1932

Abstract

Short bowel syndrome (SBS) is a rare disease that results from extensive resection of the intestine. When the remaining absorption surface of the intestine cannot absorb enough macronutrients, micronutrients, and water, SBS results in intestinal failure (IF). Patients with SBS who suffer from IF require parenteral nutrition for survival, but long-term parenteral nutrition may lead to complications such as catheter sepsis and metabolic diseases. Spontaneous intestinal adaptation occurs weeks to months after resection, resulting in hyperplasia of the remnant gut, modification of gut hormone levels, dysbiosis, and hyperphagia. Oral nutrition and presence of the colon are two major positive drivers for this adaptation. This review aims to summarize the current knowledge of the mechanisms underlying spontaneous intestinal adaptation, particularly in response to modifications of luminal content, including nutrients. In the future, dietary manipulations could be used to treat SBS.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-011720-122203
2020-08-21
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/nutr/40/1/annurev-nutr-011720-122203.html?itemId=/content/journals/10.1146/annurev-nutr-011720-122203&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Alonso S, Yilmaz ÖH 2018. Nutritional regulation of intestinal stem cells. Annu. Rev. Nutr. 38:273–301
    [Google Scholar]
  2. 2. 
    Alpers DH. 2006. Glutamine: Do the data support the cause for glutamine supplementation in humans. Gastroenterology 130:2 Suppl. 1S106–16
    [Google Scholar]
  3. 3. 
    Amiot A, Joly F, Alves A, Panis Y, Bouhnik Y, Messing B 2009. Long-term outcome of chronic intestinal pseudo-obstruction adult patients requiring home parenteral nutrition. Am. J. Gastroenterol. 104:51262–70
    [Google Scholar]
  4. 4. 
    Amiot A, Messing B, Corcos O, Panis Y, Joly F 2013. Determinants of home parenteral nutrition dependence and survival of 268 patients with non-malignant short bowel syndrome. Clin. Nutr. 32:3368–74
    [Google Scholar]
  5. 5. 
    Aunsholt L, Thymann T, Qvist N, Sigalet D, Husby S, Sangild PT 2015. Prematurity reduces functional adaptation to intestinal resection in piglets. J. Parenter. Enter. Nutr. 39:6668–76
    [Google Scholar]
  6. 6. 
    Barker N. 2014. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol. 15:119–33
    [Google Scholar]
  7. 7. 
    Barker N, van Es JH, Kuipers J, Kujala P, van den Born M et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. . Nature 449:71651003–7
    [Google Scholar]
  8. 8. 
    Bartholome AL, Albin DM, Baker DH, Holst JJ, Tappenden KA 2004. Supplementation of total parenteral nutrition with butyrate acutely increases structural aspects of intestinal adaptation after an 80% jejunoileal resection in neonatal piglets. J. Parenter. Enter. Nutr. 28:4210–22
    [Google Scholar]
  9. 9. 
    Basak O, Beumer J, Wiebrands K, Seno H, van Oudenaarden A, Clevers H 2017. Induced quiescence of Lgr5+ stem cells in intestinal organoids enables differentiation of hormone-producing enteroendocrine cells. Cell Stem Cell 20:2177–190.e4
    [Google Scholar]
  10. 10. 
    Bétry C, Lauverjat M, Mouillot T, Bergoin C, Barnoud D et al. 2019. Hyperphagia in short bowel patients: Fat-free mass is a strong predictor. Nutrition 62:146–51
    [Google Scholar]
  11. 11. 
    Beyaz S, Mana MD, Roper J, Kedrin D, Saadatpour A et al. 2016. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature 531:759253–58
    [Google Scholar]
  12. 12. 
    Bines JE, Taylor RG, Justice F, Paris MCJ, Sourial M et al. 2002. Influence of diet complexity on intestinal adaptation following massive small bowel resection in a preclinical model. J. Gastroenterol. Hepatol. 17:111170–79
    [Google Scholar]
  13. 13. 
    Booth CC, Evans KT, Menzies T, Street DF 1959. Intestinal hypertrophy following partial resection of the small bowel in the rat. Br. J. Surg. 46:198403–10
    [Google Scholar]
  14. 14. 
    Breton J, Tennoune N, Lucas N, Francois M, Legrand R et al. 2016. Gut commensal E. coli proteins activate host satiety pathways following nutrient-induced bacterial growth. Cell Metab 23:2324–34
    [Google Scholar]
  15. 15. 
    Briet F, Flourié B, Achour L, Maurel M, Rambaud J-C, Messing B 1995. Bacterial adaptation in patients with short bowel and colon in continuity. Gastroenterology 109:51446–53
    [Google Scholar]
  16. 16. 
    Brinkman AS, Murali SG, Hitt S, Solverson PM, Holst JJ, Ney DM 2012. Enteral nutrients potentiate glucagon-like peptide-2 action and reduce dependence on parenteral nutrition in a rat model of human intestinal failure. Am. J. Physiol. Gastrointest. Liver Physiol. 303:5G610–22
    [Google Scholar]
  17. 17. 
    Brubaker PL. 2018. Glucagon-like peptide-2 and the regulation of intestinal growth and function. Compr. Physiol. 8:31185–210
    [Google Scholar]
  18. 18. 
    Buchman AL, Scolapio J, Fryer J 2003. AGA technical review on short bowel syndrome and intestinal transplantation. Gastroenterology 124:41111–34
    [Google Scholar]
  19. 19. 
    Cani PD, Knauf C. 2016. How gut microbes talk to organs: the role of endocrine and nervous routes. Mol. Metab. 5:9743–52
    [Google Scholar]
  20. 20. 
    Cavin J-B, Bado A, Le Gall M 2017. Intestinal adaptations after bariatric surgery: consequences on glucose homeostasis. Trends Endocrinol. Metab. 28:5354–64
    [Google Scholar]
  21. 21. 
    Chen WJ, Yang CL, Lai HS, Chen KM 1995. Effects of lipids on intestinal adaptation following 60% resection in rats. J. Surg. Res. 58:3253–59
    [Google Scholar]
  22. 22. 
    Choi PM, Sun RC, Guo J, Erwin CR, Warner BW 2014. High-fat diet enhances villus growth during the adaptation response to massive proximal small bowel resection. J. Gastrointest. Surg. 18:2286–94
    [Google Scholar]
  23. 23. 
    Compher CW, Kinosian BP, Metz DC 2009. Ghrelin does not predict adaptive hyperphagia in patients with short bowel syndrome. J. Parenter. Enter. Nutr. 33:4428–32
    [Google Scholar]
  24. 24. 
    Crenn P, Coudray-Lucas C, Thuillier F, Cynober L, Messing B 2000. Postabsorptive plasma citrulline concentration is a marker of absorptive enterocyte mass and intestinal failure in humans. Gastroenterology 119:61496–505
    [Google Scholar]
  25. 25. 
    Crenn P, Morin MC, Joly F, Penven S, Thuillier F, Messing B 2004. Net digestive absorption and adaptive hyperphagia in adult short bowel patients. Gut 53:91279–86
    [Google Scholar]
  26. 26. 
    Cummings DE, Overduin J, Foster-Schubert KE 2004. Gastric bypass for obesity: mechanisms of weight loss and diabetes resolution. J. Clin. Endocrinol. Metab. 89:62608–15
    [Google Scholar]
  27. 27. 
    Cummings JH, Gibson GR, Macfarlane GT 1989. Quantitative estimates of fermentation in the hind gut of man. Acta Vet. Scand. Suppl. 86:76–82
    [Google Scholar]
  28. 28. 
    Cussotto S, Sandhu KV, Dinan TG, Cryan JF 2018. The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective. Front. Neuroendocrinol. 51:80–101
    [Google Scholar]
  29. 29. 
    Dahly EM, Gillingham MB, Guo Z, Murali SG, Nelson DW et al. 2003. Role of luminal nutrients and endogenous GLP-2 in intestinal adaptation to mid-small bowel resection. Am. J. Physiol. Gastrointest. Liver Physiol. 284:4G670–82
    [Google Scholar]
  30. 30. 
    Dailey MJ. 2014. Nutrient-induced intestinal adaption and its effect in obesity. Physiol. Behav. 136:74–78
    [Google Scholar]
  31. 31. 
    DelParigi A, Tschöp M, Heiman ML, Salbe AD, Vozarova B et al. 2002. High circulating ghrelin: a potential cause for hyperphagia and obesity in Prader-Willi syndrome. J. Clin. Endocrinol. Metab. 87:125461–64
    [Google Scholar]
  32. 32. 
    Devine AA, Gonzalez A, Speck KE, Knight R, Helmrath M et al. 2013. Impact of ileocecal resection and concomitant antibiotics on the microbiome of the murine jejunum and colon. PLOS ONE 8:8e73140
    [Google Scholar]
  33. 33. 
    Drucker DJ, Erlich P, Asa SL, Brubaker PL 1996. Induction of intestinal epithelial proliferation by glucagon-like peptide 2. PNAS 93:157911–16
    [Google Scholar]
  34. 34. 
    Drucker DJ, Yusta B. 2014. Physiology and pharmacology of the enteroendocrine hormone glucagon-like peptide-2. Annu. Rev. Physiol. 76:561–83
    [Google Scholar]
  35. 35. 
    Dubé PE, Rowland KJ, Brubaker PL 2008. Glucagon-like peptide-2 activates β-catenin signaling in the mouse intestinal crypt: role of insulin-like growth factor-I. Endocrinology 149:1291–301
    [Google Scholar]
  36. 36. 
    Dunel-Erb S, Chevalier C, Laurent P, Bach A, Decrock F, Le Maho Y 2001. Restoration of the jejunal mucosa in rats refed after prolonged fasting. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129:4933–47
    [Google Scholar]
  37. 37. 
    Engstrand Lilja H, Wefer H, Nyström N, Finkel Y, Engstrand L 2015. Intestinal dysbiosis in children with short bowel syndrome is associated with impaired outcome. Microbiome 3:18
    [Google Scholar]
  38. 38. 
    Fjermestad H, Hvistendahl M, Jeppesen PB 2018. Fasting and postprandial plasma citrulline and the correlation to intestinal function evaluated by 72-hour metabolic balance studies in short bowel jejunostomy patients with intestinal failure. J. Parenter. Enter. Nutr. 42:2418–26
    [Google Scholar]
  39. 39. 
    Fouquet S, Lugo-Martínez V-H, Faussat A-M, Renaud F, Cardot P et al. 2004. Early loss of E-cadherin from cell-cell contacts is involved in the onset of anoikis in enterocytes. J. Biol. Chem. 279:4143061–69
    [Google Scholar]
  40. 40. 
    Fuglestad MA, Thompson JS. 2019. Inflammatory bowel disease and short bowel syndrome. Surg. Clin. North Am. 99:61209–21
    [Google Scholar]
  41. 41. 
    Galluser M, Belkhou R, Freund JN, Duluc I, Torp N et al. 1991. Adaptation of intestinal hydrolases to starvation in rats: effect of thyroid function. J. Comp. Physiol. B 161:4357–61
    [Google Scholar]
  42. 42. 
    Garrison AP, Dekaney CM, von Allmen DC, Lund PK, Henning SJ, Helmrath MA 2009. Early but not late administration of glucagon-like peptide-2 following ileo-cecal resection augments putative intestinal stem cell expansion. Am. J. Physiol. Gastrointest. Liver Physiol. 296:3G643–50
    [Google Scholar]
  43. 43. 
    Gehart H, Clevers H. 2019. Tales from the crypt: new insights into intestinal stem cells. Nat. Rev. Gastroenterol. Hepatol. 16:119–34
    [Google Scholar]
  44. 44. 
    Gillard L, Billiauws L, Stan-Iuga B, Ribeiro-Parenti L, Jarry A-C et al. 2016. Enhanced ghrelin levels and hypothalamic orexigenic AgRP and NPY neuropeptide expression in models of jejuno-colonic short bowel syndrome. Sci. Rep. 6:28345
    [Google Scholar]
  45. 45. 
    Gillard L, Mayeur C, Robert V, Pingenot I, Le Beyec J et al. 2017. Microbiota is involved in post-resection adaptation in humans with short bowel syndrome. Front. Physiol. 8:224
    [Google Scholar]
  46. 46. 
    Gillingham MB, Kritsch KR, Murali SG, Lund PK, Ney DM 2001. Resection upregulates the IGF-I system of parenterally fed rats with jejunocolic anastomosis. Am. J. Physiol. Gastrointest. Liver Physiol. 281:5G1158–68
    [Google Scholar]
  47. 47. 
    Gregorieff A, Wrana JL. 2017. Hippo signalling in intestinal regeneration and cancer. Curr. Opin. Cell Biol. 48:17–25
    [Google Scholar]
  48. 48. 
    Grün D, Lyubimova A, Kester L, Wiebrands K, Basak O et al. 2015. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature 525:7568251–55
    [Google Scholar]
  49. 49. 
    Guan X, Karpen HE, Stephens J, Bukowski JT, Niu S et al. 2006. GLP-2 receptor localizes to enteric neurons and endocrine cells expressing vasoactive peptides and mediates increased blood flow. Gastroenterology 130:1150–64
    [Google Scholar]
  50. 50. 
    Guan X, Stoll B, Lu X, Tappenden KA, Holst JJ et al. 2003. GLP-2-mediated up-regulation of intestinal blood flow and glucose uptake is nitric oxide-dependent in TPN-fed piglets. Gastroenterology 125:1136–47
    [Google Scholar]
  51. 51. 
    Gumus Balikcioglu P, Balikcioglu M, Muehlbauer MJ, Purnell JQ, Broadhurst D et al. 2015. Macronutrient regulation of ghrelin and peptide YY in pediatric obesity and Prader-Willi syndrome. J. Clin. Endocrinol. Metab. 100:103822–31
    [Google Scholar]
  52. 52. 
    Guo M, Li Y, Wang Z, Wu B, Wang J, Li J 2013. Morphological adaptation in adult short bowel syndrome undergoing intestinal rehabilitation. J. Investig. Surg. 26:11–5
    [Google Scholar]
  53. 53. 
    Haramis A-PG, Begthel H, van den Born M, van Es J, Jonkheer S et al. 2004. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303:56641684–86
    [Google Scholar]
  54. 54. 
    Helmrath MA, Fong JJ, Dekaney CM, Henning SJ 2007. Rapid expansion of intestinal secretory lineages following a massive small bowel resection in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 292:1G215–22
    [Google Scholar]
  55. 55. 
    Hughes CA, Dowling RH. 1980. Speed of onset of adaptive mucosal hypoplasia and hypofunction in the intestine of parenterally fed rats. Clin. Sci. 59:5317–27
    [Google Scholar]
  56. 56. 
    Ireland H, Houghton C, Howard L, Winton DJ 2005. Cellular inheritance of a Cre-activated reporter gene to determine Paneth cell longevity in the murine small intestine. Dev. Dyn. 233:41332–36
    [Google Scholar]
  57. 57. 
    Jeppesen PB. 2012. Teduglutide, a novel glucagon-like peptide 2 analog, in the treatment of patients with short bowel syndrome. Ther. Adv. Gastroenterol. 5:3159–71
    [Google Scholar]
  58. 58. 
    Jeppesen PB, Fuglsang KA. 2018. Nutritional therapy in adult short bowel syndrome patients with chronic intestinal failure. Gastroenterol. Clin. North Am. 47:161–75
    [Google Scholar]
  59. 59. 
    Jeppesen PB, Hartmann B, Thulesen J, Graff J, Lohmann J et al. 2001. Glucagon-like peptide 2 improves nutrient absorption and nutritional status in short-bowel patients with no colon. Gastroenterology 120:4806–15
    [Google Scholar]
  60. 60. 
    Jeppesen PB, Hartmann B, Thulesen J, Hansen BS, Holst JJ et al. 2000. Elevated plasma glucagon-like peptide 1 and 2 concentrations in ileum resected short bowel patients with a preserved colon. Gut 47:3370–76
    [Google Scholar]
  61. 61. 
    Jeppesen PB, Mortensen PB. 1998. The influence of a preserved colon on the absorption of medium chain fat in patients with small bowel resection. Gut 43:4478–83
    [Google Scholar]
  62. 62. 
    Jeppesen PB, Mortensen PB. 2000. Intestinal failure defined by measurements of intestinal energy and wet weight absorption. Gut 46:5701–6
    [Google Scholar]
  63. 63. 
    Jeppesen PB, Pertkiewicz M, Messing B, Iyer K, Seidner DL et al. 2012. Teduglutide reduces need for parenteral support among patients with short bowel syndrome with intestinal failure. Gastroenterology 143:61473–81.e3
    [Google Scholar]
  64. 64. 
    Jeppesen PB, Sanguinetti EL, Buchman A, Howard L, Scolapio JS et al. 2005. Teduglutide (ALX-0600), a dipeptidyl peptidase IV resistant glucagon-like peptide 2 analogue, improves intestinal function in short bowel syndrome patients. Gut 54:91224–31
    [Google Scholar]
  65. 65. 
    Joly F, Baxter J, Staun M, Kelly DG, Hwa YL et al. 2017. Five-year survival and causes of death in patients on home parenteral nutrition for severe chronic and benign intestinal failure. Clin. Nutr. 37:41415–22
    [Google Scholar]
  66. 66. 
    Joly F, Dray X, Corcos O, Barbot L, Kapel N, Messing B 2009. Tube feeding improves intestinal absorption in short bowel syndrome patients. Gastroenterology 136:3824–31
    [Google Scholar]
  67. 67. 
    Joly F, Mayeur C, Bruneau A, Noordine M-L, Meylheuc T et al. 2010. Drastic changes in fecal and mucosa-associated microbiota in adult patients with short bowel syndrome. Biochimie 92:7753–61
    [Google Scholar]
  68. 68. 
    Joly F, Mayeur C, Messing B, Lavergne-Slove A, Cazals-Hatem D et al. 2009. Morphological adaptation with preserved proliferation/transporter content in the colon of patients with short bowel syndrome. Am. J. Physiol. Gastrointest. Liver Physiol. 297:1G116–23
    [Google Scholar]
  69. 69. 
    Koopmann MC, Chen X, Holst JJ, Ney DM 2010. Sustained glucagon-like peptide-2 infusion is required for intestinal adaptation, and cessation reverses increased cellularity in rats with intestinal failure. Am. J. Physiol. Gastrointest. Liver Physiol. 299:6G1222–30
    [Google Scholar]
  70. 70. 
    Koopmann MC, Liu X, Boehler CJ, Murali SG, Holst JJ, Ney DM 2009. Colonic GLP-2 is not sufficient to promote jejunal adaptation in a PN-dependent rat model of human short bowel syndrome. J. Parenter. Enter. Nutr. 33:6629–38
    [Google Scholar]
  71. 71. 
    Korinek V, Barker N, Moerer P, van Donselaar E, Huls G et al. 1998. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19:4379–83
    [Google Scholar]
  72. 72. 
    Ksiazyk J, Piena M, Kierkus J, Lyszkowska M 2002. Hydrolyzed versus nonhydrolyzed protein diet in short bowel syndrome in children. J. Pediatr. Gastroenterol. Nutr. 35:5615–18
    [Google Scholar]
  73. 73. 
    Kuppens RJ, Diène G, Bakker NE, Molinas C, Faye S et al. 2015. Elevated ratio of acylated to unacylated ghrelin in children and young adults with Prader-Willi syndrome. Endocrine 50:3633–42
    [Google Scholar]
  74. 74. 
    Lach G, Schellekens H, Dinan TG, Cryan JF 2018. Anxiety, depression, and the microbiome: a role for gut peptides. Neurotherapeutics 15:136–59
    [Google Scholar]
  75. 75. 
    Lai SW, de Heuvel E, Wallace LE, Hartmann B, Holst JJ et al. 2017. Effects of exogenous glucagon-like peptide-2 and distal bowel resection on intestinal and systemic adaptive responses in rats. PLOS ONE 12:7e0181453
    [Google Scholar]
  76. 76. 
    Lamprecht G, Bodammer P. 2016. Nutritional strategies to enhance adaptation in intestinal failure. Curr. Opin. Organ Transplant. 21:2140–46
    [Google Scholar]
  77. 77. 
    Lapthorne S, Pereira-Fantini PM, Fouhy F, Wilson G, Thomas SL et al. 2013. Gut microbial diversity is reduced and is associated with colonic inflammation in a piglet model of short bowel syndrome. Gut Microbes 4:3212–21
    [Google Scholar]
  78. 78. 
    Larraufie P, Roberts GP, McGavigan AK, Kay RG, Li J et al. 2019. Important role of the GLP-1 axis for glucose homeostasis after bariatric surgery. Cell Rep 26:61399–408.e6
    [Google Scholar]
  79. 79. 
    Lauronen J, Pakarinen MP, Kuusanmäki P, Savilahti E, Vento P et al. 1998. Intestinal adaptation after massive proximal small-bowel resection in the pig. Scand. J. Gastroenterol. 33:2152–58
    [Google Scholar]
  80. 80. 
    Le Gall M, Thenet S, Aguanno D, Jarry A-C, Genser L et al. 2019. Intestinal plasticity in response to nutrition and gastrointestinal surgery. Nutr. Rev. 77:3129–43
    [Google Scholar]
  81. 81. 
    Lee Y-S, Kim T-Y, Kim Y, Lee S-H, Kim S et al. 2018. Microbiota-derived lactate accelerates intestinal stem-cell-mediated epithelial development. Cell Host Microbe 24:6833–46.e6
    [Google Scholar]
  82. 82. 
    Lindemans CA, Calafiore M, Mertelsmann AM, O'Connor MH, Dudakov JA et al. 2015. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528:7583560–64
    [Google Scholar]
  83. 83. 
    Lugo-Martínez V-H, Petit CS, Fouquet S, Le Beyec J, Chambaz J et al. 2009. Epidermal growth factor receptor is involved in enterocyte anoikis through the dismantling of E-cadherin-mediated junctions. Am. J. Physiol. Gastrointest. Liver Physiol. 296:2G235–44
    [Google Scholar]
  84. 84. 
    Mahe MM, Aihara E, Schumacher MA, Zavros Y, Montrose MH et al. 2013. Establishment of gastrointestinal epithelial organoids. Curr. Protoc. Mouse Biol. 3:4217–40
    [Google Scholar]
  85. 85. 
    Maljaars PWJ, Peters HPF, Mela DJ, Masclee AAM 2008. Ileal brake: a sensible food target for appetite control. A review. Physiol. Behav. 95:3271–81
    [Google Scholar]
  86. 86. 
    Mao J, Hu X, Xiao Y, Yang C, Ding Y et al. 2013. Overnutrition stimulates intestinal epithelium proliferation through β-catenin signaling in obese mice. Diabetes 62:113736–46
    [Google Scholar]
  87. 87. 
    Marchix J, Goddard G, Helmrath MA 2018. Host-gut microbiota crosstalk in intestinal adaptation. Cell. Mol. Gastroenterol. Hepatol. 6:2149–62
    [Google Scholar]
  88. 88. 
    Martin CA, Perrone EE, Longshore SW, Toste P, Bitter K et al. 2009. Intestinal resection induces angiogenesis within adapting intestinal villi. J. Pediatr. Surg. 44:61077–82
    [Google Scholar]
  89. 89. 
    Martin GR, Wallace LE, Hartmann B, Holst JJ, Demchyshyn L et al. 2005. Nutrient-stimulated GLP-2 release and crypt cell proliferation in experimental short bowel syndrome. Am. J. Physiol. Gastrointest. Liver Physiol. 288:3G431–38
    [Google Scholar]
  90. 90. 
    Martin GR, Wallace LE, Sigalet DL 2004. Glucagon-like peptide-2 induces intestinal adaptation in parenterally fed rats with short bowel syndrome. Am. J. Physiol. Gastrointest. Liver Physiol. 286:6G964–72
    [Google Scholar]
  91. 91. 
    Massagué J. 2012. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 13:10616–30
    [Google Scholar]
  92. 92. 
    Mayeur C, Gillard L, Le Beyec J, Bado A, Joly F, Thomas M 2016. Extensive intestinal resection triggers behavioral adaptation, intestinal remodeling and microbiota transition in short bowel syndrome. Microorganisms 4:116
    [Google Scholar]
  93. 93. 
    Mayeur C, Gratadoux J-J, Bridonneau C, Chegdani F, Larroque B et al. 2013. Faecal D/L lactate ratio is a metabolic signature of microbiota imbalance in patients with short bowel syndrome. PLOS ONE 8:1e54335
    [Google Scholar]
  94. 94. 
    McDuffie LA, Bucher BT, Erwin CR, Wakeman D, White FV, Warner BW 2011. Intestinal adaptation after small bowel resection in human infants. J. Pediatr. Surg. 46:61045–51
    [Google Scholar]
  95. 95. 
    McNeil NI. 1984. The contribution of the large intestine to energy supplies in man. Am. J. Clin. Nutr. 39:2338–42
    [Google Scholar]
  96. 96. 
    Messing B, Crenn P, Beau P, Boutron-Ruault MC, Rambaud J-C, Matuchansky C 1999. Long-term survival and parenteral nutrition dependence in adult patients with the short bowel syndrome. Gastroenterology 117:51043–50
    [Google Scholar]
  97. 97. 
    Messing B, Pigot F, Rongier M, Morin MC, Ndeïndoum U, Rambaud J-C 1991. Intestinal absorption of free oral hyperalimentation in the very short bowel syndrome. Gastroenterology 100:61502–8
    [Google Scholar]
  98. 98. 
    Molina A, Pita A, Farriol M, Virgili N, Soler J, Gómez JM 2000. Serum leptin concentrations in patients with short-bowel syndrome. Clin. Nutr. 19:5333–38
    [Google Scholar]
  99. 99. 
    Neelis EG, Olieman, JF Hulst, JM de Koning, BAE Wijnen, RMH Rings EHHM 2016. Promoting intestinal adaptation by nutrition and medication. Best Pract. Res. Clin. Gastroenterol. 30:2249–61
    [Google Scholar]
  100. 100. 
    Nightingale JM, Kamm MA, van der Sijp JR, Ghatei MA, Bloom SR, Lennard-Jones JE 1996. Gastrointestinal hormones in short bowel syndrome. Peptide YY may be the “colonic brake” to gastric emptying. Gut 39:2267–72
    [Google Scholar]
  101. 101. 
    Nightingale JM, Kamm MA, van der Sijp JR, Morris GP, Walker ER et al. 1993. Disturbed gastric emptying in the short bowel syndrome. Evidence for a “colonic brake. .” Gut 34:91171–76
    [Google Scholar]
  102. 102. 
    Nordgaard I, Hansen BS, Mortensen PB 1994. Colon as a digestive organ in patients with short bowel. Lancet 343:8894373–76
    [Google Scholar]
  103. 103. 
    Nordgaard I, Hansen BS, Mortensen PB 1996. Importance of colonic support for energy absorption as small-bowel failure proceeds. Am. J. Clin. Nutr. 64:2222–31
    [Google Scholar]
  104. 104. 
    Nosworthy MG, Dodge ME, Bertolo RF, Brunton JA 2016. Enterally delivered dipeptides improve small intestinal inflammatory status in a piglet model of intestinal resection. Clin. Nutr. 35:4852–58
    [Google Scholar]
  105. 105. 
    Nusse R, Clevers H. 2017. Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell 169:6985–99
    [Google Scholar]
  106. 106. 
    O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep 7:7688–93
    [Google Scholar]
  107. 107. 
    Peck BCE, Shanahan MT, Singh AP, Sethupathy P 2017. Gut microbial influences on the mammalian intestinal stem cell niche. Stem Cells Int 2017:5604727
    [Google Scholar]
  108. 108. 
    Pironi L, Arends J, Baxter J, Bozzetti F, Peláez RB et al. 2015. ESPEN endorsed recommendations. Definition and classification of intestinal failure in adults. Clin. Nutr. 34:2171–80
    [Google Scholar]
  109. 109. 
    Pironi L, Goulet O, Buchman A, Messing B, Gabe S et al. 2012. Outcome on home parenteral nutrition for benign intestinal failure: a review of the literature and benchmarking with the European prospective survey of ESPEN. Clin. Nutr. 31:6831–45
    [Google Scholar]
  110. 110. 
    Qandeel HG, Alonso F, Hernandez DJ, Madhavan S, Duenes JA et al. 2011. Peptide absorption after massive proximal small bowel resection: mechanisms of ileal adaptation. J. Gastrointest. Surg. 15:91537–47
    [Google Scholar]
  111. 111. 
    Queipo-Ortuño MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM et al. 2013. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLOS ONE 8:5e65465
    [Google Scholar]
  112. 112. 
    Quinn R. 2005. Comparing rat's to human's age: How old is my rat in people years. Nutrition 21:6775–77
    [Google Scholar]
  113. 113. 
    Reigstad CS, Salmonson CE, Rainey JF 3rd, Szurszewski JH, Linden DR et al. 2014. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J 29:41395–403
    [Google Scholar]
  114. 114. 
    Richmond CA, Shah MS, Deary LT, Trotier DC, Thomas H et al. 2015. Dormant intestinal stem cells are regulated by PTEN and nutritional status. Cell Rep 13:112403–11
    [Google Scholar]
  115. 115. 
    Rowland KJ, Trivedi S, Lee D, Wan K, Kulkarni RN et al. 2011. Loss of glucagon-like peptide-2-induced proliferation following intestinal epithelial insulin-like growth factor-1-receptor deletion. Gastroenterology 141:62166–75.e7
    [Google Scholar]
  116. 116. 
    Sancho R, Cremona CA, Behrens A 2015. Stem cell and progenitor fate in the mammalian intestine: Notch and lateral inhibition in homeostasis and disease. EMBO Rep 16:5571–81
    [Google Scholar]
  117. 117. 
    Sangild PT, Ney DM, Sigalet DL, Vegge A, Burrin D 2014. Animal models of gastrointestinal and liver diseases. Animal models of infant short bowel syndrome: translational relevance and challenges. Am. J. Physiol. Gastrointest. Liver Physiol. 307:12G1147–68
    [Google Scholar]
  118. 118. 
    Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG et al. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:7330415–18
    [Google Scholar]
  119. 119. 
    Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:7244262–65
    [Google Scholar]
  120. 120. 
    Schall KA, Holoyda KA, Grant CN, Levin DE, Torres ER et al. 2015. Adult zebrafish intestine resection: a novel model of short bowel syndrome, adaptation, and intestinal stem cell regeneration. Am. J. Physiol. Gastrointest. Liver Physiol. 309:3G135–45
    [Google Scholar]
  121. 121. 
    Scott RB, Kirk D, MacNaughton WK, Meddings JB 1998. GLP-2 augments the adaptive response to massive intestinal resection in rat. Am. J. Physiol. 275:5G911–21
    [Google Scholar]
  122. 122. 
    Seidner DL, Joly F, Youssef NN 2015. Effect of teduglutide, a glucagon-like peptide 2 analog, on citrulline levels in patients with short bowel syndrome in two phase III randomized trials. Clin. Transl. Gastroenterol. 6:e93
    [Google Scholar]
  123. 123. 
    Sigalet DL, Bawazir O, Martin GR, Wallace LE, Zaharko G et al. 2006. Glucagon-like peptide-2 induces a specific pattern of adaptation in remnant jejunum. Dig. Dis. Sci. 51:91557–66
    [Google Scholar]
  124. 124. 
    Sigalet DL, Martin GR, Butzner JD, Buret A, Meddings JB 2005. A pilot study of the use of epidermal growth factor in pediatric short bowel syndrome. J. Pediatr. Surg. 40:5763–68
    [Google Scholar]
  125. 125. 
    Steinert RE, Feinle-Bisset C, Asarian L, Horowitz M, Beglinger C, Geary N 2017. Ghrelin, CCK, GLP-1, and PYY(3–36): secretory controls and physiological roles in eating and glycemia in health, obesity, and after RYGB. Physiol. Rev. 97:1411–63
    [Google Scholar]
  126. 126. 
    Stephens RW, Arhire L, Covasa M 2018. Gut microbiota: from microorganisms to metabolic organ influencing obesity. Obesity 26:5801–9
    [Google Scholar]
  127. 127. 
    Stubbs RJ, Hopkins M, Finlayson GS, Duarte C, Gibbons C, Blundell JE 2018. Potential effects of fat mass and fat-free mass on energy intake in different states of energy balance. Eur. J. Clin. Nutr. 72:5698–709
    [Google Scholar]
  128. 128. 
    Sugimoto S, Ohta Y, Fujii M, Matano M, Shimokawa M et al. 2018. Reconstruction of the human colon epithelium in vivo. Cell Stem Cell 22:2171–176.e5
    [Google Scholar]
  129. 129. 
    Sukhotnik I, Coran AG, Pollak Y, Kuhnreich E, Berkowitz D, Saxena AK 2017. Activated Notch signaling cascade is correlated with stem cell differentiation toward absorptive progenitors after massive small bowel resection in a rat. Am. J. Physiol. Gastrointest. Liver Physiol. 313:3G247–55
    [Google Scholar]
  130. 130. 
    Sukhotnik I, Mor-Vaknin N, Drongowski RA, Miselevich I, Coran AG, Harmon CM 2004. Effect of dietary fat on early morphological intestinal adaptation in a rat with short bowel syndrome. Pediatr. Surg. Int. 20:6419–24
    [Google Scholar]
  131. 131. 
    Sukhotnik I, Shiloni E, Krausz MM, Yakirevich E, Sabo E et al. 2003. Low-fat diet impairs postresection intestinal adaptation in a rat model of short bowel syndrome. J. Pediatr. Surg. 38:81182–87
    [Google Scholar]
  132. 132. 
    Sun RC, Choi PM, Diaz-Miron J, Sommovilla J, Guo J et al. 2015. High-protein diet improves postoperative weight gain after massive small-bowel resection. J. Gastrointest. Surg. 19:3451–57
    [Google Scholar]
  133. 133. 
    Tappenden KA. 2014. Intestinal adaptation following resection. J. Parenter. Enter. Nutr. 38:1 Suppl.23S–31S
    [Google Scholar]
  134. 134. 
    Tappenden KA, Thomson AB, Wild GE, McBurney MI 1996. Short-chain fatty acids increase proglucagon and ornithine decarboxylase messenger RNAs after intestinal resection in rats. J. Parenter. Enter. Nutr. 20:5357–62
    [Google Scholar]
  135. 135. 
    Tappenden KA, Thomson AB, Wild GE, McBurney MI 1997. Short-chain fatty acid-supplemented total parenteral nutrition enhances functional adaptation to intestinal resection in rats. Gastroenterology 112:3792–802
    [Google Scholar]
  136. 136. 
    Thymann T, Stoll B, Mecklenburg L, Burrin DG, Vegge A et al. 2014. Acute effects of the glucagon-like peptide 2 analogue, teduglutide, on intestinal adaptation in short bowel syndrome. J. Pediatr. Gastroenterol. Nutr. 58:6694–702
    [Google Scholar]
  137. 137. 
    van der Heijden M, Vermeulen L 2019. Stem cells in homeostasis and cancer of the gut. Mol. Cancer 18:166
    [Google Scholar]
  138. 138. 
    Vanderhoof JA, Grandjean CJ, Kaufman SS, Burkley KT, Antonson DL 1984. Effect of high percentage medium-chain triglyceride diet on mucosal adaptation following massive bowel resection in rats. J. Parenter. Enter. Nutr. 8:6685–89
    [Google Scholar]
  139. 139. 
    Vegge A, Thymann T, Lund P, Stoll B, Bering SB et al. 2013. Glucagon-like peptide-2 induces rapid digestive adaptation following intestinal resection in preterm neonates. Am. J. Physiol. Gastrointest. Liver Physiol. 305:4G277–85
    [Google Scholar]
  140. 140. 
    Weser E, Babbitt J, Hoban M, Vandeventer A 1986. Intestinal adaptation. Different growth responses to disaccharides compared with monosaccharides in rat small bowel. Gastroenterology 91:61521–27
    [Google Scholar]
  141. 141. 
    Williams JM, Duckworth CA, Burkitt MD, Watson AJM, Campbell BJ, Pritchard DM 2015. Epithelial cell shedding and barrier function: a matter of life and death at the small intestinal villus tip. Vet. Pathol. 52:3445–55
    [Google Scholar]
  142. 142. 
    Wong VWY, Stange DE, Page ME, Buczacki S, Wabik A et al. 2012. Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol. 14:4401–8
    [Google Scholar]
  143. 143. 
    Xiao W, Feng Y, Holst JJ, Hartmann B, Yang H, Teitelbaum DH 2014. Glutamate prevents intestinal atrophy via luminal nutrient sensing in a mouse model of total parenteral nutrition. FASEB J 28:52073–87
    [Google Scholar]
  144. 144. 
    Yilmaz ÖH, Katajisto P, Lamming DW, Gültekin Y, Bauer-Rowe KE et al. 2012. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486:7404490–95
    [Google Scholar]
  145. 145. 
    Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T et al. 2012. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 18:4618–23
    [Google Scholar]
  146. 146. 
    Yusta B, Matthews D, Koehler JA, Pujadas G, Kaur KD, Drucker DJ 2019. Localization of glucagon-like peptide-2 receptor expression in the mouse. Endocrinology 160:81950–63
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-011720-122203
Loading
/content/journals/10.1146/annurev-nutr-011720-122203
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error