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

  • 1,907
    views
  • 286
    downloads
  • 43
    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
    Yuchen Zhang, Yitang Sun ... Kaixiong Ye
    Research Article

    Background:

    Circulating omega-3 and omega-6 polyunsaturated fatty acids (PUFAs) have been associated with various chronic diseases and mortality, but results are conflicting. Few studies examined the role of omega-6/omega-3 ratio in mortality.

    Methods:

    We investigated plasma omega-3 and omega-6 PUFAs and their ratio in relation to all-cause and cause-specific mortality in a large prospective cohort, the UK Biobank. Of 85,425 participants who had complete information on circulating PUFAs, 6461 died during follow-up, including 2794 from cancer and 1668 from cardiovascular disease (CVD). Associations were estimated by multivariable Cox proportional hazards regression with adjustment for relevant risk factors.

    Results:

    Risk for all three mortality outcomes increased as the ratio of omega-6/omega-3 PUFAs increased (all Ptrend <0.05). Comparing the highest to the lowest quintiles, individuals had 26% (95% CI, 15–38%) higher total mortality, 14% (95% CI, 0–31%) higher cancer mortality, and 31% (95% CI, 10–55%) higher CVD mortality. Moreover, omega-3 and omega-6 PUFAs in plasma were all inversely associated with all-cause, cancer, and CVD mortality, with omega-3 showing stronger effects.

    Conclusions:

    Using a population-based cohort in UK Biobank, our study revealed a strong association between the ratio of circulating omega-6/omega-3 PUFAs and the risk of all-cause, cancer, and CVD mortality.

    Funding:

    Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institute of Health under the award number R35GM143060 (KY). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

    1. Ecology
    2. Epidemiology and Global Health
    Aleksandra Kovacevic, David RM Smith ... Lulla Opatowski
    Research Article

    Non-pharmaceutical interventions implemented to block SARS-CoV-2 transmission in early 2020 led to global reductions in the incidence of invasive pneumococcal disease (IPD). By contrast, most European countries reported an increase in antibiotic resistance among invasive Streptococcus pneumoniae isolates from 2019 to 2020, while an increasing number of studies reported stable pneumococcal carriage prevalence over the same period. To disentangle the impacts of the COVID-19 pandemic on pneumococcal epidemiology in the community setting, we propose a mathematical model formalizing simultaneous transmission of SARS-CoV-2 and antibiotic-sensitive and -resistant strains of S. pneumoniae. To test hypotheses underlying these trends five mechanisms were built into the model and examined: (1) a population-wide reduction of antibiotic prescriptions in the community, (2) lockdown effect on pneumococcal transmission, (3) a reduced risk of developing an IPD due to the absence of common respiratory viruses, (4) community azithromycin use in COVID-19 infected individuals, (5) and a longer carriage duration of antibiotic-resistant pneumococcal strains. Among 31 possible pandemic scenarios involving mechanisms individually or in combination, model simulations surprisingly identified only two scenarios that reproduced the reported trends in the general population. They included factors (1), (3), and (4). These scenarios replicated a nearly 50% reduction in annual IPD, and an increase in antibiotic resistance from 20% to 22%, all while maintaining a relatively stable pneumococcal carriage. Exploring further, higher SARS-CoV-2 R0 values and synergistic within-host virus-bacteria interaction mechanisms could have additionally contributed to the observed antibiotic resistance increase. Our work demonstrates the utility of the mathematical modeling approach in unraveling the complex effects of the COVID-19 pandemic responses on AMR dynamics.