Pediatric Surgery International

, Volume 21, Issue 12, pp 947–953 | Cite as

Advances in short bowel syndrome: an updated review

  • Igor Sukhotnik
  • Arnold G. Coran
  • Alexander Kramer
  • Eitan Shiloni
  • Jorge G. Mogilner
Review Article


Short bowel syndrome (SBS) continues to be an important clinical problem due to its high mortality and morbidity as well as its devastating socioeconomic effects. The past 3 years have witnessed many advances in the investigation of this condition, with the aim of elucidating the cellular and molecular mechanisms of intestinal adaptation. Such information may provide opportunities to exploit various factors that act as growth agents for the remaining bowel mucosa and may suggest new therapeutic strategies to maintain gut integrity, eliminate dependence on total parenteral nutrition, and avoid the need for intestinal transplantation. This review summarizes current research on SBS over the last few years.


Intestine Adaptation Short bowel syndrome Research Intestinal growth 


  1. 1.
    Sigalet DL (2001) Short bowel syndrome in infants and children: an overview. Semin Pediatr Surg 10:49–55CrossRefPubMedGoogle Scholar
  2. 2.
    Vanderhoof JA (1996) Short bowel syndrome. Neonat Gastroenterol 23:377–386Google Scholar
  3. 3.
    Booth IW, Lander AD (1998) Short bowel syndrome. Bailliere’s Clin Gastroenterol 12:739–772Google Scholar
  4. 4.
    DiBaise JK, Young RJ, Vanderhoof JA (2004) Intestinal rehabilitation and the short bowel syndrome. Am J Gastroenterol 99:1386–1395CrossRefPubMedGoogle Scholar
  5. 5.
    Coran AG, Spivak D, Teitelbaum DH (1999) An analysis of the morbidity and mortality of short bowel syndrome in the pediatric age group. Eur J Pediatr Surg 9:228–230PubMedGoogle Scholar
  6. 6.
    O’Brien DP, Nelson LA, Huang FS, Warner BW (2001) Intestinal adaptation: structure, function, and regulation. Semin Pediatr Surg 10:56–64CrossRefPubMedGoogle Scholar
  7. 7.
    Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedGoogle Scholar
  8. 8.
    Fan XQ, Guo YJ (2001) Apoptosis in oncology. Cell Res 11:1–7PubMedCrossRefGoogle Scholar
  9. 9.
    Que FG, Gores GJ (1996) Cell death by apoptosis: basic concepts and disease relevance for the gastroenterologist. Gastroenterology 110:1238–1243CrossRefPubMedGoogle Scholar
  10. 10.
    Jarboe MD, Juno RJ, Bernal NP, Knott AW, Zhang Y, Erwin CR, Warner BW (2004) Bax deficiency rescues resection-induced enterocyte apoptosis in mice with perturbed EGF receptor function. Surgery 136:121–126CrossRefPubMedGoogle Scholar
  11. 11.
    Juno RJ, Knott AW, Profitt SA, Jarboe MD, Zhang Y, Erwin CR, Warner BW (2004) Preventing enterocyte apoptosis after massive small bowel resection does not enhance adaptation of the intestinal mucosa. J Pediatr Surg 39:907–911CrossRefPubMedGoogle Scholar
  12. 12.
    Levine GM, Deren JJ, Yezdimir E (1976) Small bowel resection: oral intake is the stimulus for hyperplasia. Am J Dig Dis 21:542–546CrossRefPubMedGoogle Scholar
  13. 13.
    Lentze MJ (1989) Intestinal adaptation in short-bowel syndrome. Eur J Pediatr 148:294–299PubMedCrossRefGoogle Scholar
  14. 14.
    Menge H, Grafe M, Lorenz-Meyer H, Riecken EO (1975) The influence of food intake on the development of structural and functional adaptation following ileal resection in the rat. Gut 16:468–472PubMedCrossRefGoogle Scholar
  15. 15.
    Park JHY, Grandjean CJ, Hart MH, Vanderhoof JA (1989) Effects of dietary linoleic acid on mucosal adaptation after small bowel resection. Digestion 44:57–65PubMedGoogle Scholar
  16. 16.
    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 20:419–424PubMedGoogle Scholar
  17. 17.
    Sukhotnik I, Mor-Vaknin N, Drongowski RA, Coran AG, Harmon CM (2004) Effect of dietary fat on fat absorption and concomitant plasma and tissue fat composition in a rat model of short bowel syndrome. Pediatr Surg Int 20:185–191CrossRefPubMedGoogle Scholar
  18. 18.
    Sukhotnik I, Shiloni E, Krausz MM, Yakirevich E, Sabo E, Mogilner J, Coran AG, Harmon CM (2003) Low-fat diet impairs postresection intestinal adaptation in a rat model of short bowel syndrome. J Pediatr Surg 38:1182–1187CrossRefPubMedGoogle Scholar
  19. 19.
    Sukhotnik I, Gork AS, Chen M, Drongowski RA, Coran AG, Harmon CM (2001) Effect of low fat diet on lipid absorption and fatty-acid transport following bowel resection. Pediatr Surg Int 17:259–264CrossRefPubMedGoogle Scholar
  20. 20.
    Sukhotnik I, Lerner A, Sabo E, Krausz MM, Siplovich L, Coran AG, Mogilner J, Shiloni E (2003) Effects of enteral arginine supplementation on the structural intestinal adaptation in a rat model of short bowel syndrome. Dig Dis Sci 48:1346–1351PubMedCrossRefGoogle Scholar
  21. 21.
    Kirk SJ, Barbul A (1990) Role of arginine in trauma, sepsis and immunity. JPEN 14(5 suppl):226S–229SGoogle Scholar
  22. 22.
    Swartz-Basile DA, Wang L, Tang Y, Pitt HA, Rubin DC, Levin MS (2003) Vitamin A deficiency inhibits intestinal adaptation by modulating apoptosis, proliferation, and enterocyte migration. Am J Physiol Gastrointest Liver Physiol 285:G424–G432PubMedGoogle Scholar
  23. 23.
    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 39:267–272PubMedCrossRefGoogle Scholar
  24. 24.
    Shulman DI, Hu CS, Duckett G, Lavallee-Grey M (1992) Effects of short-term growth hormone therapy in rats undergoing 75% small intestinal resection. J Pediatr Gastroenterol Nutr 14:3–11PubMedCrossRefGoogle Scholar
  25. 25.
    Mainoya JR (1982) Influence of bovine growth hormone on water and NaCl absorption by the rat proximal jejunum and distal ileum. Comp Biochem Physiol 71:477–479CrossRefGoogle Scholar
  26. 26.
    Avissar NE, Ziegler TR, Toia L, Gu L, Ray EC, Berlanga-Acosta J, Sax HC (2004) ATB0/ASCT2 expression in residual rabbit bowel is decreased after massive enterectomy and is restored by growth hormone treatment. J Nutr 134:2173–2177PubMedGoogle Scholar
  27. 27.
    Wilmore DW, Lacey JM, Soultanakis RP, Bosch RL, Byrne TA (1997) Factors predicting a successful outcome after pharmacologic bowel compensation. Ann Surg 226:288–292CrossRefPubMedGoogle Scholar
  28. 28.
    Matarese LE, Seidner DL, Steiger E (2004) Growth hormone, glutamine, and modified diet for intestinal adaptation. J Am Diet Assoc 104:1265–1272CrossRefPubMedGoogle Scholar
  29. 29.
    Sukhotnik I, Shiloni E, Mogilner J, Lurie M, Hirsh M, Coran AG., M.M Krausz (2005) Effect of gender and sex hormones on structural intestinal adaptation following massive small bowel resection in rat. J Pediatr Surg 40:489–495CrossRefPubMedGoogle Scholar
  30. 30.
    Drucker DJ (2002) Gut adaptation and the glucagon-like peptides. Gut 50:428–435CrossRefPubMedGoogle Scholar
  31. 31.
    Litvak DA, Hellmich MR, Evers BM, Banker NA, Townsend CM Jr (1998) Glucagon-like peptide 2 is a potent growth factor for small intestine and colon. J Gastrointest Surg 2:146–150CrossRefPubMedGoogle Scholar
  32. 32.
    Martin GR, Wallace LE, Hartmann B, Holst JJ, Demchyshyn L, Toney K, Sigalet DL: Nutrient stimulated GLP-2 release and crypt cell proliferation in experimental short bowel syndrome. Am J Physiol Gastrointest Liver Physiol (in press)Google Scholar
  33. 33.
    Uluutku AH, Akin ML, Kurt Y, Yucel E, Cermik H, Avsar K, Celenk T (2004) Bombesin in short bowel syndrome. J Invest Surg 17:135–141CrossRefPubMedGoogle Scholar
  34. 34.
    Sukhotnik I, Khateeb K, Krausz MM, Sabo E, Siplovich L, Coran AG, Shiloni E (2002) Sandostatin impairs postresection intestinal adaptation in a rat model of short bowel syndrome. Dig Dis Sci 47:2095–2102PubMedCrossRefGoogle Scholar
  35. 35.
    Sukhotnik I, Yakirevich E, Coran AG, L.Siplovich, Hirsh M, Sabo E, Krausz M, Shiloni E (2002) Effect of transforming growth factor-alpha on intestinal adaptation in a rat model of short bowel syndrome. J Surg Res 108:235–242CrossRefPubMedGoogle Scholar
  36. 36.
    Lund PK (1994) Insulin-like growth factors. In: Dockray G, Walsh JH (eds) Gut peptides: biochemistry and physiology. Raven, New YorkGoogle Scholar
  37. 37.
    Lund PK (1998) Molecular basis of intestinal adaptation: the role of the insulin-like growth factor system. Ann N Y Acad Sci 859:18–36PubMedCrossRefGoogle Scholar
  38. 38.
    Lund PK, Moats-Staats BM, Hynes MA, Simmons JG, Jansen M, D’Ercole AJ, Van Wyk JJ (1986) Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. J Biol Chem 261:14539–14544PubMedGoogle Scholar
  39. 39.
    Han VK, Lund PK, Lee DC, D’Ercole AJ (1988) Expression of somatomedin/insulin-like growth factor messenger ribonucleic acids in the human fetus: identification, characterization, and tissue distribution. J Clin Endocrinol Metab 66:422–429PubMedCrossRefGoogle Scholar
  40. 40.
    Ziegler TR, Mantell MP, Chow JC, Rombeau JL, Smith RJ (1996) Gut adaptation and the insulin-like growth factor system: regulation by glutamine and IGF-1 administration. Am J Physiol 271:G866–G875PubMedGoogle Scholar
  41. 41.
    Vanderhoof JA, McCusker RH, Clark R, Mohammadpour H, Blackwood DJ, Harty RF, Park JH (1992) Truncated and native insulinlike growth factor I enhance mucosal adaptation after jejunoileal resection. Gastroenterology 102:1949–1956PubMedGoogle Scholar
  42. 42.
    Sukhotnik I, Mogilner J, Shamir R, Shehadeh N, Bejar J, Hirsh M, Coran AG (2005) Effect of subcutaneous insulin on intestinal adaptation in a rat model of short bowel syndrome. Pediatr Surg Int 21: 132–137CrossRefPubMedGoogle Scholar
  43. 43.
    Yang H, Antony PA, Wildhaber BE, Teitelbaum DH (2004) Intestinal intraepithelial lymphocyte gamma delta-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J Immunol 172:4151–4158PubMedGoogle Scholar
  44. 44.
    Asensio AB, Garcia-Urkia N, Aldazabal P, Bachiller P, Garcia-Arenzana JM, Eizaguirre I (2003) Incidence of bacterial translocation in four different models of experimental short bowel syndrome. Cir Pediatr 16:20–25PubMedGoogle Scholar
  45. 45.
    O’Brien DP, Nelson LA, Kemp CJ (2002) Intestinal permeability and bacterial translocation are uncoupled after small bowel resection. J Pediatr Surg 37:390–394CrossRefPubMedGoogle Scholar
  46. 46.
    Wildhaber BE, Yang H, Coran AG, Teitelbaum DH (2003) Gene alteration of intestinal intraepithelial lymphocytes in response to massive small bowel resection. Pediatr Surg Int 19:310–315CrossRefPubMedGoogle Scholar
  47. 47.
    Sukhotnik I, Krausz MM, Sabo E, Resnick M, Hirsh M, Mannheim D, Shiloni E (2003) Endotoxemia inhibits intestinal adaptation in a rat model of short bowel syndrome. Shock 19:66–70CrossRefPubMedGoogle Scholar
  48. 48.
    Forchielli ML, Walker WA (2003) Nutritional factors contributing to the development of cholestasis during total parenteral nutrition. Adv Pediatr 50:245–267PubMedGoogle Scholar
  49. 49.
    Quiros-Tejeira RE, Ament ME, Reyen L, Herzog F, Merjanian M, Olivares-Serrano N, Vargas JH (2004) Long-term parenteral nutritional support and intestinal adaptation in children with short bowel syndrome: a 25-year experience. J Pediatr 145:157–163CrossRefPubMedGoogle Scholar
  50. 50.
    Weber TR, Keller MS (2002) Adverse effects of liver dysfunction and portal hypertension on intestinal adaptation in short bowel syndrome in children. Am J Surg 184:582–586CrossRefPubMedGoogle Scholar
  51. 51.
    Lillehei RC, Manax WG, Lyons GW, Dietzman RH (1966) Transplantation of gastrointestinal organs, including small intestine and stomach. Gastroenterology 51:936–948PubMedGoogle Scholar
  52. 52.
    Atalay F, Ozcay N, Gundogdu H, Orug T, Gungor A, Akoglu M (2003) Evaluation of the outcomes of short bowel syndrome and indications for intestinal transplantation. Transplant Proc 35:3054–3056CrossRefPubMedGoogle Scholar
  53. 53.
    Grikscheit TC, Siddique A, Ochoa ER, Srinivasan A, Alsberg E, Hodin RA, Vacanti JP (2004) Tissue-engineered small intestine improves recovery after massive small bowel resection. Ann Surg 240:748–754CrossRefPubMedGoogle Scholar
  54. 54.
    Gunsar C, Vatansever HS, Arslan OA, Sencan A, Muftuoglu S, Ozbilgin K, Kaymaz F, Mir E (2004) The maturity of intestinal neomucosa: integrin expression and ultrastructural aspects. J Pediatr Surg 39:1368–1375CrossRefPubMedGoogle Scholar
  55. 55.
    Wang ZQ, Watanabe Y, Toki A (2003) Experimental assessment of small intestinal submucosa as a small bowel graft in a rat model. Pediatr Surg 38:1596–1601CrossRefGoogle Scholar
  56. 56.
    McDoniel K, Taylor B, Huey W, Eiden K, Everett S, Fleshman J, Buchman TG, Alpers D, Klein S (2004) Use of clonidine to decrease intestinal fluid losses in patients with high-output short-bowel syndrome. J Parenter Enteral Nutr 28:265–268CrossRefGoogle Scholar
  57. 57.
    Kato J, Sakamoto J, Teramukai S, Kojima H, Nakao A (2004) A prospective within-patient comparison clinical trial on the effect of parenteral cimetidine for improvement of fluid secretion and electrolyte balance in patients with short bowel syndrome. Hepatogastroenterology 51:1742–1746PubMedGoogle Scholar
  58. 58.
    Seguy D, Vahedi K, Kapel N, Souberbielle JC, Messing B (2003) Low-dose growth hormone in adult home parenteral nutrition-dependent short bowel syndrome patients: a positive study. Gastroenterology 124:293–302CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Igor Sukhotnik
    • 1
  • Arnold G. Coran
    • 2
    • 3
  • Alexander Kramer
    • 4
  • Eitan Shiloni
    • 4
  • Jorge G. Mogilner
    • 1
  1. 1.Department of Pediatric Surgery BBnai Zion Medical CenterHaifaIsrael
  2. 2.Carmel Medical Center, Rappaport Faculty of MedicineHaifaIsrael
  3. 3.Section of Pediatric Surgery, C.S. Mott Children’s HospitalUniversity of Michigan Medical SchoolAnn ArborUSA
  4. 4.Department of General SurgeryCarmel Medical Center, Rappaport Faculty of MedicineHaifaIsrael

Personalised recommendations