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Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae

Hookworms are soil-transmitted helminths that use immune-evasive strategies to persist in the human duodenum where they are responsible for anemia and protein loss. Given their location and immune regulatory effects, hookworms likely impact the bacterial microbiota. However, microbiota studies strug...

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Autores principales: Ducarmon, Q. R., Hoogerwerf, M. A., Janse, J. J., Geelen, A. R., Koopman, J. P. R., Zwittink, R. D., Goeman, J. J., Kuijper, E. J., Roestenberg, M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7714523/
https://www.ncbi.nlm.nih.gov/pubmed/33222610
http://dx.doi.org/10.1080/19490976.2020.1840764
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author Ducarmon, Q. R.
Hoogerwerf, M. A.
Janse, J. J.
Geelen, A. R.
Koopman, J. P. R.
Zwittink, R. D.
Goeman, J. J.
Kuijper, E. J.
Roestenberg, M.
author_facet Ducarmon, Q. R.
Hoogerwerf, M. A.
Janse, J. J.
Geelen, A. R.
Koopman, J. P. R.
Zwittink, R. D.
Goeman, J. J.
Kuijper, E. J.
Roestenberg, M.
author_sort Ducarmon, Q. R.
collection PubMed
description Hookworms are soil-transmitted helminths that use immune-evasive strategies to persist in the human duodenum where they are responsible for anemia and protein loss. Given their location and immune regulatory effects, hookworms likely impact the bacterial microbiota. However, microbiota studies struggle to deconvolute the effect of hookworms from confounders such as coinfections and malnutrition. We thus used an experimental human hookworm infection model to explore temporal changes in the gut microbiota before and during hookworm infection. Volunteers were dermally exposed to cumulative dosages of 50, 100 or 150 L3 Necator americanus larvae. Fecal samples were collected for microbiota profiling through 16S rRNA gene amplicon sequencing at weeks zero, four, eight, fourteen and twenty. During the acute infection phase (trial week zero to eight) no changes in bacterial diversity were detected. During the established infection phase (trial week eight to twenty), bacterial richness (Chao1, p = .0174) increased significantly over all volunteers. No relation was found between larval dosage and diversity, stability or relative abundance of individual bacterial taxa. GI symptoms were associated with an unstable microbiota during the first eight weeks and rapid recovery at week twenty. Barnesiella, amongst other taxa, was more abundant in volunteers with more GI symptoms throughout the study. In conclusion, this study showed that clinical GI symptoms following N. americanus infection are associated with temporary microbiota instability and relative abundance of specific bacterial taxa. These results suggest a possible role of hookworm-induced enteritis on microbiota stability.
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spelling pubmed-77145232020-12-10 Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae Ducarmon, Q. R. Hoogerwerf, M. A. Janse, J. J. Geelen, A. R. Koopman, J. P. R. Zwittink, R. D. Goeman, J. J. Kuijper, E. J. Roestenberg, M. Gut Microbes Research Paper Hookworms are soil-transmitted helminths that use immune-evasive strategies to persist in the human duodenum where they are responsible for anemia and protein loss. Given their location and immune regulatory effects, hookworms likely impact the bacterial microbiota. However, microbiota studies struggle to deconvolute the effect of hookworms from confounders such as coinfections and malnutrition. We thus used an experimental human hookworm infection model to explore temporal changes in the gut microbiota before and during hookworm infection. Volunteers were dermally exposed to cumulative dosages of 50, 100 or 150 L3 Necator americanus larvae. Fecal samples were collected for microbiota profiling through 16S rRNA gene amplicon sequencing at weeks zero, four, eight, fourteen and twenty. During the acute infection phase (trial week zero to eight) no changes in bacterial diversity were detected. During the established infection phase (trial week eight to twenty), bacterial richness (Chao1, p = .0174) increased significantly over all volunteers. No relation was found between larval dosage and diversity, stability or relative abundance of individual bacterial taxa. GI symptoms were associated with an unstable microbiota during the first eight weeks and rapid recovery at week twenty. Barnesiella, amongst other taxa, was more abundant in volunteers with more GI symptoms throughout the study. In conclusion, this study showed that clinical GI symptoms following N. americanus infection are associated with temporary microbiota instability and relative abundance of specific bacterial taxa. These results suggest a possible role of hookworm-induced enteritis on microbiota stability. Taylor & Francis 2020-11-23 /pmc/articles/PMC7714523/ /pubmed/33222610 http://dx.doi.org/10.1080/19490976.2020.1840764 Text en © 2020 The Author(s). Published with license by Taylor & Francis Group, LLC. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Ducarmon, Q. R.
Hoogerwerf, M. A.
Janse, J. J.
Geelen, A. R.
Koopman, J. P. R.
Zwittink, R. D.
Goeman, J. J.
Kuijper, E. J.
Roestenberg, M.
Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title_full Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title_fullStr Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title_full_unstemmed Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title_short Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae
title_sort dynamics of the bacterial gut microbiota during controlled human infection with necator americanus larvae
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7714523/
https://www.ncbi.nlm.nih.gov/pubmed/33222610
http://dx.doi.org/10.1080/19490976.2020.1840764
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