Mapping imported malaria in Bangladesh using parasite genetic and human mobility data

  1. Hsiao-Han Chang
  2. Amy Wesolowski
  3. Ipsita Sinha
  4. Christopher G Jacob
  5. Ayesha Mahmud
  6. Didar Uddin
  7. Sazid Ibna Zaman
  8. Md Amir Hossain
  9. M Abul Faiz
  10. Aniruddha Ghose
  11. Abdullah Abu Sayeed
  12. M Ridwanur Rahman
  13. Akramul Islam
  14. Mohammad Jahirul Karim
  15. M Kamar Rezwan
  16. Abul Khair Mohammad Shamsuzzaman
  17. Sanya Tahmina Jhora
  18. M M Aktaruzzaman
  19. Eleanor Drury
  20. Sonia Gonçalves
  21. Mihir Kekre
  22. Mehul Dhorda
  23. Ranitha Vongpromek
  24. Olivo Miotto
  25. Kenth Engø-Monsen
  26. Dominic Kwiatkowski
  27. Richard J Maude
  28. Caroline Buckee  Is a corresponding author
  1. Harvard T H Chan School of Public Health, United States
  2. Johns Hopkins Bloomberg School of Public Health, United States
  3. Mahidol University, Thailand
  4. Wellcome Sanger Institute, United Kingdom
  5. Chittagong Medical College, Bangladesh
  6. Chittagong Medical College Hospital, Bangladesh
  7. Shaheed Suhrawardy Medical College, Bangladesh
  8. BRAC Centre, Bangladesh
  9. National Malaria Elimination Programme, Bangladesh
  10. World Health Organization, Bangladesh
  11. Directorate General of Health Services, Bangladesh
  12. The WorldWide Antimalarial Resistance Network (WWARN), Thailand
  13. Telenor Group, Norway

Abstract

For countries aiming for malaria elimination, travel of infected individuals between endemic areas undermines local interventions. Quantifying parasite importation has therefore become a priority for national control programs. We analyzed epidemiological surveillance data, travel surveys, parasite genetic data, and anonymized mobile phone data to measure the spatial spread of malaria parasites in southeast Bangladesh. We developed a genetic mixing index to estimate the likelihood of samples being local or imported from parasite genetic data and inferred the direction and intensity of parasite flow between locations using an epidemiological model integrating the travel survey and mobile phone calling data. Our approach indicates that, contrary to dogma, frequent mixing occurs in low transmission regions in the southwest, and elimination will require interventions in addition to reducing imported infections from forested regions. Unlike risk maps generated from clinical case counts alone, therefore, our approach distinguishes areas of frequent importation as well as high transmission.

Data availability

All genetic data are included in Supplementary file 4 and all travel matrices are included in Supplementary file 5.

Article and author information

Author details

  1. Hsiao-Han Chang

    Department of Epidemiology, Harvard T H Chan School of Public Health, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Amy Wesolowski

    Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6320-3575
  3. Ipsita Sinha

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6574-310X
  4. Christopher G Jacob

    Malaria Programme, Wellcome Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Ayesha Mahmud

    Department of Epidemiology, Harvard T H Chan School of Public Health, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Didar Uddin

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  7. Sazid Ibna Zaman

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  8. Md Amir Hossain

    Department of Medicine, Chittagong Medical College, Chittagong, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  9. M Abul Faiz

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  10. Aniruddha Ghose

    Chittagong Medical College Hospital, Chittagong, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  11. Abdullah Abu Sayeed

    Chittagong Medical College Hospital, Chittagong, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  12. M Ridwanur Rahman

    Shaheed Suhrawardy Medical College, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  13. Akramul Islam

    BRAC Centre, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  14. Mohammad Jahirul Karim

    National Malaria Elimination Programme, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  15. M Kamar Rezwan

    Vector-Borne Disease Control, World Health Organization, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  16. Abul Khair Mohammad Shamsuzzaman

    Communicable Disease Control, Directorate General of Health Services, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  17. Sanya Tahmina Jhora

    Communicable Disease Control, Directorate General of Health Services, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  18. M M Aktaruzzaman

    National Malaria Elimination Programme, Dhaka, Bangladesh
    Competing interests
    The authors declare that no competing interests exist.
  19. Eleanor Drury

    Malaria Programme, Wellcome Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  20. Sonia Gonçalves

    Malaria Programme, Wellcome Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  21. Mihir Kekre

    Malaria Programme, Wellcome Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  22. Mehul Dhorda

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  23. Ranitha Vongpromek

    The WorldWide Antimalarial Resistance Network (WWARN), Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  24. Olivo Miotto

    Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  25. Kenth Engø-Monsen

    Telenor Research, Telenor Group, Fornebu, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1618-7597
  26. Dominic Kwiatkowski

    Malaria Programme, Wellcome Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  27. Richard J Maude

    Department of Epidemiology, Harvard T H Chan School of Public Health, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  28. Caroline Buckee

    Department of Epidemiology, Harvard T H Chan School of Public Health, Boston, United States
    For correspondence
    cbuckee@hsph.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8386-5899

Funding

National Institute of General Medical Sciences (U54GM088558)

  • Hsiao-Han Chang

Burroughs Wellcome Fund

  • Amy Wesolowski

Bill and Melinda Gates Foundation (CPT000390)

  • Ipsita Sinha
  • Sazid Ibna Zaman
  • Richard J Maude

Medical Research Council (G0600718)

  • Christopher G Jacob
  • Eleanor Drury
  • Sonia Gonçalves
  • Mihir Kekre
  • Dominic Kwiatkowski

National Institute of General Medical Sciences (R35GM124715-02)

  • Caroline Buckee

Bill and Melinda Gates Foundation (OPP1118166)

  • Christopher G Jacob
  • Olivo Miotto
  • Caroline Buckee

Bill and Melinda Gates Foundation (OPP1129596)

  • Ipsita Sinha
  • Sazid Ibna Zaman
  • Richard J Maude

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

Reviewing Editor

  1. Neil M Ferguson, Imperial College London, United Kingdom

Version history

  1. Received: November 9, 2018
  2. Accepted: March 14, 2019
  3. Accepted Manuscript published: April 2, 2019 (version 1)
  4. Version of Record published: April 23, 2019 (version 2)

Copyright

© 2019, Chang 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

  • 4,033
    views
  • 583
    downloads
  • 76
    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. Hsiao-Han Chang
  2. Amy Wesolowski
  3. Ipsita Sinha
  4. Christopher G Jacob
  5. Ayesha Mahmud
  6. Didar Uddin
  7. Sazid Ibna Zaman
  8. Md Amir Hossain
  9. M Abul Faiz
  10. Aniruddha Ghose
  11. Abdullah Abu Sayeed
  12. M Ridwanur Rahman
  13. Akramul Islam
  14. Mohammad Jahirul Karim
  15. M Kamar Rezwan
  16. Abul Khair Mohammad Shamsuzzaman
  17. Sanya Tahmina Jhora
  18. M M Aktaruzzaman
  19. Eleanor Drury
  20. Sonia Gonçalves
  21. Mihir Kekre
  22. Mehul Dhorda
  23. Ranitha Vongpromek
  24. Olivo Miotto
  25. Kenth Engø-Monsen
  26. Dominic Kwiatkowski
  27. Richard J Maude
  28. Caroline Buckee
(2019)
Mapping imported malaria in Bangladesh using parasite genetic and human mobility data
eLife 8:e43481.
https://doi.org/10.7554/eLife.43481

Share this article

https://doi.org/10.7554/eLife.43481

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.