Local human movement patterns and land use impact exposure to zoonotic malaria in Malaysian Borneo

  1. Kimberly M Fornace  Is a corresponding author
  2. Neal Alexander
  3. Tommy R Abidin
  4. Paddy M Brock
  5. Tock H Chua
  6. Indra Vythilingam
  7. Heather M Ferguson
  8. Benny O Manin
  9. Meng L Wong
  10. Sui H Ng
  11. Jon Cox
  12. Chris Drakeley
  1. London School of Hygiene and Tropical Medicine, United Kingdom
  2. Universiti Malaysia Sabah, Malaysia
  3. University of Glasgow, United Kingdom
  4. University of Malaya, Malaysia

Abstract

Human movement into insect vector and wildlife reservoir habitats determines zoonotic disease risks; however, few data are available to quantify the impact of land use on pathogen transmission. Here, we utilise GPS tracking devices and novel applications of ecological methods to develop fine-scale models of human space use relative to land cover to assess exposure to the zoonotic malaria Plasmodium knowlesi in Malaysian Borneo. Combining data with spatially explicit models of mosquito biting rates, we demonstrate the role of individual heterogeneities in local space use in disease exposure. At a community level, our data indicate that areas close to both secondary forest and houses have the highest probability of human P. knowlesi exposure, providing quantitative evidence for the importance of ecotones. Despite higher biting rates in forests, incorporating human movement space use into exposure estimates illustrates the importance of intensified interactions between pathogens, insect vectors and people around habitat edges.

Data availability

Data on human subjects is not available due to ethical restrictions around sharing identifiable information. All other data is publicly available with relevant links or publications included. Code to reproduce this analysis is available on GitHub or as supplementary information.

The following previously published data sets were used

Article and author information

Author details

  1. Kimberly M Fornace

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    For correspondence
    Kimberly.Fornace@lshtm.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5484-241X
  2. Neal Alexander

    Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Tommy R Abidin

    Department of Pathobiology and Medical Diagnostics, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  4. Paddy M Brock

    Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Tock H Chua

    Department of Pathobiology and Medical Diagnostics, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8984-8723
  6. Indra Vythilingam

    Parasitology Department, University of Malaya, Kuala Lumpur, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  7. Heather M Ferguson

    Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Benny O Manin

    Department of Pathobiology and Medical Diagnostics, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0726-6146
  9. Meng L Wong

    Parasitology Department, University of Malaya, Kuala Lumpur, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  10. Sui H Ng

    Department of Pathobiology and Medical Diagnostics, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  11. Jon Cox

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Chris Drakeley

    Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4863-075X

Funding

Medical Research Council (G1100796)

  • Kimberly M Fornace
  • Neal Alexander
  • Tommy R Abidin
  • Paddy M Brock
  • Tock H Chua
  • Indra Vythilingam
  • Heather M Ferguson
  • Benny O Manin
  • Meng L Wong
  • Sui H Ng
  • Jon Cox
  • Chris Drakeley

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ben Cooper, Mahidol Oxford Tropical Medicine Research Unit, Thailand

Ethics

Human subjects: This study was approved by the Medical Research Sub-Committee of the Malaysian Ministry of Health (NMRR-12-537-12568) and the Research Ethics Committee of the London School of Hygiene and Tropical Medicine (6531). Written informed consent was obtained from all participants or parents or guardians and assent obtained from children under 18.

Version history

  1. Received: April 10, 2019
  2. Accepted: October 15, 2019
  3. Accepted Manuscript published: October 22, 2019 (version 1)
  4. Version of Record published: October 25, 2019 (version 2)

Copyright

© 2019, Fornace et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,943
    views
  • 291
    downloads
  • 46
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Kimberly M Fornace
  2. Neal Alexander
  3. Tommy R Abidin
  4. Paddy M Brock
  5. Tock H Chua
  6. Indra Vythilingam
  7. Heather M Ferguson
  8. Benny O Manin
  9. Meng L Wong
  10. Sui H Ng
  11. Jon Cox
  12. Chris Drakeley
(2019)
Local human movement patterns and land use impact exposure to zoonotic malaria in Malaysian Borneo
eLife 8:e47602.
https://doi.org/10.7554/eLife.47602

Share this article

https://doi.org/10.7554/eLife.47602

Further reading

    1. Epidemiology and Global Health
    Xiaoxin Yu, Roger S Zoh ... David B Allison
    Review Article

    We discuss 12 misperceptions, misstatements, or mistakes concerning the use of covariates in observational or nonrandomized research. Additionally, we offer advice to help investigators, editors, reviewers, and readers make more informed decisions about conducting and interpreting research where the influence of covariates may be at issue. We primarily address misperceptions in the context of statistical management of the covariates through various forms of modeling, although we also emphasize design and model or variable selection. Other approaches to addressing the effects of covariates, including matching, have logical extensions from what we discuss here but are not dwelled upon heavily. The misperceptions, misstatements, or mistakes we discuss include accurate representation of covariates, effects of measurement error, overreliance on covariate categorization, underestimation of power loss when controlling for covariates, misinterpretation of significance in statistical models, and misconceptions about confounding variables, selecting on a collider, and p value interpretations in covariate-inclusive analyses. This condensed overview serves to correct common errors and improve research quality in general and in nutrition research specifically.

    1. Ecology
    2. Epidemiology and Global Health
    Emilia Johnson, Reuben Sunil Kumar Sharma ... Kimberly Fornace
    Research Article

    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.