The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes
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 c...
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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2016-09-01
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Series: | eLife |
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Online Access: | https://elifesciences.org/articles/17716 |
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doaj-8c9663e828074e969792198bebce2e92 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
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 |
spellingShingle |
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 The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes eLife Human African Trypanosomiasis skin reservoir transmission trypanosomes Trypanosoma brucei gambiense |
author_facet |
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 |
author_sort |
Paul Capewell |
title |
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes |
title_short |
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes |
title_full |
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes |
title_fullStr |
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes |
title_full_unstemmed |
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes |
title_sort |
skin is a significant but overlooked anatomical reservoir for vector-borne african trypanosomes |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2016-09-01 |
description |
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. |
topic |
Human African Trypanosomiasis skin reservoir transmission trypanosomes Trypanosoma brucei gambiense |
url |
https://elifesciences.org/articles/17716 |
work_keys_str_mv |
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doaj-8c9663e828074e969792198bebce2e922021-05-05T00:35:46ZengeLife Sciences Publications LtdeLife2050-084X2016-09-01510.7554/eLife.17716The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomesPaul Capewell0Christelle Cren-Travaillé1Francesco Marchesi2Pamela Johnston3Caroline Clucas4Robert A Benson5Taylor-Anne Gorman6Estefania Calvo-Alvarez7Aline Crouzols8Grégory Jouvion9Vincent Jamonneau10William Weir11M Lynn Stevenson12Kerry O'Neill13Anneli Cooper14Nono-raymond Kuispond Swar15Bruno Bucheton16Dieudonné Mumba Ngoyi17Paul Garside18Brice Rotureau19Annette MacLeod20https://orcid.org/0000-0002-0150-5049Wellcome 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 KingdomTrypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, FranceVeterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United KingdomVeterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United KingdomWellcome 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 KingdomCollege 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 KingdomWellcome 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 KingdomTrypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, FranceTrypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, FranceHuman Histopathology and Animal Models Unit, Institut Pasteur, Paris, FranceInstitut de Recherche pour le Développement, Unité Mixte de Recherche IRD-CIRAD 177, Campus International de Baillarguet, Montpellier, FranceWellcome 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 KingdomVeterinary Diagnostic Services, Veterinary School, University of Glasgow, Glasgow, United KingdomWellcome 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 KingdomWellcome 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 KingdomUniversity of Kinshasa, Kinshasa, Democratic Republic of the CongoInstitut de Recherche pour le Développement, Unité Mixte de Recherche IRD-CIRAD 177, Campus International de Baillarguet, Montpellier, FranceDepartment of Parasitology, National Institute of Biomedical Research, Kinshasa, Democratic Republic of the CongoCollege 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 KingdomTrypanosome Transmission Group, Trypanosome Cell Biology Unit, INSERM U1201, Paris, France; Department of Parasites and Insect Vectors, Institut Pasteur, Paris, FranceWellcome 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 KingdomThe 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.https://elifesciences.org/articles/17716Human African TrypanosomiasisskinreservoirtransmissiontrypanosomesTrypanosoma brucei gambiense |