Healing Of Intestinal Moses

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Vol. 22, No. 4 April 2000

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Refereed Peer Review

FOCAL POINT ★Primary intestinal healing occurs by direct bridging of the cut intestinal layers with fibrous connective tissue when good apposition of wound margins is achieved.

KEY FACTS ■ The submucosa has a high collagen content and is responsible for anchoring intestinal sutures. ■ The greater omentum plays a vital role in healing intestinal wounds. ■ Growth factors are important in regulating fibroplasia and angiogenesis in healing intestinal wounds. ■ Intestinal wounds heal best with sutures that are placed relatively close together under moderate tension. ■ The risk for anastomotic leakage is significantly increased in the presence of peritonitis.

Healing of Intestinal Anastomoses * University of Illinois

Bradley R. Coolman, DVM, MS Nicole Ehrhart, VMD, MS Sandra Manfra Marretta, DVM ABSTRACT: Intestinal wounds heal in three overlapping phases that are similar to the healing pattern of other tissue. The lag phase begins immediately and is characterized primarily by local inflammation that lasts approximately 4 days. The proliferative phase, or period of fibroplasia, begins around day 3 and lasts until day 14 after the wound was incurred. Intestinal wound strength approaches that of normal bowel by the end of the proliferative phase. The maturation phase occurs from days 10 to 180 after the wound was incurred and is associated with collagen cross-linking and a slow gain in strength.

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ntestinal wounds may heal directly across the defect if intestinal layers are in close contact with each other (primary healing) or by indirectly bridging the defect with increased amounts of collagen and neovascularization if intestinal layers are inverting, everting, or overlapping (secondary healing). Secondary healing of intestinal anastomoses is most common with all types of suture patterns. Many factors influence intestinal healing. Factors controlled by veterinary surgeons include blood supply, tissue handling, suture material, and anastomotic technique. Patient factors that influence intestinal healing include age, nutritional status, and presence of infection.

ANATOMY The basic microscopic anatomy of the canine alimentary tract is similar from the stomach to the large intestine.1,2 The intestinal wall consists of four layers: the tunica mucosa, tela submucosa, tunica muscularis, and tunica serosa1,2 (Figure 1). The mucosa consists of epithelial lining, supportive lamina propria composed of loose reticular fibers, and muscularis mucosa (thin layer of smooth muscle).1,2 The epithelial surface is covered with innumerable villi that increase the absorptive surface area of the gut. The thickness of the epithelium and the nature of villi vary from region to region in the canine gastrointestinal (GI) tract. The lamina propria is composed of loose connective tissue meshed in a reticular fiber framework. Within the lamina propria are blood and lymph vessels, fibrocytes, smooth muscle cells, leukocytes, plasma cells, and mast cells. The muscularis mucosa is composed of thin inner circular and outer longitudinal layers of smooth muscle, *A companion article entitled “Historical Perspective of Intestinal Anastomosis in Veterinary Surgery” appeared in the March 2000 (Vol. 22, No. 3) issue of Compendium.

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which allow the mucosa to roll same as that of other tissue.4–9 1,2 into folds. However, intestinal wounds The submucosa connecting regain strength more rapidly the mucous membrane to the than do cutaneous wounds.4,5 tunica muscularis consists The healing process can be mainly of coarse, loosely woloosely divided into three overven, collagenous and elastic lapping phases: lag, proliferafibers with a submucosal plexus tive, and maturation.4–9 of nerves, blood vessels, and lymThe lag phase of healing, phatics.1,2 Because of its high which begins immediately after content of connective tissue, the wound is incurred and lasts the submucosa provides most for about 4 days,4–9 is characof the strength for the GI tract terized by immediate vascular and is used for anchoring suconstriction, fibrin clot formatures during intestinal surgery.3 tion, inflammation, and epBiochemical analysis shows Figure 1—Photomicrograph of the histologic layers of the ithelial migration. This phase that the submucosa contains canine small intestine. (Trichrome Masson stain; original is the most critical period for 68% type I collagen, 20% type magnification, ×10) intestinal wound healing beIII collagen, and 12% type V cause the anastomotic sutures collagen.4 provide nearly all wound The tunica muscularis constrength during this period. sists of a relatively thick inner Most intestinal dehiscence ocMucosa circular layer and a thinner outcurs during the lag phase.4–6,10,11 Submucosa er longitudinal layer of smooth Increased inflammation proMuscularis circular muscle.1,2 The inner circular longs this phase and delays inMuscularis longitudinal layer serves to segment and Serosa testinal wound healing. mix ingesta, whereas the outer The proliferative (or reparalongitudinal layer primarily tive) phase of healing begins functions to propel ingesta on day 3 and lasts until day through the GI tract. 1 The 14.4–9 Logarithmic proliferaserosa consists of a thin layer tion of fibroblasts occurs in of connective tissue that covthis period, during which ers the muscular coat.1,2 A laylarge amounts of collagen are er of mesothelial cells that produced. Wound strength composes the peritoneum Figure 2—Primary healing of the intestinal wall as achieved increases rapidly; and by day covers the outer surface. The with direct apposition of the submucosal layers. (Adapted 14, the strength of wounded serous coat adheres closely to from Jansen A, Becker AE, Brummelkamp WH, et al: The intestine approaches that of the muscular coat; the com- importance of the apposition of the submucosal intestinal normal bowel.7,8 Studies have bined layers are often referred layers for primary wound healing of intestinal anastomosis. shown that the increased Surg Gynecol Obstet 152:51–58, 1981; with permission) to as the seromuscular layer.2 wound strength during the Blood supply to the intestiproliferative phase parallels nal wall comes from the arcuate mesenteric arteries that the rising collagen content of wounded tissue.7,8 Healing penetrate the tunica muscularis, branch off to create a wounds have a higher proportion of type III collagen subserosal plexus and intermuscular plexus, and then than normal tissue does.8 continue into the tela submucosa where they form the The maturation phase proceeds from days 10 to 180 submucosal plexus.1,2 The submucosal vascular plexus after the wound is incurred.4–9 This phase of wound provides the primary blood supply to the GI tract.2 Arhealing is less important from a clinical standpoint beterioles from the submucosal plexus supply the tunica cause bowel strength is already adequate to prevent mucosa and give rise to the capillary network in the inleakage or dehiscence. During the maturation phase, a testinal villi.1,2 slow increase in wound strength is observed as the collagen fibers reorganize, mature, and return to normal OVERVIEW OF INTESTINAL WOUND HEALING proportions.7,8 The basic healing pattern of intestinal wounds is the Jansen and colleagues12 performed experiments on small ROLE OF SUBMUCOSA ■ INTESTINAL BLOOD SUPPLY ■ HEALING PHASES

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intestine healing in dogs and infection.13–17 Thus many surreported that histologic wound geons recommend wrapping healing depended on the accuintestinal anastomoses with the racy of apposing the layers of omentum during surgery. The Mucosa Submucosa bowel wall. These researchers omentum must be viable to asMuscularis circular compared conventional dousist healing—free omental Muscularis longitudinal ble-layer, hand-sewn inverting grafts have been shown to be Serosa anastomoses with those created ineffective.5,16 Leakage rates of using a magnetized anastomotexperimental anastomoses are ic ring apparatus that inverted high in dogs when the omenand compressed the mucosa tum has been removed, espeand submucosa, resulting in dicially when everting suture patrect apposition of both submuterns are used.18,19 However, cosal layers and sloughing of protection from the omentum trapped mucosa. Direct bridgenables healing of severely ing of the defect and rapid compromised intestinal anastorestoration of epithelium was moses that would otherwise described when good apposi- Figure 3—The secondary intestinal healing that occurs leak.14,17 tion of submucosal, muscular, with everting intestinal anastomoses. (Adapted from Macrophages are important and serosal layers was achieved Jansen A, Becker AE, Brummelkamp WH, et al: The im- during wound debridement using the anastomotic ring ap- portance of the apposition of the submucosal intestinal in the lag phase of healing.4 paratus (Figure 2).12 This pat- layers for primary wound healing of intestinal anastomosis. They also produce humeral tern was described as primary Surg Gynecol Obstet 152:51–58, 1981; with permission) growth factors that modulate intestinal healing.12 fibroplasia and angiogenesis In cases of poor apposition in healing wounds. Important of intestinal layers (handgrowth factors produced by sewn everting, inverting, and macrophages include transoverlapping anastomoses), a forming growth factor-β (TGFdifferent pattern of healing β), platelet-derived growth facwas observed. The anastotor (PDGF), epidermal growth Mucosa moses bridged with increased factor (EGF), and many cySubmucosa amounts of collagen tissue, tokines.20,21 By producing these Muscularis circular the vascular pattern was irreghumeral factors, macrophages Muscularis longitudinal Serosa ular with increased neovascuplay an important role in conlarization from the submutrolling the metabolism of cosal plexus, and bridging of wounds. the epithelial defect in the The healing of experimental mucosal layer was prolonged wounds is reportedly facilitat(Figures 3 and 4). This type ed by TGF-β, PDGF, and of wound healing with indiEGF.20 Topical application of rect bridging of the anastoTGF-β accelerates intestinal motic defect was called secwound healing in pigs.4 Exondary intestinal healing. 12 perimental intestinal anastoThe researchers concluded moses created in rats with enthat direct apposition of sub- Figure 4—The secondary intestinal healing that occurs hanced macrophage function mucosal layers is required for with inverting intestinal anastomoses. (Adapted from had increased collagen crossprimary intestinal healing. Jansen A, Becker AE, Brummelkamp WH, et al: The im- linking and greater tensile The greater omentum is im- portance of the apposition of the submucosal intestinal strength at day 3 than did unportant in the healing of GI layers for primary wound healing of intestinal anastomosis. treated controls.20 However, in wounds.5,13 The omentum seals Surg Gynecol Obstet 152:51–58, 1981; with permission) this study, the wound concenthe anastomotic suture line, trations of TGF-β and PDGF provides an external vascular supply, establishes lymphatic were lower in rats with enhanced macrophage function drainage, gives rise to granulation tissue, and helps control than in controls.20 The researchers concluded that inINVERTING ANASTOMOSIS ■ DIRECT AND INDIRECT BRIDGING ■ GROWTH FACTORS

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testinal wound healing clearly depends on combinations of many growth factors and cytokines and that accelerated healing may depend on stimulation of certain factors and inhibition of others.

FACTORS AFFECTING INTESTINAL WOUND HEALING Increased inflammation in intestinal anastomoses prolongs the lag phase of healing and delays the return of strength at the suture line.22,23 Inflammation activates collagenases in the intestinal wall that, along with proteolytic enzymes from granulocytes, degrade existing collagen and weaken the foundations in which anastomotic sutures are placed.4,5,23 Numerous factors affect intestinal wound healing. Factors under the surgeon’s control are monitoring the blood supply, handling tissue gently, and choosing the appropriate suture material and anastomotic technique. Other factors that affect healing include age of the patient, its nutritional status, and presence of infection and concurrent diseases. Blood Supply Delivery of adequate blood supply and tissue oxygen is essential for healing intestinal anastomoses.4 Because hydroxylation of lysine and proline during collagen synthesis depends on adequate oxygen delivery, inadequate blood supply delays collagen formation.4 Intrinsic vasculature must be preserved, and tissue of questionable viability or with marginal perfusion should be removed. Cutting the bowel edges at a 60˚ angle from the mesenteric border has been recommended to ensure adequate blood supply at the antimesenteric aspect.6 Hypovolemia and severe anemia can compromise oxygenation and should be corrected before surgery. However, mild normovolemic anemia does not impair oxygen transport and has no effect on intestinal wound healing.4 Surgical Technique Appropriate surgical technique dictates that surgeons handle tissue gently, use fine instruments, dissect tissue sharply, ensure adequate hemostasis, and avoid tissue necrosis. Tissue must remain moist, and spillage of intestinal contents must be avoided. Although experimental anastomoses in healthy dogs heal with widely spaced sutures (up to 16 mm apart),24 improved healing patterns are achieved by placing sutures relatively close (2 to 4 mm) under moderate tension.25 Knots should be tied securely but should not strangulate or cut into tissue. Careful tissue handling and meticulous surgical technique minimize damage to critical blood vessels as well as tissue edema and necrosis.23 In addition, mobilizing bowel ends adequately is important to prevent

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tension on the anastomosis—tension can decrease perfusion and predispose wound dehiscence.26

Suture Material There is no ideal suture material for intestinal anastomosis. Both absorbable and nonabsorbable sutures of synthetic and natural origins have been successfully used.4,5,23 The suture should be strong enough to provide mechanical support but fine enough to minimize tissue trauma and inflammatory response to a foreign body. Because the intestine rapidly regains strength, suture materials only need to retain holding strength for a maximum of 10 to 14 days after anastomosis.23 Suture material is a foreign body and thus can produce an inflammatory response.23 Chromic gut causes an increased inflammatory response, is rapidly degraded by phagocytosis, and is therefore not recommended for intestinal anastomosis.4,5 Multifilament sutures have increased tissue drag that can increase tissue damage and inflammation caused by friction during placement.23 In addition, multifilament materials produce a scaffold in which microorganisms can proliferate and thus should be avoided in the bowel.4,5 Synthetic absorbable monofilament (i.e., polydioxanone, polyglyconate) and synthetic nonabsorbable monofilament (i.e., nylon, polypropylene, stainless-steel) sutures are associated with the least amount of inflammation and are thus best suited for anastomosis.4,5,23 Because of the rapid return to normal strength, nonabsorbable sutures have no advantage over slowly absorbable synthetic suture material. Suture sizes of 3-0 to 5-0 are recommended for closing GI wounds in small animals.5,6 Suture Pattern The suture pattern significantly affects the amount of inflammation and anastomotic healing. Inverting suture patterns are the most widely used patterns in human intestinal surgery.4 Inverting patterns form an immediate serosal seal and are associated with fewer adhesions than may occur with everting patterns.7,23 However, the inverted cuff of tissue typically loses its blood supply, becomes edematous, and eventually undergoes necrosis. The larger the inverted cuff of tissue, the more severe the inflammatory reaction and the greater the risk for luminal obstruction.7 Secondary healing patterns are typically observed with inverting anastomotic techniques.12 Everting suture patterns cause less initial narrowing of the intestinal lumen than do inverting techniques. However, everting patterns are associated with increased adhesion formation and greater incidence of anastomotic leakage.7,23 Many published studies have compared inverting and everting anastomoses through-

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out the GI tract.27–37 It is clear that with everting anastomoses, the role of the omentum and other peritoneal defense mechanisms is increased because of the need to seal the anastomosis and assist in healing.17–19 Although everting patterns do not initially impinge on intestinal lumen, stenosis of the anastomosis may result from extraluminal adhesions and increased fibroplasia.4,5 Ideally, approximating anastomotic patterns for end– to-end anastomoses would cause no luminal obstruction, have minimal adhesions, and result in primary intestinal healing. However, mucosal–mucosal apposition results in eversion of extramucosal intestinal layers.37 Published studies document that approximating anastomotic techniques generally result in eversion of the mucosa, extensive adhesions, and secondary patterns of healing in the intestine.38–40 Simple continuous patterns for intestinal anastomosis are associated with better gross and histologic apposition of intestinal layers and have similar clinical results compared with simple interrupted patterns.39,41

Single- Versus Double-Layer Anastomoses Although Lembert, Halsted, and Connell all recommended one-layer anastomoses, two-layer closures of intestine became more common after Czerny modified the Lembert technique.23 Double-row inverting techniques became popular because they were believed to provide more security against leakage.23 However, twolayer anastomoses have been shown to cause more tissue strangulation and edema, greater inflammatory response, greater loss of collagen content, delayed healing, and higher rates of bowel obstruction than do single-layer closures.4,23,42 Thus single-layer anastomotic closures are preferred for most applications.4,5,43 Stapled Anastomoses Mechanical stapling devices can also be used to create inverting or everting end–end, end–side, or side–side intestinal anastomoses.37,44–54 Reported advantages of stapled anastomoses over hand-sewn techniques include decreased tissue manipulation, shorter surgical time, preservation of vascular supply, and superior initial strength. 37,44–53 Mechanical stapling devices have been successfully used for small and large intestinal anastomoses in dogs and cats.51–54 Experiments have shown that stapled anastomoses heal with minimal inflammatory response and have greater initial wound strength than do sutured anastomoses.37,44,45,48,49 However, published studies reporting less inflammation with stapled intestinal anastomoses compared stainless-steel staples with chromic gut, which is known to cause an intense inflammatory response.44,48,51 One study found that hand-sewn intestinal anastomoses

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had greater strength, increased lumen diameter, and more rapid healing than did stapled anastomoses.50 Early reports concluded that stapled everting GI anastomoses generally healed by primary intention in contrast to hand-sewn inverting anastomoses, which often healed by secondary intention and had a marked inflammatory response.18,37,44,48 This nomenclature is confusing because the primary-intention healing described in these reports is not the same process as the primary intestinal healing described by Jansen and colleagues.12 All stapled intestinal anastomoses result in either eversion or inversion of intestinal wall, depending on the technique and instrument used.53 Therefore, healing of stapled anastomoses will proceed by indirect bridging by collagen fibers, or secondary intestinal healing.12

Sutureless Intestinal Anastomoses A biofragmentable anastomotic ring (BAR) for intestinal anastomoses was first described by Hardy and coworkers.55 This intraluminal device is made from absorbable polyglycolic acid and barium sulfate to render it radiopaque.55–59 The BAR creates an inverting anastomosis in which the cut intestinal ends are compressed by the device and eventually undergo necrosis, which results in fragmentation of the device and passing with feces.55–59 The immediate anastomotic strength of the BAR is higher than that of sutured or stapled intestinal anastomoses, and the bursting strength during the lag and proliferative phases of healing is similar.56–58 Healing is equivalent to hand-sewn and stapled inverting anastomoses (secondary intestinal healing), but less microscopic inflammation and foreign body reaction occur during the maturation phase of healing because the implants fragment and pass within 12 to 23 days.56 The BAR is histologically associated with increased muscular inversion and fewer adhesions than occur with appositional sutured anastomoses.59 The lumen diameter of the healed BAR anastomosis is similar to that of other anastomotic techniques.55,59 Age The incidence of anastomotic complications in humans increases with advancing age.4 Although this association may be secondary to concurrent diseases more common in older patients, research has shown that advanced age alone does not suppress the tensile strength, bursting strength, or collagen content of intestinal anastomoses.60 Retrospective studies of GI wound dehiscence in dogs found no association between age and dehiscence rate.10,61 Nutritional Status Both prolonged and short-term malnutrition diminish

APPROXIMATING PATTERNS ■ MECHANICAL STAPLING ■ BIOFRAGMENTABLE ANASTOMOTIC RING

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anastomotic healing.4 The reason for decreased GI healing in malnourished patients probably results from hypoproteinemia, lack of amino acids needed for collagen synthesis, and decreased immunocompetence associated with malnutrition.4 Early enteral nutrition should be provided to GI surgical patients when possible because it helps prevent ileus and sustains the intestinal barrier, thereby helping prevent bacterial translocation.4,5 Total parenteral nutrition should be considered in patients with severe malnutrition and when nutrient requirements cannot be met by enteral feeding for prolonged periods.62

Infection Peritonitis and local infection lead to a higher rate of anastomotic dehiscence by increasing inflammation and promoting collagenase activity.7,22,63,64 In one study,63 experimental infection resulted in lowered bursting pressures and collagen content for ileal anastomoses. Dogs with peritonitis have a significantly higher rate of GI wound dehiscence.10 The risk for anastomotic leakage is reportedly increased by a factor of 20 for small intestinal anastomoses in the presence of peritonitis.64 Humans with peritonitis requiring intestinal surgery generally have a temporary enterostomy until the infection is controlled.4,22 However, primary healing of GI anastomoses in the presence of generalized peritonitis has been documented.64 SUMMARY To optimize GI wound healing, surgeons should use atraumatic technique and attempt to accurately align the transected layers of bowel wall. Single-layer, approximating, or mildly inverting anastomoses completed with 3-0 to 5-0 synthetic monofilament sutures in simple interrupted or simple continuous fashion are preferred. Sutures should be inserted 2 to 4 mm from the wound edge, through the submucosal layer of bowel wall, spaced at 2to 4-mm intervals, and placed under moderate tension for optimal anastomotic healing. Anastomoses created with automated stapling devices also have good clinical results in small animals. Advanced age, poor nutrition, and infection may all increase the risk for intestinal wound dehiscence. REFERENCES 1. Dellman HD: Textbook of Veterinary Histology, ed 4. Philadelphia, Lea & Febiger, 1993, pp 177–182. 2. Evans HE, Christensen GC: Miller’s Anatomy of the Dog, ed 2. Philadelphia, WB Saunders Co, 1979, pp 482–483. 3. Halsted WS: Circular suture of the intestine—An experimental study. Am J Med Sci 94:436–461, 1887. 4. Thornton FJ, Barbul A: Healing in the gastrointestinal tract. Surg Clin North Am 77:549–573, 1997. 5. Ellison GW: Wound healing in the gastrointestinal tract. Semin Vet Med Surg (Small Anim) 4:287–293, 1989. 6. Richardson DC: Intestinal surgery: A review. Compend Con-

tin Educ Pract Vet 3(3):259–270, 1981. 7. Kodura MJ, Rolandelli RH: Experimental studies on the healing of colonic anastomoses. J Surg Res 48:504–515, 1990. 8. Hendriks T, Mastboom WJB: Healing of experimental intestinal anastomoses: Parameters for repair. Dis Colon Rectum 33:891–901, 1990. 9. Pascoe JR, Peterson PR: Intestinal healing and methods of anastomosis. Vet Clin North Am Equine Pract 5:309–333, 1989. 10. Allen DA, Smeak DD, Schertel ER: Prevalence of small intestinal dehiscence and associated clinical factors: A retrospective study of 121 dogs. JAAHA 28:70–76, 1992. 11. Irvin TT, Goligher JC: Aetiology of disruption of intestinal anastomoses. Br J Surg 60:461–464, 1973. 12. Jansen A, Becker AE, Brummelkamp WH, et al: The importance of the apposition of the submucosal intestinal layers for primary wound healing of intestinal anastomosis. Surg Gynecol Obstet 152:51–58, 1981. 13. Hosgood G: The omentum—Forgotten organ: Physiology and potential surgical applications in dogs and cats. Compend Contin Educ Pract Vet 12(1):45–50, 1990. 14. Adams W, Ctercteko G, Bilous M: Effect of omental wrap on the healing and vascularity of compromised intestinal anastomoses. Dis Colon Rectum 35:731–738, 1992. 15. McLachlin AD, Denton DW: Omental protection of intestinal anastomoses. Am J Surg 125:134–140, 1973. 16. Carter DC, Jenkins DHR, Whitfield HN: Omental reinforcement of intestinal anastomoses: An experimental study in the rabbit. Br J Surg 59:129–133, 1972. 17. Denton DW: Omental protection of intestinal anastomoses. Rev Surg 26:447–448, 1972. 18. Ravitch MM: Some considerations on the healing of intestinal anastomoses. Surg Clin North Am 49:627–635, 1969. 19. Abramowitz HB, Butcher HR: Everting and inverting anastomoses: An experimental study of comparative safety. Am J Surg 121:52–56, 1971. 20. Compton R, Williams D, Browder W: The beneficial effect of enhanced macrophage function on the healing of bowel anastomoses. Am Surg 62:14–18, 1996. 21. Basson MD: Mucosal healing and adaptation in the small intestine. Curr Opin Gen Surg 1:138–46, 1994. 22. Ballantyne GH: Intestinal suturing: Review of the experimental foundations for traditional doctrines. Dis Colon Rectum 26:836–843, 1983. 23. Ballantyne GH: The experimental basis of intestinal suturing: Effects of surgical technique, inflammation, and infection on wound healing. Dis Colon Rectum 27:61–71, 1984. 24. Hardy KJ: Suture anastomosis: An experimental study using limited suturing of the small bowel in the dog. Arch Surg 97:586–589, 1968. 25. Waninger J, Kauffmann GW, Ifat AS, Farthmann EH: Influence of the distance between interrupted sutures and the tension of sutures on the healing of experimental colonic anastomoses. Am J Surg 163:319–323, 1992. 26. Shikata JI, Shida T: Effects of tension on local blood flow in experimental intestinal anastomoses. J Surg Res 40:105–111, 1986. 27. Mellish RWP: Inverting or everting sutures for bowel anastomoses. J Pediatr Surg 1:260–265, 1966. 28. Getzen LC, Roe RD, Holloway CK: Comparative study of intestinal anastomotic healing in inverted and everted closures. Surg Gynecol Obstet 123:1219–1227, 1966. 29. Ravitch MM, Canalis F, Weinshelbaum A, McCormick J: Studies on intestinal healing: III. Observations on everting intestinal anastomoses. Ann Surg 166:670–680, 1967. 30. Canalis F, Ravitch MM: Study of healing of inverting and everting intestinal anastomoses. Surg Gynecol Obstet 126:109– 114, 1968. 31. Ott BS, Doyle MD, Greenawald KA: Single layer everted in-

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testinal anastomosis. JAVMA 153:1742–1753, 1968. 32. Gill W, Fraser J, Carter DC, Hill R: Everted intestinal anastomosis. Surg Gynecol Obstet 128:1297–1303, 1969. 33. Rusca JA, Bornside GH, Cohn I: Everting versus inverting gastrointestinal anastomoses: Bacterial leakage and anastomotic disruption. Ann Surg 169:727–735, 1969. 34. Kho E, Replogle R, Ravitch MM: Studies of intestinal healing: IV. Prevention of adhesions following inverting and everting bowel anastomoses with promethazine and dexamethasone. Arch Surg 98:764–765, 1969. 35. Abramowitz HB, McAlister WH: A comparative study of small bowel anastomoses by angiography and microangiography. Surgery 66:564–569, 1969. 36. Kho E, Ravitch MM: Studies in intestinal healing: V. Bacterial population in intestinal anastomoses. Am J Surg 120: 32–34, 1970. 37. Ravitch MM: Observations on the healing of wounds of the intestines. Surgery 77:665–673, 1975. 38. DeHoff WD, Nelson W, Lumb WV: Simple interrupted approximating technique for intestinal anastomosis. JAAHA 9:483–489, 1973. 39. Ellison GW, Jokinen MP, Park RD: End-to-end approximating intestinal anastomosis in the dog: A comparative fluorescein dye, angiographic, and histopathologic evaluation. JAAHA 18:729–736, 1982. 40. Bone DL, Duckett KE, Patton CS, Krahwinkel DJ: Evaluation of anastomoses of small intestine in dogs: Crushing versus noncrushing suturing techniques. Am J Vet Res 44:2043– 2048, 1983. 41. Weisman DL, Smeak DD, Birchard SJ, et al: Comparison of a continuous suture pattern with simple interrupted pattern for enteric closure in dogs and cats: 83 cases (1991–1997). JAVMA 214:1507–1510, 1999. 42. Orr NWM: A single-layer intestinal anastomosis. Br J Surg 56:771–774, 1969. 43. Chittmittrapap S, Kitisisn P, Navicharern P: One layer continuous anastomosis of the alimentary tract with absorbable polydioxanone suture. J Med Assoc Thai 76:264–270, 1993. 44. Ravitch MM, Lane R, Cornell WP, et al: Closure of duodenal, gastric and intestinal stumps with wire staples: Experimental and clinical studies. Ann Surg 163:573–579, 1966. 45. Ravitch MM, Rivarola A: Enteroanastomosis with an automatic instrument. Surgery 59:270–277, 1966. 46. Ravitch MM, Steichen FM: Technics of staple suturing in the gastrointestinal tract. Ann Surg 175:815–837, 1972. 47. Ravitch MM, Ong TH, Gazzola L: A new, precise, and rapid technique of intestinal resection and anastomosis with staples. Surg Gynecol Obstet 139:6–10, 1974. 48. Ballantyne GH, Burke JB, Rogers G, et al: Accelerated wound healing with stapled enteric suture lines: An experimental study comparing traditional sewing techniques and a stapling device. Ann Surg 201:360–364, 1985. 49. Berman S, Hashizume M, Yang Y, et al: Intraoperative hemostasis and wound healing in intestinal anastomoses using the ILA stapling device. Am J Surg 155:520–525, 1988. 50. Dziki AJ, Duncan MD, Harmon JW, et al: Advantages of handsewn over stapled bowel anastomosis. Dis Colon Rectum 34:442–448, 1991.

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51. Hess JL, McCurnin DM, Riley MG, Koehler KJ: Pilot study for comparison of chromic catgut suture and mechanically applied staples in enteroanastomoses. JAAHA 17:409–414, 1981. 52. Ullman SL, Pavletic MM, Clark GN: Open intestinal anastomosis with surgical stapling equipment in 24 dogs and cats. Vet Surg 20:385–391, 1991. 53. Ullman SL: Surgical stapling of the small intestine. Vet Clin North Am Small Anim Pract 24:305–322, 1994. 54. Stoloff D, Snider TG, Crawford MP, et al: End-to-end colonic anastomosis: A comparison of techniques in normal dogs. Vet Surg 13:76–82, 1984. 55. Hardy TG, Pace WG, Maney JW, et al: A biofragmentable ring for sutureless bowel anastomosis. An experimental study. Dis Colon Rectum 28:484–490, 1985. 56. McCue JL, Phillips RKS: Sutureless intestinal anastomoses. Br J Surg 78:1291–1296, 1991. 57. Bundy CA, Jacobs DM, Zera RT, et al: Comparison of bursting pressure of sutured, stapled, and BAR anastomoses. Int J Colorect Dis 8:1–3, 1993. 58. Maney JW, Katz AR, Li LK, et al: Biofragmentable bowel anastomosis ring: Comparative efficacy study in dogs. Surgery 103:56–62, 1988. 59. Huss BT, Payne JT, Johnson GC, et al: Comparison of a biofragmentable anastomosis ring with appositional suturing for subtotal colectomy in cats. Vet Surg 23:466–474, 1994. 60. Stoop MJ, Dirksen R, Hendriks T: Advanced age alone does not suppress anastomotic healing in the intestine. Surgery 119:15–19, 1996. 61. Wyle KB, Hosgood G: Mortality and morbidity of small and large intestinal surgery in dogs and cats: 74 cases (1980– 1992). JAAHA 30:469–474, 1994. 62. Reuter JD, Marks SL, Quinton RR, Farver TB: Use of total parenteral nutrition in dogs: 209 cases (1988–1995). J Vet Emerg Crit Care 8:201–213, 1998. 63. Hesp FLEM, Hendriks T, Lubbers EJC, DeBoer HNM: Wound healing in the intestinal wall: Effects of infection on experimental ileal and colonic anastomoses. Dis Colon Rectum 27:462–467, 1984. 64. DeGraff JS, Goor HV, Bleichrodt RP: Primary small bowel anastomosis in generalized peritonitis. Eur J Surg 162:55– 58, 1996.

About the Authors When this article was submitted for publication, Dr. Coolman was chief surgical resident at the College of Veterinary Medicine, University of Illinois, Urbana, Illinois. He is currently affiliated with Veterinary Surgical Services, Fort Wayne, Indiana. Drs. Ehrhart and Manfra Marretta are affiliated with the Department of Veterinary Clinical Sciences, College of Veterinary Medicine, University of Illinois, Urbana, Illinois. Drs. Ehrhart and Manfra Maretta are Diplomates of the American College of Veterinary Surgeons, and Dr. Manfra Marretta is a Diplomate of the American Veterinary Dental College.