{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T05:30:40Z","timestamp":1780378240248,"version":"3.54.1"},"reference-count":45,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T00:00:00Z","timestamp":1627430400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000062","name":"National Institute of Diabetes and Digestive and Kidney Diseases","doi-asserted-by":"publisher","award":["R01DK105829"],"award-info":[{"award-number":["R01DK105829"]}],"id":[{"id":"10.13039\/100000062","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000062","name":"National Institute of Diabetes and Digestive and Kidney Diseases","doi-asserted-by":"publisher","award":["R01DK090379"],"award-info":[{"award-number":["R01DK090379"]}],"id":[{"id":"10.13039\/100000062","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>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.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Objective<\/jats:title>\n<jats:p>We develop a mathematical model that links nutrient absorption in the upper and lower GI tract in two steps.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Methods<\/jats:title>\n<jats:p>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\u2019s 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.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Results<\/jats:title>\n<jats:p>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.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec005\">\n<jats:title>Conclusion<\/jats:title>\n<jats:p>The mathematical model developed here provides an important framework for describing the effect of clinical interventions on the colon\u2019s microorganisms.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0253542","type":"journal-article","created":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T17:32:04Z","timestamp":1627493524000},"page":"e0253542","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Developing a model for estimating the activity of colonic microbes after intestinal surgeries"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3442-6088","authenticated-orcid":true,"given":"Andrew","family":"Marcus","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Taylor L.","family":"Davis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruce E.","family":"Rittmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John K.","family":"DiBaise","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elvis A.","family":"Carnero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen","family":"Corbin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven R.","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosa","family":"Krajmalnik-Brown","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,7,28]]},"reference":[{"key":"pone.0253542.ref001","article-title":"Compositional and functional features of the gastrointestinal microbiome and their effects on human health","author":"EB Hollister","year":"2014","journal-title":"Gastroenterology"},{"key":"pone.0253542.ref002","article-title":"Brain\u2013gut\u2013microbiome interactions in obesity and food addiction","author":"A Gupta","year":"2020","journal-title":"Nature Reviews Gastroenterology and Hepatology"},{"key":"pone.0253542.ref003","article-title":"Brain-Gut-Microbiota Axis and Mental Health","author":"TG Dinan","year":"2017","journal-title":"Psychosomatic Medicine"},{"key":"pone.0253542.ref004","article-title":"The contribution of the large intestine to energy supplies in man","author":"NI McNeil","year":"1984","journal-title":"Am J Clin Nutr"},{"key":"pone.0253542.ref005","article-title":"The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism","author":"G Den Besten","year":"2013","journal-title":"Journal of Lipid Research"},{"key":"pone.0253542.ref006","article-title":"Diet rapidly and reproducibly alters the human gut microbiome","author":"LA David","year":"2014","journal-title":"Nature"},{"key":"pone.0253542.ref007","article-title":"pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures","author":"ZE Ilhan","year":"2017","journal-title":"mSphere"},{"key":"pone.0253542.ref008","doi-asserted-by":"crossref","first-page":"2365","DOI":"10.1073\/pnas.0812600106","article-title":"Human gut microbiota in obesity and after gastric bypass","volume":"106","author":"H Zhang","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0253542.ref009","article-title":"Temporospatial shifts in the human gut microbiome and metabolome after gastric bypass surgery","author":"ZE Ilhan","year":"2020","journal-title":"npj Biofilms Microbiomes"},{"key":"pone.0253542.ref010","article-title":"Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation","author":"V Tremaroli","year":"2015","journal-title":"Cell Metab"},{"key":"pone.0253542.ref011","article-title":"Gut microbiota controls adipose tissue expansion, gut barrier and glucose metabolism: Novel insights into molecular targets and interventions using prebiotics","author":"L Geurts","year":"2014","journal-title":"Beneficial Microbes"},{"key":"pone.0253542.ref012","article-title":"Gastrointestinal physiology","author":"J. McLaughlin","year":"2009","journal-title":"Surgery"},{"key":"pone.0253542.ref013","article-title":"Gut microbiota and its possible relationship with obesity","author":"JK DiBaise","year":"2008","journal-title":"Mayo Clin Proc"},{"key":"pone.0253542.ref014","article-title":"Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota","author":"MG Espey","year":"2013","journal-title":"Free Radical Biology and Medicine"},{"key":"pone.0253542.ref015","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1093\/ajcn\/64.2.222","article-title":"Importance of colonic support for energy absorption as small-bowel failure proceeds","volume":"64","author":"I Nordgaard","year":"1996","journal-title":"Am J Clin Nutr"},{"key":"pone.0253542.ref016","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1136\/gut.29.6.809","article-title":"Nitrogen losses from the human small bowel: obligatory losses and the effect of physical form of food","volume":"29","author":"A Chacko","year":"1988","journal-title":"Gut"},{"key":"pone.0253542.ref017","article-title":"Effect of water flow and chemical environment on microbiota growth and composition in the human colon","author":"J Cremer","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0253542.ref018","article-title":"Modelling the emergent dynamics and major metabolites of the human colonic microbiota","author":"H Kettle","year":"2015","journal-title":"Environ Microbiol"},{"key":"pone.0253542.ref019","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/j.jbiosc.2013.09.015","article-title":"Assessing the influence of reactor system design criteria on the performance of model colon fermentation units","volume":"117","author":"AS Moorthy","year":"2014","journal-title":"J Biosci Bioeng"},{"key":"pone.0253542.ref020","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.jtbi.2010.05.040","article-title":"Mathematical modelling of carbohydrate degradation by human colonic microbiota","volume":"266","author":"R Mu\u00f1oz-Tamayo","year":"2010","journal-title":"J Theor Biol"},{"key":"pone.0253542.ref021","article-title":"The theoretical bases of indirect calorimetry: A review","author":"E. Ferrannini","year":"1988","journal-title":"Metabolism"},{"key":"pone.0253542.ref022","unstructured":"WHO\/FAO. Food energy\u2013methods of analysis and conversion factors. Report of a technical workshop. FAO Food Nutr Pap. 2003. ISSN 0254-4725."},{"key":"pone.0253542.ref023","article-title":"Metabolizable energy of macronutrients","author":"G. Livesey","year":"1995","journal-title":"American Journal of Clinical Nutrition"},{"key":"pone.0253542.ref024","article-title":"Chemical Oxygen Demand Can Be Converted to Gross Energy for Food Items Using a Linear Regression Model","author":"TL Davis","year":"2020","journal-title":"J Nutr"},{"key":"pone.0253542.ref025","article-title":"Studies of intestinal digestion and absorption in the human","author":"B Borgstrom","year":"1957","journal-title":"J Clin Invest"},{"key":"pone.0253542.ref026","article-title":"The role of malabsorption in bariatric surgery","author":"VN Prachand","year":"2009","journal-title":"World Journal of Surgery"},{"key":"pone.0253542.ref027","article-title":"Anatomical study of the length of the human intestine","author":"G Hounnou","year":"2002","journal-title":"Surg Radiol Anat."},{"key":"pone.0253542.ref028","article-title":"Effects of Meat Cooking, and of Ingested Amount, on Protein Digestion Speed and Entry of Residual Proteins into the Colon: A Study in Minipigs","author":"ML Bax","year":"2013","journal-title":"PLoS One"},{"key":"pone.0253542.ref029","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1111\/j.1365-2672.1991.tb02739.x","article-title":"The control and consequences of bacterial fermentation in the human colon","volume":"70","author":"JH Cummings","year":"1991","journal-title":"Journal of Applied Bacteriology"},{"key":"pone.0253542.ref030","article-title":"Passage of carbohydrate into the colon. Direct measurements in humans","author":"AM Stephen","year":"1983","journal-title":"Gastroenterology"},{"key":"pone.0253542.ref031","article-title":"Ileal recovery of nutrients and mucin in humans fed total enteral formulas supplemented with soy fiber","author":"KA Lien","year":"1996","journal-title":"Am J Clin Nutr"},{"key":"pone.0253542.ref032","article-title":"The effect of ingestion of guar gum on ileostomy effluent","author":"SE Higham","year":"1992","journal-title":"Br J Nutr"},{"key":"pone.0253542.ref033","article-title":"Influence of nutrition on acid-base balance\u2014Metabolic aspects","author":"T. Remer","year":"2001","journal-title":"Eur J Nutr"},{"key":"pone.0253542.ref034","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.wasman.2007.03.028","article-title":"Hydrolysis kinetics in anaerobic degradation of particulate organic material: An overview.","volume":"28","author":"VA Vavilin","year":"2008","journal-title":"Waste Manag"},{"key":"pone.0253542.ref035","article-title":"Colonic fermentation: metabolic and clinical implications","author":"KH Soergel","year":"1994","journal-title":"in Investig"},{"key":"pone.0253542.ref036","volume-title":"Environmental biotechnology: principles and applications","author":"BE Rittmann","year":"2020","edition":"2"},{"key":"pone.0253542.ref037","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1023\/A:1013116728817","article-title":"Protein degradation during anaerobic wastewater treatment: derivation of stoichiometry","volume":"12","author":"IR Ramsay","year":"2001","journal-title":"Biodegradation"},{"key":"pone.0253542.ref038","article-title":"Absorption of Short Chain Fatty Acids in Man","author":"AM Dawson","year":"1964","journal-title":"Proc Soc Exp Biol Med"},{"key":"pone.0253542.ref039","article-title":"Absorption of short-chain fatty acids by the colon","author":"H Ruppin","year":"1980","journal-title":"Gastroenterology"},{"key":"pone.0253542.ref040","article-title":"Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides","author":"DL Topping","year":"2001","journal-title":"Physiological Reviews"},{"key":"pone.0253542.ref041","article-title":"Intestinal adaptation after massive intestinal resection","author":"AR Weale","year":"2005","journal-title":"Postgraduate Medical Journal"},{"key":"pone.0253542.ref042","article-title":"Modelling approaches for studying the microbiome","author":"M Kumar","year":"2019","journal-title":"Nature Microbiology"},{"key":"pone.0253542.ref043","article-title":"Integrative and quantitative bioenergetics: Design of a study to assess the impact of the gut microbiome on host energy balance","author":"KD Corbin","year":"2020","journal-title":"Contemp Clin Trials Commun"},{"key":"pone.0253542.ref044","article-title":"Predicting metabolic adaptation, body weight change, and energy intake in humans","author":"KD Hall","year":"2010","journal-title":"Am J Physiol\u2014Endocrinol Metab"},{"key":"pone.0253542.ref045","article-title":"A computational model to determine energy intake during weight loss","author":"DM Thomas","year":"2010","journal-title":"Am J Clin Nutr"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0253542","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T17:32:36Z","timestamp":1627493556000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0253542"}},"subtitle":[],"editor":[{"given":"Franck","family":"Carbonero","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,7,28]]},"references-count":45,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7,28]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0253542","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,28]]}}}