Historical Perspective Of Intestinal Anastomosis In Veterinary Surgery

V CE

Vol. 22, No. 3 March 2000

Refereed Peer Review

FOCAL POINT ★ Single-layer, approximating suture patterns are currently recommended for end-to-end intestinal anastomosis in small animal surgery.

KEY FACTS ■ The modern era of intestinal surgery began in the early 1800s. ■ The fundamental doctrines of intestinal anastomosis were established in human surgery by the beginning of the 20th century and are still practiced today. ■ In the 1950s, it was proven that serosal inversion is not necessary for the healing of intestinal wounds. ■ Approximating anastomosis techniques were first described in the 1960s and first appeared in the veterinary literature in the 1970s. ■ The human surgical literature generally classifies intestinal anastomoses as inverting or everting and largely ignores the concept of end-to-end approximation of cut intestinal layers.

Historical Perspective of Intestinal Anastomosis in Veterinary Surgery University of Illinois

Bradley R. Coolman, DVM, MS Nicole Ehrhart, VMD, MS Sandra Manfra Marretta, DVM ABSTRACT: Information on intestinal anastomosis in the veterinary surgical literature before the 1940s is scarce. To understand the current methods advocated for suturing intestinal wounds in animals, it is important to study the modern history of human intestinal surgery. Single-layer, approximating suture patterns are currently recommended for intestinal wound closure in veterinary surgery. Approximating suture patterns typically cause mucosal eversion and would be classified as everting patterns in the human literature.

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efore the 19th century, surgical treatment of intestinal wounds was rarely successful and elective surgical procedures involving the gastrointestinal (GI) tract were not attempted. Early in the first century AD, Celsus recorded attempts to suture the intestine but spoke disparagingly of its use.1 In 87 AD, Abulkasem recommended using the jaws of large ants to unite intestinal wounds.1 He also referred to catgut made from the intestines of sheep as suture material.1 The oldest reported intestinal suturing technique is the glover’s suture.1 Senn used a picture from a 1739 surgical textbook to illustrate the technique (Figure 1). The glover’s suture was a simple continuous stitch in which the ends, instead of being tied, were left long and pulled externally through the abdominal wound. The suture was intended to approximate the intestinal wound and was used to prevent leakage of intestinal contents and to keep the injured intestine in close contact with the external wound. If the patient survived, the suture was pulled from the wound in 5 to 9 days when the intestine was “healed.”1 Other ancient surgical methods involved the use of a few large-diameter sutures; use of bone, trachea, or wood stents; or attempts to invaginate the cut ends of intestine.1 Most surgeons advised bringing the visceral wound in close contact with the external wound and holding the intestine in position with one

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or two large sutures through the mesentery or the intestinal wall (Figure 2).1 The intent of these techniques was to use the peritoneum to seal the wound or to form an “artificial anus,” especially in complete transverse lacerations of the intestine. These methods stemmed from clinical observations of several patients who survived complete transverse “fatal” intestinal wounds that spontaneously adhered to the external wound and formed enterostomies.1 As late as 1818, prominent sur- Figure 1—Glover’s suture. (From Senn N: Enterorgeons commonly stated that su- rhaphy: Its history, technique, and present status. turing the intestine was very dan- JAMA 21:215–235, 1893) gerous.1 The mortality rate was higher for patients who had intestinal wounds sutured than for those whose intestinal wounds were left to heal naturally.

Dupuytren, his mentor.4,5 Nevertheless, in an 1893 review of intestinal surgery, Senn stated that Lembert’s technique and practices represented a sudden shift from ancient to modern methods and that Lembert’s principle of using the serous coat to procure early and permanent adhesions would never be rejected.1 Lister (1867) is credited with another important discovery in the advancement of intestinal surgery: asepsis.5 Lister advocated the use of aseptic suture material and the principles of antiseptic surgery. Although the concept of aseptic technique initially met with resistance and was slow to catch on, in 1893 Senn gave credit for the rapid success of intestinal surgery to Lister’s methods, which helped MODERN HISTORY reduce the incidence of septic Current principles of intestinal peritonitis and surgical wound surgery originated in the early infection.1 19th century. In 1812, Travers In 1883, Czerny modified first reported that the entire cirLembert’s technique into a twocumference of cut extremities of layer, inverting anastomosis, a divided intestine needed to be which became widely used in in contact to heal properly.2 Unthe 20th century. 6 In 1887, like his contemporaries, Travers Halsted reported the imporused a small, round sewing neetance of the submucosal layer in dle to place multiple full-thick- Figure 2—Large suture passed through the mesen- suturing GI wounds (Figure 3).7 tery and surrounding the intestine. (From Senn N: ness silk sutures at close intervals Enterorrhaphy: Its history, technique, and present He stated that a delicate thread to prevent leakage of ingesta and status. JAMA 21:215–235, 1893) of submucosa was considerably to increase the mechanical stronger and better able to hold strength of the anastomosis. He a stitch than was a coarse shred emphasized the importance of uniform apposition and of the entire thickness of the muscular and serous stated that the type of suture used was a secondary concoats.7 Halsted advocated a single-layer closure and em2 cern as long as the contact was secure. Travers knotted phasized the importance of surgical technique and the sutures, cut the threads short, and did not fasten asepsis for successful intestinal healing. In 1892, Conthe intestine to the abdominal wall. He reported sucnell introduced a single-layer, continuous inverting sucessful healing of intestinal anastomoses in dogs with ture pattern.8 The major advantages of Connell’s tech2 his mucosal appositional (everting) technique. nique were the speed of the operation and reduction of In 1826, Lembert reported that serosa-to-serosa conthe number of knots left in the wound.8 tact of the divided intestine, achieved by inverting suThat same year, Murphy described the use of an interture patterns, was necessary for intestinal healing.3 Lemlocking metallic button (Figure 4) designed to create a bert’s technique became a fundamental principle of sutureless, inverting, end-to-end intestinal anastomosis.9 intestinal surgery, and he became known as the founder After the ends of the intestine had healed sufficiently, of modern intestinal surgery.1 However, Lembert himthe inverted cuff of tissue would slough and the button self gave credit for the idea of serosal apposition to and necrotic tissue would pass with the feces. Murphy’s PRINCIPLES OF INTESTINAL SURGERY ■ ASEPSIS ■ TWO- VS. SINGLE-LAYER CLOSURE

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button was widely used by surgeons around the turn of the 20th century. In a 1923 review, Kerr detailed the development of intestinal surgery and identified the Murphy button as being one of the most brilliant contributions ever made to surgery.10 Kerr also claimed that this device advanced intestinal surgery more than did any other factor.10 Nevertheless, Murphy’s button was largely replaced by hand-sewn intestinal anastomosis techniques in human patients by the 1920s.10 By the beginning of the 20th century, about 250 methods for intestinal suturing had been described and the fundamental doctrines of intestinal anastomosis were firmly established. 10 These principles included: (1) apposing the serosal surfaces of the intestine around the full circumference using an inverting suture technique, (2) including the tough submucosa in the suture bites, (3) performing the anastomosis in an environment free of contamination and trauma, (4) using aseptic surgical technique, (5) maintaining adequate blood supply to tissue, and (6) avoiding tension on the anastomosis. 1,10 These basic tenets are still considered the cardinal principles of intestinal anastomosis in human surgery.11,12

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resort (i.e., when it was the only hope to save a patient’s life).14 The textbook described use of an inverting Lembert pattern to perform end-to-end small intestinal anastomosis and mentioned various mechanical devices, such as the Murphy button, that require no sutures. McCunn admitted that, in his experience with enterorrhaphy, the results were not good, although there had been some successes.14 The second edition of Canine Figure 3—Passage of the needle through the intestiSurgery (1949) described the Parnal wall into the submucosal coat. (From Halsted WS: Circular suture of the intestine—An experi- ker-Kerr technique (a closed, single-layer, inverting end-to-end mental study. Am J Med Sci 94:436–461, 1887) intestinal anastomosis) as such a theoretically perfect method that, when executed precisely, there can be little reason for failure.15 This reference is probably the reason that most veterinary surgery textbooks from the 1950s and 1960s recommended the technique.16–21 The fifth edition of Canine Surgery (1965) illustrated an open, single-layer, inverting small intestinal anastomosis technique in addition to the Parker-Kerr method.20

IMPORTANT ADVANCES In 1951, Gambee described a single-layer, inverting technique for intestinal anastomosis (Figure 5).22 He reported good results with the technique and challenged the practice of douFigure 4—The Murphy button, which was designed ble-layer closure in the GI tract, EARLY VETERINARY to create a sutureless intestinal anastomosis. (From REPORTS which was widely used in huMcCunn J: Hobday’s Surgical Diseases of the Dog Information on surgical treat- and Cat, ed 4. Baltimore, Williams & Wilkins, man surgery. Gambee stated ment of intestinal diseases in the 1941, pp 180–213; with permission) that each suture placed must small animal veterinary literature have a definite purpose or else is generally lacking before the not be used.23 Gambee’s work established the value of single-layer intestinal closure; 1940s. The first edition of Canine Surgery was published however, many prominent surgeons continued to use in 1939.13 No description of how to perform intestinal anastomosis was given; readers were told to proceed double-layer closures. based on their training and experience and were directed The first challenges to Lembert’s principles of inverto human surgical texts for additional information.13 sion and serosal contact also appeared in the 1950s.24–26 In a 1941 small animal surgery textbook, McCunn In the following years, numerous reports that studied stated that the prognosis is always grave for enterorrhavarious inverting and everting suture patterns for enphy in the dog.14 He advocated intestinal surgery as a last teroanastomosis appeared.27–40 Much of this research BASIC TENETS ■ PARKER-KERR TECHNIQUE ■ SINGLE-LAYER INVERTING TECHNIQUE

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was performed in dogs. The reamount of lumen narrowing, sults of these studies varied wideomental adhesions, and mural fily and often had contradicting brosis was smallest with the apconclusions. However, by the end positional crushing pattern and of the 1960s, it was firmly estabgreatest with the everting pattern. lished that the intestine would In 1973, DeHoff and coheal adequately without inversion workers compared single-layer and serosal contact. inverting, everting, and approxThe earliest descriptions of evertimating jejunal anastomoses in ing intestinal anastomoses in the puppies.53 They stated that the goal of the approximating techveterinary literature appeared in nique is gentle apposition of the 1960s.27,41,42 In 1968, Ott and colleagues compared single-layer, the anastomosed edges and that inverting anastomosis with evertthe cut intestine may invert, eving anastomosis in the small inert, or approximate when brought testine of 100 dogs.33 They coninto apposition.53 The illustraFigure 5—The Gambee suture technique, an apcluded that the everting technique tions in their article clearly showed proximating method described as a single-layer, inwas stronger and was associated verting suture pattern.22,23 (From Orsher RJ, Rosen mucosal eversion at the anastowith less compromise of the lu- E: Small intestine, in Slatter D [ed]: Textbook of moses, and they reported that men diameter and fewer compli- Small Animal Surgery, ed 2. Philadelphia, WB Saun- eversion of the mucosa was evications. dent in histologic examination ders Co, 1993, pp 593–612; with permission) In 1968, Poth and Gold deof all approximating anastoscribed a “new technique” for inmoses. They concluded that, 1 testinal anastomosis (Figure 6).43 month after surgery, the apThey stated that it seemed more proximating technique had lowreasonable to approximate the er morbidity and produced less severed intestine by true end-on scar tissue formation at the anreconstruction rather than invertastomosis than did the inverting ing or everting the intestinal wall.43 or everting techniques. They reported that the end-on, In 1976, Reinertson comsimple interrupted suture was the pared three patterns for equine simplest possible stitch and advo- Figure 6—Poth and Gold’s crushing appositional jejunal anastomosis: a modified suture. (From Orsher RJ, Rosen E: Small intestine, cated a crushing technique, which in Slatter D [ed]: Textbook of Small Animal Surgery, Gambee appositional suture, a cut through all layers except the ed 2. Philadelphia, WB Saunders Co, 1993, pp simple interrupted everting susubmucosa. Despite this recom- 593–612; with permission) ture, and a double-row invertmendation, relatively few reports ing suture.54 He reported that the inverting technique had in the human surgical literature minimal adhesions but predisposed the patient to indiscuss approximating suturing techniques,31,43–46 and approximating methods of intestinal anastomosis are testinal obstruction. The everting technique avoided lunot mentioned in current human surgery textbooks.12,47–48 minal compromise but predisposed the intestine to leakage and had increased adhesions, which led to exAPPROXIMATING HAND-SEWN ANASTOMOSIS tramural fibrosis that limited intestinal extensibility. In contrast to the human literature, most published The modified Gambee technique resulted in near-norreports in the recent veterinary literature involve apmal lumen diameter, minimal adhesions, and adequate proximating, end-to-end techniques for intestinal anasstrength and thus was deemed safe and effective for tomosis. Simple interrupted approximating anastomoend-to-end intestinal anastomosis in horses.54 The reports of Bennett, DeHoff, and Reinertson and sis has become the technique of choice for end-to-end their colleagues seem to be responsible for establishing anastomosis in small animal surgery.49–51 The first report in the veterinary literature discussing the single-layer, interrupted, approximating technique approximating intestinal anastomosis appeared in for end-to-end intestinal anastomosis in veterinary 1970.52 Bennett and Zydeck52 compared single-layer evsurgery. It is interesting that the everting technique erting, inverting, and appositional crushing end-to-end used by Reinertson54 is identical to the approximating technique used by DeHoff and coworkers.53 It should jejunal anastomoses in six dogs and concluded that the EVERTING ANASTOMOSIS ■ APPROXIMATING ANASTOMOSIS ■ MODIFIED GAMBEE TECHNIQUE

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also be pointed out that the Gambee suture technique,22 which Reinertson considered an appositional suture, is considered to be an inverting pattern in the human literature. In the middle 1970s, the single-layer, interrupted, end-to-end approximating technique for intestinal anastomosis first appeared in small animal surgery textbooks.55,56 In addition to the new approximating techniques, these texts describe traditional inverting, everting, and double-layer techniques for intestinal closure. In 1981, Ellison reviewed techniques for end-to-end intestinal anastomosis in dogs.57 He pointed out the difficulty in avoiding some degree of mucosal eversion when either a crushing or noncrushing approximating pattern is used and cautioned that, as a result, modification of healing like that associated with everting patterns may occur.57 He concluded that, with proper surgical technique, any anastomotic suture pattern could be used successfully in the canine intestine but that approximating patterns offer the least compromise of lumen diameter and early superior healing. In 1982, Ellison and colleagues58 compared simple interrupted approximating, simple interrupted crushing, and simple continuous approximating techniques for end-to-end intestinal anastomosis in dogs. In all techniques, the needle passage excluded the mucosa in an attempt to minimize eversion. However, these researchers reported that 65% of the simple interrupted approximating anastomoses had mucosal eversion; 62% of the simple interrupted crushing anastomoses had mucosal eversion or tissue overlap; and 38% of the simple continuous approximating anastomoses had eversion, inversion, or tissue overlap.58 In 1982, Bellenger was the first to report results of experimental appositional anastomosis of the jejunum in cats.59 He compared single-layer inverting and single-layer appositional patterns in six cats. He concluded that the inverting technique caused substantially more luminal impingement than did the appositional technique and that the histologic continuity of layers was superior to that associated with the appositional method. The primary complications were intestinal obstruction in two of six inverting anastomoses and leakage in one of six appositional anastomoses.59 In 1983, Bone and coworkers compared simple interrupted crushing and noncrushing approximating anastomoses in the canine jejunum.60 They reported that neither suture pattern produced consistent mucosal apposition, which varied from inverted to apposed to everted. The histologic illustrations in this report clearly showed eversion of the mucosa and healing of the anastomoses by bridging fibroplasia.60 These studies of end-to-end intestinal anastomosis

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show that true approximation of the histologic layers of ends of cut intestine is infrequently achieved, even under experimental surgical conditions. Eversion, inversion, and overlapping of the intestinal ends most frequently occur with approximating techniques, as reported by DeHoff, Ellison, and Bone and their colleagues, and may explain why discussions of approximating intestinal anastomosis are lacking in the human surgical literature. Recently, Weisman and colleagues reported that a modified simple continuous pattern for closure of intestinal incisions is an acceptable alternative to the simple interrupted pattern in dogs and cats.61 Reported advantages of a simple continuous enteric closure include surgical speed, decreased tissue handling, improved apposition of intestinal layers, and a low rate of clinical complications. 61 Simple continuous approximating anastomosis has been shown experimentally to achieve better continuity of the histologic intestinal layers than do simple interrupted approximating techniques.58

STAPLED INTESTINAL ANASTOMOSIS The current automated stapling instruments for intestinal anastomosis originated in the former Soviet Union after World War II.62 These stapling devices were first tested in the United States in the 1960s and became widely accepted for use in human surgical patients in the 1970s.62–64 Automated intestinal stapling devices allow rapid, secure, inverting anastomosis of the intestine and are typically used to create antiperistaltic side-to-side (functional end-to-end) or true end-to-end anastomoses.65 Reported complication rates for stapled anastomoses are similar to those for conventional handsewn methods.66 Hess and coworkers published the first veterinary study that compared mechanically stapled with handsewn small intestinal anastomoses.67 Although the outcomes of the two techniques were similar, the mechanical staples were applied more consistently and required less surgical time than did the sutures.67 Stoloff and colleagues compared stapled and hand-sewn colonic anastomoses in dogs.68 They reported less tissue reaction, improved healing, and fewer adhesions with the inverted stapled anastomosis.68 In 1991, Ullman and colleagues reported good clinical results in 24 dogs and cats that had open intestinal anastomosis performed with automated surgical staplers.69 The primary postsurgical complications were anastomotic leakage (2 of 24 cases) and localized abscess formation (1 of 24 cases). 69 No long-term complications were observed in the 23 surviving patients. Favorable results have also been published for colonic anastomosis with automated staplers in cats.70,71

APPOSITIONAL ANASTOMOSIS ■ STAPLING DEVICES ■ AUTOMATED STAPLERS

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Surgical stapling devices have numerous potential applications in small animal GI surgery. The primary limitations to widespread use of these devices are the cost of the instruments and lack of familiarity with automated intestinal stapling techniques. A biofragmentable ring for intestinal anastomosis has been experimentally tested in dogs72,73 and cats74 and has been used clinically in humans.75 The ring is similar to the Murphy button except that it is composed of polyglycolic acid and thus breaks down approximately 12 days after implantation.74 The remains of the device eventually pass with the feces. Experimental data show that colonic anastomoses achieved with a biofragmentable ring have higher initial bursting strength and similar healing patterns compared with sutured and stapled anastomoses.73 Clinical application of the biofragmentable anastomosis ring has not been reported in the veterinary literature.

SUMMARY Because the intestine is a dynamic, soft tissue organ and not a rigid tube (as portrayed in many textbook illustrations), eversion of the mucosa from the cut ends and retraction of the outer seromuscular layers occur. Although direct, end-to-end apposition of the intestinal layers is a reasonable goal and primary healing of the intestinal wall can occur, 44,58 such healing is rarely achieved even under ideal surgical settings. Indeed, a critical review of the literature shows that true histologic approximation of the layers of intestine is infrequent, mucosal eversion is common, and secondary healing of approximating end-to-end anastomoses is the most common scenario. Veterinary surgeons are aware of the difficulty in achieving true approximation of the cut intestine and have tried to minimize mucosal eversion by either trimming the exposed mucosa or taking modified bites that exclude the mucosa altogether or invert the mucosal layer. The end result of these modifications is often inversion of the histologic intestinal layers rather than apposition. Automated surgical stapling devices and biofragmentable anastomotic rings can also be used to rapidly create efficient enteroanstomoses in small animals. These devices typically create inverting anastomoses and have complication rates similar to those of handsewn methods. Widespread use of intestinal stapling equipment by veterinarians has been limited by cost and lack of familiarity with stapling techniques. Despite the 40 years of research that has challenged Lembert’s principle of serosal inversion, single-layer inverting techniques remain the most widely used methods for hand-sewn end-to-end anastomosis of the intestine in human surgery.12,47–48 In veterinary surgery, the BIOFRAGMENTABLE RING ■ COST FACTOR

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single-layer, approximating technique for intestinal anastomosis has become widely accepted.49–51 There are several reasons veterinarians have accepted the approximating technique for intestinal anastomosis. First, the technique is simple to perform and has yielded consistent results. Second, the lumen of canine and feline intestine is narrower than that of the human intestine; thus postanastomotic stricture after the inverting technique is more of a concern in veterinary patients. Third, postsurgical abdominal adhesions, which occur more frequently with noninverting intestinal anastomoses, are less of a clinical concern in small animals than in humans. Finally, veterinary surgeons are less strongly tied to Lembert and 175 years of surgical doctrine than are human surgeons. Nearly 200 years after the start of the “modern era of intestinal surgery,”1 veterinary surgeons have arrived at an approximating technique for hand-sewn end-to-end intestinal anastomosis that is almost identical to the method described by Travers in 1812.2 Just as Lembert has been called the founder of modern intestinal surgery, perhaps Travers should be regarded as the founder of modern veterinary intestinal surgery.

REFERENCES 1. Senn N: Enterorrhaphy: Its history, technique, and present status. JAMA 21:215–235, 1893. 2. Travers B: An inquiry into the process of nature in repairing injuries of the intestines: Illustrating the treatment of penetrating wounds and strangulated hernia. London, UK, Longman, Hurst, Rees, Orne, and Brown, 1812. 3. Lembert A: Nouveau procede d’enterorraphie. Repertoire General d’Anatome et de Physiologie Pathologique 2:3–101, 1826. 4. Ravitch MM: Observations on the healing of wounds of the intestines. Surgery 77:665–673, 1975. 5. Brieger GH: The development of surgery, in Sabiston DC (ed): Textbook of Surgery. Philadelphia, WB Saunders Co, 1997, pp 1–15. 6. Czerny V: Uber darmresection bei gangranosen hernien. Sammlung Klinischer Vortrage 201:1689–1702, 1883. 7. Halsted WS: Circular suture of the intestine—An experimental study. Am J Med Sci 94:436–461, 1887. 8. Connell ME: An experimental contribution looking to an improved technique in enterorrhaphy whereby the number of knots is reduced to two, or even one. Med Rec 42:335– 337, 1892. 9. Murphy JB: Cholecysto-intestinal, gastro-intestinal, enterointestinal anastomosis, and approximation without sutures (original research). New York Med Rec 42:665–712, 1892. 10. Kerr HH: The development of intestinal surgery. JAMA 81:641–647, 1923. 11. Mossa AR, Hart ME, Easter DW: Surgical complications, in Sabiston DC (ed): Textbook of Surgery. Philadelphia, WB Saunders Co, 1997, pp 341–356.

12. Nelson RL: Surgical techniques and care of obstruction of the small intestine, in Nyhus LM, Baker RJ (eds): Mastery of Surgery, ed 2. Boston, Little, Brown and Co, 1992, pp 1154– 1161. 13. Lacroix JV: Canine Surgery. Evanston, IL, North American Veterinarian, 1939, pp 21–22. 14. McCunn J: Hobday’s Surgical Diseases of the Dog and Cat, ed 4. Baltimore, Williams & Wilkins,1941, pp 180–213. 15. Lacroix JV, Hoskins HP: Canine Surgery, ed 2. Evanston, IL, North American Veterinarian, 1949, pp 318–320. 16. Frank ER: Veterinary Surgery Notes, ed 5. Minneapolis, Burgess, 1950, pp 21–23. 17. Frank ER: Veterinary Surgery, ed 6. Minneapolis, Burgess, 1959, pp 20–22. 18. Lacroix JV, Hoskins HP: Canine Surgery, ed 3. Evanston, IL, North American Veterinarian, 1952, pp 396–401. 19. Mayer K, Lacroix JV, Hoskins HP: Canine Surgery, ed 4. Evanston, IL, North American Veterinarian, 1957, pp 441– 448. 20. Larson LH: Stomach and small intestine, in Archibold J (ed): Canine Surgery, ed 5. Santa Barbara, American Veterinary Publications, 1965, pp 494–534. 21. Leonard EP: Fundamentals of Small Animal Surgery. Philadelphia, WB Saunders Co, 1968, pp 194–202. 22. Gambee LP: Single layer open intestinal anastomosis applicable to small as well as large intestine. West J Surg 59:1–5, 1951. 23. Gambee LP: Ten years’ experience with a single layer anastomosis in colon surgery. Am J Surg 92:222–227, 1956. 24. Hertzler JH, Tuttle WM: Experimental method for everting end-to-end anastomosis in the gastrointestinal tract. Arch Surg 65:398, 1952. 25. Galluzi W, Possenti B: The everting suture applied to perform an end-to-end anastomosis on the small bowel. Minerva Chir 9:1008, 1954. 26. Ravitch MM: Some considerations on the healing of intestinal anastomoses. Surg Clin North Am 49:627–635, 1969. 27. Knowles RP: Eversion technique for intestinal anastomosis. Proc AVMA Ann Meet:192–193, 1964. 28. Mellish RWP: Inverting or everting sutures for bowel anastomoses. J Pediatr Surg 1:260–265, 1966. 29. Getzen LC, Roe RD, Holloway CK: Comparative study of intestinal anastomotic healing in inverted and everted closures. Surg Gynecol Obstet 123:1219–1227, 1966. 30. Ravitch MM, Canalis F, Weinshelbaum A, McCormick J: Studies on intestinal healing: III. Observations on everting intestinal anastomoses. Ann Surg 166:670–680, 1967. 31. Loeb MJ: Comparative strength of inverted, everted, and end-on intestinal anastomoses. Surg Gynecol Obstet 125:301– 304, 1967. 32. Canalis F, Ravitch MM: Study of healing of inverting and everting intestinal anastomoses. Surg Gynecol Obstet 126:109– 114, 1968. 33. Ott BS, Doyle MD, Greenawald KA: Single layer everted intestinal anastomosis. JAVMA 153:1742–1753, 1968. 34. Gill W, Fraser J, Carter DC, Hill R: Everted intestinal anastomosis. Surg Gynecol Obstet 128:1297–1303, 1969. 35. Rusca JA, Bornside GH, Cohn I: Everting versus inverting gastrointestinal anastomoses: Bacterial leakage and anastomotic disruption. Ann Surg 169:727–735, 1969. 36. Kho E, Replogle R, Ravitch MM: Studies of intestinal heal-

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About the Authors When this article was submitted for publication, Dr. Coolman was the 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, School of Veterinary Medicine, University of Illinois, Urbana, Illinois. Dr. Ehrhart is a Diplomate of the American College of Veterinary Surgeons, and Dr. Manfra Marretta is a Diplomate of the American College of Veterinary Surgeons and the American Veterinary Dental College.