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

Author:

Capewell Paul123,Cren-Travaillé Christelle45,Marchesi Francesco6,Johnston Pamela6,Clucas Caroline123,Benson Robert A278,Gorman Taylor-Anne12378,Calvo-Alvarez Estefania45,Crouzols Aline45,Jouvion Grégory9,Jamonneau Vincent10,Weir William123,Stevenson M Lynn6,O'Neill Kerry123,Cooper Anneli123,Swar Nono-raymond Kuispond11,Bucheton Bruno10,Ngoyi Dieudonné Mumba12,Garside Paul278,Rotureau Brice45,MacLeod Annette123ORCID

Affiliation:

1. Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom

2. College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom

3. Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom

4. Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France

5. Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France

6. Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom

7. Institute of Infection, Immunology and Inflammation, University of Glasgow, Glasgow, United Kingdom

8. Glasgow Biomedical Research Centre, University of Glasgow, Glasgow, United Kingdom

9. Human Histopathology and Animal Models Unit, Institut Pasteur, Paris, France

10. Institut de Recherche pour le Développement, Unité Mixte de Recherche IRD-CIRAD 177, Campus International de Baillarguet, Montpellier, France

11. University of Kinshasa, Kinshasa, Democratic Republic of the Congo

12. Department of Parasitology, National Institute of Biomedical Research, Kinshasa, 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.

Funder

Wellcome Trust

Agence Nationale de la Recherche

Institut Pasteur

Institut National de la Santé et de la Recherche Médicale

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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