1. Epidemiology and Global Health
  2. Microbiology and Infectious Disease
Download icon

The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes

  1. Paul Capewell
  2. Christelle Cren-Travaillé
  3. Francesco Marchesi
  4. Pamela Johnston
  5. Caroline Clucas
  6. Robert A Benson
  7. Taylor-Anne Gorman
  8. Estefania Calvo-Alvarez
  9. Aline Crouzols
  10. Grégory Jouvion
  11. Vincent Jammoneau
  12. William Weir
  13. M Lynn Stevenson
  14. Kerry O'Neill
  15. Anneli Cooper
  16. Nono-raymond Kuispond Swar
  17. Bruno Bucheton
  18. Dieudonné Mumba Ngoyi
  19. Paul Garside
  20. Brice Rotureau
  21. Annette MacLeod  Is a corresponding author
  1. College of Medical, Veterinary and Life Sciences, United Kingdom
  2. Institut Pasteur, France
  3. University of Glasgow, United Kingdom
  4. Institut de Recherche pour le Développement, France
  5. University of Kinshasa, Democratic Republic of the Congo
  6. National Institute of Biomedical Research, Democratic Republic of the Congo
Short Report
  • Cited 55
  • Views 16,861
  • Annotations
Cite this article as: eLife 2016;5:e17716 doi: 10.7554/eLife.17716

Abstract

The role of mammalian skin in harbouring and transmitting arthropod-borne protozoan parasites has been overlooked for decades as these pathogens have been regarded primarily as blood-dwelling organisms. Intriguingly, infections with low or undetected blood parasites are common, particularly in the case of Human African Trypanosomiasis caused by Trypanosoma brucei gambiense. We hypothesise, therefore, the skin represents an anatomic reservoir of infection. Here we definitively show that substantial quantities of trypanosomes exist within the skin following experimental infection, which can be transmitted to the tsetse vector, even in the absence of detectable parasitaemia. Importantly, we demonstrate the presence of extravascular parasites in human skin biopsies from undiagnosed individuals. The identification of this novel reservoir requires a re-evaluation of current diagnostic methods and control policies. More broadly, our results indicate that transmission is a key evolutionary force driving parasite extravasation that could further result in tissue invasion-dependent pathology.

Article and author information

Author details

  1. Paul Capewell

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Christelle Cren-Travaillé

    Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Francesco Marchesi

    Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Pamela Johnston

    Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Caroline Clucas

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Robert A Benson

    Institute of Infection, Immunology and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Taylor-Anne Gorman

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Estefania Calvo-Alvarez

    Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Aline Crouzols

    Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Grégory Jouvion

    Human Histopathology and Animal Models Unit, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Vincent Jammoneau

    Unité Mixte de Recherche IRD-CIRAD 177, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  12. William Weir

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. M Lynn Stevenson

    Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  14. Kerry O'Neill

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  15. Anneli Cooper

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  16. Nono-raymond Kuispond Swar

    University of Kinshasa, Kinshasa, Democratic Republic of the Congo
    Competing interests
    The authors declare that no competing interests exist.
  17. Bruno Bucheton

    Unité Mixte de Recherche IRD-CIRAD 177, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  18. Dieudonné Mumba Ngoyi

    Department of Parasitology, National Institute of Biomedical Research, Kinshasa, Democratic Republic of the Congo
    Competing interests
    The authors declare that no competing interests exist.
  19. Paul Garside

    Institute of Infection, Immunology and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7933-0915
  20. Brice Rotureau

    Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  21. Annette MacLeod

    Wellcome Trust Centre for Molecular Parasitology, College of Medical, Veterinary and Life Sciences, Glasgow, United Kingdom
    For correspondence
    annette.macleod@glasgow.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0150-5049

Funding

Wellcome trust (Senior Fellowship (Annette Macleod) - 095201/Z/10/Z)

  • Paul Capewell
  • Caroline Clucas
  • William Weir
  • Anneli Cooper
  • Annette MacLeod

Wellcome trust (Wellcome Trust Centre for Molecular Parasitology Core Funding - 085349)

  • Paul Capewell
  • Caroline Clucas
  • William Weir
  • Anneli Cooper
  • Annette MacLeod

Agence Nationale de la Recherche (Young Researcher Grant (ANR-14-CE14-0019-01))

  • Brice Rotureau

Agence Nationale de la Recherche (Post-doctoral fellowship (ANR-14-CE14-0019-01))

  • Estefania Calvo-Alvarez

Agence Nationale de la Recherche (Investissement d'Avenir programme, Laboratoire d'Excellence (ANR-10-LABX-62-IBEID))

  • Paul Capewell

Institut Pasteur (N/A)

  • Estefania Calvo-Alvarez
  • Aline Crouzols
  • Grégory Jouvion
  • Brice Rotureau

Institut National de la Santé et de la Recherche Médicale (N/A)

  • Estefania Calvo-Alvarez
  • Aline Crouzols
  • Grégory Jouvion
  • Brice Rotureau

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

Ethics

Animal experimentation: This study was conducted and licenced under Home Office and SAPO regulations in the UK and in strict accordance with the recommendations from the Guide for the Care and Use of Laboratory Animals of the European Union (European Directive 2010/63/UE) and the French Government. The protocol was approved by the "Comité d'éthique en expérimentation animale de l'Institut Pasteur" CETEA 89 (Permit number: 2012-0043 and 2016-0017) and carried out in compliance with Institut Pasteur Biosafety Committee (protocol CHSCT 12.131).

Reviewing Editor

  1. Photini Sinnis, Johns Hopkins Bloomberg School of Public Health, United States

Publication history

  1. Received: May 12, 2016
  2. Accepted: September 12, 2016
  3. Accepted Manuscript published: September 22, 2016 (version 1)
  4. Version of Record published: October 14, 2016 (version 2)

Copyright

© 2016, Capewell 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

  • 16,861
    Page views
  • 1,071
    Downloads
  • 55
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

  1. Further reading

Further reading

  1. The parasites that cause African sleeping sickness can hide in the skin of healthy people.

    1. Epidemiology and Global Health
    2. Microbiology and Infectious Disease
    Sha Joe Zhu et al.
    Tools and Resources