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Developing a model for estimating the activity of colonic microbes after intestinal surgeries

BACKGROUND: The large intestine provides a compensatory role in energy recovery when surgical interventions such as extensive small intestinal resections or bypass operations lower the efficiency of nutrient absorption in the upper gastrointestinal (GI) tract. While microorganisms in the colon are k...

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Autores principales: Marcus, Andrew, Davis, Taylor L., Rittmann, Bruce E., DiBaise, John K., Carnero, Elvis A., Corbin, Karen, Smith, Steven R., Krajmalnik-Brown, Rosa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318292/
https://www.ncbi.nlm.nih.gov/pubmed/34319981
http://dx.doi.org/10.1371/journal.pone.0253542
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author Marcus, Andrew
Davis, Taylor L.
Rittmann, Bruce E.
DiBaise, John K.
Carnero, Elvis A.
Corbin, Karen
Smith, Steven R.
Krajmalnik-Brown, Rosa
author_facet Marcus, Andrew
Davis, Taylor L.
Rittmann, Bruce E.
DiBaise, John K.
Carnero, Elvis A.
Corbin, Karen
Smith, Steven R.
Krajmalnik-Brown, Rosa
author_sort Marcus, Andrew
collection PubMed
description BACKGROUND: The large intestine provides a compensatory role in energy recovery when surgical interventions such as extensive small intestinal resections or bypass operations lower the efficiency of nutrient absorption in the upper gastrointestinal (GI) tract. While microorganisms in the colon are known to play vital roles in recovering energy, their contributions remain to be qualified and quantified in the small intestine resection. OBJECTIVE: We develop a mathematical model that links nutrient absorption in the upper and lower GI tract in two steps. METHODS: First, we describe the effects of small intestine resection on the ileocecal output (ICO), which enters the colon and provides food for microbes. Second, we describe energy recovered by the colon’s microorganisms via short-chain fatty acid (SCFA) production. We obtain model parameters by performing a least-squares regression analysis on clinical data for subjects with normal physiology and those who had undergone small intestine resection. RESULTS: For subjects with their intestines intact, our model provided a metabolizable energy value that aligns well with the traditional Atwater coefficients. With removal of the small intestine, physiological absorption became less efficient, and the metabolizable energy decreased. In parallel, the inefficiencies in physiological absorption by the small intestine are partly compensated by production of short-chain fatty acids (SCFA) from proteins and carbohydrates by microorganisms in the colon. The colon recovered more than half of the gross energy intake when the entire small intestine was removed. Meanwhile, the quality of energy absorbed changed, because microbe-derived SCFAs, not the original components of food, become the dominant form of absorbed energy. CONCLUSION: The mathematical model developed here provides an important framework for describing the effect of clinical interventions on the colon’s microorganisms.
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spelling pubmed-83182922021-07-31 Developing a model for estimating the activity of colonic microbes after intestinal surgeries Marcus, Andrew Davis, Taylor L. Rittmann, Bruce E. DiBaise, John K. Carnero, Elvis A. Corbin, Karen Smith, Steven R. Krajmalnik-Brown, Rosa PLoS One Research Article BACKGROUND: The large intestine provides a compensatory role in energy recovery when surgical interventions such as extensive small intestinal resections or bypass operations lower the efficiency of nutrient absorption in the upper gastrointestinal (GI) tract. While microorganisms in the colon are known to play vital roles in recovering energy, their contributions remain to be qualified and quantified in the small intestine resection. OBJECTIVE: We develop a mathematical model that links nutrient absorption in the upper and lower GI tract in two steps. METHODS: First, we describe the effects of small intestine resection on the ileocecal output (ICO), which enters the colon and provides food for microbes. Second, we describe energy recovered by the colon’s microorganisms via short-chain fatty acid (SCFA) production. We obtain model parameters by performing a least-squares regression analysis on clinical data for subjects with normal physiology and those who had undergone small intestine resection. RESULTS: For subjects with their intestines intact, our model provided a metabolizable energy value that aligns well with the traditional Atwater coefficients. With removal of the small intestine, physiological absorption became less efficient, and the metabolizable energy decreased. In parallel, the inefficiencies in physiological absorption by the small intestine are partly compensated by production of short-chain fatty acids (SCFA) from proteins and carbohydrates by microorganisms in the colon. The colon recovered more than half of the gross energy intake when the entire small intestine was removed. Meanwhile, the quality of energy absorbed changed, because microbe-derived SCFAs, not the original components of food, become the dominant form of absorbed energy. CONCLUSION: The mathematical model developed here provides an important framework for describing the effect of clinical interventions on the colon’s microorganisms. Public Library of Science 2021-07-28 /pmc/articles/PMC8318292/ /pubmed/34319981 http://dx.doi.org/10.1371/journal.pone.0253542 Text en © 2021 Marcus et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Marcus, Andrew
Davis, Taylor L.
Rittmann, Bruce E.
DiBaise, John K.
Carnero, Elvis A.
Corbin, Karen
Smith, Steven R.
Krajmalnik-Brown, Rosa
Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title_full Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title_fullStr Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title_full_unstemmed Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title_short Developing a model for estimating the activity of colonic microbes after intestinal surgeries
title_sort developing a model for estimating the activity of colonic microbes after intestinal surgeries
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318292/
https://www.ncbi.nlm.nih.gov/pubmed/34319981
http://dx.doi.org/10.1371/journal.pone.0253542
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