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Sci Adv. 2015 Mar 20;1(2):e1400026. doi: 10.1126/sciadv.1400026. eCollection 2015 Mar.

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

Author information

1
Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK.
2
Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK. ; Paul G. Allen School for Global Animal Health, Washington State University, Pullman, WA 99164-7090, USA.
3
Royal (Dick) School of Veterinary Studies, University of Edinburgh, The Roslin Building, Easter Bush, Midlothian EH25 9RG, UK. ; The Roslin Institute, University of Edinburgh, The Roslin Building, Easter Bush, Midlothian EH25 9RG, UK.
4
Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK. ; The James Hutton Institute, Craigiebuckler, Aberdeen AB15 8QH, UK.
5
International Livestock Research Institute, P.O. Box 30709, Nairobi 00100, Kenya.
6
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa.
7
International Livestock Research Institute, P.O. Box 30709, Nairobi 00100, Kenya. ; School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK.
8
Natural Resources Institute Finland (Luke), Green technology, FI-31600 Jokioinen, Finland.
9
Henry Wellcome Building, Institute of Biodiversity, Animal Health and Comparative Medicine, Garscube Campus, College of Medical, Veterinary and Life Sciences, University of Glasgow, Bearsden Road, Glasgow G61 1QH, UK.
10
Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, Kings Buildings, West Mains Road, Edinburgh EH9 3JT, UK. ; Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, Australia.
11
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK.

Abstract

Many individual hosts are infected with multiple parasite species, and this may increase or decrease the pathogenicity of the infections. This phenomenon is termed heterologous reactivity and is potentially an important determinant of both patterns of morbidity and mortality and of the impact of disease control measures at the population level. Using infections with Theileria parva (a tick-borne protozoan, related to Plasmodium) in indigenous African cattle [where it causes East Coast fever (ECF)] as a model system, we obtain the first quantitative estimate of the effects of heterologous reactivity for any parasitic disease. In individual calves, concurrent co-infection with less pathogenic species of Theileria resulted in an 89% reduction in mortality associated with T. parva infection. Across our study population, this corresponds to a net reduction in mortality due to ECF of greater than 40%. Using a mathematical model, we demonstrate that this degree of heterologous protection provides a unifying explanation for apparently disparate epidemiological patterns: variable disease-induced mortality rates, age-mortality profiles, weak correlations between the incidence of infection and disease (known as endemic stability), and poor efficacy of interventions that reduce exposure to multiple parasite species. These findings can be generalized to many other infectious diseases, including human malaria, and illustrate how co-infections can play a key role in determining population-level patterns of morbidity and mortality due to parasite infections.

KEYWORDS:

East Coast fever; Epidemiology; Mathematical model; Theileria parva; case fatality; cattle; endemic stability; heterologous protection; malaria; vaccination

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