Scientific papers| Volume 189, ISSUE 2, P155-160, February 2005

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An evaluation of low molecular weight heparin and hyperbaric oxygen treatment in the prevention of intra-abdominal adhesions and wound healing



      Abdominal surgery can lead to intra-abdominal adhesions with significant morbidity and mortality. To prevent adhesions, an experimental study was planned to designate the effects of low molecular weight (LMW) heparins and hyperbaric oxygen (HBO) therapy both on the formation of adhesions and wound healing.


      Thirty-eight Wistar albino rats underwent laparotomy to cause intra-abdominal adhesions by mechanical abrasion of the cecum and ethanol application. The rats were divided into 4 groups. In the control group (group 1) no further management was undertaken. Group 2 was treated by Enoxaparine Na, group 3 received HBO therapy, and group 4 was given both enoxaparine Na and HBO treatment.


      There was a statistically significant difference between the control and enoxaparine Na groups regarding adhesions. Statistically significant differences were observed between groups 1 and 4 and between groups 1 and 3 regarding the hydroxyproline content of the abdominal wounds. In the pathologic analysis of the abdominal wounds, there was no statistically significant difference between any of the groups, including the control group, regarding inflammation. Statistically significant differences were observed regarding angiogenesis between the control group and groups 3 and 4. There was also a statistically significant difference regarding fibrosis between groups 1 and 4.


      Enoxaparine Na decreased intra-abdominal adhesions, and HBO therapy had no beneficial effect on adhesions. Enoxaparine Na had no harmful effects on wound healing, and HBO therapy increased the process of wound healing.


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        • Menzies D.
        • Ellis H.
        Intestinal obstruction from adhesion—how big is the problem?.
        Ann R Coll Surg Engl. 1990; 72: 60-63
        • Reijnen M.M.
        • Bleichrodt R.P.
        • van Goor H.
        Pathophysiology of intra-abdominal adhesion and abscess formation, and the effect of hyaluronan.
        Br J Surg. 2003; 90: 533-541
        • Beck D.E.
        • Opelka F.G.
        • Bailey H.R.
        • et al.
        Incidence of small-bowel obstruction and adhesiolysis after open colorectal and general surgery.
        Dis Colon Rectum. 1999; 42: 241-248
        • Ellis H.
        • Moran B.J.
        • Thompson J.N.
        • et al.
        Adhesion-related hospital readmissions after abdominal and pelvic surgery.
        Lancet. 1999; 353: 1476-1480
        • Becker J.M.
        • Dayton M.T.
        • Fazio V.W.
        • et al.
        Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane.
        J Am Coll Surg. 1996; 183: 297-306
        • Ellis H.
        Internal overhealing.
        World J Surg. 1980; 4: 303-306
        • Gupta S.
        • Jain P.K.
        Low-dose heparin in experimental peritonitis.
        Eur Surg Res. 1985; 17: 167-172
        • Hau T.
        • Simmons R.L.
        Heparin in the treatment of experimental peritonitis.
        Ann Surg. 1978; 187: 294-298
        • Turkcapar A.G.
        • Ozarslan C.
        • Erdem E.
        • et al.
        The effectiveness of low molecular weight heparin on adhesion formation in experimental rat model.
        Int Surg. 1995; 80: 92-94
        • Lehman E.P.
        • Boys F.
        The prevention of peritoneal adhesions with heparin. An experimental study.
        Ann Surg. 1940; 111: 427-435
        • Thompson J.N.
        • Whawell S.A.
        Pathogenesis and prevention of adhesion formation.
        Br J Surg. 1995; 82: 3-5
        • Sahin Y.
        • Saglam A.
        Synergistic effects of carboxymethylcellulose and low molecular weight heparin in reducing adhesion formation in the rat uterine horn model.
        Acta Obstet Gynecol Scand. 1994; 73: 70-73
        • Tayyar M.
        • Basbug M.
        The effects of intraperitoneal piroxicam and low molecular weight heparin in prevention of adhesion reformation in rat uterine horn.
        Res Exp Med (Berl). 1999; 198: 269-275
        • UHMS Committee
        Hyperbaric Oxygen Therapy A Committee Report. Undersea and Hyperbaric Medical Society, Maryland1999: 3-7
        • Liebman S.M.
        • Langer J.C.
        • Marshall J.S.
        • et al.
        Role of mast cells in peritoneal adhesion formation.
        Am J Surg. 1993; 165: 127-130
        • Zhang Y.D.
        • Yao W.
        • Wu C.X.
        • et al.
        Topical application of halcinonide cream reduces the severity and incidence of intraperitoneal adhesions in a rat model.
        Am J Surg. 2002; 184: 74-77
        • Evans D.M.
        • McAree K.
        • Guyton D.P.
        • et al.
        Dose dependency and wound healing aspects of the use of tissue plasminogen activator in the prevention of intra-abdominal adhesions.
        Am J Surg. 1993; 165: 229-232
        • Kivirikko K.I.
        • Laitinen O.
        • Prockop D.J.
        Modifications of a specific assay for hydroxyproline in urine.
        Anal Biochem. 1967; 19: 249-255
        • Vrijland W.W.
        • Tseng L.N.
        • Eijkman H.J.
        • et al.
        Fewer intraperitoneal adhesions with use of Hyaluronic acid-carboxymethylcellulose membrane; a randomized clinical trial.
        Ann Surg. 2002; 235: 193-199
        • Luijendijk R.W.
        • de Lange D.C.
        • Wauters C.C.
        • et al.
        Foreign material in postoperative adhesions.
        Ann Surg. 1996; 223: 242-248
        • Milligan D.W.
        • Raftery A.T.
        Observations on the pathogenesis of peritoneal adhesions.
        Br J Surg. 1974; 61: 274-280
        • Thompson J.N.
        • Petarson-Brown S.
        • Harbourne T.
        • et al.
        Reduced human peritoneal plasminogen activating activity.
        Br J Surg. 1989; 76: 382-384
        • Raftery A.T.
        Regeneration of peritoneum.
        J Anat. 1979; 129: 659-664
        • Whawell S.A.
        • Wang Y.
        • Fleming K.A.
        • et al.
        Localization of plasminogen activator inhibitor-1 production in inflamed appendix by in situ mRNA hybridization.
        J Pathol. 1993; 169: 67-71
        • Weitz J.I.
        Low-molecular weight heparins.
        N Engl J Med. 1997; 337: 688-698
        • Carter C.J.
        • Kelton J.G.
        • Hirsh J.
        • et al.
        The relationship between the hemorrhagic and antithrombotic properties of low molecular weight heparin in rabbits.
        Blood. 1982; 59: 1239-1245
        • Andriuoli G.
        • Mastacchi R.
        • Barbanti M.
        • et al.
        Comparison of the antithrombotic and hemorrhagic effects of heparin and a new low molecular weight heparin in the rat.
        Haemostasis. 1985; 15: 324
        • Jorneskog G.
        • Brismar K.
        • Fagrell B.
        Low molecular weight heparin seems to improve local capillary circulation and healing of chronic foot ulcers in diabetic patients.
        Vasa. 1993; 22: 137-142
        • Li Y.
        • Shin V.Y.
        • Cheuk C.Y.
        • et al.
        A 3.0-kDa low molecular weight heparin promotes gastric ulcer healing rats.
        Aliment Pharmacol Ther. 2001; 15: 2009-2017
        • Sudhalter J.
        • Folkman J.
        • Svahn C.M.
        • et al.
        Importance of size, sulfation and anticoagulant activity in the potentiation of acidic fibroblast growth factor by heparin.
        J Biol Chem. 1989; 264: 6892-6897
        • Barzu T.
        • Lormeau J.C.
        • Petitou M.
        • et al.
        Heparin-derived oligosaccharides.
        J Cell Physiol. 1989; 140: 538-548
        • Rosenberg R.D.
        • Damus P.S.
        The purification and mechanism of action of human antithrombin-heparin cofactor.
        J Biol Chem. 1973; 248: 6490-6505
        • Walker F.J.
        • Esmon C.T.
        Interactions between heparin and factor Xa. Inhibition of prothrombin activation.
        Biochim Biophys Acta. 1979; 585: 405-415
        • Markwardt F.
        • Klocking H.P.
        Heparin induced release of plasminogen activator.
        Haemostasis. 1977; 6: 370-374
        • Orita H.
        • Campeau J.D.
        • Gale J.A.
        • et al.
        Differential secretion of plasminogen activator activity by postsurgical activated macrophages.
        J Surg Res. 1986; 41: 569-573
        • Gimbel M.
        • Hunt T.
        Wound healing and hyperbaric oxygenation.
        in: Kindwall E.P. Whelan H.T. Hyperbaric Medicine Practice, Revised Edition. Best Publishing Company, Flagstaff, AZ2002: 169-204
        • Takahashi H.
        HBO in adhesive or incomplete ileus associated with abdominal surgery.
        in: Kindwall E.P. Whelan H.T. Hyperbaric Medicine Practice, Revised Edition. Best Publishing Company, Flagstaff, AZ2002: 929-935
        • Sumen G.
        • Cimsit M.
        • Eroglu L.
        Hyperbaric oxygen treatment reduces carrageenan-induced acute inflammation in rats.
        Eur J Pharmacol. 2001; 431: 265-268