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Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection

Soil-transmitted helminths and Mycobacterium tuberculosis frequently coincide geographically and it is hypothesized that gastrointestinal helminth infection may exacerbate tuberculosis (TB) disease by suppression of Th1 and Th17 responses. However, few studies have focused on latent TB infection (LT...

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Autores principales: O'Shea, Matthew K., Fletcher, Thomas E., Muller, Julius, Tanner, Rachel, Matsumiya, Magali, Bailey, J. Wendi, Jones, Jayne, Smith, Steven G., Koh, Gavin, Horsnell, William G., Beeching, Nicholas J., Dunbar, James, Wilson, Duncan, Cunningham, Adam F., McShane, Helen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6302045/
https://www.ncbi.nlm.nih.gov/pubmed/30619265
http://dx.doi.org/10.3389/fimmu.2018.02893
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author O'Shea, Matthew K.
Fletcher, Thomas E.
Muller, Julius
Tanner, Rachel
Matsumiya, Magali
Bailey, J. Wendi
Jones, Jayne
Smith, Steven G.
Koh, Gavin
Horsnell, William G.
Beeching, Nicholas J.
Dunbar, James
Wilson, Duncan
Cunningham, Adam F.
McShane, Helen
author_facet O'Shea, Matthew K.
Fletcher, Thomas E.
Muller, Julius
Tanner, Rachel
Matsumiya, Magali
Bailey, J. Wendi
Jones, Jayne
Smith, Steven G.
Koh, Gavin
Horsnell, William G.
Beeching, Nicholas J.
Dunbar, James
Wilson, Duncan
Cunningham, Adam F.
McShane, Helen
author_sort O'Shea, Matthew K.
collection PubMed
description Soil-transmitted helminths and Mycobacterium tuberculosis frequently coincide geographically and it is hypothesized that gastrointestinal helminth infection may exacerbate tuberculosis (TB) disease by suppression of Th1 and Th17 responses. However, few studies have focused on latent TB infection (LTBI), which predominates globally. We performed a large observational study of healthy adults migrating from Nepal to the UK (n = 645). Individuals were screened for LTBI and gastrointestinal parasite infections. A significant negative association between hookworm and LTBI-positivity was seen (OR = 0.221; p = 0.039). Hookworm infection treatment did not affect LTBI conversions. Blood from individuals with hookworm had a significantly greater ability to control virulent mycobacterial growth in vitro than from those without, which was lost following hookworm treatment. There was a significant negative relationship between mycobacterial growth and eosinophil counts. Eosinophil-associated differential gene expression characterized the whole blood transcriptome of hookworm infection and correlated with improved mycobacterial control. These data provide a potential alternative explanation for the reduced prevalence of LTBI among individuals with hookworm infection, and possibly an anti-mycobacterial role for helminth-induced eosinophils.
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spelling pubmed-63020452019-01-07 Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection O'Shea, Matthew K. Fletcher, Thomas E. Muller, Julius Tanner, Rachel Matsumiya, Magali Bailey, J. Wendi Jones, Jayne Smith, Steven G. Koh, Gavin Horsnell, William G. Beeching, Nicholas J. Dunbar, James Wilson, Duncan Cunningham, Adam F. McShane, Helen Front Immunol Immunology Soil-transmitted helminths and Mycobacterium tuberculosis frequently coincide geographically and it is hypothesized that gastrointestinal helminth infection may exacerbate tuberculosis (TB) disease by suppression of Th1 and Th17 responses. However, few studies have focused on latent TB infection (LTBI), which predominates globally. We performed a large observational study of healthy adults migrating from Nepal to the UK (n = 645). Individuals were screened for LTBI and gastrointestinal parasite infections. A significant negative association between hookworm and LTBI-positivity was seen (OR = 0.221; p = 0.039). Hookworm infection treatment did not affect LTBI conversions. Blood from individuals with hookworm had a significantly greater ability to control virulent mycobacterial growth in vitro than from those without, which was lost following hookworm treatment. There was a significant negative relationship between mycobacterial growth and eosinophil counts. Eosinophil-associated differential gene expression characterized the whole blood transcriptome of hookworm infection and correlated with improved mycobacterial control. These data provide a potential alternative explanation for the reduced prevalence of LTBI among individuals with hookworm infection, and possibly an anti-mycobacterial role for helminth-induced eosinophils. Frontiers Media S.A. 2018-12-14 /pmc/articles/PMC6302045/ /pubmed/30619265 http://dx.doi.org/10.3389/fimmu.2018.02893 Text en Copyright © 2018 O'Shea, Fletcher, Muller, Tanner, Matsumiya, Bailey, Jones, Smith, Koh, Horsnell, Beeching, Dunbar, Wilson, Cunningham and McShane. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
O'Shea, Matthew K.
Fletcher, Thomas E.
Muller, Julius
Tanner, Rachel
Matsumiya, Magali
Bailey, J. Wendi
Jones, Jayne
Smith, Steven G.
Koh, Gavin
Horsnell, William G.
Beeching, Nicholas J.
Dunbar, James
Wilson, Duncan
Cunningham, Adam F.
McShane, Helen
Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title_full Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title_fullStr Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title_full_unstemmed Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title_short Human Hookworm Infection Enhances Mycobacterial Growth Inhibition and Associates With Reduced Risk of Tuberculosis Infection
title_sort human hookworm infection enhances mycobacterial growth inhibition and associates with reduced risk of tuberculosis infection
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6302045/
https://www.ncbi.nlm.nih.gov/pubmed/30619265
http://dx.doi.org/10.3389/fimmu.2018.02893
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