Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density

  1. John Bradley
  2. Will Stone
  3. Dari FA DA
  4. Isabelle Morlais
  5. Alassane Dicko
  6. Anna Cohuet
  7. Wamdaogo M Guelbeogo
  8. Almahamoudou Mahamar
  9. Sandrine Nsango
  10. Harouna M Soumaré
  11. Halimatou Diawara
  12. Kjerstin Lanke
  13. Wouter Graumans
  14. Rianne Siebelink-Stoter
  15. Marga van de Vegte-Bolmer
  16. Ingrid Chen
  17. Alfred Tiono
  18. Bronner Pamplona Gonçalves
  19. Roland Gosling
  20. Robert W Sauerwein
  21. Chris Drakeley
  22. Thomas S Churcher  Is a corresponding author
  23. Teun Bousema
  1. London School of Hygiene and Tropical Medicine, United Kingdom
  2. Radboud University Medical Center, Netherlands
  3. Institut de Recherche en Sciences de la Santé, Burkina Faso
  4. Institut de Recherche pour le Développement, France
  5. University of Science, Techniques and Technologies of Bamako, Mali
  6. Centre National de Recherche et de Formation sur le Paludisme, Burkina Faso
  7. Université de Douala, Cameroon
  8. University of California, San Francisco, United States
  9. Imperial College London, United Kingdom

Abstract

Understanding the importance of gametocyte density on human-to-mosquito transmission is of immediate relevance to malaria control. Previous work (Churcher et al., 2013) indicated a complex relationship between gametocyte density and mosquito infection. Here we use data from 148 feeding experiments on naturally infected gametocyte carriers to show that the relationship is much simpler and depends on both female and male parasite density. The proportion of mosquitoes infected is primarily determined by the density of female gametocytes though transmission from low gametocyte densities may be impeded by a lack of male parasites. Improved precision of gametocyte quantification simplifies the shape of the relationship with infection increasing rapidly before plateauing at higher densities. The mean number of oocysts per mosquito rises quickly with gametocyte density but continues to increase across densities examined. The work highlights the importance of measuring both female and male gametocyte density when estimating the human reservoir of infection.

Data availability

All raw data can be found in Source Data Supplements to the relevant figures

Article and author information

Author details

  1. John Bradley

    MRC Tropical Epidemiology Group, 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:" 0000-0002-9449-4608
  2. Will Stone

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Dari FA DA

    Institut de Recherche en Sciences de la Santé, Bobo-Dioulasso, Burkina Faso
    Competing interests
    The authors declare that no competing interests exist.
  4. Isabelle Morlais

    MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Alassane Dicko

    Malaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, Mali
    Competing interests
    The authors declare that no competing interests exist.
  6. Anna Cohuet

    MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Wamdaogo M Guelbeogo

    Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
    Competing interests
    The authors declare that no competing interests exist.
  8. Almahamoudou Mahamar

    MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Sandrine Nsango

    Faculté de Médecine et des Sciences Pharmaceutiques, Université de Douala, Douala, Cameroon
    Competing interests
    The authors declare that no competing interests exist.
  10. Harouna M Soumaré

    MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Halimatou Diawara

    MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Kjerstin Lanke

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Wouter Graumans

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3952-6491
  14. Rianne Siebelink-Stoter

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  15. Marga van de Vegte-Bolmer

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  16. Ingrid Chen

    Global Health Group, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Alfred Tiono

    Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou, Burkina Faso
    Competing interests
    The authors declare that no competing interests exist.
  18. Bronner Pamplona Gonçalves

    Department of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  19. Roland Gosling

    Global Health Group, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Robert W Sauerwein

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  21. Chris Drakeley

    Department of Immunology and Infection, 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
  22. Thomas S Churcher

    MRC Centre for Outbreak Analysis and Modelling, Infectious Disease Epidemiology, Imperial College London, London, United Kingdom
    For correspondence
    thomas.churcher@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8442-0525
  23. Teun Bousema

    Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2666-094X

Funding

Bill and Melinda Gates Foundation (AFIRM OPP1034789)

  • Chris Drakeley
  • Teun Bousema

European Commission (ERC-2014-StG 639776)

  • Will Stone
  • Teun Bousema

PATH (Malaria Vaccine Iniative)

  • Dari FA DA
  • Isabelle Morlais
  • Anna Cohuet
  • Teun Bousema

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

Reviewing Editor

  1. Urszula Krzych, Walter Reed Army Institute of Research, United States

Version history

  1. Received: December 21, 2017
  2. Accepted: May 26, 2018
  3. Accepted Manuscript published: May 31, 2018 (version 1)
  4. Version of Record published: June 21, 2018 (version 2)

Copyright

© 2018, Bradley 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. John Bradley
  2. Will Stone
  3. Dari FA DA
  4. Isabelle Morlais
  5. Alassane Dicko
  6. Anna Cohuet
  7. Wamdaogo M Guelbeogo
  8. Almahamoudou Mahamar
  9. Sandrine Nsango
  10. Harouna M Soumaré
  11. Halimatou Diawara
  12. Kjerstin Lanke
  13. Wouter Graumans
  14. Rianne Siebelink-Stoter
  15. Marga van de Vegte-Bolmer
  16. Ingrid Chen
  17. Alfred Tiono
  18. Bronner Pamplona Gonçalves
  19. Roland Gosling
  20. Robert W Sauerwein
  21. Chris Drakeley
  22. Thomas S Churcher
  23. Teun Bousema
(2018)
Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density
eLife 7:e34463.
https://doi.org/10.7554/eLife.34463

Share this article

https://doi.org/10.7554/eLife.34463

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