B ^a,k   De Bronsvoort, C B Mark ^c,d   Hanotte, Olivier ^h   Coetzer, Koos ^g   Toye, Philip G ^f   more..

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^f INTERNATIONAL LIVESTOCK RESEARCH INSTITUTE   (Kenya)

^g UNIVERSITY OF PRETORIA   (South Africa)

^h UNIVERSITY OF NOTTINGHAM   (United Kingdom)

ⁱ FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^j UNIVERSITY OF GLASGOW   (United Kingdom)

^k AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^l UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PLANTS (BOTANY);

CO-INFECTIONS; INFECTIOUS DISEASE; PARASITE INFECTION; PATHOGENIC SPECIES; POPULATION LEVELS; QUANTITATIVE ESTIMATES; THEILERIA PARVA; WEAK CORRELATION;

DISEASES;

EID: 84953737172     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1400026     Document Type: Article

References (34)

1. C. Dye, B. G. Williams, The population dynamics and control of tuberculosis. Science 328, 856-861 (2010).
2. A. F. Read, L H. Taylor, The ecology of genetically diverse infections. Science 292,1099-1102 (2001).
3. J. Lello, B. Boag, A. Fenton, I. R. Stevenson, P. J. Hudson, Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840-844 (2004).
4. S. Telfer, X. Lambin, R. Birtles, P. Beldomenico, S. Burthe, S. Paterson, M. Begon, Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243-246 (2010).
5. P. J. Hotez, A. Kamath, Neglected tropical diseases in sub-Saharan Africa: Review of their prevalence, distribution, and disease burden. PLOS Negl. Trop. Dis. 3, e412 (2009).
6. S. Shrestha, B. Foxman, D. M. Weinberger, C. Steiner, C. Viboud, P. Rohani, Identifying the interaction between influenza and pneumococcal pneumonia using incidence data. ScI. TransI. Med. 5, 191ra84 (2013).
7. A. L. Graham, Ecological rules governing helminth-microparasite coinfection. Proc. Natl. Acad. ScI. U.S.A. 105, 566-570 (2008).
8. S. Sharma, P. G. Thomas, The two faces of heterologous immunity: Protection or immu-nopathology. J. Leukoc. Biol. 95, 405-416 (2014).
9. R. M. Welch, J. W. Che, M. A. Brehm, L. K. Selin, Heterologous immunity between viruses. Immunol. Rev. 235, 244-266 (2010).
10. P. E. M. Fine, Variation in protection by BCG: Implications of and for heterologous immunity. Lancet 346, 1339-1345 (1995).
11. G. S. Nelson, in Parasitic Zoonoses Clinical and Experimental Studies, E. J. L. Soulsby, Ed. (Academic Press, New York, 1974), pp. 273-285.
12. T. N. Williams, K. Maitland, S. Bennett, M. Ganczakowski, T. E. A. Peto, C. I. Newbold, D. K. Bowden, D. J. Weatherall, J .B. Clegg, High incidence of malaria in a-thalassaemic children. Nature 383, 522-525 (1996).
13. A. L. Graham, T. J. Lamb, A. F. Read, J. E. Allen, Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. J. Infect. Dis. 191, 410-421 (2005).
14. S. M. Thumbi, B. M. de C. Bronsvoort, E. J. Poole, H. Kiara, P. G. Toye, M. N. Mbole-Kariuki, I. Conradie, A. Jennings, I. G. Handel, J. A. W. Coetzer, J. C A. Steyl, O. Hanotte, M. E. J. Woolhouse, Parasite co-infections and their impact on survival of indigenous cattle. PLOS One 9, e76324 (2014).
15. S. M. Thumbi, B. M. de C. Bronsvoort, H. Kiara, P. G. Toye, J. Poole, M. Ndila, I. Conradie, A. Jennings, I. G. Handel, J. A. W. Coetzer, J. Steyl, O. Hanotte, M. E. J. Woolhouse, Mortality in East African shorthorn zebu cattle under one year: Predictors of infectious-disease mortality. BMC Vet. Res. 9, 175 (2013).
16. J. A. W. Coetzer, R. C. Tustin, Eds. Infectious Diseases of Livestock (Oxford Univ. Press, Cape Town, ed. 2, 2004), vol. 1.
17. W. I. Morrison, D. McKeever, Current status of vaccine development against Theileria parasites. Parasitology 133, S169-S187 (2006).
18. H. Kiara, A. Jennings, B. M. de C. Bronsvoort, I. G. Handel, S. T. Mwangi, M. Mbole-Kariuki, I. Conradie van Wyk, E. J. Poole, O. Hanotte, J. A. W. Coetzer, M. E. J. Woolhouse, P. G. Toye, A longitudinal assessment of the serological response to Theileria parva and other tick-borne parasites from birth to one year in a cohort of indigenous calves in western Kenya. Parasitology 141, 1289-1298 (2014).
19. C. A. L. Oura, B. B. Asiimwe, W. Weir, G. W. Lubega, A. Tait, Population genetic analysis and sub-structuring of Theileria parva in Uganda. Mol. Biochem. Parasitol. 140, 229-239 (2005).
20. G. S. Cumming, Using habitat models to map diversity: pan-African species richness of ticks (Acari: Ixodida). J. Biogeogr. 27, 427-440 (2000).
21. P. G. Coleman, B. D. Perry, M. E. J. Woolhouse, Endemic stability-A veterinary idea applied to human public health. Lancet 357, 1284-1286 (2001).
22. M. C. Bruce, A. Macheso, L. A. Kelly-Hope, S. Nkhoma, A. McConnachie, M. E. Molyneaux, Effect of transmission setting and mixed species infections on clinical measures of malaria in MalawI. PLOS One 3, e2775 (2008).
23. E. A. Okiro, A. Al-Taiar, H. Reyburn, R. Idro, J. A. Berkley, R. W. Snow, Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malar. J. 8, 4 (2009).
24. A. Ross, N. Maire, L. Molineaux, T. Smith, An epidemiologic model of severe morbidity and mortality caused by Plasmodium falciparum. Am. J. Trop. Med. Hyg. 75, S63-S73 (2006).
25. B. J. Mans, R. Pienaar, A. A. Latif, F. T. Potgieter, Diversity in the 18S SSU rRNA V4 hyper-variable region of Theileria spp. in Cape buffalo {Syncerus coffer) and cattle from southern Africa. Parasitology 138, 766-779 (2011).
26. B. M. de C Bronsvoort, S. M.Thumbi, E. J. Poole, H. Kiara, O. Tosas Auguet, I.G. Handel, A. Jennings, I. Conradie, M. N. Mbole-Kariuki, P. G. Toye, O. Hanotte, J. A. W. Coetzer, M. E. J. Woolhouse, Design and descriptive epidemiology of the Infectious Diseases of East African Livestock (IDEAL) project, a longitudinal calf cohort study in western Kenya. BMC Vet. Res. 9, 171 (2013).
27. I. Conradie van Wyk, A. Goddard, B. M. de C Bronsvoort, J. A. W. Coetzer, I. G. Handel, O. Hanotte, A. Jennings, M. Lesosky, H. Kiara, S. M. Thumbi, P. Toye, M. W. Woolhouse, B. L Penzhorn, The impact of co-infections on the haematological profile of East African Short-horn Zebu calves. Parasitology 141, 374-388 (2014).
28. D. E. Radley, C. G. D. Brown, M. J. Burridge, M. P. Cunningham, M. A. Peirce, R. E. Purnell, East Coast fever: Quantitative studies of Theileria parva in cattle. Exp. Parasitol. 36, 278-287 (1974).
29. J. M. Gubbels, A. P. de Vos, M. van der weide, J. Viseras, L. M. Schouls, E. de Vries, F. Jongejan, Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J. Clin. Microbiol. 37, 1782-1789 (1999).
30. D. O. Odongo, J. D. Sunter, H. K. Kiara, R. A. Skilton, R. P. Bishop, A nested PCR assay exhibits enhanced sensitivity for detection of Theileria parva infections in bovine blood samples from carrier animals. Parasitol. Res. 106, 357-365 (2009).
31. C. A. L. Oura, D. O. Odongo, G. W. Lubega, P. R. Spooner, A. Tait, R. P. Bishop, A panel of microsatellite and minisatellite markers for the characterisation of field isolates of Theileria parva. Int. J. Parasitol. 33, 1641-1653 (2003).
32. S. G. Ndungu, C. G. D. Brown, T. T. Dolan, In vivo comparison of susceptibility between Bos indicus and Bos taurus cattle types to Theileria parva infection. Onderstepoort. J. Vet. Res. 72, 13-22 (2005).
33. M. N. Mbole-Kariuki, T. Sonstegard, A. Orth, S. M. Thumbi, B. M. de C Bronsvoort, H. Kiara, P. Toye, I. Conradie, A. Jennings, K. Coetzer, M. E. J. Woolhouse, O. Hanotte, M. Tapio, Genome-wide analysis reveals the ancient and recent admixture history East African Shorthorn Zebu (EASZ) from Western Kenya. Heredity 113, 297-305 (2014).
34. G. G. R. Murray, M. E. J. Woolhouse, M. Tapio, M. N. Mbole-Kariuki, T. S. Sonstegard, S. M. Thumbi, A E Jennings, I. Conradie van Wyk, M. Chase-Topping, H. Kiara, P. Toye, K Coetzer, B. M. de C Bronsvoort, 0. Hanotte, Genetic susceptibility to infectious disease in East African Shorthorn Zebu: A genome-wide analysis of the effect of heterozygosity and exotic introgression. BMC Evol. Biol. 13, 246 (2013).