Original Communications| Volume 128, ISSUE 1, P99-104, July 2000

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Effect of local and remote ischemia-reperfusion injury on healing of colonic anastomoses


      Background: Although the effect of locally applied ischemia-reperfusion (I-R) injury on gastrointestinal anastomoses has been studied, to our knowledge there is no previous study that investigates the effect of remote I-R injury on gastrointestinal anastomotic healing. The aim of this study was to investigate and compare the effects of local I-R injury and remote I-R injury on the healing of colonic anastomoses. Methods: Anastomosis of the right colon was performed in 30 rats that were divided into 5 groups. Group 1 was the control group. In Group 2, I-R was applied to the colonic segment containing the anastomosis. Unilateral lower extremity I-R, unilateral renal I-R, and segmental small intestinal I-R was applied to the rats in Groups 3, 4, and 5, respectively, at the same time as colonic anastomosis. On the fourth postoperative day, animals were killed and bursting pressure and tissue hydroxyproline concentration of the anastomoses were analyzed and compared. Results: The mean bursting pressure values were: 143 mm Hg in Group 1, 40.8 mm Hg in Group 2, 82.8 mm Hg in Group 3, 46.1 mm Hg in Group 4, and 52.3 mm Hg in Group 5 (P <.0001; 1-way analysis of variance). Mean tissue hydroxyproline concentration values were: 5.3 μg/mg in Group 1, 1.6 μg/mg in Group 2, 2.2 μg/mg in Group 3, 1.3 μg/mg in Group 4, and 1.5 μg/mg in Group 5 (P <.0001, 1-way analysis of variance). Bursting pressure and tissue hydroxyproline concentration values had a good correlation r = 0.86, P <.001, Pearson correlation analysis). Conclusions: This study showed that I-R injury is a systemic phenomenon, and remote organ I-R can significantly delay anastomotic healing. This has to be kept in mind when constructing an intestinal anastomosis in the presence of local or remote I-R injury. (Surgery 2000;128:99-104)
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        • McMillen MA
        • Huribal M
        • Sumpio B.
        Common pathway of endothelial-leukocyte interaction in shock, ischemia, and reperfusion.
        Am J Surg. 1993; 166: 557-562
        • Hill J
        • Lindsay TF
        • Ortiz F
        • et al.
        Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat.
        J Immunol. 1992; 149: 1723-1728
        • Sisley AC
        • Desai T
        • Harig JM
        • et al.
        Neutrophil depletion attenuates human intestinal reperfusion injury.
        J Surg Res. 1994; 57: 192-196
        • Seekamp A
        • Mulligan MS
        • Till GO
        • et al.
        Role of β2 integrins and ICAM-1 in lung injury following ischemia-reperfusion of rat hind limbs.
        Am J Pathol. 1993; 143: 464-472
        • Seekamp A
        • Warren JS
        • Remick DG
        • et al.
        Requirements for tumor necrosis factor-α and interleukin-1 in limb ischemia/ reperfusion injury and associated lung injury.
        Am J Pathol. 1993; 143: 453-463
        • Seekamp A
        • Till GO
        • Mulligan MS
        • et al.
        Role of selectins in local and remote tissue injury following ischemia and reperfusion.
        Am J Pathol. 1994; 144: 592-598
        • Sorkine P
        • Setton A
        • Halpern P
        • et al.
        Soluble tumor necrosis factor receptors reduce bowel ischemia-induced lung permeability and neutrophil sequestration.
        Crit Care Med. 1995; 23: 1377-1381
        • Yassin MMI
        • Barros D'Sa AAB
        • Parks G
        • et al.
        Mortality following lower limb ischemia-reperfusion: a systemic inflammatory response?.
        World J Surg. 1996; 20: 961-967
        • Anner H
        • Kaufman RP
        • Valeri CR
        • et al.
        Reperfusion of ischemic lower limbs increases pulmonary microvascular permeability.
        J Trauma. 1988; 28: 607-610
        • LaNoue JL
        • Turnage RH
        • Kadesky KM
        • et al.
        The effect of intestinal reperfusion on renal function and perfusion.
        J Surg Res. 1996; 64: 19-25
        • Welbourn R
        • Goldman G
        • O'Riordan M
        • et al.
        Role for tumor necrosis factor as mediator of lung injury following lower torso ischemia.
        J Appl Physiol. 1991; 70: 2645-2649
        • DemirogĞullari B
        • Sönmez K
        • Türkyilmaz Z
        • et al.
        Comparison of consequent small bowel anastomoses after transient ischemia: an experimental study in rats.
        J Pediatr Surg. 1998; 33: 91-93
        • Kuzu MA
        • Köksoy C
        • Kale IT
        • et al.
        Reperfusion injury delays healing of intestinal anastomosis in a rat.
        Am J Surg. 1998; 176: 348-351
        • Bergman I
        • Loxley R.
        Two improved and simplified methods for the spectrophotometric determination of OH-proline.
        Anal Chem. 1963; 35: 1961-1965
        • Gerkin TM
        • Oldham KT
        • Guice KS
        • et al.
        Intestinal ischemia-reperfusion injury causes pulmonary endothelial cell ATP depletion.
        Ann Surg. 1993; 217: 48-56
        • Willoughby RPN
        • Harris KA
        • Carson MW
        • et al.
        Intestinal mucosal permeability to 51Cr-ethylenediaminetetraacetic acid is increased after bilateral lower extremity ischemia-reperfusion in the rat.
        Surgery. 1996; 120: 547-553
        • Yokoyama Y
        • Beckman JS
        • Beckman TK
        • et al.
        Circulating xanthine oxidase: potential mediator of ischemic injury.
        Am J Physiol. 1990; 258: G564-G570
        • Friedl HP
        • Smith DJ
        • Till GO
        • et al.
        Ischemia-reperfusion in humans: appearance of xanthine oxidase activity.
        Am J Pathol. 1990; 136: 491-495
        • Tan S
        • Gelman S
        • Wheat JK
        • et al.
        Circulating xanthine oxidase in human ischemia reperfusion.
        South Med J. 1995; 88: 479-482
        • Terada LS
        • Dormish JJ
        • Shanley PF
        • et al.
        Circulating xanthine oxidase mediates lung neutrophil sequestration after intestinal ischemia-reperfusion.
        Am J Physiol. 1992; 63: L394-L401
        • Hendriks T
        • Mastboom WJB
        Healing of experimental intestinal anastomoses: parameters for repair.
        Dis Colon Rectum. 1990; 33: 891-901
        • Koruda MJ
        • Rolandelli RH
        Experimental studies on the healing of colonic anastomoses.
        J Surg Res. 1990; 48: 504-515
        • Kologlu M
        • Sayek I
        • Kologlu LB
        • et al.
        Effect of persistently elevated intraabdominal pressure on healing of colonic anastomoses.
        Am J Surg. 1999; 178: 293-297
        • Graham MF
        • Blomquist P
        • Zederfeldt B.
        The alimentary canal.
        in: First ed. Wound healing: biochemical and clinical aspects. WB Saunders Co, Philadelphia1992: 433-449
        • Thornton FJ
        • Barbul A.
        Healing in the gastrointestinal tract.
        Surg Clin North Am. 1997; 77: 549-573
        • Ahrendt GM
        • Gardner K
        • Barbul A.
        Loss of colonic structural collagen impairs healing during intra-abdominal sepsis.
        Arch Surg. 1994; 129: 1179-1183
        • Ahrendt GM
        • Tantry US
        • Barbul A.
        Intra-abdominal sepsis impairs colonic reparative collagen synthesis.
        Am J Surg. 1996; 171: 102-107
        • Kashiwagi H.
        The lower limit of tissue blood flow for safe colonic anastomosis: an experimental study using laser Doppler velocimetry.
        Surg Today. 1993; 23: 430-438
        • Senagore A
        • Milsom JW
        • Walshaw RK
        • et al.
        Intramural pH: quantitative measurement for predicting colorectal anastomotic healing.
        Dis Colon Rectum. 1990; 33: 175-179
        • Sheridan WG
        • Lowndes RH
        • Young HL
        Tissue oxygen tension as a predictor of colonic anastomotic healing.
        Dis Colon Rectum. 1987; 30: 867-871