Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa

  1. Sofonias K Tessema  Is a corresponding author
  2. Amy Wesolowski
  3. Anna Chen
  4. Maxwell Murphy
  5. Jordan Wilheim
  6. Anna-Rosa Mupiri
  7. Nick W Ruktanonchai
  8. Victor A Alegana
  9. Andrew J Tatem
  10. Munyaradzi Tambo
  11. Bradley Didier
  12. Justin M Cohen
  13. Adam Bennett
  14. Hugh JW Sturrock
  15. Roland Gosling
  16. Michelle S Hsiang
  17. David L Smith
  18. Davis R Mumbengegwi
  19. Jennifer L Smith
  20. Bryan Greenhouse
  1. University of California, San Francisco, United States
  2. Johns Hopkins Bloomberg School of Public Health, United States
  3. University of Namibia, Namibia
  4. University of Southampton, United Kingdom
  5. Clinton Health Access Initiative, United States
  6. University of Washington, United States
  7. University of Texas Southwestern Medical Center, United States

Abstract

Local and cross-border importation remain major challenges to malaria elimination and are difficult to measure using traditional surveillance data. To address this challenge, we systematically collected parasite genetic data and travel history from thousands of malaria cases across northeastern Namibia and estimated human mobility from mobile phone data. We observed strong fine-scale spatial structure in local parasite populations, providing positive evidence that the majority of cases were due to local transmission. This result was largely consistent with estimates from mobile phone and travel history data. However, genetic data identified more detailed and extensive evidence of parasite connectivity over hundreds of kilometers than the other data, within Namibia and across the Angolan and Zambian borders. Our results provide a framework for incorporating genetic data into malaria surveillance and provide evidence that both strengthening of local interventions and regional coordination are likely necessary to eliminate malaria in this region of Southern Africa.

Data availability

All data generated or analyzed during this study are included in the manuscript and supplementary files.

Article and author information

Author details

  1. Sofonias K Tessema

    Department of Medicine, University of California, San Francisco, San Francisco, United States
    For correspondence
    SofoniasK.Tessema@ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1057-5310
  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. Anna Chen

    Department of Medicine, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Maxwell Murphy

    Department of Medicine, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0332-4388
  5. Jordan Wilheim

    Department of Medicine, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Anna-Rosa Mupiri

    Multidisciplinary Research Center, University of Namibia, Windhoek, Namibia
    Competing interests
    The authors declare that no competing interests exist.
  7. Nick W Ruktanonchai

    Geography and Environment, University of Southampton, Southampton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Victor A Alegana

    Geography and Environment, University of Southampton, Southampton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Andrew J Tatem

    Geography and Environment, University of Southampton, Southampton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Munyaradzi Tambo

    Multidisciplinary Research Center, University of Namibia, Windhoek, Namibia
    Competing interests
    The authors declare that no competing interests exist.
  11. Bradley Didier

    Clinton Health Access Initiative, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Justin M Cohen

    Clinton Health Access Initiative, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Adam Bennett

    Institute of Global Health Sciences, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Hugh JW Sturrock

    Institute of Global Health Sciences, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Roland Gosling

    Global Health Group, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Michelle S Hsiang

    Institute of Global Health Sciences, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. David L Smith

    Institute of Health Metrics and Evaluation, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4367-3849
  18. Davis R Mumbengegwi

    Multidisciplinary Research Center, University of Namibia, Windhoek, Namibia
    Competing interests
    The authors declare that no competing interests exist.
  19. Jennifer L Smith

    Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Bryan Greenhouse

    Department of Medicine, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Bill and Melinda Gates Foundation

  • Sofonias K Tessema
  • Bryan Greenhouse

Burroughs Wellcome Fund

  • Amy Wesolowski

National Institutes of Health

  • Amy Wesolowski

Chan Zuckerberg Biohub

  • Bryan Greenhouse

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

Ethics

Human subjects: Ethical approval for the study was obtained from the Institutional Review Boards of the University of Namibia and the University of California, San Francisco (Identification numbers 15-17422 and 14-14576). Informed consent was obtained from all participants or the parents of all children participated in the Zambezi study. For the Kavango study, IRB approval was obtained but no informed consent was collected as all samples (used RDTs) and de-identified data were collected during routine surveillance.

Copyright

© 2019, Tessema 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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  1. Sofonias K Tessema
  2. Amy Wesolowski
  3. Anna Chen
  4. Maxwell Murphy
  5. Jordan Wilheim
  6. Anna-Rosa Mupiri
  7. Nick W Ruktanonchai
  8. Victor A Alegana
  9. Andrew J Tatem
  10. Munyaradzi Tambo
  11. Bradley Didier
  12. Justin M Cohen
  13. Adam Bennett
  14. Hugh JW Sturrock
  15. Roland Gosling
  16. Michelle S Hsiang
  17. David L Smith
  18. Davis R Mumbengegwi
  19. Jennifer L Smith
  20. Bryan Greenhouse
(2019)
Using parasite genetic and human mobility data to infer local and cross-border malaria connectivity in Southern Africa
eLife 8:e43510.
https://doi.org/10.7554/eLife.43510

Share this article

https://doi.org/10.7554/eLife.43510

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    1. Epidemiology and Global Health
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    Background:

    Biological aging exhibits heterogeneity across multi-organ systems. However, it remains unclear how is lifestyle associated with overall and organ-specific aging and which factors contribute most in Southwest China.

    Methods:

    This study involved 8396 participants who completed two surveys from the China Multi-Ethnic Cohort (CMEC) study. The healthy lifestyle index (HLI) was developed using five lifestyle factors: smoking, alcohol, diet, exercise, and sleep. The comprehensive and organ-specific biological ages (BAs) were calculated using the Klemera–Doubal method based on longitudinal clinical laboratory measurements, and validation were conducted to select BA reflecting related diseases. Fixed effects model was used to examine the associations between HLI or its components and the acceleration of validated BAs. We further evaluated the relative contribution of lifestyle components to comprehension and organ systems BAs using quantile G-computation.

    Results:

    About two-thirds of participants changed HLI scores between surveys. After validation, three organ-specific BAs (the cardiopulmonary, metabolic, and liver BAs) were identified as reflective of specific diseases and included in further analyses with the comprehensive BA. The health alterations in HLI showed a protective association with the acceleration of all BAs, with a mean shift of –0.19 (95% CI −0.34, –0.03) in the comprehensive BA acceleration. Diet and smoking were the major contributors to overall negative associations of five lifestyle factors, with the comprehensive BA and metabolic BA accounting for 24% and 55% respectively.

    Conclusions:

    Healthy lifestyle changes were inversely related to comprehensive and organ-specific biological aging in Southwest China, with diet and smoking contributing most to comprehensive and metabolic BA separately. Our findings highlight the potential of lifestyle interventions to decelerate aging and identify intervention targets to limit organ-specific aging in less-developed regions.

    Funding:

    This work was primarily supported by the National Natural Science Foundation of China (Grant No. 82273740) and Sichuan Science and Technology Program (Natural Science Foundation of Sichuan Province, Grant No. 2024NSFSC0552). The CMEC study was funded by the National Key Research and Development Program of China (Grant No. 2017YFC0907305, 2017YFC0907300). The sponsors had no role in the design, analysis, interpretation, or writing of this article.