eLife (Sep 2016)
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes
- Paul Capewell,
- Christelle Cren-Travaillé,
- Francesco Marchesi,
- Pamela Johnston,
- Caroline Clucas,
- Robert A Benson,
- Taylor-Anne Gorman,
- Estefania Calvo-Alvarez,
- Aline Crouzols,
- Grégory Jouvion,
- Vincent Jamonneau,
- William Weir,
- M Lynn Stevenson,
- Kerry O'Neill,
- Anneli Cooper,
- Nono-raymond Kuispond Swar,
- Bruno Bucheton,
- Dieudonné Mumba Ngoyi,
- Paul Garside,
- Brice Rotureau,
- Annette MacLeod
Affiliations
- Paul Capewell
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- Christelle Cren-Travaillé
- Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France
- Francesco Marchesi
- Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
- Pamela Johnston
- Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
- Caroline Clucas
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- Robert A Benson
- College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Institute of Infection, Immunology and Inflammation, University of Glasgow, Glasgow, United Kingdom; Glasgow Biomedical Research Centre, University of Glasgow, Glasgow, United Kingdom
- Taylor-Anne Gorman
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom; Institute of Infection, Immunology and Inflammation, University of Glasgow, Glasgow, United Kingdom; Glasgow Biomedical Research Centre, University of Glasgow, Glasgow, United Kingdom
- Estefania Calvo-Alvarez
- Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France
- Aline Crouzols
- Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France
- Grégory Jouvion
- Human Histopathology and Animal Models Unit, Institut Pasteur, Paris, France
- Vincent Jamonneau
- Institut de Recherche pour le Développement, Unité Mixte de Recherche IRD-CIRAD 177, Campus International de Baillarguet, Montpellier, France
- William Weir
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- M Lynn Stevenson
- Veterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United Kingdom
- Kerry O'Neill
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- Anneli Cooper
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- Nono-raymond Kuispond Swar
- University of Kinshasa, Kinshasa, Democratic Republic of the Congo
- Bruno Bucheton
- Institut de Recherche pour le Développement, Unité Mixte de Recherche IRD-CIRAD 177, Campus International de Baillarguet, Montpellier, France
- Dieudonné Mumba Ngoyi
- Department of Parasitology, National Institute of Biomedical Research, Kinshasa, Democratic Republic of the Congo
- Paul Garside
- College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Institute of Infection, Immunology and Inflammation, University of Glasgow, Glasgow, United Kingdom; Glasgow Biomedical Research Centre, University of Glasgow, Glasgow, United Kingdom
- Brice Rotureau
- Trypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France
- Annette MacLeod
- ORCiD
- Wellcome Trust Centre for Molecular Parasitology, University of Glasgow, Glasgow, United Kingdom; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom; Henry Wellcome Building for Comparative Medical Sciences, University of Glasgow, Glasgow, United Kingdom
- DOI
- https://doi.org/10.7554/eLife.17716
- Journal volume & issue
-
Vol. 5
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.
Keywords