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Bowel anastomosis by inverting and everting techniques
Journal of Surgical Research Clinical
and Laboratory
Volume
BOWEL AND
7
Number
E.
ANASTOMOSIS EVERTING
HEALEY, AND
JR., H.
M.D., STEPHEN
IN 1812 Travers [ 131, in his classic monograph entitled “Inquiry into the Process of Nature in Repairing Injuries of the Intestines,” was the first investigator to emphasize the necessity of coapting the peritoneal surfaces serosa-to-serosa in the repair of the intestines. This principle was later popularized in a publication by Lembert [lo] in 1826. Lembert maintained that the apposition of the peritoneal surfaces of the bowel results in the proliferation of large quantities of fibrin which hermetically seals the suture line, thereby preventing leakage of infected intestinal contents into the peritoneal cavity. This finding resulted in the frequently repeated statement that the success of gastrointestinal surgery depends only partially upon the dexterity of the surgeon, and chiefly upon the bactericidal and fibrinogenic properties of the peritoneum. Another surgical dictum which resulted from Lembert’s publication is that intestinal healing is only possible by inverting serosa-to-serosa, although he did not specifically state this to be so, nor has there been From the Departments of Surgery and Pathology, The University of Texas, Austin, Tex., and the M. D. Anderson Hospital and Tumor Institute, Houston, TeX. This work was supported in part by U.S. National Institutes of Health Grant GM-12345-01 and by a grant-in-aid from Ethicon, Inc., Somerville, N.J. Submitted for publication Aug. 5, 1966.
July 1967
7,
BY INVERTING TECHNIQUES
An Experimental JOHN
Investigation
Stud!]
CHARLES GALLAGER,
M.
MC
BRIDE,
M.D.,
M.D.
any experimental work to support such a dictum. The first practical application of these surgical dicta was performed by Dieffenbach [l] in 1836, who performed the first end-toend anastomosis of the small intestine in a human being. An important surgical principle in intestinal repair which has not been emphasized is that advocated by Halsted [2], who stated that it is imperative that an intestinal suture must include the submucosal layer, the strongest layer of the bowel wall, in order to achieve adequate intestinal healing. In a survey of the ten most recent textbooks of surgical techniques only one was found which advocated adherence to Halsted’s principle in intestinal repair. With the exception of the button technique proposed by Murphy [ll] in 1892 there has been no challenge of the fundamental surgical procedure of intestinal inverting suture repair, Our interest in the process of intestinal repair was initiated by studies on the nonsuture repair of the gastrointestinal tract using various liquid plastic adhesives which we had previously used to repair blood vessels [3] and bronchial stumps [6], Attempts at nonsuture bowel closure by the inverting technique were completely unsuccessful. However, by everting the bowel wall, fixing the everted cuffs in position by means of a specially de299
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7 NO.
signed clamp, stripping the mucosa from the everted cuffs, and adhering the submucosal layers, intestinal nonsuture anastomosis was possible [ 121. Since such an everting technique was against all surgical principles, we decided to reevaluate various methods of endto-end intestinal repair. This report is a more comprehensive presentation of material presented in October I964 at the Surgical Forum of the American College of Surgeons [4].
MATERIALS
AND
METHODS
Adult mongrel dogs were used in all of these experimental end-to-end bowel anastomoses. No oral feedings were given to these animals during the 24 hours preoperatively, and an enema was administered the night before operation. No antibiotic bowel preparation was used in these experiments. Sodium pentobarbital (15 mg. per kilogram of body weight) was injected intravenously for induction anesthesia. An endotracheal tube was inserted and an oxygen-ether combination was used for supplemental anesthesia. The abdomen was opened through a midline incision. Postoperatively, I cc. of penicillin (200,000 U) and streptomycin (1 gm.) was administered and continued daily for five days. The animals were offered full kennel rations on the first postoperative day. In each experimental group, the animals were sacrificed at 24 hours, at weekly intervals up to one month, at monthly intervals up to six months and a final followup sacrifice at one year. The animals were divided into four experimental groups ( Fig. 1) : Group I (inversion) : -This group consisted of 20 animals representing 10 ileal and 10 colonic end-to-end anastomoses in which conventional inverting suture technique was used. The small bowel repairs were performed by a running Connell suture of 3-O chromic catgut and the large bowel by 3-O chromic catgut interrupted sutures. Group II (submucosal apposition): This group consisted of 18 animals representing nine small bowel and nine large bowel anas300
7,
1967
JULY
GROUP I - lNVER.SlON
/
GROUP 1fI.W - EVERSlON
GROUP /I - FLAT
Fig. 1. Types of bowel closure. In both Groups III and IV the bowel wall is everted and the mucosa stripped from the everted cuffs. In Group III the wall was approximated with sutures, whereas in Group IV a plastic adhesive was used in closure. tomoses. In these animals the serosal and muscular layers were excised for a distance of one-half centimeter from the site of transection on both proximal and distal segments of bowel. The mucosa was also removed for the same distance from each bowel segment. The remaining submucosal layer of bowel was then approximated by interrupted sutures in the large bowel and a continuous interlocking suture in the small bowel. Group III (ever&on with sutures): Small and large bowel anastomoses were performed in each of 10 animals by an everting technique in which a special clamp, or anastomat, which is described below, was used. The mucosa was curetted from the everted cuffs, and closure of the cuffs was accomplished by a 3-O chromic catgut running suture. Group IV (eversion-nonsuture): By the use of a technique similar to that used on Group III in 10 small bowel and 10 large bowel repairs, closure was accomplished by the application of a liquid plastic adhesive, isobutyl cyanoacrylate (Eastman 910 homologue* ). The clamp, or anastomat, used in both Groups III and IV has been described in a previous publication [5]. It consists of two parts, each a mirror image of the other with * Supplied
by
Ethicon,
Inc.,
Somerville,
N.J.
HEALEY
ET
AL.:
BOWEL
ANASTOMOSIS
BY
INVERTING
AND
EVERTING
TECHNIQUES
the mucosa curetted from the everted cuffs. In Group III, a running suture was used to approximate the everted cuffs, whereas in Group IV, the everted submucosa was dried and a few drops of the liquid plastic applied. The cuffs were then brought together by pressure exerted by a flat-tipped forcep. This pressure initiated the polymerization reaction. After a wait of about 30 seconds to a minute, the clamps were opened and removed from the bowel (Fig. 2).
RESULTS
Fig. 2. Nonsuture bowel repair. (A) Each end of the transected bowel is everted over the rings and fixed in position by a rubber O-ring which is cut after the clamps are closed. (B) the everted cuffs are dried and the plastic adhesive applied and polymerized by pressure. (C) The shanks are opened and separated at their pivot point. (D) The spring attachment is compressed, opening the ring which permits its removal.
of a shank with a ring welded to its distal end. The two parts may be joined at th e pivot point to permit opening and closing of the clamp. A spring attachment on the distal end breaks the ring to allow application or removal of the clamp from the bowel, To achieve the everting technique for closure, one end of the bowel is everted over the ring of the clamp and fixed in position by the placement of a rubber O-ring. A similar procedure is performed on the opposite end of the bowel, and the clamps are joined at their pivot point and closed, bringing the proximal and distal segments into apposition. The rubber O-rings are cut and discarded and each
part
consisting
All four methods of repair resulted in primary healing of the intestinal tract. There was one failure in each of the four groups, including two small bowel and two large bowel repairs ( Table 1) . The two small bowel failures were due to intestinal obstruction: One occurred in the submucosal apposition (Group II) and one in the everting with suture technique (Group III), The two large bowel failures were the result of leakage at the anastomotic site with a resultant peritonitis as the cause of death. One of these large bowel failures occurred in the conventional closure (Group I) and the other in the nonsuture closure (Group IV). Adhesions were not a significant problem in any of the four groups of repair. Knightly et al. [9] classified the extent of peritoneal adhesions as follows: 0, no adhesions; 1, a single adhesive strand; 2, minimal but multiple visTable
Group I II III IV
1.
Bowel
Failures
Small
Bowel
Large
Bowel
No.
Failures
No.
Failures
10 9 10 10
0 1” 1c 0
10 9 10 10
la 0 0 la
Total
Total No.
Failures
20 18 20 20 78
1 1 1 1 4
a Leakage. tj Intraluminal obstruction. (’ Kinking, adhesive reaction.
301
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7
NO.
7,
JULY
ceral adhesions which may be easily disrupted; 3, moderate visceral adhesions but with no parietal attachment; and 4, extensive visceral adhesions with parietal extensions. None of the biopsies in the four groups under consideration could be classified in this last group. It is of interest to note, however, that in these regularly biopsied specimens there was in all the experimental groups a definite relationship between the extent of adhesions and the time of biopsy; in other words, the longer the period of survival, the fewer adhesions. A breakdown of the four groups revealed that in those in whom repair was performed by eversion with sutures adhesive reaction was most prominent,
C
1967
but there was little if any difference in the other three groups. Microscopic examination of the healing process of the bowel by interval biopsies showed a somewhat similar reaction in all groupswhether by inversion, submucosal apposition, or everting techniques (Fig. 3). Initially, an acute inflammatory reaction and fibroblastic reaction occurs characterized by the presence of polymorphonuclear leukocytes, plasma, and fibrin. This acute reaction clears within seven to fourteen days but was more pronounced and persistent in the group in which an everting closure with sutures was performed. Healing in all caseswas by a fibrous union, Muco-
D
Fig. 3. Histological appearance at the repair site of intestinal anastomosis one month postoperative. (A) Inverting technique. (B) Submucosa-to-submucosa. (C) Everting with sutures. (D) Everting, nonsuture technique. 302
HEALEY
ET
AL.:
BOWEL
ANASTOMOSIS
sal regeneration is usually complete at two weeks; however, in the nonsuture closure complete regeneration may be delayed to three or four weeks. Serosal healing was complete in all groups at one month. Smooth muscle regeneration was seen as early as one month in the nonsuture group in the fibrous scar tissue and in all groups at two months. A wedgeshaped scar was observed in all groups except those in which direct submucosal apposition was performed. In this case, the fibrous scar was more linear in appearance. Foreign body reaction was no greater in the nonsuture technique than in the suture techniques. In previous studies using a methyl-2-cyanoacrylate plastic in the nonsuture closure of bowel it was histologically impossible to stain the plastics. However, under reduced illumination the plastic appears as refractile bodies at the repair site. The methyl-2-cyanoacrylate plastic nearest the lumenal side disappears early in the first week while that located in the seromuscular layer may persist as long as from three to five months [ 121. The isobutyl cyanoacrylate used in this study apparently does not possess this absorptive characteristic, for it may still be found grossly at the anastomotic site up to one year postoperatively.
DISCUSSION It is of interest to note that since Lembert put forth his surgical dictum in 1826, in which he emphasized the necessity of coapting the peritoneal layer of bowel in order to achieve intestinal healing, this principle has never been challenged, This procedure necessarily results in an inversion of the bowel wall resulting in a varying degree of lumenal narrowing, depending upon the ability of the operator. Use of an everting technique might eliminate this postoperative complication. We have been most impressed with the low postoperative morbidity of those animals in which an everting closure has been achieved. This low morbidity may be due either to the lack of lumenal narrowing or the short period of intestinal obstruction during the application of the anastomat which averages about 4 minutes.
BY
INVERTING
AND
EVERTINC
TECHNIQUES
To our knowledge only one other group of investigators has attempted to evaluate the effects of an everting anastomosis of the bowel. This work was presented by Holloway, Roe, and Getzen of the San Diego Naval Hospital in an exhibit at the annual meeting of the American College of Surgeons in Chicago in 1964 [7]. In addition to their experimental work in dogs, which compared favorably with our own experimental work on everting bowel anastomosis, they performed twenty everted gastroduodenostomies in conjunction with hemigastrectomy and bilateral vagotomy for peptic ulcer disease in humans. Eight of these patients were gastroscoped six to twelve weeks postoperatively and compared with a control group of 10 patients who had an inverting gastroduodenostomy. All of the inverted anastomotic stomachs contained residual food after I2 or more hours, whereas the everted anastomotic stomachs contained none. In addition 80% of the inverted anastomoses exhibited associated edema, hyperemia, and enlarged rugae at the anastomotic site, whereas similar findings were significantly less in the everted
group PI. We realize that old ideas die hard, particularly in the field of surgery, but perhaps a reevaluation of certain principles of intestinal healing should be initiated in order to affirm or refute the findings presented by our own studies and those of Holloway et al. [7], We do not feel that nonsuture intestinal anastomosis will gain clinical acceptance until the ideal plastic becomes available. A procedure using plastic will probably gain its first clinical acceptance in gastrointestinal surgery as a reinforcement of suture line, as in duodenal closure, in which the number of sutures required in conventional closure can be reduced. It is our hope that this work may serve as an impetus to other investigators to reevaluate certain principles of intestinal wound healing and to reaffirm Halsted’s less emphasized principle of the importance of including the submucosal layer in bowel suturing over Lembert’s dictum of the importance of serosato-serosa approximation in our surgical teaching. 303
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7 NO.
SUMMARY In this experimental study the surgical dictum that it is necessary to coapt serosa-toserosa in order to obtain intestinal healing is challenged. A control group of large and small bowel anastomoses is compared with experimental groups in which direct submucosal apposition and everting techniques both by suture and nonsuture reapproximation of bowel are performed. Primary healing was obtained in all groups, Histologically a similar reaction was observed whether the anastomosis was by inversion, submucosal apposition, or everting techniques. Of significance was the low morbidity rate in the animals in which the bowel anastomoses were everted. The rate of morbidity is low probably because the intestinal lumen is not narrowed at the anastomotic site. From the results of this study Halsted’s principle of including the submucosal layer in the bowel closure is much more important in intestinal healing than is Lembert’s dictum of serosa-to-serosa approximation.
REFERENCES 1.
2.
304
Dieffenbach, J. F., cited by Leonardo, R. A. History of Surgery. New York: Froben Press, 1943. P. 281. Halsted, W. S. Circular sutures of the intestines: An experimental study. Amer. J. Med. Sci. 94:436, 1887.
7,
JULY
3.
4.
5.
6.
7.
8. 9.
10.
11.
12.
13.
1967 Healey, J. E., Jr., Clark, R. L., Gallager, H. S., O’Neill. P.. and Sheena. K. S. The nonsuture repair of blood vessels. Ann. Surg. 155:817, 1962. Healey, J. E., Jr., McBride, C. M., and Gallager, H. S. Is serosa-to-serosa approximation necessary in intestinal anastomosis? Surg. Forum 15:297, 1964. Healey, J. E., Jr., and Moore, E. B. An anastomosing instrument for ductal repairs. Amer. .I. Surg. 109:689, 1965. Healey, J. E., Jr., Sheena, K. S., Gallager, H. S., and Clark, R. L. Bronchial closure following pneumonectomy utilizing a plastic adhesive. Ann. Surg. 159:172, 1964. Holloway, C. K., Roe, R. D., and Getzen, L. C. Exhibit, American College of Surgeons Meeting, Chicago, Illinois, Oct. 1964. Holloway, C. K. Personal communication, July, 1966. Knightly, J. J., Agostino, D., and Cliffton, E. Effect of fibronolysin and heparin on the formation of peritoneal adhesive. Surgery 52:250, 1962. Lembert, A. Memoire sur l’enteroraphie avec la Description dun Procede Nouveau pour Pratiquer cette Operation Chirurgicale. Report Gen. D’Anat. Physiol. Path. 2~100, 1826. Murphy, J. B. Cholecystointestinal, gastrointestinal, enterointestinal anastomosis and approximation without sutures. Med. Rec. N.Y. 42: 665, 1892. O’Neill, P., Healey, J. E., Jr., Clark, R. L., and Gallager, H. S. Nonsuture intestinal anastomosis. Amer. J. Surg. 104:761, 1962. 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: Longman, 1812. Pp. 132-134.
and Laboratory
Volume
BOWEL AND
7
Number
E.
ANASTOMOSIS EVERTING
HEALEY, AND
JR., H.
M.D., STEPHEN
IN 1812 Travers [ 131, in his classic monograph entitled “Inquiry into the Process of Nature in Repairing Injuries of the Intestines,” was the first investigator to emphasize the necessity of coapting the peritoneal surfaces serosa-to-serosa in the repair of the intestines. This principle was later popularized in a publication by Lembert [lo] in 1826. Lembert maintained that the apposition of the peritoneal surfaces of the bowel results in the proliferation of large quantities of fibrin which hermetically seals the suture line, thereby preventing leakage of infected intestinal contents into the peritoneal cavity. This finding resulted in the frequently repeated statement that the success of gastrointestinal surgery depends only partially upon the dexterity of the surgeon, and chiefly upon the bactericidal and fibrinogenic properties of the peritoneum. Another surgical dictum which resulted from Lembert’s publication is that intestinal healing is only possible by inverting serosa-to-serosa, although he did not specifically state this to be so, nor has there been From the Departments of Surgery and Pathology, The University of Texas, Austin, Tex., and the M. D. Anderson Hospital and Tumor Institute, Houston, TeX. This work was supported in part by U.S. National Institutes of Health Grant GM-12345-01 and by a grant-in-aid from Ethicon, Inc., Somerville, N.J. Submitted for publication Aug. 5, 1966.
July 1967
7,
BY INVERTING TECHNIQUES
An Experimental JOHN
Investigation
Stud!]
CHARLES GALLAGER,
M.
MC
BRIDE,
M.D.,
M.D.
any experimental work to support such a dictum. The first practical application of these surgical dicta was performed by Dieffenbach [l] in 1836, who performed the first end-toend anastomosis of the small intestine in a human being. An important surgical principle in intestinal repair which has not been emphasized is that advocated by Halsted [2], who stated that it is imperative that an intestinal suture must include the submucosal layer, the strongest layer of the bowel wall, in order to achieve adequate intestinal healing. In a survey of the ten most recent textbooks of surgical techniques only one was found which advocated adherence to Halsted’s principle in intestinal repair. With the exception of the button technique proposed by Murphy [ll] in 1892 there has been no challenge of the fundamental surgical procedure of intestinal inverting suture repair, Our interest in the process of intestinal repair was initiated by studies on the nonsuture repair of the gastrointestinal tract using various liquid plastic adhesives which we had previously used to repair blood vessels [3] and bronchial stumps [6], Attempts at nonsuture bowel closure by the inverting technique were completely unsuccessful. However, by everting the bowel wall, fixing the everted cuffs in position by means of a specially de299
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7 NO.
signed clamp, stripping the mucosa from the everted cuffs, and adhering the submucosal layers, intestinal nonsuture anastomosis was possible [ 121. Since such an everting technique was against all surgical principles, we decided to reevaluate various methods of endto-end intestinal repair. This report is a more comprehensive presentation of material presented in October I964 at the Surgical Forum of the American College of Surgeons [4].
MATERIALS
AND
METHODS
Adult mongrel dogs were used in all of these experimental end-to-end bowel anastomoses. No oral feedings were given to these animals during the 24 hours preoperatively, and an enema was administered the night before operation. No antibiotic bowel preparation was used in these experiments. Sodium pentobarbital (15 mg. per kilogram of body weight) was injected intravenously for induction anesthesia. An endotracheal tube was inserted and an oxygen-ether combination was used for supplemental anesthesia. The abdomen was opened through a midline incision. Postoperatively, I cc. of penicillin (200,000 U) and streptomycin (1 gm.) was administered and continued daily for five days. The animals were offered full kennel rations on the first postoperative day. In each experimental group, the animals were sacrificed at 24 hours, at weekly intervals up to one month, at monthly intervals up to six months and a final followup sacrifice at one year. The animals were divided into four experimental groups ( Fig. 1) : Group I (inversion) : -This group consisted of 20 animals representing 10 ileal and 10 colonic end-to-end anastomoses in which conventional inverting suture technique was used. The small bowel repairs were performed by a running Connell suture of 3-O chromic catgut and the large bowel by 3-O chromic catgut interrupted sutures. Group II (submucosal apposition): This group consisted of 18 animals representing nine small bowel and nine large bowel anas300
7,
1967
JULY
GROUP I - lNVER.SlON
/
GROUP 1fI.W - EVERSlON
GROUP /I - FLAT
Fig. 1. Types of bowel closure. In both Groups III and IV the bowel wall is everted and the mucosa stripped from the everted cuffs. In Group III the wall was approximated with sutures, whereas in Group IV a plastic adhesive was used in closure. tomoses. In these animals the serosal and muscular layers were excised for a distance of one-half centimeter from the site of transection on both proximal and distal segments of bowel. The mucosa was also removed for the same distance from each bowel segment. The remaining submucosal layer of bowel was then approximated by interrupted sutures in the large bowel and a continuous interlocking suture in the small bowel. Group III (ever&on with sutures): Small and large bowel anastomoses were performed in each of 10 animals by an everting technique in which a special clamp, or anastomat, which is described below, was used. The mucosa was curetted from the everted cuffs, and closure of the cuffs was accomplished by a 3-O chromic catgut running suture. Group IV (eversion-nonsuture): By the use of a technique similar to that used on Group III in 10 small bowel and 10 large bowel repairs, closure was accomplished by the application of a liquid plastic adhesive, isobutyl cyanoacrylate (Eastman 910 homologue* ). The clamp, or anastomat, used in both Groups III and IV has been described in a previous publication [5]. It consists of two parts, each a mirror image of the other with * Supplied
by
Ethicon,
Inc.,
Somerville,
N.J.
HEALEY
ET
AL.:
BOWEL
ANASTOMOSIS
BY
INVERTING
AND
EVERTING
TECHNIQUES
the mucosa curetted from the everted cuffs. In Group III, a running suture was used to approximate the everted cuffs, whereas in Group IV, the everted submucosa was dried and a few drops of the liquid plastic applied. The cuffs were then brought together by pressure exerted by a flat-tipped forcep. This pressure initiated the polymerization reaction. After a wait of about 30 seconds to a minute, the clamps were opened and removed from the bowel (Fig. 2).
RESULTS
Fig. 2. Nonsuture bowel repair. (A) Each end of the transected bowel is everted over the rings and fixed in position by a rubber O-ring which is cut after the clamps are closed. (B) the everted cuffs are dried and the plastic adhesive applied and polymerized by pressure. (C) The shanks are opened and separated at their pivot point. (D) The spring attachment is compressed, opening the ring which permits its removal.
of a shank with a ring welded to its distal end. The two parts may be joined at th e pivot point to permit opening and closing of the clamp. A spring attachment on the distal end breaks the ring to allow application or removal of the clamp from the bowel, To achieve the everting technique for closure, one end of the bowel is everted over the ring of the clamp and fixed in position by the placement of a rubber O-ring. A similar procedure is performed on the opposite end of the bowel, and the clamps are joined at their pivot point and closed, bringing the proximal and distal segments into apposition. The rubber O-rings are cut and discarded and each
part
consisting
All four methods of repair resulted in primary healing of the intestinal tract. There was one failure in each of the four groups, including two small bowel and two large bowel repairs ( Table 1) . The two small bowel failures were due to intestinal obstruction: One occurred in the submucosal apposition (Group II) and one in the everting with suture technique (Group III), The two large bowel failures were the result of leakage at the anastomotic site with a resultant peritonitis as the cause of death. One of these large bowel failures occurred in the conventional closure (Group I) and the other in the nonsuture closure (Group IV). Adhesions were not a significant problem in any of the four groups of repair. Knightly et al. [9] classified the extent of peritoneal adhesions as follows: 0, no adhesions; 1, a single adhesive strand; 2, minimal but multiple visTable
Group I II III IV
1.
Bowel
Failures
Small
Bowel
Large
Bowel
No.
Failures
No.
Failures
10 9 10 10
0 1” 1c 0
10 9 10 10
la 0 0 la
Total
Total No.
Failures
20 18 20 20 78
1 1 1 1 4
a Leakage. tj Intraluminal obstruction. (’ Kinking, adhesive reaction.
301
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7
NO.
7,
JULY
ceral adhesions which may be easily disrupted; 3, moderate visceral adhesions but with no parietal attachment; and 4, extensive visceral adhesions with parietal extensions. None of the biopsies in the four groups under consideration could be classified in this last group. It is of interest to note, however, that in these regularly biopsied specimens there was in all the experimental groups a definite relationship between the extent of adhesions and the time of biopsy; in other words, the longer the period of survival, the fewer adhesions. A breakdown of the four groups revealed that in those in whom repair was performed by eversion with sutures adhesive reaction was most prominent,
C
1967
but there was little if any difference in the other three groups. Microscopic examination of the healing process of the bowel by interval biopsies showed a somewhat similar reaction in all groupswhether by inversion, submucosal apposition, or everting techniques (Fig. 3). Initially, an acute inflammatory reaction and fibroblastic reaction occurs characterized by the presence of polymorphonuclear leukocytes, plasma, and fibrin. This acute reaction clears within seven to fourteen days but was more pronounced and persistent in the group in which an everting closure with sutures was performed. Healing in all caseswas by a fibrous union, Muco-
D
Fig. 3. Histological appearance at the repair site of intestinal anastomosis one month postoperative. (A) Inverting technique. (B) Submucosa-to-submucosa. (C) Everting with sutures. (D) Everting, nonsuture technique. 302
HEALEY
ET
AL.:
BOWEL
ANASTOMOSIS
sal regeneration is usually complete at two weeks; however, in the nonsuture closure complete regeneration may be delayed to three or four weeks. Serosal healing was complete in all groups at one month. Smooth muscle regeneration was seen as early as one month in the nonsuture group in the fibrous scar tissue and in all groups at two months. A wedgeshaped scar was observed in all groups except those in which direct submucosal apposition was performed. In this case, the fibrous scar was more linear in appearance. Foreign body reaction was no greater in the nonsuture technique than in the suture techniques. In previous studies using a methyl-2-cyanoacrylate plastic in the nonsuture closure of bowel it was histologically impossible to stain the plastics. However, under reduced illumination the plastic appears as refractile bodies at the repair site. The methyl-2-cyanoacrylate plastic nearest the lumenal side disappears early in the first week while that located in the seromuscular layer may persist as long as from three to five months [ 121. The isobutyl cyanoacrylate used in this study apparently does not possess this absorptive characteristic, for it may still be found grossly at the anastomotic site up to one year postoperatively.
DISCUSSION It is of interest to note that since Lembert put forth his surgical dictum in 1826, in which he emphasized the necessity of coapting the peritoneal layer of bowel in order to achieve intestinal healing, this principle has never been challenged, This procedure necessarily results in an inversion of the bowel wall resulting in a varying degree of lumenal narrowing, depending upon the ability of the operator. Use of an everting technique might eliminate this postoperative complication. We have been most impressed with the low postoperative morbidity of those animals in which an everting closure has been achieved. This low morbidity may be due either to the lack of lumenal narrowing or the short period of intestinal obstruction during the application of the anastomat which averages about 4 minutes.
BY
INVERTING
AND
EVERTINC
TECHNIQUES
To our knowledge only one other group of investigators has attempted to evaluate the effects of an everting anastomosis of the bowel. This work was presented by Holloway, Roe, and Getzen of the San Diego Naval Hospital in an exhibit at the annual meeting of the American College of Surgeons in Chicago in 1964 [7]. In addition to their experimental work in dogs, which compared favorably with our own experimental work on everting bowel anastomosis, they performed twenty everted gastroduodenostomies in conjunction with hemigastrectomy and bilateral vagotomy for peptic ulcer disease in humans. Eight of these patients were gastroscoped six to twelve weeks postoperatively and compared with a control group of 10 patients who had an inverting gastroduodenostomy. All of the inverted anastomotic stomachs contained residual food after I2 or more hours, whereas the everted anastomotic stomachs contained none. In addition 80% of the inverted anastomoses exhibited associated edema, hyperemia, and enlarged rugae at the anastomotic site, whereas similar findings were significantly less in the everted
group PI. We realize that old ideas die hard, particularly in the field of surgery, but perhaps a reevaluation of certain principles of intestinal healing should be initiated in order to affirm or refute the findings presented by our own studies and those of Holloway et al. [7], We do not feel that nonsuture intestinal anastomosis will gain clinical acceptance until the ideal plastic becomes available. A procedure using plastic will probably gain its first clinical acceptance in gastrointestinal surgery as a reinforcement of suture line, as in duodenal closure, in which the number of sutures required in conventional closure can be reduced. It is our hope that this work may serve as an impetus to other investigators to reevaluate certain principles of intestinal wound healing and to reaffirm Halsted’s less emphasized principle of the importance of including the submucosal layer in bowel suturing over Lembert’s dictum of the importance of serosato-serosa approximation in our surgical teaching. 303
JOURNAL
OF
SURGICAL
RESEARCH
VOL.
7 NO.
SUMMARY In this experimental study the surgical dictum that it is necessary to coapt serosa-toserosa in order to obtain intestinal healing is challenged. A control group of large and small bowel anastomoses is compared with experimental groups in which direct submucosal apposition and everting techniques both by suture and nonsuture reapproximation of bowel are performed. Primary healing was obtained in all groups, Histologically a similar reaction was observed whether the anastomosis was by inversion, submucosal apposition, or everting techniques. Of significance was the low morbidity rate in the animals in which the bowel anastomoses were everted. The rate of morbidity is low probably because the intestinal lumen is not narrowed at the anastomotic site. From the results of this study Halsted’s principle of including the submucosal layer in the bowel closure is much more important in intestinal healing than is Lembert’s dictum of serosa-to-serosa approximation.
REFERENCES 1.
2.
304
Dieffenbach, J. F., cited by Leonardo, R. A. History of Surgery. New York: Froben Press, 1943. P. 281. Halsted, W. S. Circular sutures of the intestines: An experimental study. Amer. J. Med. Sci. 94:436, 1887.
7,
JULY
3.
4.
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1967 Healey, J. E., Jr., Clark, R. L., Gallager, H. S., O’Neill. P.. and Sheena. K. S. The nonsuture repair of blood vessels. Ann. Surg. 155:817, 1962. Healey, J. E., Jr., McBride, C. M., and Gallager, H. S. Is serosa-to-serosa approximation necessary in intestinal anastomosis? Surg. Forum 15:297, 1964. Healey, J. E., Jr., and Moore, E. B. An anastomosing instrument for ductal repairs. Amer. .I. Surg. 109:689, 1965. Healey, J. E., Jr., Sheena, K. S., Gallager, H. S., and Clark, R. L. Bronchial closure following pneumonectomy utilizing a plastic adhesive. Ann. Surg. 159:172, 1964. Holloway, C. K., Roe, R. D., and Getzen, L. C. Exhibit, American College of Surgeons Meeting, Chicago, Illinois, Oct. 1964. Holloway, C. K. Personal communication, July, 1966. Knightly, J. J., Agostino, D., and Cliffton, E. Effect of fibronolysin and heparin on the formation of peritoneal adhesive. Surgery 52:250, 1962. Lembert, A. Memoire sur l’enteroraphie avec la Description dun Procede Nouveau pour Pratiquer cette Operation Chirurgicale. Report Gen. D’Anat. Physiol. Path. 2~100, 1826. Murphy, J. B. Cholecystointestinal, gastrointestinal, enterointestinal anastomosis and approximation without sutures. Med. Rec. N.Y. 42: 665, 1892. O’Neill, P., Healey, J. E., Jr., Clark, R. L., and Gallager, H. S. Nonsuture intestinal anastomosis. Amer. J. Surg. 104:761, 1962. 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: Longman, 1812. Pp. 132-134.