Skip to main content

Advertisement

Log in

Ischemic preconditioning improves stability of intestinal anastomoses in rats

  • Original Article
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Background

The aim of our study was to establish whether ischemic preconditioning (IPC) directly before performing a small bowel anastomosis has an effect on anastomotic stability and healing.

Material and methods

Forty male Wistar rats were randomized to five groups: control (CO, n = 8) with preparation of the superior mesenteric artery (SMA) but without IPC. IPC groups had different intervals of ischemia (occlusion of the SMA) and reperfusion: 10 min ischemia and 20 min reperfusion (IPC10/20, n = 7), 10 min ischemia and 30 min reperfusion (IPC10/30, n = 8), 15 min ischemia and 20 min reperfusion (IPC15/20, n = 8), and 15 min ischemia and 30 min reperfusion (IPC15/30, n = 9). On the fourth postoperative day, the animals were relaparotomized: bursting pressure, hydroxyproline concentration, and histological ischemia mucosal injury scale of the anastomosis were assessed.

Results

Four days after operation, the mean bursting pressure was 73 ± 6 mmHg in the control group, whereas it was significantly higher in IPC10/20 (113 ± 11 mmHg; p = 0.018), IPC10/30 (110 ± 13 mmHg; p = 0.001), and IPC15/30 (124 ± 9 mmHg; p = 0.003). IPC15/20 did not show a significant difference (63 ± 2 mmHg; p = 0.4). We did not find a significant effect regarding hydroxyproline concentration, but IPC diminished mucosal injury.

Conclusions

IPC directly before performing a small bowel anastomosis has a time-dependent beneficial effect on anastomotic stability, thus indicating a new clinical approach to improve the healing process of intestinal anastomosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Fielding LP, Stewart-Brown S, Blesovsky L, Kearney G (1980) Anastomotic integrity after operations for large-bowel cancer: a multicentre study. Br Med J 281:411–414

    Article  PubMed  CAS  Google Scholar 

  2. Thompson SK, Chang EY, Jobe BA (2006) Clinical review: healing in gastrointestinal anastomoses, part I. Microsurgery 26:131–136

    Article  PubMed  Google Scholar 

  3. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136

    PubMed  CAS  Google Scholar 

  4. Koti RS, Yang W, Dashwood MR, Davidson BR, Seifalian AM (2002) Effect of ischemic preconditioning on hepatic microcirculation and function in a rat model of ischemia reperfusion injury. Liver Transpl 8:1182–1191

    Article  PubMed  Google Scholar 

  5. Pang CY, Neligan P, Zhong A, He W, Xu H, Forrest CR (1997) Effector mechanism of adenosine in acute ischemic preconditioning of skeletal muscle against infarction. Am J Physiol 273:R887–R895

    PubMed  CAS  Google Scholar 

  6. Obermaier R, von Dobschuetz E, Drognitz O, Hopt UT, Benz S (2004) Ischemic preconditioning attenuates capillary no-reflow and leukocyte adherence in postischemic pancreatitis. Langenbecks Arch Surg 389:511–516

    Article  PubMed  CAS  Google Scholar 

  7. Glazier SS, O'Rourke DM, Graham DI, Welsh FA (1994) Induction of ischemic tolerance following brief focal ischemia in rat brain. J Cereb Blood Flow Metab 14:545–553

    PubMed  CAS  Google Scholar 

  8. Sakurai M, Hayashi T, Abe K, Aoki M, Sadahiro M, Tabayashi K (1998) Enhancement of heat shock protein expression after transient ischemia in the preconditioned spinal cord of rabbits. J Vasc Surg 27:720–725

    Article  PubMed  CAS  Google Scholar 

  9. Turman MA, Bates CM (1997) Susceptibility of human proximal tubular cells to hypoxia: effect of hypoxic preconditioning and comparison to glomerular cells. Ren Fail 19:47–60

    Article  PubMed  CAS  Google Scholar 

  10. Du ZY, Hicks M, Winlaw D, Spratt P, Macdonald P (1996) Ischemic preconditioning enhances donor lung preservation in the rat. J Heart Lung Transplant 15:1258–1267

    PubMed  CAS  Google Scholar 

  11. Li Y, Roth S, Laser M, Ma JX, Crosson CE (2003) Retinal preconditioning and the induction of heat-shock protein 27. Invest Ophthalmol Vis Sci 44:1299–1304

    Article  PubMed  Google Scholar 

  12. Hotter G, Closa D, Prados M et al (1996) Intestinal preconditioning is mediated by a transient increase in nitric oxide. Biochem Biophys Res Commun 222:27–32

    Article  PubMed  CAS  Google Scholar 

  13. Aksoyek S, Cinel I, Avlan D et al (2002) Intestinal ischemic preconditioning protects the intestine and reduces bacterial translocation. Shock 18:476–480

    Article  PubMed  Google Scholar 

  14. Cinel I, Avlan D, Cinel L et al (2003) Ischemic preconditioning reduces intestinal epithelial apoptosis in rats. Shock 19:588–592

    Article  PubMed  CAS  Google Scholar 

  15. Sola A, De Oca J, Gonzalez R et al (2001) Protective effect of ischemic preconditioning on cold preservation and reperfusion injury associated with rat intestinal transplantation. Ann Surg 234:98–106

    Article  PubMed  CAS  Google Scholar 

  16. Vlasov TD, Smirnov DA, Nutfullina GM (2002) Preconditioning of the small intestine to ischemia in rats. Neurosci Behav Physiol 32:449–453

    Article  PubMed  CAS  Google Scholar 

  17. Wu B, Ootani A, Iwakiri R et al (2004) Ischemic preconditioning attenuates ischemia–reperfusion-induced mucosal apoptosis by inhibiting the mitochondria-dependent pathway in rat small intestine. Am J Physiol Gastrointest Liver Physiol 286:G580–G587

    Article  PubMed  CAS  Google Scholar 

  18. Ferencz A, Szanto Z, Borsiczky B et al (2002) The effects of preconditioning on the oxidative stress in small-bowel autotransplantation. Surgery 132:877–884

    Article  PubMed  Google Scholar 

  19. Mallick IH, Yang W, Winslet MC, Seifalian AM (2005) Ischaemic preconditioning improves microvascular perfusion and oxygenation following reperfusion injury of the intestine. Br J Surg 92:1169–1176

    Article  PubMed  CAS  Google Scholar 

  20. Mallick IH, Yang W, Winslet MC, Seifalian AM (2005) Protective effects of ischemic preconditioning on the intestinal mucosal microcirculation following ischemia–reperfusion of the intestine. Microcirculation 12:615–625

    Article  PubMed  CAS  Google Scholar 

  21. Mallick IH, Yang W, Winslet MC, Seifalian AM (2004) Ischemia–reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 49:1359–1377

    Article  PubMed  CAS  Google Scholar 

  22. Reddy GK, Enwemeka CS (1996) A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 29:225–229

    Article  PubMed  CAS  Google Scholar 

  23. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN (1970) Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 101:478–483

    PubMed  CAS  Google Scholar 

  24. Thornton FJ, Barbul A (1997) Healing in the gastrointestinal tract. Surg Clin North Am 77:549–573

    Article  PubMed  CAS  Google Scholar 

  25. Schroder W, Stippel D, Gutschow C, Leers J, Holscher AH (2004) Postoperative recovery of microcirculation after gastric tube formation. Langenbecks Arch Surg 389:267–271

    Article  PubMed  Google Scholar 

  26. Lorentz T, Fok M, Wong J (1989) Anastomotic leakage after resection and bypass for esophageal cancer: lessons learned from the past. World J Surg 13:472–477

    Article  PubMed  CAS  Google Scholar 

  27. Sekido M, Yamamoto Y, Minakawa H et al (2003) Use of the “supercharge” technique in esophageal and pharyngeal reconstruction to augment microvascular blood flow. Surgery 134:420–424

    Article  PubMed  Google Scholar 

  28. Akiyama S, Kodera Y, Sekiguchi H et al (1998) Preoperative embolization therapy for esophageal operation. J Surg Oncol 69:219–223

    Article  PubMed  CAS  Google Scholar 

  29. Akiyama S, Ito S, Sekiguchi H et al (1996) Preoperative embolization of gastric arteries for esophageal cancer. Surgery 120:542–546

    Article  PubMed  CAS  Google Scholar 

  30. Kologlu M, Yorganci K, Renda N, Sayek I (2000) Effect of local and remote ischemia–reperfusion injury on healing of colonic anastomoses. Surgery 128:99–104

    Article  PubMed  CAS  Google Scholar 

  31. Tireli GA, Salman T, Ozbey H, Abbasoglu L, Toker G, Celik A (2003) The effect of pentoxifylline on intestinal anastomotic healing after ischemia. Pediatr Surg Int 19:88–90

    PubMed  Google Scholar 

  32. Posma LA, Bleichrodt RP, van Goor H, Hendriks T (2007) Transient profound mesenteric ischemia strongly affects the strength of intestinal anastomoses in the rat. Dis Colon Rectum 50:1070–1079

    Article  PubMed  Google Scholar 

  33. Siemonsma MA, de Hingh IH, de Man BM, Lomme RM, Verhofstad AA, Hendriks T (2003) Doxycycline improves wound strength after intestinal anastomosis in the rat. Surgery 133:268–276

    Article  PubMed  Google Scholar 

  34. Jonsson K, Jiborn H, Zederfeldt B (1987) Collagen metabolism in small intestinal anastomosis. Am J Surg 154:288–291

    Article  PubMed  CAS  Google Scholar 

  35. Brasken P (1991) Healing of experimental colon anastomosis. Eur J Surg Suppl 566:1–51

    PubMed  Google Scholar 

  36. Brasken P, Renvall S, Sandberg M (1991) Fibronectin and collagen gene expression in healing experimental colonic anastomoses. Br J Surg 78:1048–1052

    Article  PubMed  CAS  Google Scholar 

  37. Pasupathy S, Homer-Vanniasinkam S (2005) Ischaemic preconditioning protects against ischaemia/reperfusion injury: emerging concepts. Eur J Vasc Endovasc Surg 29:106–115

    Article  PubMed  CAS  Google Scholar 

  38. Sileri P, Sica G, Gentileschi P et al (2004) Ischemic preconditioning protects intestine from prolonged ischemia. Transplant Proc 36:283–285

    Article  PubMed  CAS  Google Scholar 

  39. Ishida T, Yarimizu K, Gute DC, Korthuis RJ (1997) Mechanisms of ischemic preconditioning. Shock 8:86–94

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Goran Marjanovic.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marjanovic, G., Jüttner, E., zur Hausen, A. et al. Ischemic preconditioning improves stability of intestinal anastomoses in rats. Int J Colorectal Dis 24, 975–981 (2009). https://doi.org/10.1007/s00384-009-0696-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00384-009-0696-0

Keywords

Navigation