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Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease

Inflammatory bowel disease (IBD) continues to increase in prevalence in industrialized countries. Major complications of IBD include formation of fibrotic strictures, fistulas, reduced absorptive function, cancer risk, and the need for surgery. In other chronic gastrointestinal disease models, stiff...

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Autores principales: Stewart, Daniel C., Berrie, Dalton, Li, Jian, Liu, Xinyue, Rickerson, Cooper, Mkoji, David, Iqbal, Atif, Tan, Sanda, Doty, Andria L., Glover, Sarah C., Simmons, Chelsey S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6040714/
https://www.ncbi.nlm.nih.gov/pubmed/29995938
http://dx.doi.org/10.1371/journal.pone.0200377
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author Stewart, Daniel C.
Berrie, Dalton
Li, Jian
Liu, Xinyue
Rickerson, Cooper
Mkoji, David
Iqbal, Atif
Tan, Sanda
Doty, Andria L.
Glover, Sarah C.
Simmons, Chelsey S.
author_facet Stewart, Daniel C.
Berrie, Dalton
Li, Jian
Liu, Xinyue
Rickerson, Cooper
Mkoji, David
Iqbal, Atif
Tan, Sanda
Doty, Andria L.
Glover, Sarah C.
Simmons, Chelsey S.
author_sort Stewart, Daniel C.
collection PubMed
description Inflammatory bowel disease (IBD) continues to increase in prevalence in industrialized countries. Major complications of IBD include formation of fibrotic strictures, fistulas, reduced absorptive function, cancer risk, and the need for surgery. In other chronic gastrointestinal disease models, stiffness has been shown to precede fibrosis; therefore, stiffness may be a reasonable indicator of progression toward stricture formation in IBD patients. Herein, we seek to quantify tissue stiffness and characterize fibrosis in patients with IBD and to compare mechanical properties of unaffected human tissue to common animal species used for IBD studies. Inflamed and unaffected tissue from IBD patients and unaffected tissue from mice, pigs, and cows were indented using a custom device to determine the effective stiffness. Histology was performed on matched tissues, and total RNA was isolated from IBD tissue samples and used for gene expression analysis of pro-fibrotic genes. We observed an increase in the effective stiffness (steady-state modulus, SSM) (p < 0.0001) and increased expression of the collagen type I gene (COL1A1, p = 0.01) in inflamed tissue compared to unaffected areas in our IBD patient cohort. We also found that increased staining of collagen fibers in submucosa positively correlated with SSM (p = 0.093). We determined that unaffected animal bowel stiffness is significantly greater than similar human tissues, suggesting additional limitations on animal models for translational investigations regarding stiffness-related hypotheses. Taken together, our data support development of tools for evaluation of bowel stiffness in IBD patients for prognostic applications that may enable more accurate prediction of those who will develop fibrosis and more precise prescription of aggressive therapies.
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spelling pubmed-60407142018-07-19 Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease Stewart, Daniel C. Berrie, Dalton Li, Jian Liu, Xinyue Rickerson, Cooper Mkoji, David Iqbal, Atif Tan, Sanda Doty, Andria L. Glover, Sarah C. Simmons, Chelsey S. PLoS One Research Article Inflammatory bowel disease (IBD) continues to increase in prevalence in industrialized countries. Major complications of IBD include formation of fibrotic strictures, fistulas, reduced absorptive function, cancer risk, and the need for surgery. In other chronic gastrointestinal disease models, stiffness has been shown to precede fibrosis; therefore, stiffness may be a reasonable indicator of progression toward stricture formation in IBD patients. Herein, we seek to quantify tissue stiffness and characterize fibrosis in patients with IBD and to compare mechanical properties of unaffected human tissue to common animal species used for IBD studies. Inflamed and unaffected tissue from IBD patients and unaffected tissue from mice, pigs, and cows were indented using a custom device to determine the effective stiffness. Histology was performed on matched tissues, and total RNA was isolated from IBD tissue samples and used for gene expression analysis of pro-fibrotic genes. We observed an increase in the effective stiffness (steady-state modulus, SSM) (p < 0.0001) and increased expression of the collagen type I gene (COL1A1, p = 0.01) in inflamed tissue compared to unaffected areas in our IBD patient cohort. We also found that increased staining of collagen fibers in submucosa positively correlated with SSM (p = 0.093). We determined that unaffected animal bowel stiffness is significantly greater than similar human tissues, suggesting additional limitations on animal models for translational investigations regarding stiffness-related hypotheses. Taken together, our data support development of tools for evaluation of bowel stiffness in IBD patients for prognostic applications that may enable more accurate prediction of those who will develop fibrosis and more precise prescription of aggressive therapies. Public Library of Science 2018-07-11 /pmc/articles/PMC6040714/ /pubmed/29995938 http://dx.doi.org/10.1371/journal.pone.0200377 Text en © 2018 Stewart et al http://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/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Stewart, Daniel C.
Berrie, Dalton
Li, Jian
Liu, Xinyue
Rickerson, Cooper
Mkoji, David
Iqbal, Atif
Tan, Sanda
Doty, Andria L.
Glover, Sarah C.
Simmons, Chelsey S.
Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title_full Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title_fullStr Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title_full_unstemmed Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title_short Quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
title_sort quantitative assessment of intestinal stiffness and associations with fibrosis in human inflammatory bowel disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6040714/
https://www.ncbi.nlm.nih.gov/pubmed/29995938
http://dx.doi.org/10.1371/journal.pone.0200377
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