Agricultural intensification, priming for persistence and the emergence of Nipah virus: a lethal bat-borne zoonosis

Author:

Pulliam Juliet R. C.12,Epstein Jonathan H.3,Dushoff Jonathan1,Rahman Sohayati A.45,Bunning Michel6,Jamaluddin Aziz A.7,Hyatt Alex D.8,Field Hume E.9,Dobson Andrew P.1,Daszak Peter3

Affiliation:

1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA

2. Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA

3. EcoHealth Alliance (formerly Wildlife Trust), 460 West 34th Street, 17th Floor, New York, NY 10001, USA

4. Department of Veterinary Services, Veterinary Research Institute, Ipoh, Perak, Malaysia

5. Universiti Putra Malaysia, Serdang, Selangor, Malaysia

6. 59th, Medical Wing, Lackland Air Force Base, USAF, San Antonio, TX 78201, USA

7. Department of Veterinary Services, Ministry of Agriculture, Putrajaya, Malaysia

8. Australian Animal Health Laboratory, Commonwealth Scientific and Industrial Research Organization (CSIRO), Geelong, Victoria, Australia

9. Biosecurity Sciences Laboratory, Department of Employment, Economic Development and Innovation, Brisbane, Queensland, Australia

Abstract

Emerging zoonoses threaten global health, yet the processes by which they emerge are complex and poorly understood. Nipah virus (NiV) is an important threat owing to its broad host and geographical range, high case fatality, potential for human-to-human transmission and lack of effective prevention or therapies. Here, we investigate the origin of the first identified outbreak of NiV encephalitis in Malaysia and Singapore. We analyse data on livestock production from the index site (a commercial pig farm in Malaysia) prior to and during the outbreak, on Malaysian agricultural production, and from surveys of NiV's wildlife reservoir (flying foxes). Our analyses suggest that repeated introduction of NiV from wildlife changed infection dynamics in pigs. Initial viral introduction produced an explosive epizootic that drove itself to extinction but primed the population for enzootic persistence upon reintroduction of the virus. The resultant within-farm persistence permitted regional spread and increased the number of human infections. This study refutes an earlier hypothesis that anomalous El Niño Southern Oscillation-related climatic conditions drove emergence and suggests that priming for persistence drove the emergence of a novel zoonotic pathogen. Thus, we provide empirical evidence for a causative mechanism previously proposed as a precursor to widespread infection with H5N1 avian influenza and other emerging pathogens.

Publisher

The Royal Society

Subject

Biomedical Engineering,Biochemistry,Biomaterials,Bioengineering,Biophysics,Biotechnology

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