Pathophysiology of intra-abdominal adhesion and abscess formation, and the effect of hyaluronan

British Journal of Surgery - Tập 90 Số 5 - Trang 533-541 - 2003
Michel M.P.J. Reijnen1, Robert P. Bleichrodt1, Harry van Goor1
1Department of Surgery, University Medical Centre st. Radboud, Nijmegen, The Netherlands

Tóm tắt

AbstractBackground

Intra-abdominal adhesions and abscesses cause significant morbidity and mortality. The formation of fibrin in the abdominal cavity is a common pathophysiological pathway for both. The aim of this review was to investigate the pathophysiology of intra-abdominal adhesions and abscesses, and to explore the possible sites of action of hyaluronan.

Methods

Data were reviewed from the literature using the Medline database.

Results

Both surgery and peritonitis disturb the equilibrium between coagulation and fibrinolysis in the abdominal cavity in favour of the coagulation system. Hyaluronan-based agents reduce adhesion formation after surgery. Moreover, hyaluronan solution reduces abscess formation in experimental peritonitis. Possible mechanisms of action include mechanical separation of wound surfaces, improvement of peritoneal healing, modulation of the inflammatory response and enhanced fibrinolysis.

Conclusion

Diminished fibrin degradation is a common pathway for the formation of adhesions and abscesses. The potential of hyaluronan-based agents to reduce intra-abdominal adhesions and abscesses in abdominal surgery and sepsis is a promising new concept. Elucidating the mechanisms involved and the clinical application of hyaluronan in peritonitis are challenges for future research.

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Tài liệu tham khảo

Menzies, 1992, Peritoneal adhesions. Incidence, cause, and prevention, Surg Annu, 24, 27

Soules, 1982, The prevention of postoperative pelvic adhesions: an animal study comparing barrier methods with dextran 70, Am J Obstet Gynecol, 143, 829, 10.1016/0002-9378(82)90018-7

Stovall, 1989, Predictors of pelvic adhesions, J Reprod Med, 34, 345

Van Der Krabben, 2000, Morbidity and mortality of inadvertent enterotomy during adhesiotomy, Br J Surg, 87, 467, 10.1046/j.1365-2168.2000.01394.x

Ivarsson, 1997, Cost of bowel obstruction resulting from adhesions, Eur J Surg, 163, 679

Holmdahl, 1999, Making and covering of surgical footprints, Lancet, 353, 1456, 10.1016/S0140-6736(99)90061-2

Rotstein, 1992, Role of fibrin deposition in the pathogenesis of intraabdominal infection, Eur J Clin Microbiol Infect Dis, 11, 1064, 10.1007/BF01967800

Raftery, 1973, Regeneration of peritoneal and visceral peritoneum. A light microscopical study, Br J Surg, 60, 293, 10.1002/bjs.1800600412

Holmdahl, 1996, Fibrinolysis in human peritoneum during operation, Surgery, 119, 701, 10.1016/S0039-6060(96)80196-6

Holmdahl, 1998, Depression of peritoneal fibrinolysis during operation is a local response to trauma, Surgery, 123, 539, 10.1067/msy.1998.86984

Vipond, 1990, Peritoneal fibrinolytic activity and intra-abdominal adhesions, Lancet, 335, 1120, 10.1016/0140-6736(90)91125-T

Vipond, 1994, Effect of experimental peritonitis and ischaemia on peritoneal fibrinolytic-activity, Eur J Surg, 160, 471

van Goor, 1996, Coagulation and fibrinolytic responses of human peritoneal fluid and plasma to bacterial peritonitis, Br J Surg, 83, 1133, 10.1002/bjs.1800830833

van Goor, 1994, Fibrinolytic activity in the abdominal cavity of rats with faecal peritonitis, Br J Surg, 81, 1046, 10.1002/bjs.1800810740

Ivarsson, 1998, Expression and kinetics of fibrinolytic components in plasma and peritoneum during abdominal surgery, Fibrinolysis Proteolysis, 12, 61, 10.1016/S0268-9499(98)80009-X

Bakkum, 1996, Long-term analysis of peritoneal plasminogen activator activity and adhesion formation after surgical trauma in the rat model, Fertil Steril, 66, 1018, 10.1016/S0015-0282(16)58700-7

Scott-Coombes, 1995, Human intraperitoneal fibrinolytic response to elective surgery, Br J Surg, 82, 414, 10.1002/bjs.1800820346

Scott-Coombes, 1995, The operative peritoneal fibrinolytic response to abdominal operation, Eur J Surg, 161, 395

Mignatti, 1993, Biology and biochemistry of proteinases in tumor invasion, Physiol Rev, 73, 161, 10.1152/physrev.1993.73.1.161

Lu, 1992, Comparative thrombolytic properties of tissue-type plasminogen activator (t-PA), single-chain urokinase-type plasminogen activator (u-PA) and K1K2Pu (a t-PA/u-PA chimera) in a combined arterial and venous thrombosis model in the dog, J Am Coll Cardiol, 19, 1350, 10.1016/0735-1097(92)90344-M

Vassalli, 1994, Tumour biology. Membrane proteases in focus, Nature, 370, 14, 10.1038/370014a0

Andreasen, 1990, Plasminogen activator inhibitors: hormonally regulated serpins, Mol Cell Endocrinol, 68, 1, 10.1016/0303-7207(90)90164-4

Holmdahl, 1997, Plasminogen activators and inhibitors in peritoneal tissue, APMIS, 105, 25, 10.1111/j.1699-0463.1997.tb00535.x

Hellebrekers, 2000, Short-term effect of surgical trauma on rat peritoneal fibrinolytic activity and its role in adhesion formation, Thromb Haemost, 84, 876, 10.1055/s-0037-1614131

Ivarsson, 1998, Tissue markers as predictors of postoperative adhesions, Br J Surg, 85, 1549, 10.1046/j.1365-2168.1998.00859.x

Whawell, 1993, Plasminogen activator inhibitor 2 reduces peritoneal fibrinolytic activity in inflammation, Br J Surg, 80, 107, 10.1002/bjs.1800800134

Duron, 1996, Contamination peropératoire de la cavité péritoneale par des microcorps étrangers, Chirurgie, 121, 175

Duron, 1993, Histoire naturelle des adherences intrapéritoneales postopératoires, J Chir, 130, 385

Luijendijk, 1996, Foreign material in postoperative adhesions, Ann Surg, 223, 242, 10.1097/00000658-199603000-00003

Richardson, 1911, Studies on peritoneal adhesions. With a contribution to the treatment of denuded bowel surfaces, Ann Surg, 54, 758, 10.1097/00000658-191112000-00004

Boys, 1942, The prophylaxis of peritoneal adhesions. A review of the literature, Surgery, 11, 118

Wiseman, 1999, Peritoneal Surgery, 401

Wright, 1950, Prevention of postoperative adhesions in rabbits with streptococcal metabolites, Proc Soc Exp Biol Med, 75, 602, 10.3181/00379727-75-18278

James, 1965, The effect of streptokinase on experimental intraperitoneal adhesion formation, J Pathol Bacteriol, 90, 279, 10.1002/path.1700900132

Lai, 1998, Tissue plasminogen activator reduces intraperitoneal adhesion after intestinal resection in rats, J Formos Med Assoc, 97, 323

Orita, 1991, Inhibition of postsurgical adhesions in a standardized rabbit model: intraperitoneal treatment with tissue plasminogen activator, Int J Fertil, 36, 172

Montz, 1991, The ability of recombinant tissue plasminogen activator to inhibit post-radical pelvic surgery adhesions in the dog model, Am J Obstet Gynecol, 165, 1539, 10.1016/S0002-9378(12)90796-6

Vipond, 1994, Experimental adhesion prophylaxis with recombinant tissue plasminogen activator, Ann R Coll Surg Engl, 76, 412

Buckenmaier, 1999, Comparison of antiadhesive treatments using an objective rat model, Am Surg, 65, 274, 10.1177/000313489906500320

Doody, 1989, Recombinant tissue plasminogen activator reduces adhesion formation in a rabbit uterine horn model, Fertil Steril, 51, 509, 10.1016/S0015-0282(16)60563-0

Menzies, 1989, Intra-abdominal adhesions and their prevention by topical tissue plasminogen activator, J R Soc Med, 82, 534, 10.1177/014107688908200909

Menzies, 1991, The role of plasminogen activator in adhesion prevention, Surg Gynecol Obstet, 172, 362

Dunn, 1993, Effect of varying days of tissue plasminogen activator therapy on the prevention of postsurgical adhesions in a rabbit model, J Surg Res, 54, 242, 10.1006/jsre.1993.1038

Dunn, 1991, Synergistic effect of intraperitoneally administered calcium channel blockade and recombinant tissue plasminogen activator to prevent adhesion formation in an animal model, Am J Obstet Gynecol, 164, 1327, 10.1016/0002-9378(91)90708-Y

Evans, 1993, Dose dependency and wound healing aspects of the use of tissue plasminogen activator in the prevention of intra-abdominal adhesions, Am J Surg, 165, 229, 10.1016/S0002-9610(05)80516-1

Lehman, 1940, The prevention of peritoneal adhesions with heparin. An experimental study, Ann Surg, 111, 427, 10.1097/00000658-194003000-00009

Fukasawa, 1991, Inhibition of postsurgical adhesions in a standardized rabbit model. II. Intraperitoneal treatment with heparin, Int J Fertil, 36, 296

Lu, 1998, Heparinization on pericardial substitutes can reduce adhesion and epicardial inflammation in the dog, J Thorac Cardiovasc Surg, 115, 1111, 10.1016/S0022-5223(98)70411-8

Noishiki, 1987, Antiadhesive collagen membrane with heparin slow release, J Bioact Compat Polym, 2, 325, 10.1177/088391158700200404

Chalkiadakis, 1983, The effect of heparin upon fibrinopurulent peritonitis in rats, Surg Gynecol Obstet, 157, 257

Turkcapar, 1995, The effectiveness of low molecular weight heparin on adhesion formation in experimental rat model, Int Surg, 80, 92

Gupta, 1985, Low-dose heparin in experimental peritonitis, Eur Surg Res, 17, 167, 10.1159/000128463

O'Leary, 1979, The effects of a minidose of heparin on peritonitis in rats, Surg Gynecol Obstet, 148, 571

Tayyar, 1999, The effects of intraperitoneal piroxicam and low molecular weight heparin in prevention of adhesion reformation in rat uterine horn, Res Exp Med, 198, 269, 10.1007/s004330050110

Vela, 1999, The effects of minidose heparin and low molecular weight heparin on peritonitis in the rat, Am Surg, 65, 473, 10.1177/000313489906500521

Siegler, 1980, Prevention of postoperative adhesions in rabbits with ibuprofen, a nonsteroidal anti-inflammatory agent, Fertil Steril, 34, 46, 10.1016/S0015-0282(16)44838-7

Swolin, 1967, Die einwirkung von grossen, intraperitonealen dosen glukokorticoid auf die bildung von postoperativen adhäsionen. Klinische studien mit hilfe des laparoskopes an operierten extrauteringraviditäten, Acta Obstet Gynecol Scand, 46, 204, 10.3109/00016346709158197

Jansen, 1985, Failure of intraperitoneal adjuncts to improve the outcome of pelvic operations in young women, Am J Obstet Gynecol, 153, 363, 10.1016/0002-9378(85)90072-9

Larsson, 1997, Peritoneal Adhesions, 331, 10.1007/978-3-642-60433-1_41

Nishimura, 1983, Biochemical evaluation of postsurgical wound repair: prevention of intraperitoneal adhesion formation with ibuprofen, J Surg Res, 34, 219, 10.1016/0022-4804(83)90063-X

Wiseman, 1994, Time-dependent effect of tolmetin sodium in a rabbit uterine adhesion model, J Invest Surg, 7, 527, 10.3109/08941939409015369

Celebioglu, 1999, The effect of tenoxicam on intraperitoneal adhesions and prostaglandin E2 levels in mice, Anesth Analg, 88, 939, 10.1213/00000539-199904000-00048

LeGrand, 1995, Comparative efficacy of nonsteroidal anti-inflammatory drugs and anti-thromboxane agents in a rabbit adhesion-prevention model, J Invest Surg, 8, 187, 10.3109/08941939509023141

LeGrand, 1994, Efficacy of tolmetin sodium for adhesion prevention in rabbit and rat models, J Surg Res, 56, 67, 10.1006/jsre.1994.1011

Muzii, 1998, Postoperative adhesion prevention with low-dose aspirin: effect through the selective inhibition of thromboxane production, Hum Reprod, 13, 1486, 10.1093/humrep/13.6.1486

Nagler, 1998, Halofuginone—an inhibitor of collagen type I synthesis—prevents postoperative formation of abdominal adhesions, Ann Surg, 227, 575, 10.1097/00000658-199804000-00021

Nagler, 1999, Halofuginone, an inhibitor of collagen type I synthesis, prevents postoperative adhesion formation in the rat uterine horn model, Am J Obstet Gynecol, 180, 558, 10.1016/S0002-9378(99)70254-1

Claypool, 1910, A study in the prevention of adhesions, JAMA, 55, 312, 10.1001/jama.1910.04330040048017

Vogel, 1898, Clinical and experimental study of peritoneal adhesion occurring after laparotomy, Deutsche Zeit Chir, ixiii, 296

Wiseman, 1999, Metaanalysis of the safety and efficacy of an adhesion barrier (Interceed TC7) in laparotomy, J Reprod Med, 44, 325

Farquhar, 2002

Sawada, 2000, Postoperative adhesion prevention with an oxidized regenerated cellulose adhesion barrier in infertile women, J Reprod Med, 45, 387

Hellebrekers, 2000, Effects of five different barrier materials on postsurgical adhesion formation in the rat, Hum Reprod, 15, 1358, 10.1093/humrep/15.6.1358

Rotstein, 1988, Prevention of intra-abdominal abscesses by fibrinolysis using recombinant tissue plasminogen activator, J Infect Dis, 158, 766, 10.1093/infdis/158.4.766

van Goor, 1994, Effect of recombinant tissue plasminogen activator on intra-abdominal abscess formation in rats with generalized peritonitis, J Am Coll Surg, 179, 407

Prinz, 1986, Effect of heparin and heparin fractions on experimental abscess formation, Arch Surg, 121, 1173, 10.1001/archsurg.1986.01400100081016

Rosenthal, 1988, Prevention of intra-abdominal abscesses with fibrinolytic agents, Can J Surg, 31, 98

McRitchie, 1989, Delayed administration of tissue plasminogen activator reduces intra-abdominal abscess formation, Arch Surg, 124, 1406, 10.1001/archsurg.1989.01410120052011

Meyer, 1934, The polysaccharide of the vitreous humor, J Biol Chem, 107, 629, 10.1016/S0021-9258(18)75338-6

Balazs, 1986, Nomenclature of hyaluronic acid, Biochem J, 235, 903, 10.1042/bj2350903

Fraser, 1997, Hyaluronan: its nature, distribution, functions and turnover, J Intern Med, 242, 27, 10.1046/j.1365-2796.1997.00170.x

Weigel, 1988, The role of hyaluronic acid in inflammation and wound healing, Int J Tissue React, 10, 355

Oksala, 1995, Expression of proteoglycans and hyaluronan during wound healing, J Histochem Cytochem, 43, 125, 10.1177/43.2.7529785

Brecht, 1986, Increased hyaluronate synthesis is required for fibroblast detachment and mitosis, Biochem J, 239, 445, 10.1042/bj2390445

Mian, 1986, Analysis of cell-growth-phase-related variations in hyaluronate synthase activity of isolated plasma-membrane fractions of cultured human skin fibroblasts, Biochem J, 237, 333, 10.1042/bj2370333

Abatelango, 1982, Cell detachment mediated by hyaluronic acid, Exp Cell Res, 137, 73, 10.1016/0014-4827(82)90009-X

Barnhart, 1979, Detachment variants of Chinese hamster cells. Hyaluronic acid as a modulator of cell detachment, Exp Cell Res, 119, 327, 10.1016/0014-4827(79)90360-4

Turley, 1992, Hyaluronan and cell locomotion, Cancer Metastasis Rev, 11, 21, 10.1007/BF00047600

Toole, 1997, Hyaluronan in morphogenesis, J Intern Med, 242, 35, 10.1046/j.1365-2796.1997.00171.x

Toole, 1991, Cell Biology of Extracellular Matrix, 2nd, 305, 10.1007/978-1-4615-3770-0_10

Abatangelo, 1983, Healing of hyaluronic acid-enriched wounds: histological observations, J Surg Res, 35, 410, 10.1016/0022-4804(83)90030-6

King, 1991, Beneficial actions of exogenous hyaluronic acid on wound healing, Surgery, 109, 76

Bertram, 1999, Intraperitoneal transplantation of isologous mesothelial cells for prevention of adhesions, Eur J Surg, 165, 705, 10.1080/11024159950189780

Lucas, 1996, Effect of rat mesenchymal stem cells on development of abdominal adhesions after surgery, J Surg Res, 62, 229, 10.1006/jsre.1996.0200

Reijnen, 2000, The antiadhesive agent sodium hyaluronate increases the proliferation rate of human peritoneal mesothelial cells, Fertil Steril, 74, 146, 10.1016/S0015-0282(00)00571-9

Reijnen, 2001, Sodium hyaluronate increases the fibrinolytic response of human peritoneal mesothelial cells exposed to tumor necrosis factor alpha, Arch Surg, 136, 291, 10.1001/archsurg.136.3.291

Reijnen, 2002, Time course of peritoneal tissue plasminogen activator after colonic surgery: effect of hyaluronan-based antiadhesive agents and bacterial peritonitis, Br J Surg, 89, 103, 10.1046/j.0007-1323.2001.01966.x

Presti, 1994, Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl (OH·) radicals is dependent on hyaluronan molecular mass, Cell Biochem Funct, 12, 281, 10.1002/cbf.290120409

Tamoto, 1994, High-molecular-weight hyaluronic acids inhibit chemotaxis and phagocytosis but not lysosomal enzyme release induced by receptor-mediated stimulations in guinea pig phagocytes, Microbiol Immunol, 38, 73, 10.1111/j.1348-0421.1994.tb01746.x

West, 1989, The Biology of Hyaluronan, 187

Riese, 2000, Production of IL-6 and MCP-1 by the human peritoneum in vivo during major abdominal surgery, Shock, 14, 91, 10.1097/00024382-200014020-00002

Pirnazar, 1999, Bacteriostatic effects of hyaluronic acid, J Periodontol, 70, 370, 10.1902/jop.1999.70.4.370

Kvam, 1995, Oxygen-derived free radical (ODFR) action on hyaluronan (HA), on two HA ester derivatives, and on the metabolism of articular chondrocytes, Exp Cell Res, 218, 79, 10.1006/excr.1995.1133

Fukuda, 1997, Hyaluronic acid inhibits interleukin-1-induced superoxide anion in bovine chondrocytes, Inflamm Res, 46, 114, 10.1007/s000110050132

Cortivo, 1996, Antioxidant effects of hyaluronan and its alpha-methyl-prednisolone derivative in chondrocyte and cartilage cultures, Semin Arthritis Rheum, 26, 492, 10.1016/S0049-0172(96)80030-8

Foschi, 1990, Hyaluronic acid prevents oxygen free-radical damage to granulation tissue: a study in rats, Int J Tissue React, 12, 333

Wisniewski, 1996, TSG-6, a glycoprotein associated with arthritis, and its ligand hyaluronan exert opposite effects in a murine model of inflammation, Pflugers Arch, 431, R225, 10.1007/BF02346350

Fries, 1998, The Chemistry, Biology and Medical Applications of Hyaluronan and its Derivates, 149

Akatsuka, 1993, Suppressive effects of hyaluronic acid on elastase release from rat peritoneal leucocytes, J Pharm Pharmacol, 45, 110, 10.1111/j.2042-7158.1993.tb03693.x

Hiro, 1986, Hyaluronic acid is an endogenous inducer of interleukin-1 production by human monocytes and rabbit macrophages, Biochem Biophys Res Commun, 140, 715, 10.1016/0006-291X(86)90790-4

Kobayashi, 1997, Hyaluronic acid-specific regulation of cytokines by human uterine fibroblasts, Am J Physiol, 273, C1151, 10.1152/ajpcell.1997.273.4.C1151

Dale, 1996, Hyaluronate capsule and surface M protein in resistance to opsonization of group A streptococci, Infect Immun, 64, 1495, 10.1128/iai.64.5.1495-1501.1996

Moses, 1997, Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus, Infect Immun, 65, 64, 10.1128/iai.65.1.64-71.1997

Becker, 1996, Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane: a prospective, randomized, double-blind multicenter study, J Am Coll Surg, 183, 297

Diamond, 1996, Reduction of adhesions after uterine myomectomy by Seprafilm membrane (HAL-F): a blinded, randomized, multicenter clinical study. Seprafilm Adhesion Study Group, Fertil Steril, 66, 904, 10.1016/S0015-0282(16)58716-0

Vrijland, 2002, Fewer intraperitoneal adhesions with use of hyaluronic acid–carboxymethyl-cellulose membrane: a randomized clinical trial, Ann Surg, 235, 193, 10.1097/00000658-200202000-00006

Beck, 2003, Prospective, randomized, multicenter, controlled study of the safety of Seprafilm® Adhesion Barrier in abdominopelvic surgery, Dis Colon Rectum, 10.1007/s10350-004-6739-2

Johns, 2001, Reduction of postsurgical adhesions with Intergel adhesion prevention solution: a multicenter study of safety and efficacy after conservative gynecologic surgery, Fertil Steril, 76, 595, 10.1016/S0015-0282(01)01954-9

Lundorff, 2001, Reduction of post-surgical adhesions with ferric hyaluronate gel: a European study, Hum Reprod, 16, 1982, 10.1093/humrep/16.9.1982

De Iaco, 2001, Efficacy of a hyaluronan derivative gel in postsurgical adhesion prevention in the presence of inadequate hemostasis, Surgery, 130, 60, 10.1067/msy.2001.115102

Belluco, 2001, Prevention of postsurgical adhesions with an autocrosslinked hyaluronan derivative gel, J Surg Res, 100, 217, 10.1006/jsre.2001.6248

Kocak, 1999, Reduction of adhesion formation with cross-linked hyaluronic acid after peritoneal surgery in rats, Fertil Steril, 72, 873, 10.1016/S0015-0282(99)00368-4

Diamond, 1998, Reduction of de novo postsurgical adhesions by intraoperative precoating with Sepracoat (HAL-C) solution: a prospective, randomized, blinded, placebo-controlled multicenter study. The Sepracoat Adhesion Study Group, Fertil Steril, 69, 1067, 10.1016/S0015-0282(98)00057-0

Reijnen, 1999, Prevention of intra-abdominal abscesses and adhesions using a hyaluronic acid solution in a rat peritonitis model, Arch Surg, 134, 997, 10.1001/archsurg.134.9.997

Reijnen, 2001, Polyanionic polysaccharides reduce intra-abdominal adhesion and abscess formation in a rat peritonitis model, J Surg Res, 101, 248, 10.1006/jsre.2001.6288

Ghellai, 2000, Role of a hyaluronate-based membrane in the prevention of peritonitis-induced adhesions, J Gastrointest Surg, 4, 310, 10.1016/S1091-255X(00)80081-5

Breborowicz, 2001, Intraperitoneal hyaluronan administration in conscious rats: absorption, metabolism, and effects on peritoneal fluid dynamics, Perit Dial Int, 21, 130, 10.1177/089686080102100204

Toole, 2002, Hyaluronan–cell interactions in cancer and vascular disease, J Biol Chem, 277, 4593, 10.1074/jbc.R100039200

Tan, 2001, Sodium hyaluronate enhances colorectal tumour cell metastatic potential in vitro and in vivo, Br J Surg, 88, 246, 10.1046/j.1365-2168.2001.01664.x

Haverlag, 1999, Hyaluronate-based coating solution for prevention of surgical adhesions has no major effect on adhesion and growth of intraperitoneal tumour cells, Eur J Surg, 165, 791, 10.1080/11024159950189609