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• W2790560460 abstract "Short-bowel syndrome represents the most common cause of intestinal failure and occurs when the remaining intestine cannot support fluid and nutrient needs to sustain adequate physiology and development without the use of supplemental parenteral nutrition. After intestinal loss or damage, the remnant bowel undergoes multifactorial compensatory processes, termed adaptation, which are largely driven by intraluminal nutrient exposure. Previous studies have provided insight into the biological processes and mediators after resection, however, there still remains a gap in the knowledge of more comprehensive mechanisms that drive the adaptive responses in these patients. Recent data support the microbiota as a key mediator of gut homeostasis and a potential driver of metabolism and immunomodulation after intestinal loss. In this review, we summarize the emerging ideas related to host-microbiota interactions in the intestinal adaptation processes. Short-bowel syndrome represents the most common cause of intestinal failure and occurs when the remaining intestine cannot support fluid and nutrient needs to sustain adequate physiology and development without the use of supplemental parenteral nutrition. After intestinal loss or damage, the remnant bowel undergoes multifactorial compensatory processes, termed adaptation, which are largely driven by intraluminal nutrient exposure. Previous studies have provided insight into the biological processes and mediators after resection, however, there still remains a gap in the knowledge of more comprehensive mechanisms that drive the adaptive responses in these patients. Recent data support the microbiota as a key mediator of gut homeostasis and a potential driver of metabolism and immunomodulation after intestinal loss. In this review, we summarize the emerging ideas related to host-microbiota interactions in the intestinal adaptation processes. SummaryIntestinal adaptation is a multifactorial compensatory process that occurs in the remaining bowel of intestinal failure patients after small-bowel loss or damage. This review provides an overview of the current knowledge on host-microbiota interactions and their potential ability to modulate the intestinal adaptive response. Intestinal adaptation is a multifactorial compensatory process that occurs in the remaining bowel of intestinal failure patients after small-bowel loss or damage. This review provides an overview of the current knowledge on host-microbiota interactions and their potential ability to modulate the intestinal adaptive response. Intestinal failure (IF) describes a state of reduced absorptive function in which the intestine cannot support fluid, electrolyte, or micronutrient needs that are required to sustain adequate physiology and growth without the use of intravenous supplemental parenteral nutrition (PN) and/or fluids.1Dehmer J.J. Fuller M.K. Helmrath M.A. Management of pediatric intestinal failure.Adv Pediatr. 2011; 58: 181-194Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 2Pironi L. Arends J. Baxter J. Bozzetti F. Pelaez R.B. Cuerda C. Forbes A. Gabe S. Gillanders L. Holst M. Jeppesen P.B. Joly F. Kelly D. Klek S. Irtun O. Olde Damink S.W. Panisic M. Rasmussen H.H. Staun M. Szczepanek K. Van Gossum A. Wanten G. Schneider S.M. Shaffer J. Home Artificial NChronic Intestinal FAcute Intestinal Failure Special Interest Groups of EESPEN endorsed recommendations. Definition and classification of intestinal failure in adults.Clin Nutr. 2015; 34: 171-180Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar Because of continued reliance on PN, IF has a high incidence of morbidity and mortality, and is associated with complications including gastric hypersecretion, dysbiosis, D-lactic acidosis, catheter-related bloodstream infections, and intestinal failure–associated liver disease.1Dehmer J.J. Fuller M.K. Helmrath M.A. Management of pediatric intestinal failure.Adv Pediatr. 2011; 58: 181-194Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 3Cole C.R. Frem J.C. Schmotzer B. Gewirtz A.T. Meddings J.B. Gold B.D. Ziegler T.R. The rate of bloodstream infection is high in infants with short bowel syndrome: relationship with small bowel bacterial overgrowth, enteral feeding, and inflammatory and immune responses.J Pediatr. 2010; 156 (947 e1): 941-947Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar Although there are multiple etiologies resulting in IF, short-bowel syndrome (SBS) is the most common cause in both pediatric (50%) and adult (75%) populations.4Wales P.W. Christison-Lagay E.R. Short bowel syndrome: epidemiology and etiology.Semin Pediatr Surg. 2010; 19: 3-9Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar SBS is the result of extensive surgical resection resulting from disease entities such as necrotizing enterocolitis (NEC), gastroschisis, Hirschsprung’s disease, volvulus, intestinal atresia, Crohn’s disease, pseudo-obstruction, or microvillus inclusion.1Dehmer J.J. Fuller M.K. Helmrath M.A. Management of pediatric intestinal failure.Adv Pediatr. 2011; 58: 181-194Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 2Pironi L. Arends J. Baxter J. Bozzetti F. Pelaez R.B. Cuerda C. Forbes A. Gabe S. Gillanders L. Holst M. Jeppesen P.B. Joly F. Kelly D. Klek S. Irtun O. Olde Damink S.W. Panisic M. Rasmussen H.H. Staun M. Szczepanek K. Van Gossum A. Wanten G. Schneider S.M. Shaffer J. Home Artificial NChronic Intestinal FAcute Intestinal Failure Special Interest Groups of EESPEN endorsed recommendations. Definition and classification of intestinal failure in adults.Clin Nutr. 2015; 34: 171-180Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar The multidisciplinary management of SBS has been well reviewed and focuses on gaining independence from PN.1Dehmer J.J. Fuller M.K. Helmrath M.A. Management of pediatric intestinal failure.Adv Pediatr. 2011; 58: 181-194Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar However, one major gap in clinical management is the strategies used to avoid attenuated functional ability of the remaining bowel with management decisions that we can control: diet, probiotics, antisecretion medications, and/or oral antibiotics. One example of this concept is the use of broad-spectrum antibiotics for the management of sepsis and the associated decrease in functional absorptive capacity of the bowel owing to presumable changes of the enteric flora. How do other long-term therapies that alter the microbiota affect the functional nutritional profile of patients? To address this, the first goal is to understand the mechanisms that alter the normal existing flora and contribute to the development of dysbiosis in patients with IF. The effect of the microbiota and the metabolism of luminal nutrients on the adaptive response are areas of active research and are the focus of this review. Intestinal adaptation is a spontaneous physiological compensatory process that occurs after intestinal resection to restore the digestive and absorptive capacity of the intestine. Traditionally, animal models relied on morphometric changes of the remnant bowel to measure the adaptive response. Because access to human adaptive bowel sample is not always feasible, secondary measurements such as plasma citrulline levels or absorption of inert sugars have been developed to evaluate intestinal adaptation. Different surgical animal models have been designed to better understand the premise of SBS and intestinal adaptation to find new therapies. Three common types of resection performed in SBS patients have been studied in animals: small-bowel resection (jejunoileal anastomosis), ileocecal resection (jejunocolic anastomosis), and extensive small-bowel and colon resection that results in a high-output jejunostomy.4Wales P.W. Christison-Lagay E.R. Short bowel syndrome: epidemiology and etiology.Semin Pediatr Surg. 2010; 19: 3-9Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, 5Sangild P.T. Ney D.M. Sigalet D.L. Vegge A. Burrin D. Animal models of gastrointestinal and liver diseases. Animal models of infant short bowel syndrome: translational relevance and challenges.Am J Physiol Gastrointest Liver Physiol. 2014; 307: G1147-G1168Crossref PubMed Scopus (24) Google Scholar In human beings, small-bowel resection (SBR) is associated with rapid adaptation and has the best clinical outcome. These factors have led to the SBR model being the most represented in SBS animal models.6Helmrath M.A. Erwin C.R. Shin C.E. Warner B.W. Enterocyte apoptosis is increased following small bowel resection.J Gastrointest Surg. 1998; 2: 44-49Crossref PubMed Scopus (80) Google Scholar, 7Dowling R.H. Booth C.C. Structural and functional changes following small intestinal resection in the rat.Clin Sci. 1967; 32: 139-149PubMed Google Scholar, 8Turner J.M. Wales P.W. Nation P.N. Wizzard P. Pendlebury C. Sergi C. Ball R.O. Pencharz P.B. Novel neonatal piglet models of surgical short bowel syndrome with intestinal failure.J Pediatr Gastroenterol Nutr. 2011; 52: 9-16Crossref PubMed Scopus (27) Google Scholar, 9Schall K.A. Holoyda K.A. Grant C.N. Levin D.E. Torres E.R. Maxwell A. Pollack H.A. Moats R.A. Frey M.R. Darehzereshki A. Al Alam D. Lien C. Grikscheit T.C. Adult zebrafish intestine resection: a novel model of short bowel syndrome, adaptation, and intestinal stem cell regeneration.Am J Physiol Gastrointest Liver Physiol. 2015; 309: G135-G145Crossref PubMed Google Scholar, 10Sigalet D.L. Martin G.R. Mechanisms underlying intestinal adaptation after massive intestinal resection in the rat.J Pediatr Surg. 1998; 33: 889-892Abstract Full Text PDF PubMed Scopus (0) Google Scholar However, jejunocolic anastomosis and jejunostomy are the most common surgeries resulting in clinical IF, usually as a consequence of NEC disease–related or distal small bowel lesions. The ileocecal resection (ICR) model represents a model of jejunocolic anastomosis that has been investigated in rodents as well as in pigs.11Dekaney C.M. Fong J.J. Rigby R.J. Lund P.K. Henning S.J. Helmrath M.A. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice.Am J Physiol Gastrointest Liver Physiol. 2007; 293: G1013-G1022Crossref PubMed Scopus (0) Google Scholar, 12Gillingham M.B. Dahly E.M. Carey H.V. Clark M.D. Kritsch K.R. Ney D.M. Differential jejunal and colonic adaptation due to resection and IGF-I in parenterally fed rats.Am J Physiol Gastrointest Liver Physiol. 2000; 278: G700-G709Crossref PubMed Google Scholar The jejunostomy is the least common surgical model in animal studies, however, these patients are the most challenging to manage clinically because of the massive loss of tissue and its associated functions.13Vegge A. Thymann T. Lund P. Stoll B. Bering S.B. Hartmann B. Jelsing J. Qvist N. Burrin D.G. Jeppesen P.B. Holst J.J. Sangild P.T. Glucagon-like peptide-2 induces rapid digestive adaptation following intestinal resection in preterm neonates.Am J Physiol Gastrointest Liver Physiol. 2013; 305: G277-G285Crossref PubMed Scopus (0) Google Scholar, 14Aunsholt L. Thymann T. Qvist N. Sigalet D. Husby S. Sangild P.T. Prematurity reduces functional adaptation to intestinal resection in piglets.JPEN J Parenter Enteral Nutr. 2015; 39: 668-676Crossref PubMed Scopus (7) Google Scholar The discrepancy between animal models of SBS and what is encountered clinically should be recognized when discussing long-term intestinal adaptation in SBS and IF patients. In experimental models, the remnant bowel undergoes macroscopic and microscopic structural changes within 48 hours after resection.11Dekaney C.M. Fong J.J. Rigby R.J. Lund P.K. Henning S.J. Helmrath M.A. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice.Am J Physiol Gastrointest Liver Physiol. 2007; 293: G1013-G1022Crossref PubMed Scopus (0) Google Scholar Macroscopically, the small bowel dilates and elongates. Microscopically, the adaptive responsive is characterized by stem cell expansion and an increased crypt cell proliferation resulting in taller villi and deeper crypts.6Helmrath M.A. Erwin C.R. Shin C.E. Warner B.W. Enterocyte apoptosis is increased following small bowel resection.J Gastrointest Surg. 1998; 2: 44-49Crossref PubMed Scopus (80) Google Scholar, 11Dekaney C.M. Fong J.J. Rigby R.J. Lund P.K. Henning S.J. Helmrath M.A. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice.Am J Physiol Gastrointest Liver Physiol. 2007; 293: G1013-G1022Crossref PubMed Scopus (0) Google Scholar An increase in enterocyte apoptosis also is observed after resection, and is suggested to be a response to counterbalance enhanced proliferation and maintain homeostasis.6Helmrath M.A. Erwin C.R. Shin C.E. Warner B.W. Enterocyte apoptosis is increased following small bowel resection.J Gastrointest Surg. 1998; 2: 44-49Crossref PubMed Scopus (80) Google Scholar Taken together, the bowel is adapting by increasing its available surface area to accommodate for the surgical loss thereof. After intestinal resection, an early expansion of secretory cell lineages, including Goblet and Paneth cells, occurs while the number of absorptive enterocytes increases at a later time point.15Helmrath M.A. Fong J.J. Dekaney C.M. Henning S.J. Rapid expansion of intestinal secretory lineages following a massive small bowel resection in mice.Am J Physiol Gastrointest Liver Physiol. 2007; 292: G215-G222Crossref PubMed Scopus (0) Google Scholar Early hemodynamic alterations also may contribute to local angiogenesis as well as increased tissue oxygen utilization.16Martin C.A. Perrone E.E. Longshore S.W. Toste P. Bitter K. Nair R. Guo J. Erwin C.R. Warner B.W. Intestinal resection induces angiogenesis within adapting intestinal villi.J Pediatr Surg. 2009; 44: 1077-1083Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 17Rowland K.J. Yao J. Wang L. Erwin C.R. Maslov K.I. Wang L.V. Warner B.W. Immediate alterations in intestinal oxygen saturation and blood flow after massive small bowel resection as measured by photoacoustic microscopy.J Pediatr Surg. 2012; 47: 1143-1149Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar Collectively, these changes support mucosal growth, lead to an increase in transporter cells, and promote a slower bowel transit time; ultimately enhancing the absorptive capacity of the remaining bowel.18Tappenden K.A. Intestinal adaptation following resection.JPEN J Parenter Enteral Nutr. 2014; 38: 23S-31SCrossref PubMed Scopus (64) Google Scholar, 19Weale A.R. Edwards A.G. Bailey M. Lear P.A. Intestinal adaptation after massive intestinal resection.Postgrad Med J. 2005; 81: 178-184Crossref PubMed Scopus (50) Google Scholar Because of the invasiveness of required procedures, limited data sets exist in human patients; however, similar morphologic changes have been observed.20Thompson J.S. Langnas A.N. Pinch L.W. Kaufman S. Quigley E.M. Vanderhoof J.A. Surgical approach to short-bowel syndrome. Experience in a population of 160 patients.Ann Surg. 1995; 222: 600-607Crossref PubMed Google Scholar McDuffie et al21McDuffie L.A. Bucher B.T. Erwin C.R. Wakeman D. White F.V. Warner B.W. Intestinal adaptation after small bowel resection in human infants.J Pediatr Surg. 2011; 46: 1045-1051Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar showed that increased villus height and crypt depth correlated with the length of the small bowel resected in pediatric NEC patients. Studies also have described enterocyte hyperplasia as well as changes in villus and crypt size after small-bowel resection or jejunoileal bypass.22Doldi S.B. Intestinal adaptation following jejuno-ileal bypass.Clin Nutr. 1991; 10: 138-145Abstract Full Text PDF PubMed Scopus (26) Google Scholar, 23Joly F. Mayeur C. Bruneau A. Noordine M.L. Meylheuc T. Langella P. Messing B. Duee P.H. Cherbuy C. Thomas M. Drastic changes in fecal and mucosa-associated microbiota in adult patients with short bowel syndrome.Biochimie. 2010; 92: 753-761Crossref PubMed Scopus (55) Google Scholar In contrast, some reports did not find significant morphometric changes after bowel resection in SBS patients, suggesting that the propensity for adaptation may not be universal in humans.24O'Keefe S.J. Haymond M.W. Bennet W.M. Oswald B. Nelson D.K. Shorter R.G. Long-acting somatostatin analogue therapy and protein metabolism in patients with jejunostomies.Gastroenterology. 1994; 107: 379-388Abstract Full Text PDF PubMed Google Scholar, 25Ziegler T.R. Fernandez-Estivariz C. Gu L.H. Bazargan N. Umeakunne K. Wallace T.M. Diaz E.E. Rosado K.E. Pascal R.R. Galloway J.R. Wilcox J.N. Leader L.M. Distribution of the H+/peptide transporter PepT1 in human intestine: up-regulated expression in the colonic mucosa of patients with short-bowel syndrome.Am J Clin Nutr. 2002; 75: 922-930Crossref PubMed Scopus (160) Google Scholar SBS animal models have been helpful in understanding some of the underlying processes occurring during intestinal adaptation and therefore in finding novel therapies that enhance adaptation. For example, glucagon-like peptide 2 (GLP-2) was found to be a potent epithelial trophic factor in surgical animal models, and this eventually led to the release of teduglutide (analog of GLP-2) for SBS patients.26Scott R.B. Kirk D. MacNaughton W.K. Meddings J.B. GLP-2 augments the adaptive response to massive intestinal resection in rat.Am J Physiol. 1998; 275: G911-G921Crossref PubMed Google Scholar, 27Jeppesen P.B. Teduglutide, a novel glucagon-like peptide 2 analog, in the treatment of patients with short bowel syndrome.Therap Adv Gastroenterol. 2012; 5: 159-171Crossref PubMed Scopus (0) Google Scholar, 28Jeppesen P.B. Gilroy R. Pertkiewicz M. Allard J.P. Messing B. O’Keefe S.J. Randomised placebo-controlled trial of teduglutide in reducing parenteral nutrition and/or intravenous fluid requirements in patients with short bowel syndrome.Gut. 2011; 60: 902-914Crossref PubMed Scopus (172) Google Scholar, 29Seidner D.L. Schwartz L.K. Winkler M.F. Jeejeebhoy K. Boullata J.I. Tappenden K.A. Increased intestinal absorption in the era of teduglutide and its impact on management strategies in patients with short bowel syndrome-associated intestinal failure.JPEN J Parenter Enteral Nutr. 2013; 37: 201-211Crossref PubMed Scopus (0) Google Scholar Teduglutide has been shown to increase structural adaptation with increased villus height and crypt depth as well as to improve intestinal absorptive capacity with a reduction in PN use in patients with end jejunostomy (Table 1).28Jeppesen P.B. Gilroy R. Pertkiewicz M. Allard J.P. Messing B. O’Keefe S.J. Randomised placebo-controlled trial of teduglutide in reducing parenteral nutrition and/or intravenous fluid requirements in patients with short bowel syndrome.Gut. 2011; 60: 902-914Crossref PubMed Scopus (172) Google Scholar, 30Jeppesen P.B. Hartmann B. Thulesen J. Graff J. Lohmann J. Hansen B.S. Tofteng F. Poulsen S.S. Madsen J.L. Holst J.J. Mortensen P.B. 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Long-term teduglutide for the treatment of patients with intestinal failure associated with short bowel syndrome.Clin Transl Gastroenterol. 2016; 7: e142Crossref PubMed Scopus (30) Google ScholarTable 1Intestinal Adaptation Factors and HormonesLimitationsHuman studiesAnimal studiesStructural adaptationFunctional adaptationStructural adaptationFunctional adaptationGHaSomatropin (Zorbtive, EMD Serono, Inc, Rockland, MA) and glutamine (NutreStore, Anderson Packaging, Inc, Rockford, IL) were approved by the FDA in 2003 and 2004 for clinical use in patients with SBS.No change44Scolapio J.S. Camilleri M. Fleming C.R. Oenning L.V. Burton D.D. Sebo T.J. Batts K.P. Kelly D.G. Effect of growth hormone, glutamine, and diet on adaptation in short-bowel syndrome: a randomized, controlled study.Gastroenterology. 1997; 113: 1074-1081Abstract Full Text Full Text PDF PubMed Scopus (230) Google ScholarAbsorptive capacity improved (weaned off PN)45Nucci A.M. Finegold D.N. Yaworski J.A. Kowalski L. Barksdale Jr., E.M. Results of growth trophic therapy in children with short bowel syndrome.J Pediatr Surg. 2004; 39: 335-339Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 46Goulet O. Dabbas-Tyan M. Talbotec C. Kapel N. Rosilio M. Souberbielle J.C. Corriol O. Ricour C. Colomb V. Effect of recombinant human growth hormone on intestinal absorption and body composition in children with short bowel syndrome.JPEN J Parenter Enteral Nutr. 2010; 34: 513-520Crossref PubMed Scopus (29) Google Scholar, 47Guo M. Lu C. Li Y. Early intestinal rehabilitation therapy ameliorates intestinal adaptation in children with short bowel syndrome: the long-term outcome.Am Surg. 2016; 82: 1215-1220PubMed Google Scholar, 48Byrne T.A. Wilmore D.W. Iyer K. Dibaise J. Clancy K. Robinson M.K. Chang P. Gertner J.M. Lautz D. Growth hormone, glutamine, and an optimal diet reduces parenteral nutrition in patients with short bowel syndrome.Ann Surg. 2005; 242: 655-661Crossref PubMed Scopus (0) Google ScholarMultiple studies used glutamine + GH44Scolapio J.S. Camilleri M. Fleming C.R. Oenning L.V. Burton D.D. Sebo T.J. Batts K.P. Kelly D.G. Effect of growth hormone, glutamine, and diet on adaptation in short-bowel syndrome: a randomized, controlled study.Gastroenterology. 1997; 113: 1074-1081Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar, 48Byrne T.A. Wilmore D.W. Iyer K. Dibaise J. Clancy K. Robinson M.K. Chang P. Gertner J.M. Lautz D. Growth hormone, glutamine, and an optimal diet reduces parenteral nutrition in patients with short bowel syndrome.Ann Surg. 2005; 242: 655-661Crossref PubMed Scopus (0) Google ScholarEffects disappeared after GH was stopped44Scolapio J.S. Camilleri M. Fleming C.R. Oenning L.V. Burton D.D. Sebo T.J. Batts K.P. Kelly D.G. Effect of growth hormone, glutamine, and diet on adaptation in short-bowel syndrome: a randomized, controlled study.Gastroenterology. 1997; 113: 1074-1081Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar, 47Guo M. Lu C. Li Y. Early intestinal rehabilitation therapy ameliorates intestinal adaptation in children with short bowel syndrome: the long-term outcome.Am Surg. 2016; 82: 1215-1220PubMed Google Scholar, 48Byrne T.A. Wilmore D.W. Iyer K. Dibaise J. Clancy K. Robinson M.K. Chang P. Gertner J.M. Lautz D. Growth hormone, glutamine, and an optimal diet reduces parenteral nutrition in patients with short bowel syndrome.Ann Surg. 2005; 242: 655-661Crossref PubMed Scopus (0) Google ScholarIncreased structural adaptation49Gu Y. Wu Z.H. Xie J.X. Jin D.Y. Zhuo H.C. Effects of growth hormone (rhGH) and glutamine supplemented parenteral nutrition on intestinal adaptation in short bowel rats.Clin Nutr. 2001; 20: 159-166Abstract Full Text PDF PubMed Scopus (0) Google ScholarSynergistic effect with glutamine49Gu Y. Wu Z.H. Xie J.X. Jin D.Y. Zhuo H.C. Effects of growth hormone (rhGH) and glutamine supplemented parenteral nutrition on intestinal adaptation in short bowel rats.Clin Nutr. 2001; 20: 159-166Abstract Full Text PDF PubMed Scopus (0) Google ScholarIncreased absorptive capacity44Scolapio J.S. Camilleri M. Fleming C.R. Oenning L.V. Burton D.D. Sebo T.J. Batts K.P. Kelly D.G. Effect of growth hormone, glutamine, and diet on adaptation in short-bowel syndrome: a randomized, controlled study.Gastroenterology. 1997; 113: 1074-1081Abstract Full Text Full Text PDF PubMed Scopus (230) Google ScholarEGFNo studiesAbsorptive capacity improved50Sigalet D.L. Martin G.R. Butzner J.D. Buret A. Meddings J.B. A pilot study of the use of epidermal growth factor in pediatric short bowel syndrome.J Pediatr Surg. 2005; 40: 763-768Abstract Full Text Full Text PDF PubMed Scopus (45) Google ScholarIncreased tolerance to EN50Sigalet D.L. Martin G.R. Butzner J.D. Buret A. Meddings J.B. A pilot study of the use of epidermal growth factor in pediatric short bowel syndrome.J Pediatr Surg. 2005; 40: 763-768Abstract Full Text Full Text PDF PubMed Scopus (45) Google ScholarNo changes in intestinal permeability50Sigalet D.L. Martin G.R. Butzner J.D. Buret A. Meddings J.B. A pilot study of the use of epidermal growth factor in pediatric short bowel syndrome.J Pediatr Surg. 2005; 40: 763-768Abstract Full Text Full Text PDF PubMed Scopus (45) Google ScholarIncreased structural adaptation51Erwin C.R. Helmrath M.A. Shin C.E. Falcone R.A. Stern L.E. Warner B.W. Intestinal overexpression of EGF in transgenic mice enhances adaptation after small bowel resection.Am J Physiol. 1999; 277: G533-G540PubMed Google Scholar, 52Shin C.E. Helmrath M.A. Falcone Jr., R.A. Fox J.W. Duane K.R. Erwin C.R. Warner B.W. Epidermal growth factor augments adaptation following small bowel resection: optimal dosage, route, and timing of administration.J Surg Res. 1998; 77: 11-16Abstract Full Text PDF PubMed Scopus (0) Google Scholar, 53Chaet M.S. Arya G. Ziegler M.M. Warner B.W. Epidermal growth factor enhances intestinal adaptation after massive small bowel resection.J Pediatr Surg. 1994; 29: 1035-1038Abstract Full Text PDF PubMed Scopus (107) Google ScholarTiming of administration is crucial52Shin C.E. Helmrath M.A. Falcone Jr., R.A. Fox J.W. Duane K.R. Erwin C.R. Warner B.W. Epidermal growth factor augments adaptation following small bowel resection: optimal dosage, route, and timing of administration.J Surg Res. 1998; 77: 11-16Abstract Full Text PDF PubMed Scopus (0) Google ScholarEnterocyte EGF receptor is not needed for normal intestinal adaptation after resection54Rowland K.J. McMellen M.E. Wakeman D. Wandu W.S. Erwin C.R. Warner B.W. Enterocyte expression of epidermal growth factor receptor is not required for intestinal adaptation in response to massive small bowel resection.J Pediatr Surg. 2012; 47: 1748-1753Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar, 55Sun R.C. Choi P.M. Guo J. Erwin C.R. Warner B.W. Insulin-like growth factor 2 and its enterocyte receptor are not required for adaptation in response to massive small bowel resection.J Pediatr Surg. 2014; 49: 966-970Abstract Full Text Full Text PDF PubMed Scopus (0) Google ScholarSynergistic effect with GLP-256Lim D.W. Levesque C.L. Vine D.F. Muto M. Koepke J.R. Nation P.N. Wizzard P.R. Li J. Bigam D.L. Brubaker P.L. Turner J.M. Wales P.W. Synergy of glucagon-like peptide-2 and epidermal growth factor coadministration on intestinal adaptation in neonatal piglets with short bowel syndrome.Am J Physiol Gastrointest Liver Physiol. 2017; 312: G390-G404Crossref PubMed Scopus (0) Google ScholarJejunal permeability decreased with combined EGF and GLP-256Lim D.W. Levesque C.L. Vine D.F. Muto M. Koepke J.R. Nation P.N. Wizzard P.R. Li J. Bigam D.L. Brubaker P.L. Turner J.M. Wales P.W. Synergy of glucagon-like peptide-2 and epidermal growth factor coadministration on intestinal adaptation in neonatal piglets with short bowel syndrome.Am J Physiol Gastrointest Liver Physiol. 2017; 312: G390-G404Crossref PubMed Scopus (0) Google ScholarNo change in fat absorption or weight gain56Lim D.W. Levesque C.L. Vine D.F. Muto M. Koepke J.R. Nation P.N. Wizzard P.R. Li J. Bigam D.L. Brubaker P.L. Turner J.M. Wales P.W. 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• W2790560460 created "2018-03-29" @default.
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• W2790560460 date "2018-01-01" @default.
• W2790560460 modified "2023-10-15" @default.
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