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Healing of experimental intestinal anastomoses

Parameters for repair

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Diseases of the Colon & Rectum

Abstract

Anastomotic dehiscence remains a major complication in surgery of the large bowel, and studies on the healing sequence of experimental anastomoses are necessary to define underlying mechanisms and find ways to improve surgical outcome, particularly in high-risk situations. For the quantitative description of anastomotic repair, both mechanical and biochemical parameters are employed, each with their own limitations. Mechanical parameters, either bursting pressure or breaking strength, only reflect growing anastomotic strength as long as disruption occurs within the anastomotic area, which is less than one week after surgery for the bursting pressure and probably up to two weeks for the breaking strength. The biochemical description of anastomotic repair has been limited to the behavior of collagen, as represented by its rather unique constituent amino acid hydroxyproline. Conclusions based on collagen concentrations—per unit weight—should be considered with caution since they may change as a consequence of changes in noncollagenous substances. In this respect, collagen content, per unit length, is probably a better parameter to describe anastomotic collagen levels. Few investigations have addressed the quality of collagen (e.g.,crosslinking or type). Since, at this time, no distinct correlations have been demonstrated between development of mechanical strength or occurrence of leakage and collagen levels in the healing anastomosis, attention should not be restricted to a description of the quantity of collagen present: the quality of anastomotic collagen should be investigated, perhaps even more so.

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References

  1. Hesp WL, Lubbers EJ, de Boer HH, Hendriks T. Anastomotic insufficiency in small bowel surgery: incidence and treatment. Langenbecks Arch Chir 1986;368:105–11.

    PubMed  CAS  Google Scholar 

  2. Schrock TR, Deveney CW, Dunphy JE. Factors contributing to leakage of colonic anastomoses. Ann Surg 1973;177:513–18.

    PubMed  CAS  Google Scholar 

  3. Fielding LP, Stewart-Brown S, Blesovsky L, Kearney G. Anastomotic integrity after operations for large-bowel cancer: a multicenter study. Br Med J 1980;281:411–14.

    Article  PubMed  CAS  Google Scholar 

  4. Khoury GA, Waxman BP. Large bowel anastomoses. 1. The healing process and sutured anastomoses—a review. Br J Surg 1983;70:61–3.

    PubMed  CAS  Google Scholar 

  5. Eckersley JR, Dudley HA. Wounds and wound healing. Br Med Bull 1988;44:423–36.

    PubMed  CAS  Google Scholar 

  6. Hermann JB, Woodward SC, Pulaski EJ. Healing of colonic anastomoses in the rat. Surg Gynecol Obstet 1964;119:269–75.

    Google Scholar 

  7. Ballantyne GH. Intestinal suturing: review of the experimental foundations for traditional doctrines. Dis Colon Rectum 1983;26:836–43.

    PubMed  CAS  Google Scholar 

  8. Houdart R, Lavergne A, Galian A, Hautefeuille P. Histopathological evolution of single-layer end-to-end intestinal anastomoses—a study of 210 colonic anastomoses in the rat, from the 2nd to 180th days. Gastroenterol Clin Biol 1983;7:465–73.

    PubMed  CAS  Google Scholar 

  9. Hunt TK. Prospective: a retrospective perspective on the nature of wounds. In: Barbul A, Pines E, Caldwell M, Hunt TK. Growth factors and other aspects of wound healing: biological and clinical implications. New York: Alan R Liss, 1988:xiii-xx.

    Google Scholar 

  10. Zederfeldt B. Factors influencing wound healing. In: Viidik A, Vuust J. Biology of collagen. London: Academic Press, 1980:347–62.

    Google Scholar 

  11. Forrest L. Current concepts in soft connective tissue wound healing. Br J Surg 1983;70:133–40.

    PubMed  CAS  Google Scholar 

  12. Smith R. Recovery and tissue repair. Br Med Bull 1985;41:295–301.

    PubMed  CAS  Google Scholar 

  13. Hastings C, van Winkle W, Barker E, Hinds J, Nichols W. Effect of suture material on healing wounds of stomach and colon. Surg Gynecol Obstet 1975;140:701–7.

    PubMed  CAS  Google Scholar 

  14. Hesp WL, Hendriks T, Schillings PH, Lubbers EJ, de Boer HHM. Histological features of wound repair: a comparison between experimental ileal and colonic anastomoses. Br J Exp Pathol 1985;66:511–18.

    PubMed  CAS  Google Scholar 

  15. Chlumsky V. Experimentelle Untersuchungen über die verschiedenen Method der Darmvereinigung. Bruns Beitr Klin Chir 1899;25:539–600.

    Google Scholar 

  16. Nelsen TS, Anders CJ. Dynamic aspects of small intestinal rupture with special consideration of anastomotic strength. Arch Surg 1966;93:309–14.

    PubMed  CAS  Google Scholar 

  17. Hjortrup A, Nordkild P, Kiaergaard J, SjØntoft E, Olesen HP. Fibrin adhesive versus sutured anastomosis: a comparative intra-individual study in the small intestine of pigs. Br J Surg 1986;73:760–1.

    PubMed  CAS  Google Scholar 

  18. Yale CE, van Gemert JV. Healing of inverted and everted intestinal anastomoses in germfree rats. Surgery 1971;69:382–8.

    PubMed  CAS  Google Scholar 

  19. Jiborn H, Ahonen J, Zederfeldt B. Healing of experimental colonic anastomoses. I. Bursting strength of the colon after left colon resection and anastomosis. Am J Surg 1978;136:587–94.

    PubMed  CAS  Google Scholar 

  20. Cronin K, Jackson DS, Dunphy JE. Changing bursting strength and collagen content of the healing colon. Surg Gynecol Obstet 1968;126:747–53.

    PubMed  CAS  Google Scholar 

  21. Irvin TT, Hunt TK. Effect of malnutrition on colonic healing. Ann Surg 1974;180:765–72.

    PubMed  CAS  Google Scholar 

  22. Minion DM, MacPherson BR, Kilam SK. Temporary ischemia and healing of colonic anastomoses. IRCS Med Sci 1982;10:498–9.

    Google Scholar 

  23. de Roy van Zuidewijn DBW, Hendriks T, Wobbes T, Klompmakers AA, de Boer HHM. Healing of experimental colonic anastomoses: effect of antineoplastic agents. Eur J Surg Oncol 1987;13:27–33.

    PubMed  Google Scholar 

  24. Wise L, McAlister W, Stein T, Schuck P. Studies on the healing of anastomoses of small and large intestines. Surg Gynecol Obstet 1975;141:190–4.

    PubMed  CAS  Google Scholar 

  25. Penninckx FM, Kerremans RP, Geboes KJ. The healing of single- and double-row stapled circular anastomoses. Dis Colon Rectum 1984;27:714–9.

    PubMed  CAS  Google Scholar 

  26. Hesp FL, Hendriks T, Lubbers EJ, deBoer HHM. Wound healing in the intestinal wall: a comparison between experimental ileal and colonic anastomoses. Dis Colon Rectum 1984;27:99–104.

    PubMed  CAS  Google Scholar 

  27. Hamilton JE. Reappraisal of open intestinal anastomoses. Ann Surg 1967;165:917–24.

    PubMed  CAS  Google Scholar 

  28. Colin JF, Elliot P, Ellis H. The effect of uraemia upon wound healing: an experimental study. Br J Surg 1979;66:793–7.

    PubMed  CAS  Google Scholar 

  29. de Roy van Zuidewijn DB, Wobbes T, Hendriks T, Klompmakers AA, de Boer HHM. The effect of antineoplastic agents on the healing of small intestinal anastomoses in the rat. Cancer 1986;58:62–6.

    PubMed  Google Scholar 

  30. Brennan SS, Foster ME, Morgan A, Leaper DJ. Prostaglandins in colonic anastomotic healing. Dis Colon Rectum 1984;27:723–5.

    PubMed  CAS  Google Scholar 

  31. Foster ME, Johnson CD, Billings PJ, Davies PW, Leaper DJ. Intraoperative antegrade lavage and anastomotic healing in acute colonic obstruction. Dis Colon Rectum 1986;29:255–9.

    PubMed  CAS  Google Scholar 

  32. Haukipuro KA, Hulkko OA, Alavaikko MJ, Laitinen ST. Sutureless colon anastomosis with fibrin glue in the rat. Dis Colon Rectum 1988;31:601–4.

    PubMed  CAS  Google Scholar 

  33. Puig LaCalle J, Greoles JM, Canal Pey G, Perez Garcia G. Rotated intestinal anastomoses. Surg Gynecol Obstet 1982;154:662–6.

    Google Scholar 

  34. Ferulano GP, Danzi M, Abate S, Fresini A, Vanni L, Califano G. Effects of CO2 laser on the healing of experimental colon anastomoses. Eur Surg Res 1984;16:127–30.

    PubMed  CAS  Google Scholar 

  35. Asencio-Arana F, Martinez-Soriano F. Stimulation of the healing of experimental colon anastomoses by low-power lasers. Br J Surg 1988;75:125–7.

    PubMed  CAS  Google Scholar 

  36. van Doorn K, de Man B, Hendriks T. The effects of lathyrogens on intestinal anastomoses in the rat. Exp Mol Pathol 1990;52:37–45.

    PubMed  Google Scholar 

  37. Hesp FL, Hendriks T, Lubbers EJ, de Boer HHM. Wound healing in the intestinal wall: effects of infection on experimental ileal and colonic anastomoses. Dis Colon Rectum 1984;27:462–7.

    PubMed  CAS  Google Scholar 

  38. Trueblood HW, Nelsen TS, Kohatsu S, Oberhelman HA. Wound healing in the colon: comparison of inverted and everted closures. Surgery 1969;65:919–30.

    PubMed  CAS  Google Scholar 

  39. Irvin TT, Hunt TK. The effect of trauma on colonic healing. Br J Surg 1974;61:430–6.

    PubMed  CAS  Google Scholar 

  40. Charoenkul V, McElhinney J, Hodgson JB. Acidification of rat colon with lactulose: its effects on the healing of colonic anastomoses. Arch Surg 1978;113:618–20.

    PubMed  CAS  Google Scholar 

  41. Rolandelli RH, Koruda MJ, Settle RG, Rombeau JL. The effect of enteral feedings supplemented with pectin on the healing of colonic anastomoses in the rat. Surgery 1986;99:703–7.

    PubMed  CAS  Google Scholar 

  42. Rolandelli RH, Koruda MJ, Settle RG, Rombeau JL. Effects of intraluminal infusion of short-chain fatty acids on the healing of colonic anastomoses in the rat. Surgery 1986;100:198–203.

    PubMed  CAS  Google Scholar 

  43. Jiborn H, Ahonen J, Zederfeldt B. Healing of experimental colonic anastomoses. II. Breaking strength of the colon after left colon resection and anastomosis. Am J Surg 1978;136:595–9.

    PubMed  CAS  Google Scholar 

  44. Hillan K, Nordlinger B, Ballet F, Puts JP, Infante R. The healing of colonic anastomoses after early intraperitoneal chemotherapy: an experimental study in rats. J Surg Res 1988;44:166–71.

    PubMed  CAS  Google Scholar 

  45. Blomquist P, Jiborn H, Zederfeldt B. The effect of relative bowel rest on healing of colonic anastomoses: breaking strength and collagen in the colonic wall following left colon resection and anastomosis in the rat. Acta Chir Scand 1984;150:671–5.

    PubMed  CAS  Google Scholar 

  46. Udén P, Blomquist P, Jiborn H, Zederfeldt B. Influence of proximal colostomy on the healing of a left colon anastomosis: an experimental study in the rat. Br J Surg 1988;75:325–9.

    PubMed  Google Scholar 

  47. Jönsson K, Jiborn H, Zederfeldt B. Breaking strength of small intestinal anastomoses. Am J Surg 1983;145:800–3.

    PubMed  Google Scholar 

  48. Arbogast R, Gay B, Höcht B. Der Einfluss des Nahtmaterials auf die mechanische Belastbarkeit von Darmanastomosen. Chirurg 1978;49:640–4.

    PubMed  CAS  Google Scholar 

  49. Blomquist P, Jiborn H, Zederfeldt B. Effect of diverting colostomy on breaking strength of anastomoses after resection of the left side of the colon: studies in the rat. Am J Surg 1985;149:712–15.

    PubMed  CAS  Google Scholar 

  50. Wilker D, Sklarek J, Waldner H, Izbicki JR, Siebeck M. Breaking strength of sutureless anastomoses under normal conditions, peritonitis and ischemia in rats. Langenbecks Arch Chir 1988;373:217–21.

    PubMed  CAS  Google Scholar 

  51. Högström H, Haglund U, Zederfeldt B. Suture technique and early breaking strength of intestinal anastomoses and laparatomy wounds. Acta Chir Scand 1985;151:441–3.

    PubMed  Google Scholar 

  52. Jönsson K, Jiborn H, Zederfeldt B. Mechanical and biochemical alterations in the intestinal wall adjacent to an anastomosis. Am J Surg 1986;151:387–90.

    PubMed  Google Scholar 

  53. Rosin RD, Exarchakos G, Gilmore OJA, Ellis H. Topical noxythiolin in colonic healing. Br J Surg 1978;65:603–6.

    PubMed  CAS  Google Scholar 

  54. Young HL, Wheeler MH. Collagenase inhibition in the healing colon. J Roy Soc Med 1983;76:32–6.

    CAS  PubMed  Google Scholar 

  55. Smith SR, Connolly JC, Crane PW, Gilmore OJ. The effect of surgical drainage materials on colonic healing. Br J Surg 1982;69:153–5.

    PubMed  CAS  Google Scholar 

  56. Bark S, Rettura G, Goldman D, Seifter E, Levenson SM, Demetriou AA. Effect of supplemental vitamin A on the healing of colon anastomosis. J Surg Res 1984;36:470–4.

    PubMed  CAS  Google Scholar 

  57. Clark RA. Potential roles of fibronectin in cutaneous wound repair. Arch Dermatol 1988;124:201–6.

    PubMed  CAS  Google Scholar 

  58. Alexander SA, Donoff RB. The glycosaminoglycans of open wounds. J Surg Res 1980;29:422–9.

    PubMed  CAS  Google Scholar 

  59. Weigel PH, Fuller GM, LeBoeuf RD. A model for the role of hyaluronic acid and fibrin in the early events during the inflammatory response and wound healing. J Theor Biol 1986;119:219–34.

    PubMed  CAS  Google Scholar 

  60. Halstead WS. Circular suture of the intestine—an experimental study. Am J Med Sci 1887;94:436–61.

    Article  Google Scholar 

  61. Lord MG, Valies P, Broughton AC. A morphologic study of the submucosa of the large intestine. Surg Gynecol Obstet 1977;145:55–60.

    PubMed  CAS  Google Scholar 

  62. Thomson HJ, Busuttil A, Eastwood MA, Smith AN, Elton RA. The submucosa of the human colon. J Ultrastruct Mol Struct Res 1986;96:22–30.

    PubMed  CAS  Google Scholar 

  63. Gabella G. The cross-ply arrangement of collagen fibres in the submucosa of the mammalian small intestine. Cell Tissue Res 1987;248:491–7.

    PubMed  CAS  Google Scholar 

  64. Komuro T. The lattice arrangement of the collagen fibres in the submucosa of the rat small intestine: scanning electron microscopy. Cell Tissue Res 1988;251:117–21.

    PubMed  CAS  Google Scholar 

  65. Miller EJ, Gay S. Collagen: an overview. In: Cunningham LW, Frederiksen DW. Methods in enzymology: structural and contractile proteins. New York: Academic Press, 1982;82:3–32.

    Google Scholar 

  66. Gay S, Viljanto J, Raekallio J, Penttinen R. Collagen types in early phases of wound healing in children. Acta Chir Scand 1978;144:205–11.

    PubMed  CAS  Google Scholar 

  67. Irvin TT, Hunt TK. Reappraisal of the healing process of anastomosis of the colon. Surg Gynecol Obstet 1974;138:741–6.

    PubMed  CAS  Google Scholar 

  68. Jiborn H, Ahonen J, Zederfeldt B. Healing of colonic anastomoses: the effect of suture technique on collagen concentration in the colonic wall. Am J Surg 1978;135:333–40.

    PubMed  CAS  Google Scholar 

  69. Hawley PR, Page Faulk W, Hunt TK, Dunphy JE. Collagenase activity in the gastro-intestinal tract. Br J Surg 1970;57:896–900.

    PubMed  CAS  Google Scholar 

  70. Hendriks T, Vereecken TH, Hesp WL, Schillings PH, de Boer HH. Loss of collagen from experimental intestinal anastomoses: early events. Exp Mol Pathol 1985;42:411–18.

    PubMed  CAS  Google Scholar 

  71. Moss G, Greenstein A, Levy S, Bierenbaum A. Maintenance of GI function after bowel surgery and immediate enteral full nutrition. I. Doubling of canine colorectal anastomotic bursting pressure and intestinal wound mature collagen content. J Parenteral Nutr 1980;4:535–8.

    Article  CAS  Google Scholar 

  72. Jönsson K, Jiborn H, Zederfeldt B. Comparison of healing in the left colon and ileum: changes in collagen content and collagen synthesis in the intestinal wall after ileal and colonic anastomoses in the rat. Acta Chir Scand 1985;151:537–41.

    PubMed  Google Scholar 

  73. Hunt TK, Hawley PR, Hale J, Goodson W, Thakral KK. Colon repair: the collagenous equilibrium. In: Hunt TK. Wound healing and wound infection: theory and surgical practice. New York: Appleton-Century-Crofts, 1980:153–9.

    Google Scholar 

  74. Ravo B. Colorectal anastomotic healing and intracolonic bypass procedure. Surg Clin North Am 1988;68:1267–94.

    PubMed  CAS  Google Scholar 

  75. Foster ME, Laycock JR, Silver IA, Leaper DJ. Hypovolaemia and healing in colonic anastomoses. Br J Surg 1985;72:831–4.

    PubMed  CAS  Google Scholar 

  76. Winsey K, Simon RJ, Levenson SM, Seifter E, Demetriou AA. Effect of supplemental vitamin A on colon anastomotic healing in rats given preoperative irradiation. Am J Surg 1987;153:153–6.

    PubMed  CAS  Google Scholar 

  77. Mastboom WJ, Hendriks T, de Boer HH. Collagen changes around intestinal anastomoses in germ-free rats. Br J Surg 1989;76:797–801.

    PubMed  CAS  Google Scholar 

  78. Irvin TT. The effect of methionine on colonic wound healing in malnourished rats. Br J Surg 1976;63:237–10.

    PubMed  CAS  Google Scholar 

  79. Jönsson K, Jiborn H, Zederfeldt B. Changes in collagen content of the small intestinal wall after anastomosis. Am J Surg 1985;150:315–17.

    PubMed  Google Scholar 

  80. Cronin K, Jackson DS, Dunphy JE. Specific activity of hydroxyproline-tritium in the healing colon. Surg Gynecol Obstet 1968;126:1061–5.

    PubMed  CAS  Google Scholar 

  81. Jiborn H, Ahonen J, Zederfeldt B. Healing of experimental colonic anastomoses. III. Collagen metabolism in the colon after left colon resection. Am J Surg 1980;139:398–405.

    PubMed  CAS  Google Scholar 

  82. Jiborn H, Ahonen J, Zederfeldt B. Healing of experimental colonic anastomoses. IV. Effect of suture technique on collagen metabolism in the colonic wall. Am J Surg 1980;139:406–413.

    PubMed  CAS  Google Scholar 

  83. Jönsson K, Jiborn H, Zederfeldt B. Collagen metabolism in small intestinal anastomoses. Am J Surg 1987;154:288–91.

    PubMed  Google Scholar 

  84. Martens MF, Hendriks T. Collagen synthesis in explants from rat intestine. Biochim Biophys Acta 1989;993:252–8.

    PubMed  CAS  Google Scholar 

  85. Martens MF, Hendriks T. Collagen synthesis in explants from rat intestinal anastomoses (in press).

  86. Chowcat NL, Savage FJ, Hembry RM, Boulos PB. Role of collagenase in colonic anastomoses: a reappraisal. Br J Surg 1988;75:330–4.

    PubMed  CAS  Google Scholar 

  87. Van der Stappen JW, Hendriks Th, de Boer HH. Collagenolytic activity extracted from intestinal anastomoses of the rat. Matrix 1989;9:238–43.

    PubMed  Google Scholar 

  88. Laurent GJ. Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am J Physiol 1987;252:C1-C9.

    PubMed  CAS  Google Scholar 

  89. Eyre DR, Paz MA, Gallop PM. Cross-linking in collagen and elastin. Ann Rev Biochem 1984;53:717–48.

    PubMed  CAS  Google Scholar 

  90. Lehto M, Sims TJ, Bailey AJ. Skeletal muscle injury—molecular changes in the collagen during healing. Res Exp Med 1985;185:95–106.

    CAS  Google Scholar 

  91. Hendriks T, Hesp WL, Klompmakers AA, Lubbers EJ, de Boer HH. Solubility of tissue hydroxyproline in experimental intestinal anastomoses. Exp Mol Pathol 1985;43:253–9.

    PubMed  CAS  Google Scholar 

  92. Lapiere CM, Nusgens B, Pierard GE. Interaction between collagen type I and type III in conditioning bundles organization. Connect Tissue Res 1977;5:21–9.

    PubMed  CAS  Google Scholar 

  93. Parry DAD. The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys Chem 1988;29:195–209.

    PubMed  CAS  Google Scholar 

  94. Svoboda ELA, Howley TP, Deporter DA. Collagen fibril diameter and its relation to collagen turnover in three soft connective tissues in the rat. Connect Tissue Res 1983;12:43–8.

    PubMed  CAS  Google Scholar 

  95. Hering TM, Marchant RE, Anderson JM. Type V collagen during granulation tissue development. Exp Mol Pathol 1983;39:219–29.

    PubMed  CAS  Google Scholar 

  96. Epstein EH, Munderloh NH. Isolation and characterization of CNBr peptides of human [α1(III)]3 collagen and tissue distibution of [α1(I)]2α2 and [α1III)3 collagens. J Biol Chem 1975;250:9304–12.

    PubMed  CAS  Google Scholar 

  97. Graham MF, Diegelmann RF, Elson CO, et al. Collagen content and types in the intestinal strictures of Crohn's disease. Gastroenterology 1988;94:257–65.

    PubMed  CAS  Google Scholar 

  98. Udén P, Blomquist P, Jiborn H, Zederfeldt B. Influence of long-term relative bowel rest on the healing of a left colon anastomosis. Dis Colon Rectum 1988;31:886–891.

    PubMed  Google Scholar 

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Hendriks, T., Mastboom, W.J.B. Healing of experimental intestinal anastomoses. Dis Colon Rectum 33, 891–901 (1990). https://doi.org/10.1007/BF02051930

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