Landscape drives zoonotic malaria prevalence in non-human primates

Author:

Johnson Emilia123ORCID,Sunil Kumar Sharma Reuben4,Ruiz Cuenca Pablo256ORCID,Byrne Isabel2ORCID,Salgado-Lynn Milena789ORCID,Suraya Shahar Zarith4,Col Lin Lee4,Zulkifli Norhadila4,Dilaila Mohd Saidi Nor4,Drakeley Chris10ORCID,Matthiopoulos Jason1ORCID,Nelli Luca1ORCID,Fornace Kimberly12311ORCID

Affiliation:

1. School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow

2. Department of Disease Control, London School of Hygiene & Tropical Medicine

3. Centre on Climate Change and Planetary Health, London School of Hygiene & Tropical Medicine

4. Faculty of Veterinary Medicine, Universiti Putra Malaysia

5. Lancaster University, Bailrigg

6. Liverpool School of Tropical Medicine, Pembroke Place Liverpool

7. School of Biosciences, Cardiff University

8. Wildlife Health, Genetic and Forensic Laboratory, Sabah Wildlife Department, Wisma Muis

9. Danau Girang Field Centre, Sabah Wildlife Department

10. Department of Infection Biology, London School of Hygiene & Tropical Medicine

11. Saw Swee Hock School of Public Health, National University of Singapore

Abstract

Zoonotic disease dynamics in wildlife hosts are rarely quantified at macroecological scales due to the lack of systematic surveys. Non-human primates (NHPs) host Plasmodium knowlesi, a zoonotic malaria of public health concern and the main barrier to malaria elimination in Southeast Asia. Understanding of regional P. knowlesi infection dynamics in wildlife is limited. Here, we systematically assemble reports of NHP P. knowlesi and investigate geographic determinants of prevalence in reservoir species. Meta-analysis of 6322 NHPs from 148 sites reveals that prevalence is heterogeneous across Southeast Asia, with low overall prevalence and high estimates for Malaysian Borneo. We find that regions exhibiting higher prevalence in NHPs overlap with human infection hotspots. In wildlife and humans, parasite transmission is linked to land conversion and fragmentation. By assembling remote sensing data and fitting statistical models to prevalence at multiple spatial scales, we identify novel relationships between P. knowlesi in NHPs and forest fragmentation. This suggests that higher prevalence may be contingent on habitat complexity, which would begin to explain observed geographic variation in parasite burden. These findings address critical gaps in understanding regional P. knowlesi epidemiology and indicate that prevalence in simian reservoirs may be a key spatial driver of human spillover risk.

Funder

Wellcome Trust

Royal Society

Ministry of Higher Education Malaysia

World Health Organization

Publisher

eLife Sciences Publications, Ltd

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