Animal Adhesion Models: Design, Variables, and Relevance

  • David M. Wiseman

Abstract

Perhaps the most commonly asked question in adhesions research is “Which is the best animal model of adhesions?” The reply “What result are you looking for?” is not intended as a facetious retort, but rather as a suggestion to the questioner to consider carefully the objectives for a particular inquiry (Table 38.1 ). Thus, models in which a favorable result is easy to obtain (“permissive models”) are suitable for early stages of research, whereas more challenging models are required for later stages. The mismatch of models and objectives can lead to costly disappointments on the part of patients, investigators, and pharmaceutical companies alike.

Keywords

Cellulose Fatigue Starch Ischemia Polysaccharide 

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References

  1. 1.
    National Research Council. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press, 1996.Google Scholar
  2. 2.
    Burgess LS, Rose RL, Colt JC, Skinner KC, Burns JW. An evaluation of operator variability in a rat cecal abrasion model for the formation of abdominal models. In: di-Zerega GS, DeCherney AH, Diamond MP, et al., eds. Pelvic Surgery: Adhesion Formation and Prevention. New York: Springer-Verlag, 1997:242–243.CrossRefGoogle Scholar
  3. 3.
    Burns JW, Skinner K, Colt J, et al. Prevention of tissue injury and postsurgical adhesions by precoating tissues with hyaluronic acid solutions. J Surg Res 1995; 59:644–652.PubMedCrossRefGoogle Scholar
  4. 4.
    Manske PR, Jones GT, Wiseman DM. Comment on “A biomechanical study of tendon adhesion reduction using a biodegradable barrier in a rabbit model.” J Appl Biomater 1990; 1:255.PubMedCrossRefGoogle Scholar
  5. 5.
    Bothin C, Midtvedt T. The role of the gastrointestinal microflora in postsurgical adhesion formation—a study in germfree rats. Eur Surg Res 1992; 24:309–312.PubMedCrossRefGoogle Scholar
  6. 6.
    Haney AF, Doty E. Comparison of the peritoneal cells elicited by oxidized regenerated cellulose (Interceed) and expanded polytetrafluoroethylene (Gore-Tex Surgical Membrane) in a murine model. Am J Obstet Gynecol 1992; 166:1137–1146.PubMedGoogle Scholar
  7. 7.
    van den Tol MP, van Stijn I, Bonthuis F, Marquet RL, Jeekel J. Reduction of intraperitoneal adhesion formation by use of non-abrasive gauze. Br J Surg 1997; 84:1410–1415.PubMedCrossRefGoogle Scholar
  8. 8.
    Montz FJ, Holschneider CH, Bozuk M, Gotlieb WH, Mar-tinez-Maza O. Interleukin 10: ability to minimize postoperative intraperitoneal adhesion formation in a murine model. Fertil Steril 1994; 61:1136–1140.PubMedGoogle Scholar
  9. 9.
    Seitz HM, Schenker JG, Epstein S, Garcia CR. Postoperative intraperitoneal adhesions: a double-blind assessment of their prevention in the monkey. Fertil Steril 1973; 24:935–940.PubMedGoogle Scholar
  10. 10.
    Glucksman DL, Warren WD. The effect of topically applied corticosteroids in the prevention of peritoneal adhesions. An experimental approach with a review of the literature. Surgery (St. Louis) 1966; 60:352–360.PubMedGoogle Scholar
  11. 11.
    Grow DR, Seltman HJ, Coddington CC, Hodgen GD. The reduction of postoperative adhesions by two different barrier methods versus control in cynomolgus monkeys: a prospective, randomized, crossover study. Fertil Steril 1994; 61:1141–1146.PubMedGoogle Scholar
  12. 12.
    Mueller PO, Hunt RJ, Allen D, Parks AH, Hay WP. Intraperitoneal use of sodium carboxymethylcellulose in horses undergoing exploratory celiotomy. Vet Surg 1995; 24:112–117.PubMedCrossRefGoogle Scholar
  13. 13.
    Baxter GM, Jackman BR, Eades SC, Tyler DE. Failure of calcium channel blockade to prevent intra-abdominal adhesions in ponies. Vet Surg 1993; 22:496–500.PubMedCrossRefGoogle Scholar
  14. 14.
    Baykal A, Onat D, Rasa K, Renda N, Sayek I. Effects of polyglycolic acid and polypropylene meshes on postoperative adhesion formation in mice. World J Surg 1997; 21:579–582.PubMedCrossRefGoogle Scholar
  15. 15.
    Wiseman DM, Trout JR, Franklin RR, Diamond MP. Meta-analysis of safety and efficacy of an adhesion barrier in (INTERCEED TC7) in laparotomy. J Reprod Med 1998; 43: 1999; 44; 325–331.Google Scholar
  16. 16.
    Haney AF, Doty E. The peritoneal response to expanded polytetrafluoroethylene and oxidized regenerated cellulose surgical adhesion barriers. Artif Cells Blood Substit Immobil Biotechnol 1996; 24:121–141.PubMedCrossRefGoogle Scholar
  17. 17.
    Haney AF, Doty E. Murine peritoneal injury and de novo adhesion formation caused by oxidized-regenerated cellulose (Interceed [TC7]) but not expanded polytetrafluoroethylene (Gore-Tex Surgical Membrane). Fertil Steril 1992; 57:202–208.PubMedGoogle Scholar
  18. 18.
    Harris ES, Morgan RF, Rodeheaver GT. Analysis of the kinetics of peritoneal adhesion formation in the rat and evaluation of potential antiadhesive agents. Surgery (St. Louis) 1995; 117:663–669.CrossRefGoogle Scholar
  19. 19.
    Ryan CK, Sax HC. Evaluation of a carboxymethylcellulose sponge for prevention of postoperative adhesions. Am J Surg 1995; 169:154–159.PubMedCrossRefGoogle Scholar
  20. 20.
    Levison ME, Pontzer RE. Peritonitis and other intra-abdominal infections. In: Mandell GL, Douglas RG, Bennett JE, eds. Principles and Practice of Infectious Diseases, 2nd Ed. New York: Wiley, 1979:476–503.Google Scholar
  21. 21.
    Esperanca MJ, Collins DL. Peritoneal dialysis efficiency in relation to body weight. J Pediatr Surg 1966; 1:162–169.CrossRefGoogle Scholar
  22. 22.
    diZerega GS, Rodgers KE. The Peritoneum. New York: Springer-Verlag, 1992.Google Scholar
  23. 23.
    Flessner MR. Peritoneal transport physiology: insights from basic research. J Am Soc Nephrol 1991; 2:122–135.PubMedGoogle Scholar
  24. 24.
    Dedrick RL. Interspecies scaling of regional drug delivery. J Pharm Sci 1986; 75:1047–1052.PubMedCrossRefGoogle Scholar
  25. 25.
    Dedrick RL, Bischoff KB. Species similarities in pharmaco-kinetics. Fed Proc 1980; 39:54–59.PubMedGoogle Scholar
  26. 26.
    Dedrick RL, Flessner MF, Collins JM, Schultz JS. A distributed model of peritoneal transport. In: Maher JF, Winchester JF, eds. Frontiers in Peritoneal Dialysis. New York: Field, Rich, 1986:31–35.Google Scholar
  27. 27.
    Dubois D, Dubois E. A formula to estimate the approximate surface area if height and weight be known. Arch Intern Med 1916; 17:863–871.CrossRefGoogle Scholar
  28. 28.
    Cromack DT, Cromack TR, Pretorius G, DeMeules JE. Development of a predictive value equation for the minimum fluid volume to completely coat the intraperitoneal surface of rodents. Surg Forum 1985; 36:477–478.Google Scholar
  29. 29.
    Krause TJ, Goldsmith NK, Ebner S, Zazanis GA, McKinnon RD. An inhibitor of cell proliferation associated with adhesion formation is suppressed by N,O-carboxymethyl chitosan. J Invest Surg 1998; 11:105–113.PubMedCrossRefGoogle Scholar
  30. 30.
    Wiseman DM, Saferstein L, Wolf S. Bioresorbable Medical Devices from Oxidized Polysaccharides Patent Application: EP 0815 879 A2, 1998.Google Scholar
  31. 31.
    Reddy S, Santanam N, Reddy PP, Rock JA, Murphy AA, Parthasarathy S. Interaction of Interceed oxidized regenerated cellulose with macrophages: a potential mechanism by which Interceed may prevent adhesions. Am J Obstet Gynecol 1997; 177:1315–1320.PubMedCrossRefGoogle Scholar
  32. 32.
    Watt PW, Harvey W, Lorimer E, Wiseman D. Use of Oxidized Cellulose and Complexes Thereof for Chronic Wound Healing. U.S. Patent Application WO 98/00-180, 1998.Google Scholar
  33. 33.
    Bellon JM, Contreras LA, Bujan J, Jurado F. Effect of phosphatidylcholine on the process of peritoneal adhesion following implantation of a polypropylene mesh prosthesis. Biomaterials 1996; 17:1369–1372.PubMedCrossRefGoogle Scholar
  34. 34.
    Myhre-Jensen O, Larsen SB, Astrup T. Fibrinolytic activity in serosal and synovial membranes. Rats, guinea pigs, and rabbits. Arch Pathol 1969; 88:623–630.Google Scholar
  35. 35.
    James DC, Ellis H, Hugh TB. The effect of streptokinase on experimental intraperitoneal adhesion formation. J Pathol Bacteriol 1965; 90:279–287.PubMedCrossRefGoogle Scholar
  36. 36.
    Wright LT, Smith DH, Rothman M, Quosh ET, Metzger WI. Prevention of postoperative adhesions in rabbits with streptococcal metabolites. Proc Soc Exp Biol Med 1950; 75:602–604.PubMedGoogle Scholar
  37. 37.
    Bouckaert PX, van Wersch JW, Schellekens LA, Evers JL, Rolland R. Haemostatic and fibrinolytic properties of peritoneal fluid in the menstrual cycle. Br J Obstet Gynaecol 1984; 91:256–259.PubMedCrossRefGoogle Scholar
  38. 38.
    Bouckaert PX, Evers JL, Doesburg WH, Schellekens LA, Rolland R. Patterns of changes in glycoproteins, polypeptides, and steroids in the peritoneal fluid of women during the periovulatory phase of the menstrual cycle. J Clin Endocrinol Metab 1986; 62:293–299.PubMedCrossRefGoogle Scholar
  39. 39.
    Bouckaert PX, Evers JL, Doesburg WH, Schellekens LA, Brombacher PH, Rolland R. Patterns of changes in proteins in the peritoneal fluid of women during the periovulatory phase of the menstrual cycle. J Reprod Fertil 1986; 77:329–336.PubMedCrossRefGoogle Scholar
  40. 40.
    Montgomery-Rice V, Shanti A, Moghissi KS, Leach RE. A comparative evaluation of Poloxamer 407 and oxidized regenerated cellulose (Interceed [TC7]*) to reduce postoperative adhesion formation in the rat uterine horn model. Fertil Steril 1993; 59:901–906.Google Scholar
  41. 41.
    Arora M, Jaroudi KA, Hamilton CJ, Dayel F. Controlled comparison of Interceed and amniotic membrane graft in the prevention of postoperative adhesions in the rabbit uterine horn model. Eur J Obstet Gynecol Reprod Biol 1994; 55:179–182.PubMedCrossRefGoogle Scholar
  42. 42.
    Haney AF, Doty E. Expanded-polytetrafluoroethylene but not oxidized regenerated cellulose prevents adhesion formation and reformation in a mouse uterine horn model of surgical injury. Fertil Steril 1993; 60:550–558.PubMedGoogle Scholar
  43. 43.
    West JL, Chowdhury SM, Sawhney AS, Pathak CP, Dunn RC, Hubbell JA. Efficacy of adhesion barriers. Resorbable hydrogel, oxidized regenerated cellulose and hyaluronic acid. J Reprod Med 1996; 41:149–154.PubMedGoogle Scholar
  44. 44.
    Ortega-Moreno J. Effects of TC7 associated to 32% dextran 70, heparin and carboxymethylcellulose in adhesion prevention in the rat. Arch Gynecol Obstet 1993; 253:27–32.PubMedCrossRefGoogle Scholar
  45. 45.
    Pagidas K, Tulandi T. Effects of Ringer’s lactate, Interceed (TC7) and Gore-Tex Surgical Membrane on postsurgical adhesion formation. Fertil Steril 1992: 57:199–201.PubMedGoogle Scholar
  46. 46.
    LeGrand EK, Rodgers KE, Girgis W, et al. Efficacy of tolmetin sodium for adhesion prevention in rabbit and rat models. J Surg Res 1994; 56:67–71.PubMedCrossRefGoogle Scholar
  47. 47.
    Best CL, Rittenhouse D, Sueldo CE. A comparison of TC7 and 32% dextran 70 for prevention of postoperative adhesions in hamsters. Obstet Gynecol 1991; 78:858–860.PubMedGoogle Scholar
  48. 48.
    Linsky CB, Cunningham T, Diamond MP, Constantine B, DeCherney AH, diZerega GS. Development of a uterine horn model of adhesions in the rabbit. Infertility 1987; 10:71–85.Google Scholar
  49. 49.
    Linsky CB, Diamond MP, Cunningham T, Constantine B, DeCherney AH, diZerega GS. Adhesion reduction in the rabbit uterine horn model using an absorbable barrier, TC-7. J Reprod Med 1987; 32:17–20.PubMedGoogle Scholar
  50. 50.
    Wiseman DM, Kamp LF, Saferstein L, Linsky CB, Gottlick LE, Diamond MP. Improving the efficacy of Interceed Barrier in the presence of blood using thrombin, heparin or a blood insensitive barrier, modified Interceed (nTC7). Prog Clin Biol Res 1993; 381:205–212.PubMedGoogle Scholar
  51. 51.
    Lo H, Maier KH, Anderson JM, Zupon MA. Inhibition of postoperative pelvic adhesions by a bioresorbable carbohydrate solution (ADCON-P). Fertil Steril 1998; (Prog Suppl):S25.Google Scholar
  52. 52.
    Johns DB, Rodgers KE, Donahue WD, Kiorpes TC, diZerega GS. Reduction of adhesion formation by postoperative administration of ionically cross-linked hyaluronic acid. Fertil Steril 1997; 68:37–42.PubMedCrossRefGoogle Scholar
  53. 53.
    Leach RE, Burns JW, Dawe EJ, Smith Barbour MD, Diamond MP. Reduction of postsurgical adhesion formation in the rabbit uterine horn model with use of hyaluronate/ carboxymethylcellulose gel. Fertil Steril 1998; 69:415–418.PubMedCrossRefGoogle Scholar
  54. 54.
    Diamond MP, Linsky CB, Cunningham T, et al. Adhesion reformation: reduction by the use of INTERCEED R (TC7) plus heparin. J Gynecol Surg 1991; 7:1–6.PubMedCrossRefGoogle Scholar
  55. 55.
    Wiseman DM, Huang WJ, Johns DB, Rodgers KE, diZerega GS. Time-dependent effect of tolmetin sodium in a rabbit uterine adhesion model. J Invest Surg 1994; 7:527–532.PubMedCrossRefGoogle Scholar
  56. 56.
    Rodgers KE, Johns DB, Girgis W, Campeau J, diZerega GS. Reduction of adhesion formation with hyaluronic acid after peritoneal surgery in rabbits. Fertil Steril 1997; 67:553–558.PubMedCrossRefGoogle Scholar
  57. 57.
    Steinleitner A, Lopez G, Suarez M, Lambert H. An evaluation of Flowgel as an intraperitoneal barrier for prevention of postsurgical adhesion reformation. Fertil Steril 1992; 57:305–308.PubMedGoogle Scholar
  58. 58.
    Maxson WS, Herbert CM, Oldfield EL, Hill GA. Efficacy of a modified oxidized cellulose fabric in the prevention of adhesion formation. Gynecol Obstet Invest 1988; 26:160–165.PubMedCrossRefGoogle Scholar
  59. 59.
    Best CL, Rittenhouse D, Vasquez C, Norng T, Subias E, Sueldo CE. Evaluation of Interceed(TC7) for reduction of postoperative adhesions in rabbits. Fertil Steril 1992; 58:817–820.PubMedGoogle Scholar
  60. 60.
    Dunn RC, Mohler M. Effect of varying days of tissue plas-minogen activator therapy on the prevention of post-surgical adhesions in a rabbit model. J Surg Res 1993; 54:242–245.PubMedCrossRefGoogle Scholar
  61. 61.
    Dunn RC, Steinleitner AJ, Lambert H. 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 1991; 164:1327–1330.PubMedGoogle Scholar
  62. 62.
    Doody KJ, Dunn RC, Buttram VC Jr. Recombinant tissue plasminogen activator reduces adhesion formation in a rabbit uterine horn model. Fertil Steril 1989; 51:509–512.PubMedGoogle Scholar
  63. 63.
    Wiseman DM, Gottlick LE, Diamond MP. Effect of throm-bin-induced hemostasis on the efficacy of an absorbable adhesion barrier. J Reprod Med 1992; 37:766–770.PubMedGoogle Scholar
  64. 64.
    Burns JW, Skinner K, Colt MJ, Burgess L, Rose R, Diamond MP. A hyaluronate based gel for the prevention of postsurgical adhesions: evaluation in two animal species. Fertil Steril 1996; 66:814–821.PubMedGoogle Scholar
  65. 65.
    Wiseman DM, Gottlick-Iarkowski L, Kamp L. Prevention of bowel adhesions using two barriers of Oxidized Regenerated Cellulose (ORC). J Invest Surg 1999, in press.Google Scholar
  66. 66.
    Swindle MM. Swine as replacements for dogs in the surgical teaching and research laboratory. Lab Anim Sci 1984; 34:383–385.PubMedGoogle Scholar
  67. 67.
    Gomez NA, Leon CJ, Iniquez SA. Use of TC7 in the prevention of adhesions in handsewn and stapled colonic anastomoses. Dis Colon Rectum 1994; 37:512–513.PubMedCrossRefGoogle Scholar
  68. 68.
    Snoj M, Ar’Rajab A, Ahren B, Bengmark S. Effect of phosphatidylcholine on postoperative adhesions after small bowel anastomosis in the rat. Br J Surg 1992; 79:427–429.PubMedCrossRefGoogle Scholar
  69. 69.
    Burns JW, Colt MJ, Burgess LS, Skinner KC. Preclinical evaluation of Seprafilm bioresorbable membrane. Eur J Surg (Suppl) 1997:40–48.Google Scholar
  70. 70.
    Menzies D, Ellis H. The role of plasminogen activator in adhesion prevention. Surg Gynecol Obstet 1991; 172:362–366.PubMedGoogle Scholar
  71. 71.
    Diamond MP, Linsky CB, Cunningham T, Constantine B, diZerega GS, DeCherney AH. A model for sidewall adhesions in the rabbit: reduction by an absorbable barrier. Microsurgery 1987; 8:197–200.PubMedCrossRefGoogle Scholar
  72. 72.
    Boyers SP, Diamond MP, DeCherney AH. Reduction of postoperative pelvic adhesions in the rabbit with Gore-Tex surgical membrane. Fertil Steril 1988; 49:1066–1070.PubMedGoogle Scholar
  73. 73.
    Snoj M, Ar’Rajab A, Ahren B, Larsson K, Bengmark S. Phospholipase-resistant phosphatidylcholine reduces intra-abdominal adhesions induced by bacterial peritonitis. Res Exp Med (Berl) 1993; 193:117–122.CrossRefGoogle Scholar
  74. 74.
    Ar’Rajab A, Ahren B, Rozga J, Bengmark S. Phosphatidylcholine prevents postoperative peritoneal adhesions: an experimental study in the rat. J Surg Res 1991; 50:212–215.PubMedCrossRefGoogle Scholar
  75. 75.
    Ar’Rajab A, Dawidson I, Sentementes J, Sikes P, Harris R, Mileski W. Enhancement of peritoneal macrophages reduces postoperative peritoneal adhesion formation. J Surg Res 1995; 58:307–312.PubMedCrossRefGoogle Scholar
  76. 76.
    Buckman RF, Woods M, Sargent L, Gervin AS. A unifying pathogenetic mechanism in the etiology of intraperitoneal adhesions. J Surg Res 1976; 20:1–5.PubMedCrossRefGoogle Scholar
  77. 77.
    Albrechtsen OK. The fibrinolytic activity of animal tissues. Acta Physiol Scand 1957; 39:284–290.PubMedCrossRefGoogle Scholar
  78. 78.
    Albrechtsen OK. The f ibrinolytic activity of human tissues. Br J Haematol 1957; 3:284–291.PubMedCrossRefGoogle Scholar
  79. 79.
    Merlo G, Fausone G, Barbero C, Castagna B. Fibrinolytic activity of the human peritoneum. Eur Surg Res 1980; 12:433–438.PubMedCrossRefGoogle Scholar
  80. 80.
    Raftery AT. Regeneration of parietal and visceral peritoneum: an electron microscopical study. J Anat 1973; 115:375–392.PubMedGoogle Scholar
  81. 81.
    Raftery AT. Method for measuring fibrinolytic activity in a single layer of cells. J Clin Pathol 1981; 34:625–629.PubMedCrossRefGoogle Scholar
  82. 82.
    Wallwiener D, Meyer A, Bastert G. Adhesion formation of the parietal and visceral peritoneum: an explanation for the controversy on the use of autologous and alloplastic barriers? Fertil Steril 1998; 69:132–137.PubMedCrossRefGoogle Scholar
  83. 83.
    Marana R, Catalano GF, Caruana P, Margutti F, Muzii L, Mancuso S. Postoperative adhesion formation and reproductive outcome using Interceed after ovarian surgery: a randomized trial in the rabbit model. Hum Reprod (Oxf) 1997; 12:1935–1938.CrossRefGoogle Scholar
  84. 84.
    Magro B, Mita P, Bracco GL, Coccia E, Scarselli G. Expanded polytetrafluoroethylene surgical membrane in ovarian surgery on the rabbit. Biocompatibility, adhesion prevention properties and ability to preserve reproductive capacity. J Reprod Med 1996; 41:73–78.PubMedGoogle Scholar
  85. 85.
    Wiskind AK, Rice VM, Dudley AG. Evaluation of adhesion formation using Interceed (TC7) absorbable adhesion barrier on ovarian surgical wounds in the rabbit model. Obstet Gynecol 1993; 81:1025–1028.PubMedGoogle Scholar
  86. 86.
    Hill-West JL, Chowdhury SM, Dunn RC, Hubbell JA. Efficacy of a resorbable hydrogel barrier, oxidized regenerated cellulose, and hyaluronic acid in the prevention of ovarian adhesions in a rabbit model. Fertil Steril 1994; 62:630–634.PubMedGoogle Scholar
  87. 87.
    Rozga J, Ahren B, Bengmark S. Prevention of adhesions by high molecular weight dextran in rats. Re-evaluation in nine experiments. Acta Chir Scand 1990; 156:763–769.PubMedGoogle Scholar
  88. 88.
    Elkins TE, Stovall TG, Warren J, Ling FW, Meyer NL. A histologie evaluation of peritoneal injury and repair: implications for adhesion formation. Obstet Gynecol 1987; 70:225–228.PubMedGoogle Scholar
  89. 89.
    Ellis H. The cause and prevention of postoperative intra-peritoneal adhesions. Surg Gynecol Obstet 1971; 133:497–511.PubMedGoogle Scholar
  90. 90.
    Treutner KH, Bertram P, Lerch MM, et al. Prevention of postoperative adhesions by single intraperitoneal medication. J Surg Res 1995; 59:764–771.PubMedCrossRefGoogle Scholar
  91. 91.
    Nagelschmidt M, Saad S. Influence of polyethylene glycol 4000 and dextran 70 on adhesion formation in rats. J Surg Res 1997; 67:113–118.PubMedCrossRefGoogle Scholar
  92. 92.
    Urman B, Gomel V, Jetha N. Effect of hyaluronic acid on postoperative intraperitoneal adhesion formation in the rat model. Fertil Steril 1991; 56:563–567.PubMedGoogle Scholar
  93. 93.
    Kaplun A, Griffel B, Halperin B, Aronson M. A model for adhesion formation by thermal injury in the abdominal cavity of the mouse. Eur Surg Res 1984; 16:131–135.PubMedCrossRefGoogle Scholar
  94. 94.
    Porter JM, Ball AP, Silver D. Mesothelial fibrinolysis. J Cardiovasc Surg 1971; 62:725–730.Google Scholar
  95. 95.
    Rappaport WD, Holcomb M, Valente J, Chvapil M. Antibiotic irrigation and the formation of intraabdominal adhesions. Am J Surg 1989; 158:435–437.PubMedCrossRefGoogle Scholar
  96. 96.
    Rodgers KE, Girgis W, diZerega GS. Effect of tolmetin sodium dihydrate on adhesion formation by intraperitoneal administration of antineoplastic agents. Cancer Chemother Pharmacol 1992; 29:248–256.PubMedCrossRefGoogle Scholar
  97. 97.
    Lehman EP, Boys F. The prevention of peritoneal adhesions with heparin. Ann Surg 1940; 111:427–435.PubMedCrossRefGoogle Scholar
  98. 98.
    Reikeras O, Nordstrand K. Use of dextran to prevent intraperitoneal adhesions caused by maize starch powder. Eur Surg Res 1985; 17:251–253.PubMedCrossRefGoogle Scholar
  99. 99.
    Farmer L, Ayoub M, Warejcka D, Southerland S, Freeman A, Solis M. Adhesion formation after intraperitoneal and extraperitoneal implantation of polypropylene mesh. Am Surg 1998; 64:144–146.PubMedGoogle Scholar
  100. 100.
    Nairn JO, Pulley D, Scanlan K, Hinshaw JR, Lanzafame RJ. Reduction of postoperative adhesions to Marlex mesh using experimental adhesion barriers in rats. J Laparo-endosc Surg 1993; 3:187–190.CrossRefGoogle Scholar
  101. 101.
    Fitzgibbons RJ Jr, Salerno GM, Filipi CJ, Hunter WJ, Watson P. A laparoscopic intraperitoneal onlay mesh technique for the repair of an indirect inguinal hernia. Ann Surg 1994; 219:144–156.PubMedCrossRefGoogle Scholar
  102. 102.
    Diamond MP, Nezhat F. Adhesions after resection of ovarian endometriomas. Fertil Steril 1993; 59:934–935.PubMedGoogle Scholar
  103. 103.
    Wiseman DM, Trout JR, Diamond MP. The rates of adhesion development and the effects of crystalloid solutions on adhesion development in pelvic surgery. Fertil Steril 1998; 70:702–711.PubMedCrossRefGoogle Scholar
  104. 104.
    Linsky CB, Diamond MP, DeCherney AH, diZerega GS, Cunningham T. Effect of blood on the efficacy of barrier adhesion reduction in the rabbit uterine horn model. Infertility 1988; 11:273–280.Google Scholar
  105. 105.
    Evans DM, McAree K, Guyton DP, Hawkins N, Stakleff K. 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.PubMedCrossRefGoogle Scholar
  106. 106.
    Tsimoyiannis EC, Tsimoyiannis JC, Sarros CJ, et al. The role of oxygen-derived free radicals in peritoneal adhesion formation induced by ileal ischaemia/reperfusion. Acta Chir Scand 1989; 155:171–174.PubMedGoogle Scholar
  107. 107.
    O’Leary JP, Wickbom G, Cha SO, Wickbom A. The role offeces, necrotic tissue, and various blocking agents in the prevention of adhesions. Ann Surg 1988; 207:693–698.PubMedCrossRefGoogle Scholar
  108. 108.
    Montz FJ, Wheeler JH, Lau LM. Inability of polyglycolic acid mesh to inhibit immediate postradical pelvic surgery adhesions. Gynecol Oncol 1990; 38:230–233.PubMedCrossRefGoogle Scholar
  109. 109.
    Montz FJ, Monk BJ, Lacy SM. Effectiveness of two barriers at inhibiting post-radical pelvic surgery adhesions. Gynecol Oncol 1993; 48:247–251.PubMedCrossRefGoogle Scholar
  110. 110.
    Gallup D, Wheelock T, Plouffe L, Metheny W. Assessment of the efficacy of INTERCED after hysterectomy in preventing adhesion formation in the rabbit model. Gynecol Oncol 1993; 50:265–266.CrossRefGoogle Scholar
  111. 111.
    Hoban LD, Pierce M, Quance J, et al. Use of polypenta-peptides of elastin to prevent postoperative adhesions: efficacy in a contaminated peritoneal model. J Surg Res 1994: 56:179–183.PubMedCrossRefGoogle Scholar
  112. 112.
    Williams-Smith H. Observations on the flora of the alimentary tract of animals and factors affecting its composition. J Pathol Bact 1965; 89:95–122.CrossRefGoogle Scholar
  113. 113.
    Toh H, Torisu M, Shimura H, et al. In vitro analysis of peritoneal adhesions in peritonitis. J Surg Res 1996; 61:250–255.PubMedCrossRefGoogle Scholar
  114. 114.
    Marcovici I, Rosenzweig BA, Brill AI, Scommegna A. Colchicine and post-inflammatory adhesions in a rabbit model: a dose-response study. Obstet Gynecol 1993; 82:216–218.PubMedGoogle Scholar
  115. 115.
    Dunselman GA, Willebrand D, Land JA, Bouckaert PX, Evers JL. A rabbit model of endometriosis. Gynecol Obstet Invest 1989; 27:29–33.PubMedCrossRefGoogle Scholar
  116. 116.
    Wright JA, Sharpe-Timms KL. Gonadotropin-releasing hormone agonist therapy reduces postoperative adhesion formation and reformation after adhesiolysis in rat models for adhesion formation and endometriosis. Fertil Steril 1995; 63:1094–1100.PubMedGoogle Scholar
  117. 117.
    Taskin O, Buhur A, Birincioglu M, et al. The effects of duration of CO2 insufflation and irrigation on peritoneal microcirculation assessed by free radical scavengers and total glutathion levels during operative laparoscopy. J Am Assoc Gynecol Laparosc 1998; 5:129–133.PubMedCrossRefGoogle Scholar
  118. 118.
    Chen MD, Teigen GA, Reynolds HT, Johnson PR, Fowler JM. Laparoscopy versus laparotomy: an evaluation of adhesion formation after pelvic and paraaortic lympha-denectomy in a porcine model. Am J Obstet Gynecol 1998: 178:499–503.PubMedCrossRefGoogle Scholar
  119. 119.
    Marana R, Luciano AA, Muzii L, Marendino VE, Mancuso S. Laparoscopy versus laparotomy for ovarian conservative surgery: a randomized trial in the rabbit model. Am J Obstet Gynecol 1994; 171:861–864.PubMedGoogle Scholar
  120. 120.
    Fielder EP, Guzick DS, Guido R, Ranbour-Shakir A, Krasnow JS. Adhesion formation from release of dermoid contents in the peritoneal cavity and effect of copious lavage: a prospective, randomized, blinded, controlled study in a rabbit model. Fertil Steril 1996; 65:852–859.PubMedGoogle Scholar
  121. 121.
    De Iaco PA, Stefanetti M, Pressato D, et al. A novel hyaluronan-based gel in laparoscopic adhesion prevention: preclinical evaluation in an animal model. Fertil Steril 1998: 69:318–323.PubMedCrossRefGoogle Scholar
  122. 122.
    Haney AF, Doty E. The formation of coalescing peritoneal adhesions requires injury to both contacting peritoneal surfaces. Fertil Steril 1994; 61:767–775.PubMedGoogle Scholar
  123. 123.
    Kaleli B, Ozden A, Aybek Z, Bostanci B. The effect of L-arginine and pentoxifylline on postoperative adhesion formation. Acta Obstet Gynecol Scand 1998; 77:377–380.PubMedCrossRefGoogle Scholar
  124. 124.
    Ortega-Moreno J, Caballero-Gomez JM. Postoperative adhesion after uterine horn surgery in the rat, with the use of TC7. Eur J Obstet Gynecol Reprod Biol 1993; 48:51–59.PubMedCrossRefGoogle Scholar
  125. 125.
    Korell M, Scheidel P, Hepp H. Experimental animal model for readhesion formation study. J Invest Surg 1994; 7:409–415.PubMedCrossRefGoogle Scholar
  126. 126.
    Wiseman DM, Johns DB. Anatomical synergy between sodium hyaluronate (HA) and INTERCEED barrier in rabbits with two types of adhesions. Fertil Steril 1993; Prog Suppl:S25.Google Scholar
  127. 127.
    Diamond MP, Cunningham T, Linsky CB, DeCherney AH. Laparoscopic application of Interceed (TC7) in the pig.J Gynecol Surg 1989; 5:145–148.CrossRefGoogle Scholar
  128. 128.
    Jibhorn H, Ahonen J, Zederfeldt B. Bursting strength of the colon after left colon resection and anastomosis. Am J Surg 1978; 136:587–594.CrossRefGoogle Scholar
  129. 129.
    Hesp FLEM, Hendriks T, Lubbers JC, de Boer HHM. Wound healing in the intestinal wall. A comparison between ileal and colonic anastomoses. Dis Colon Rectum 1984; 27:99–104.PubMedCrossRefGoogle Scholar
  130. 130.
    Medina M, Paddock HN, Connolly RJ, Schwaitzberg SD. Novel antiadhesion barrier does not prevent anastomotic healing in a rabbit model. J Invest Surg 1995; 8:179–186.PubMedCrossRefGoogle Scholar
  131. 131.
    Wise L, McAlister W, Stein T, Schuck P. Studies on the healing of anastomoses of small and large intestines. Surg Gynecol Obst 1975; 141:190–194.Google Scholar
  132. 132.
    Houston KA, McRitchie DI, Rotstein OD. Tissue plasminogen activator reverses the deleterious effect of infection on colonie wound healing. Ann Surg 1990; 211:130–135.PubMedCrossRefGoogle Scholar
  133. 133.
    Hesp FLEM, Hendriks T, Lubbers JC, de Boer HHM. Wound healing in the intestinal wall. Effects of infection on experimental ileal and colonie anastomoses. Dis Colon Rectum 1984; 27:462–467.PubMedCrossRefGoogle Scholar
  134. 134.
    Edlich RF, Panek PH, Rodeheaver GT, Turnbull VG, Kurtz LD, Edgerton MT. Physical and chemical configuration of sutures in the development of surgical infection. Ann Surg 1973; 177:679–688.PubMedCrossRefGoogle Scholar
  135. 135.
    Dunn DL, Rotstein OD, Simmons RL. Fibrin in peritonitis. IV. Synergistic intraperitoneal infection caused by Escherichia coli and Bacteroides fragilis within fibrin clots. Arch Surg 1984; 119:139–145.PubMedCrossRefGoogle Scholar
  136. 136.
    Bartlett JG, Gorbach S. An animal model of intra-abdominal sepsis. Scand J Infect Dis Suppl 1979; 19:26–29.PubMedGoogle Scholar
  137. 137.
    Miller RJ, Tzianabos A, Dethlefsen S, Gershkovich J, Burns JW, Onderdonk A. The effect of bacterial species on the infection propagation with adhesion reduction products in vivo. Fertil Steril 1998; Prog Suppl:S26.Google Scholar
  138. 138.
    Hsiang YN. Application of appropriate statistical methods in experimental surgery. J Invest Surg 1991; 4:415–421.PubMedCrossRefGoogle Scholar
  139. 139.
    Cohen J; Statistical Power Analysis for the Behavioral Sciences, 2nd Ed. Hillsdale, NJ: Lawrence Erlbaum, 1988.Google Scholar
  140. 140.
    Bowman MC, Li TC, Cooke ID. Inter-observer variability at laparoscopic assessment of pelvic adhesions. Hum Reprod (Oxf) 1995; 10:155–160.CrossRefGoogle Scholar
  141. 141.
    Corson SL, Batzer FR, Gocial B, Kelly M, Gutmann JN, Maislin G. Intra-observer and interobserver variability in scoring laparoscopic diagnosis of pelvic adhesions. Hum Reprod (Oxf) 1995; 10:161–164.CrossRefGoogle Scholar
  142. 142.
    Adhesion Scoring Group. Improvement of interobserver reproducibility of adhesion scoring systems. Fertil Steril 1994; 62:984–988.Google Scholar
  143. 143.
    Lifecore Biomedical Inc. Quarterly report form 10K. Chaska, MN. September 5, 1996.Google Scholar
  144. 144.
    Yaacobi Y, Israel AA, Goldberg EP. Prevention of postoperative abdominal adhesions by tissue precoating with polymer solutions. J Surg Res 1993; 55:422–426.PubMedCrossRefGoogle Scholar
  145. 145.
    Burns J, Colt MJ, Skrabut E, Wiseman D. Evaluation of de novo adhesion prevention in a rabbit model by precoating with a tissue protective hyaluronate solution. Fertil Steril 1997; Prog Suppl:S66.Google Scholar
  146. 146.
    Milligan DW, Raftery AT. Observations on the pathogenesis of peritoneal adhesions: a light and electron microscopical study. Br J Surg 1974; 61:274–280.PubMedCrossRefGoogle Scholar
  147. 147.
    Raftery AT. Regeneration of parietal and visceral peritoneum. A light microscopical study. Br J Surg 1973; 60:293–299.PubMedCrossRefGoogle Scholar
  148. 148.
    Schade DS, Williamson JR. The pathogenesis of peritoneal adhesions: an ultrastructural study. Ann Surg 1968; 167:500–510.PubMedCrossRefGoogle Scholar
  149. 149.
    Chegini N, Simms J, Williams RS, Masterson BJ. Identification of epidermal growth factor, transforming growth factor-alpha, and epidermal growth factor receptor in surgically induced pelvic adhesions in the rat and intraperitoneal adhesions in the human. Am J Obstet Gynecol 1994; 171:321–327.PubMedGoogle Scholar
  150. 150.
    Whawell SA, Wang Y, Fleming KA, Thompson EM, Thompson JN. Localization of plasminogen activator inhibitor-1 production in inflamed appendix by in situ hybridization.J Pathol 1993; 169:67–71.PubMedCrossRefGoogle Scholar
  151. 151.
    McKinney WP, Young MJ, Hartz A, Lee MB. The inexact use of Fisher’s Exact Test in six major medical journals. JAMA 1989; 261:3430–3433.PubMedCrossRefGoogle Scholar
  152. 152.
    Tukey JW. Comparing individual means in the analysis of variance. Biometrics 1949; 5:99–114.PubMedCrossRefGoogle Scholar
  153. 153.
    Duncan DB. Multiple range and multiple F tests. Biometrics 1955; 2:1–42.CrossRefGoogle Scholar
  154. 154.
    Dunnett CW. New tables for multiple comparisons with a control. Biometrics 1964; 20:482–491.CrossRefGoogle Scholar
  155. 155.
    Box GEP, Hunter WG, Hunter JS. Statistics for Experiments. New York: Wiley, 1978:203–207.Google Scholar
  156. 156.
    Godfery K. Comparing the means of several groups. N Engl J Med 1985; 313:1450–1456.CrossRefGoogle Scholar
  157. 157.
    SAS. Users Guide: Statistics Version 5. Cary, NC: SAS Institute, 1985:651.Google Scholar
  158. 158.
    Conover WJ, Iman RL. Rank transformations as a bridge between parametric and non-parametric statistics. Am Statist 1981; 35:124–128.Google Scholar
  159. 159.
    Strandell A, Thorburn J, Tronstad SE, et al. Effectiveness and safety of a bioresorbable carbohydrate solution for prevention of post-operative adhesions in pelvic surgery. Fertil Steril 1998; Prog Suppl:S412.Google Scholar
  160. 160.
    Reid RL, Lie K, Spence JE, Tulandi T, Yuzpe A. Clinical evaluation of the efficacy of heparin-saturated Interceed for prevention of adhesion reformation in the pelvic side-wall of the human. Prog Clin Biol Res 1993; 381:261–264.PubMedGoogle Scholar
  161. 161.
    Mais V, Ajossa S, Marongiu D, Peiretti RF, Guerriero S, Melis GB. Reduction of adhesion reformation after laparoscopic endometriosis surgery: a randomized trial with an oxidized regenerated cellulose absorbable barrier. Obstet Gynecol 1995; 86:512–515.PubMedGoogle Scholar
  162. 162.
    Mais V, Ajossa S, Piras B, Guerriero S, Marongiu G, Melis GB. Prevention of de novo adhesion formation after laparoscopic myomectomy: a randomized trial to evaluate the effectiveness of an oxidized regenerated cellulose absorbable barrier. Hum Reprod (Oxf) 1995; 10:3133–3135.Google Scholar
  163. 163.
    Keckstein J, Ulrich U, Sasse V, Roth A, Tuttlies F, Kara-georgieva E. Reduction of postoperative adhesion formation after laparoscopic ovarian cystectomy. Hum Reprod (Oxf) 1996; 11:579–582.CrossRefGoogle Scholar
  164. 164.
    Azziz R. Microsurgery alone or with INTERCEED Absorbable Adhesion Barrier for pelvic sidewall adhesion reformation. The INTERCEED (TC7) Adhesion Barrier Study Group II. Surg Gynecol Obstet 1993; 177:135–139.PubMedGoogle Scholar
  165. 165.
    Li TC, Cooke ID. The value of an absorbable adhesion barrier, Interceed, in the prevention of adhesion reformation following microsurgical adhesiolysis. Br J Obstet Gynaecol 1994; 101:335–339.PubMedCrossRefGoogle Scholar
  166. 166.
    Franklin RR. Reduction of ovarian adhesions by the use of Interceed. Ovarian Adhesion Study Group. Obstet Gynecol 1995; 86:335–340.PubMedCrossRefGoogle Scholar
  167. 167.
    Sekiba K. Use of Interceed (TC7) absorbable adhesion barrier to reduce postoperative adhesion reformation in infertility and endometriosis surgery. The Obstetrics and Gynecology Adhesion Prevention Committee. Obstet Gynecol 1992; 79:518–522.PubMedGoogle Scholar
  168. 168.
    Nordic Adhesion Prevention Study Group. The efficacy of Interceed (TC7)* for prevention of reformation of postoperative adhesions on ovaries, fallopian tubes, and fimbriae in microsurgical operations for fertility: a multicenter study. Fertil Steril 1995; 63:709–714.Google Scholar
  169. 169.
    Surrey M. Postoperative adhesion formation following myomectomy. Fertil Steril 1992; (Prog Suppl):78S–79S.Google Scholar
  170. 170.
    Van Geldorp H, Trimbos-Kemper T. INTERCEED® (TC7) Absorbable Adhesion Barrier reduces the formation of postsurgical adhesions after ovarian surgery. Fertil Steril 1994; Prog Suppl:P273 [and Johnson & Johnson Medical Protocol 3067:11C/1311.00].Google Scholar
  171. 171.
    Huang WJ, Johns DB, Kronenthal RL. Ionically Cross-linked Carboxyl-Containing Polysaccharides for Adhesion Prevention. U.S. Patent 5,532,221, 1996.Google Scholar
  172. 172.
    Thornton MH, Johns DB, Campeau JD, Hoehler F, di-Zerega GS. Clinical evaluation of 0.5% ferric hyaluronate adhesion prevention gel for the reduction of adhesions following peritoneal cavity surgery: open-label pilot study. Hum Reprod (Oxf) 1998; 13:1480–1485.CrossRefGoogle Scholar
  173. 173.
    Diamond MP. Reduction of adhesions after uterine myomectomy by Seprafilm membrane (HAL-F): a blinded, prospective, randomized, multicenter clinical study. Seprafilm Adhesion Study Group. Fertil Steril 1996; 66:904–910.PubMedGoogle Scholar
  174. 174.
    Diamond MP, DeCherney AH, Linsky CB, Cunningham T, Constantine B. Assessment of carboxymethylcellulose and 32% dextran 70 for prevention of adhesions in a rabbit uterine horn model. Int J Fertil 1988; 33:278–282.PubMedGoogle Scholar
  175. 175.
    Adhesion Study Group. Reduction of postoperative pelvic adhesions with intraperitoneal 32% dextran 70: a prospective, randomized clinical trial. Fertil Steril 1983; 40:612–619.Google Scholar
  176. 176.
    Larsson B, Lalos O, Marsk L, et al. Effect of intraperitoneal instillation of 32% dextran 70 on postoperative adhesion formation after tubal surgery. Acta Obstet Gynecol Scand 1985; 64:437–441.PubMedCrossRefGoogle Scholar
  177. 177.
    Rosenberg SM, Board JA. High-molecular weight dextran in human infertility surgery. Am J Obstet Gynecol 1984; 148:380–385.PubMedGoogle Scholar
  178. 178.
    Jansen RP. Failure of intraperitoneal adjuncts to improve the outcome of pelvic operations in young women. Am J Obstet Gynecol 1985; 153:363–371.PubMedGoogle Scholar
  179. 179.
    Diamond MP, Linsky CB, Cunningham T, et al. Synergistic effects of INTERCEED (TC7) and heparin in reducing adhesion formation in the rabbit uterine horn model. Fertil Steril 1991; 55:389–394.PubMedGoogle Scholar
  180. 180.
    Jansen RP. Failure of peritoneal irrigation with heparin during pelvic operations upon young women to reduce adhesions. Surg Gynecol Obstet 1988; 166:154–160.PubMedGoogle Scholar
  181. 181.
    Saravelos H, Li TC. Post-operative adhesions after laparoscopic electrosurgical treatment for polycystic ovarian syndrome with the application of Interceed to one ovary: a prospective randomized controlled study. Hum Reprod (Oxf) 1996; 11:992–997.CrossRefGoogle Scholar
  182. 182.
    Greenblatt EM, Casper RF. Adhesion formation after laparoscopic ovarian cautery for polycystic ovarian syndrome: lack of correlation with pregnancy rate. Fertil Steril 1993; 60:766–770.PubMedGoogle Scholar

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© Springer Science+Business Media New York 2000

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  • David M. Wiseman

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