1. Epidemiology and Global Health
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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
Research Article
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Cite this article as: eLife 2019;8:e47602 doi: 10.7554/eLife.47602

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.

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.

Reviewing Editor

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

Publication 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.

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Further reading

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    Background:

    The virus SARS-CoV-2 can exploit biological vulnerabilities (e.g. host proteins) in susceptible hosts that predispose to the development of severe COVID-19.

    Methods:

    To identify host proteins that may contribute to the risk of severe COVID-19, we undertook proteome-wide genetic colocalisation tests, and polygenic (pan) and cis-Mendelian randomisation analyses leveraging publicly available protein and COVID-19 datasets.

    Results:

    Our analytic approach identified several known targets (e.g. ABO, OAS1), but also nominated new proteins such as soluble Fas (colocalisation probability >0.9, p=1 × 10-4), implicating Fas-mediated apoptosis as a potential target for COVID-19 risk. The polygenic (pan) and cis-Mendelian randomisation analyses showed consistent associations of genetically predicted ABO protein with several COVID-19 phenotypes. The ABO signal is highly pleiotropic, and a look-up of proteins associated with the ABO signal revealed that the strongest association was with soluble CD209. We demonstrated experimentally that CD209 directly interacts with the spike protein of SARS-CoV-2, suggesting a mechanism that could explain the ABO association with COVID-19.

    Conclusions:

    Our work provides a prioritised list of host targets potentially exploited by SARS-CoV-2 and is a precursor for further research on CD209 and FAS as therapeutically tractable targets for COVID-19.

    Funding:

    MAK, JSc, JH, AB, DO, MC, EMM, MG, ID were funded by Open Targets. J.Z. and T.R.G were funded by the UK Medical Research Council Integrative Epidemiology Unit (MC_UU_00011/4). JSh and GJW were funded by the Wellcome Trust Grant 206194. This research was funded in part by the Wellcome Trust [Grant 206194]. For the purpose of open access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission.

    1. Epidemiology and Global Health
    Lawrence Lubyayi et al.
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    Background:

    Lack of early infection-exposure has been associated with increased allergy-related disease (ARD) susceptibility. In tropical Africa, little is known about which infections contribute to development of ARDs, and at which time.

    Methods:

    We used latent class analysis to characterise the early infection-exposure of participants in a Ugandan birth cohort and assessed ARDs in later childhood.

    Results:

    Of 2345 live births, 2115 children (90%) had data on infections within the first year of life while 1179 (50%) had outcome data at 9 years. We identified two latent classes of children based on first-year infection-exposure. Class 1 (32% membership), characterised by higher probabilities for malaria (80%), diarrhoea (76%), and lower respiratory tract infections (LRTI) (22%), was associated with lower prevalence of wheeze, eczema, rhinitis, and Dermatophagoides skin prick test (SPT) positivity at 9 years. Based on 5-year cumulative infection experience, class 1 (31% membership), characterised by higher probabilities for helminths (92%), malaria (79%), and LRTI (45%), was associated with lower probabilities of SPT positivity at 9 years.

    Conclusions:

    In this Ugandan birth cohort, early childhood infection-exposure, notably to malaria, helminths, LRTI, and diarrhoea, is associated with lower prevalence of atopy and ARDs in later childhood.

    Funding:

    This work was supported by several funding sources. The Entebbe Mother and Baby Study (EMaBS) was supported by the Wellcome Trust, UK, senior fellowships for AME (grant numbers 064693, 079110, 95778) with additional support from the UK Medical Research Council. LL is supported by a PhD fellowship through the DELTAS Africa Initiative SSACAB (grant number 107754). ELW received funding from MRC Grant Reference MR/K012126/1. SAL was supported by the PANDORA-ID-NET Consortium (EDCTP Reg/Grant RIA2016E-1609). HM was supported by the Wellcome’s Institutional Strategic Support Fund (grant number 204928/Z/16/Z).