The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes
- College of Medical, Veterinary and Life Sciences, United Kingdom
- Institut Pasteur, France
- University of Glasgow, United Kingdom
- Institut de Recherche pour le Développement, France
- University of Kinshasa, Democratic Republic of the Congo
- National Institute of Biomedical Research, Democratic Republic of the Congo
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
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).
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.
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The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes
eLife 5:e17716.
https://doi.org/10.7554/eLife.17716
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