The American Journal of Surgery
Volume 199, Issue 2 , Pages 223-231 , February 2010

Ischemic preconditioning of small bowel mitigates the late phase of reperfusion injury: heme oxygenase mediates cytoprotection

  • Ismail H. Mallick, M.B.B.S., M.R.C.S., M.Sc., D.I.C., Ph.D.

      Affiliations

    • Gastrointestinal and Hepatobiliary Research Unit, UCL Division of Surgery and Interventional Science, Royal Free and University College Medical School, University College London, UK
    • Department of Surgery, Royal Free Hospital, Hampstead NHS Trust, London, UK
    • ,
  • Marc C. Winslet, M.D., F.R.C.S.

      Affiliations

    • Gastrointestinal and Hepatobiliary Research Unit, UCL Division of Surgery and Interventional Science, Royal Free and University College Medical School, University College London, UK
    • Department of Surgery, Royal Free Hospital, Hampstead NHS Trust, London, UK
    • ,
  • Alexander M. Seifalian, Ph.D., FIoN

      Affiliations

    • Gastrointestinal and Hepatobiliary Research Unit, UCL Division of Surgery and Interventional Science, Royal Free and University College Medical School, University College London, UK
    • Department of Surgery, Royal Free Hospital, Hampstead NHS Trust, London, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 20 7830 2901; fax: +44 20 7472 6444

Received 11 October 2008 ,Revised 28 December 2008

References 

  1. Platell CF, Coster J, McCauley RD, et al. The management of patients with the short bowel syndrome. World J Gastroenterol. 2002;8:13–20
  2. Ghanekar A, Grant D. Small bowel transplantation. Curr Opin Crit Care. 2001;7:133–137
  3. Frezza EE, Tzalis A, Fung JJ, et al. Small bowel transplantation: current progress and clinical application. Hepatogastroenterology. 1996;43:363–376
  4. Carey HV, Mangino MJ, Southard JH. Changes in gut function during hibernation: implications for bowel transplantation and surgery. Gut. 2001;49:459–461
  5. Massberg S, Messmer K. The nature of ischemia/reperfusion injury. Transplant Proc. 1998;30:4217–4223
  6. Mallick IH, Yang W, Winslet MC, et al. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Digest Dis Sci. 2004;49:1359–1377
  7. Mallick IH, Yang W, Winslet MC, et al. Ischaemic preconditioning improves microvascular perfusion and oxygenation following reperfusion injury of the intestine. Br J Surg. 2005;92:1169–1176
  8. Pasupathy S, Homer-Vanniasinkam S. Ischaemic preconditioning protects against ischaemia/reperfusion injury: emerging concepts. Eur J Vasc Endovasc Surg. 2005;29:106–115
  9. Marber MS, Latchman DS, Walker JM, et al. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation. 1993;88:1264–1272
  10. Bolli R. The late phase of preconditioning. Circul Res. 2000;87:972–983
  11. Mallick IH, Yang W, Winslet MC, et al. Protective effects of ischemic preconditioning on the intestinal mucosal microcirculation following ischemia-reperfusion of the intestine. Microcirculation. 2005;12:615–625
  12. Otterbein L, Soares M, Yamashita K, et al. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 2003;24:449–455
  13. Wasserberg N, Pileggi A, Salqar SK, et al. Heme oxygenase-1 upregulation protects against intestinal ischemia/reperfusion injury: a laboratory based study. Int J Surg. 2007;5:216–224
  14. Takahashi T, Morita K, Akagi R, et al. Heme oxygenase-1: a novel therapeutic target in oxidative tissue injuries. Curr Med Chem. 2004;11:1545–1561
  15. Guo X, Shin VY, Cho CH. Modulation of heme oxygenase in tissue injury and its implication in protection against gastrointestinal diseases. Life Sci. 2001;69:3113–3119
  16. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol. 1987;32:497–504
  17. Mallick IH, Yang WX, Winslet MC, et al. Pyrrolidine dithiocarbamate reduces ischemia-reperfusion injury of the small intestine. World J Gastroenterol. 2005;11:7308–7313
  18. Mallick IH, Winslet MC, Seifalian AM. Pyrrolidine dithiocarbamate protects the small bowel from warm ischaemia/reperfusion injury of the intestine: the role of haem oxygenase. Clin Sci Lond. 2006;111:373–380
  19. Zimmerhackl B, Parekh N, Brinkhus H, et al. The use of fluorescent labeled erythrocytes for intravital investigation of flow and local hematocrit in glomerular capillaries in the rat. Int J Microcirc Clin Exp;198:119–29.
  20. Dunn KW, Sandoval RM, Kelly KJ, et al. Functional studies of the kidney of living animals using multicolor two-photon microscopy. Am J Physiol Cell Physiol. 2002;283:C905–C916
  21. Heuser M, Pfaar O, Gralla O, et al. Impact of gastrin-releasing peptide on intestinal microcirculation after ischemia-reperfusion in rats. Digestion. 2000;61:172–180
  22. Motterlini R, Foresti R, Intaglietta R, et al. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol. 1996;270:H107–H114
  23. Chiu CJ, McArdle AH, Brown R, et al. Intestinal mucosal lesion in low-flow states (I. A morphological, hemodynamic, and metabolic reappraisal). Arch Surg. 1970;101:478–483
  24. Pascher A, Kohler S, et al. Present status and future perspectives of intestinal transplantation. Transpl Int. 2008;21:401–414
  25. Browne BJ, Johnson CP, Roza AM, et al. Endotoxemia after small bowel transplantation. Transplant Proc. 1992;24:1107
  26. Balaz P, Kudla M, Lodererova A, et al. Preservation injury to the human small bowel graft: jejunum vs. ileum. Ann Transplant. 2007;12:15–18
  27. Wolfard A, Kaszaki J, Varga S, et al. Early microcirculatory changes after ischemic preconditioning and small bowel autotransplantation. Eur Surg Res. 2007;39:284–290
  28. Kalia N, Pockley AG, Wood RF, et al. Effects of FK409 on intestinal ischemia-reperfusion injury and ischemia-induced changes in the rat mucosal villus microcirculation. Transplantation. 2001;72:1875–1880
  29. Chien S. Rheology in the microcirculation in normal and low flow states. Advances Shock Res. 1982;8:71–80
  30. Gende OA. Carbon monoxide inhibits capacitative calcium entry in human platelets. Thromb Res. 2004;114:113–119
  31. Ollinger R, Wang H, Yamashita K, et al. Therapeutic applications of bilirubin and biliverdin in transplantation. Antioxid Redox Signal. 2007;9:2175–2185
  32. Vogt BA, Alam J, Croatt AJ, et al. Acquired resistance to acute oxidative stress (Possible role of heme oxygenase and ferritin). Lab Invest. 1995;72:474–483
  33. Morisaki HF, Katayama TF, Kotake YF, et al. Carbon monoxide modulates endotoxin-induced microvascular leukocyte adhesion through platelet-dependent mechanisms. Anesthesiology. 2002;97:701–709

PII: S0002-9610(09)00129-9

doi: 10.1016/j.amjsurg.2009.01.011

The American Journal of Surgery
Volume 199, Issue 2 , Pages 223-231 , February 2010

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