An Experimental Evaluation of Suture Materials in the Anastomosis of the Esophagus in Growing Animals LOYD
R. H.
SCHULTZ, WILLIAM
M.D.,
CELIO RODRIQUES-PEREIRA,
CLATWORTHY,
JR.,
Tbis paper is an abridgement of tbe tbesis submitted by Dr. Loyd Schultz to tbe Faculty of tbe Graduate School, Obio State University in partial fulfillment of tbe requirements for tbe degree of Master of Science in Surgery. Supported by a grant from CHILD (Cbildren’s Hospital Investigative Laboratory Division.) NLY
Accepted
Columbus,
M.D.
AND
Ohio
tissue reaction to suture materia1. This study was undertaken to evaIuate the fifth factor in canine subjects. AIthough the structure of the canine and human esophagus is roughIy comparable, minor differences exist. In the dog, there are more striated circuIar and Iongitudinal muscIe fibers, and the submucosa contains fewer mucus gIands and eIastic fibers. The arteria1 bIood suppIy of the dog’s esophagus, as described by Saint [8], corresponds to that of a human being.
twenty-three years ago esophagea1 atresia with trachea-esophagea1 fistma was a uniformIy fata congenita1 anomaIy. In 1939 Leven [I] and Ladd [2] independently reported a patient surviva1 using a staged operation in which the trachea-esophagea1 fistuIa was divided, and a cervica1 esophagostomy and a gastrostomy were created. Later an antethoracic reconstruction of the esophagus was completed. The first successfu1 singIe stage Iigation of the Iistula and primary anastomosis of the esophagus was reported by Haight and TowsIey in 1943 [?I. Since then, the single stage operation has been the treatment of choice for the usual type of anomaIy observed in approximateIy 90 per cent of these infants in whom the proxima1 esophagus terminates bIindIy, and the lower segment opens into the trachea at or near the carina. SurvivaI using this method of treatment was reported to be 50.4 per cent in a series of I 13 patients reported by DeBoer and Potts [4] in 1957. More recently Minton and CIatworthy [5] reported a surviva1 rate of 73.5 per cent in forty-nine infants. The reported incidence of strictures folIowing end to end esophageal anastomosis for this condition varies between 35 and 50 per cent [6,7]. Factors which might contribute to the formation of strictures are: (I) tension on the suture line, (2) type of anastomosis, (3) fistuIa at the anastomosis, (4) infection and (5) host
0
M.D.,
EXPERIMENTAL
METHOD
Using a transpIeura1 approach through the fourth interspace, an 8 cm. segment of midthoracic esophagus was mobiIized in twentyfive puppies. These puppies weighed between three and six pounds each. The azygos vein was divided between Iigatures, and the vagus nerve was preserved. Potts-Smith-Gibson’s cIamps were pIaced across the esophagus proximaIIy and distally. A 3 cm. segment of esophagus was resected and a two Iayer end to end anastomosis, as described by Swenson and CIatworthy [9] was accompIished with minima1 tension in each case. The same method was used in each anima1 for the anastomosis except that five different suture materials were used. These were No. 5-o silk, cotton, Dacron@ and chromic catgut and No. 6-o wire. In order to minimize technical experience as a factor, one anima1 was operated on using each suture materia1 and the sequence then repeated. If an anima1 died from Ieakage through a fistuIa, another anima1 was operated on using the same materia1 for the anastomosis.
for publication
843
June 26, 1962. American
Journal
of Surgery,
Volume
log.
December
1962
SchuItz,
Rodriques-Pereira
and CIatworthy
FIG. I. Silicone rubber moId (SiIastic RTV 502~) of the esophagus one month after a chromic catgut anastomosis. There is a stricture of the anastomosis which corresponds to the narrow segment in the rubber mold. For this reason there were seven animaIs with a wire anastomosis, six with cotton and four each of siIk, Dacron and chromic catgut. There were four survivors with each suture materia1 studied. The intercosta1, thoracic muscIes and fascia were sutured with No. 4-0 chromic sutures. The skin was cIosed with subcuticuIar stitches to avoid the necessity of suture remova1. Thoracotomy tube drainage without suction was used for three hours then removed if there was no evidence of air Ieakage. The puppies were aIIowed water by mouth six hours after surgery and advanced to fuI1 feedings the foIIowing morning. Roentgenograms of barium esophageal swaIIows were taken at monthIy intervaIs. One anima1 with an anastomosis of each suture materia1 was sacrificed at one and two months. Two animaIs with each suture materia1 were observed for three months; at which time, the animaIs were sacrificed and an autopsy was performed on each. Prior to fixation of the esophagus for tissue sections, moIds were made using a siIicone eIastomer obtained through the cooperation of the Dow Corning Center for MedicaI Research. The basic component of this materia1 These is siIicone rubber (SiIastic@ RTV 502)*. moIds recorded the most minute detaiIs of the esophagea1 Iumen. (Fig. I.) The usua1 preparation technics were used * Dow Corning Corporation, MidIand, Michigan.
for tissue sections of the specimens obtained by sacrificing the animaIs. Parafined sIides were made of the esophagea1 anastomosis after fixation with IO per cent formaIin. These were stained by the hematoxyIin and eosin technic. The microscopic tissue reaction to suture materia1 was determined by a method simiIar to that used by Dettinger and Bowers [IO]. This method evaIuates the density of ceIIuIar infiItration around the suture and the width of the GbrobIastic tissue response. The predominant ceIIs around the suture were round ceIIs, pIasma ceIIs and foreign body giant ceIIs. These were graded between one (rare cells) and ten (dense ceIIuIar aggregates). (TabIe I.) TABLE AVERAGE
CELLULAR
I
RESPONSE
TO
SUTURES*
Time After ImpIantation
(Days)
Suture
Silk. ............. Cotton. .......... Dacron@. ......... Wire. ............ Chromic. ........
30
60
90
2.5 3.0 2.5
2.3 3.0
2.3 2.8
2.0
2.0
2.0
2.0
2.0
10.0
8.0
4.0
* Summary of average cellular response of the tissue to the suture materials used in this study. The most marked response was found to chromic catgut.
844
An Experimenta
EvaIuation
of Suture
FIG. 2. Roentgenogram ing a silk anastomosis.
MateriaIs
in Anastomosis
of Esophagus
in Animals
of barium fiNed esophagus one and two months followThere is narrowing at the suture lint with proximal
dilatation.
The width of fibrobIastic tissue reaction was measured in miIlimeters for each suture and the average of five measurements was obtained. (Table II.)
the immediate postoperative period. Two of these had been sutured with cotton and three with wire. In one anima1 of the four sutured with Silk. siIk, a stricture deveIoped. (Fig. 2.) No anastomotic leaks were noted. MicroscopicaIIy, the suture material was stiI1 visibIe ninety days after surgery, but fragmentation of the suture fibers by fibrobIastic ingrowth was present. Thirty days after surgery, the inflammatory ceI1 infiItration around the suture fragments consisted of moderate numbers of plasma ceIIs and large mononucIear phagocytes. Frequent foreign body giant ceIIs were observed. The inff ammatory ceI1 reaction decreased considerabIy sixty days after surgery, although the foreign body giant ceIIs persisted throughout the period of study. The zone of fibrosis
RESULTS
The resuIts of this study are summarized in TabIe III. Strictures were seen on the roentgenograms and confirmed by siIicone rubber moIds in four animaIs. One was sutured with siIk, one with cotton and two with chromic catgut. These strictures were associated with proxima1 diIatation of the esophagus in each case. A Ieak at the site of anastomosis developed in five of the twenty-five animals, and they died in TABLE WIDTH
OF
FIBROBLASTIC
II TISSUE
RESPONSE
Time After Implantation
(MM.)*
(Days)
TABLE SUMMAKT
Suture
OF
RESULTS
-
OF
III EXPERIMENTAL
I
STL’DY
Tissue Rcaction
30
60
Silk.
0.23
0.18
0.16
Cotton.
0.25
0.25
0.20
SiIk.
4
I
0
Moderate
Dacron
0.20
0.10
0. IO
6
I
2
Moderate
Wire.
0.20
Cotton.
0.20
0.10
Dacron
4
0
0
Slight
Chromic
0.45
0.45
0.40
Wire
7 4
0
3
Slight
90
Suture
Animals
Stricture
Fistula
-
__~~
Chromic.
* The average width of the fibroblastic tissue reaction in the esophagus to suture materia1 at thirty, sixty and ninety days.
TotaI..
__
Marked ._...__~_.
~~.
25 4
845
0
2 ___
5
-... ---
i
SchuItz,
Rodriques-Pereira
and
CIatworthy
FIG. 3. Esophagogram one, two and three months after surgery. Cotton was used in the anastomosis. The dilatation proximal to the stricture on the one month fiIm decreased on later films.
Dacron. No stricture nor fIstuIa deveIoped in any of these animaIs. Microscopic studies showed no absorption of the Dacron suture three months after impIantation. The ceIIuIar tissue reaction was sIight and onIy occasiona foreign body giant ceIIs were seen in the vicinity of the suture materia1. (Fig. 5.) The zone of fibrosis around the Dacron was narrow at each interva1 of study. Wire. Seven anastomoses were done with wire. There were three postoperative Ieaks and deaths. No strictures occurred in the four
around the suture was 0.23 mm. in width at thirty days, but decreased to 0.16 mm. by the ninetieth day. (TabIe II.) Cotton. Six esophagea1 anastomoses were done with cotton. Of these, a fistuIa at the suture Iine deveIoped in two of the dogs, and they died in the earIy postoperative period. One stricture occurred in the four survivors. tissue response to (Fig. 3.) The microscopic cotton sutures was simiIar to that observed from siIk. (TabIes I and II and Fig. 4.) Dacron. Four anastomoses were done with
FIG. 4. Cotton suture sixty days after impIantation in the esophagus. The suture is fragmented; there is a moderate infiltration of pIasma cells, Iymphocytes and foreign body giant ceIIs. The zone of fibrosis can be seen surrounding the suture fragments. (Hematoxylin and eosin stain, origina magnification x 100.)
846
An Experimenta
EvaIuation
of Suture
Materiak
in Anastomosis
of Esophagus
in AnimaIs
FIG. 5. Photomicrograph of a Dacron@ suture two mc)nths after implantation in the esophageal wall. There is a moderate infiltration of lymphocytes and macrophages around the suture m;lterixl. (liematosylin and cosin stain, original magnification X loo.)
visible thirty days after surgery. After that, the sutures were compIeteIy absorbed. ,4ppreciable leukocyte infiltration was seen around the suture fragments thirty days after surgery. nloderate numbers of plasma cells and large mononuclear phagocytes were also observed. This reaction continued to be prominent throughout the period of study. At three
survivors. The celIuIar and fIbrobIastic tissue response was similar to that of Dacron. (TabIes I and II.) Chromic Catgut. Four anastomoses were done using chromic catgut. In two of these animaIs strictures developed. (Fig. 6.) No postoperative fistula was noted. MicroscopicalIy, smaII fragments of chromic suture were
FIG. 6. Roentgenogram of barium fiIIed esophagus one and two months foIIowing a chromic catgut anastomosis. There is persistent narrowing at the anastomosis.
847
Schukz,
Rodriques-Pereira
months, the chromic sutures were the only ones studied which continued to show significant inffammatory ceI1 infiltration. (Table II.) Extensive fibrosis was observed around the anastomosis throughout the period of study. (Table III.) COMMENTS
Experience at the CoIumbus ChiIdren’s Hospita1 with infants who have esophagea1 atresia with trachea-esophagea1 fistuIa shows that symptomatic strictures frequentIy foIIow a singIe-stage primary anastomosis of the esoThis compIication is assophageal segments. ciated with significant morbidity and mortaIity. Of twenty-three children with postoperative strictures recentIy studied at this hospita1, five required a second resection of the anastomosis, and five died from aspiration pneumonia which was believed to be related to the stricture. Since the formation of a stricture at the site of an anastomosis is so serious, any method by which its incidence can be reduced is worth studying. AI1 sutures in use now produce tibroblastic tissue response and subsequent scarring. Sutures serve a single purpose: to hold tissues Sufficient unti1 heaIing produces together tensiIe strength to prevent wound separation. Once this point is reached, the idea1 suture wouId disappear. In the esophagus, high tensile strength and low tissue reaction to the suture are important. The suture materia1 must be easy to handle and the knot should not sIip. SiIk has been routineIy used at the CoIumbus ChiIdren’s Hospital as the suture material for esophageal anastomosis. Tissue sections through the anastomosis in those patients in whom a second resection was necessary, because of stricture, have shown considerabIe round ceII and foreign body giant ceI1 i&ration. This experimenta project was designed to test onIy the effect of suture materia1 on stricture formation of the esophagus. Other factors which contribute to stricture formation in cIinica1 cases were carefuIIy avoided. Excessive mobilization of the esophagus, tension on the suture line and infection were not evaIuated. The esophageal anastomosis was made on segments of equa1 thickness and diameter rather than segments of disproportionate size as found in infants with the common type of esophagea1 atresia and trachea-esophagea1 fistuIa. In these children, the anastomosis is
and CIatworthy more compIicated since the dista1 esophagus Iacks both the bIood suppIy and muscuIar hypertrophy found in the upper segment. Strictures developed in four animaIs; in one with siIk, one with cotton sutures and two with chromic catgut. Wire and Dacron produced the Ieast fibroblastic tissue response and no strictures. Both of these sutures have drawbacks, however. Wire is difficult to manage, especiaIIy deep in a surgica1 wound. The sharp cut. ends contribute to breaks in the sterile technic through penetration of surgica1 gIoves. The tendency of wire sutures to cut through tissue has been noted by Postlethwait et al. [I I]. These factors may have contributed to the high incidence of postoperative Ieakage from wire anastomoses in this study. Dacron sutures are easy to handle, but knot slippage is a major drawback. This can be minimized if three throws are used. Another hazard of Dacron is its potentia1 carcinogenic effect. Oppenheimer et al. [12] observed that in eight of forty-one animals mesenchyma1 sarcomas developed after impIantation of solid Dacron fibers and that in two of forty-two animals sarcomas deveIoped after perforated Dacron was implanted. While similar findings have not. been reported in human beings, this characteristic of Dacron mitigates against its use. SiIk and cotton produce more tissue response than Dacron or wire. Both of these materiaIs are easiIy manageable and have been widely used for esophageal anastomosis. Cotton sutures have a Iow initial tensiIe strength but gain IO to 30 per cent when wet. Their knot hoIding abiIity is Iess than siIk [I?]. In two of the six dogs in whom we used cotton, postoperative fistulas deveIoped and the dogs died. Chromic catgut produces considerabIe tissue response with early invasion of polymorphonucIear cells. The rate of absorption of chromic catgut has been shown to vary with the size of the suture. SmaIIer sutures are absorbed more slowIy than larger sutures because they produce a less-pronounced cellular response. Strictures deveIoped in two of the four puppies in whom chromic catgut was used. There were no postoperative fistuIae. SUMMARY
Postoperative strictures often foIIow primary end to end anastomosis of the esophagus for esophagea1 atresia and trachea-esophagea1 fistula. The purpose of this study was to evaIuate
An Experimenta
EvaIuation
of Suture
Materials
the tendency of different suture materiaIs to produce strictures of the esophagus in growing animaIs. A 3 cm. segment of esophagus was resected in twenty-five puppies. The esophagea1 continuity was re-established without tension using a two Iayer end to end anastomosis. Twenty of the animals survived. In the surviving animals, four anastomoses were performed using each of the foIIowing sutures: silk, cotton, chromic catgut, Dacron and wire. Each anastomosis was studied by serial roentgenograms, by siIicone rubber moIds of the esophagus and by microscopic tissue sections. The five deaths were caused by Ieakage at the site of anastomosis. Three of these Ieaks occurred when wire was used and two when cotton was used. The roentgenograms and rubber moIds showed four strictures of the esophagus. Two of these occurred with the catgut, one with silk and one with cotton. No strictures occurred with Dacron or wire. Microscopic sections of the anastomosis showed the tissue response to be greatest to chromic catgut, Iess to silk and cotton and the least to Dacron and wire. This experimenta study was too small to make any conclusions. The resuIts suggest that wire and chromic catgut are unsatisfactory suture materiaIs for esophagea1 anastomosis in growing animals.
in Anastomosis
2.
3.
4.
5.
6.
7.
8. g.
of Esophagus
in Animals
cessfut extrapleural Iigation of fistuIous communication and cervica1 esophagostomy. J. Tboracic Surg., 10: 648, 1941. LADD, W. E. The surgica1 treatment of esophageal atresia with trachea-esophageal flstula. New Englund J. Med., 230: 626, 1944. HAIGIIT, C. and TOWSLEY, II. A. Congenital atresia of the esophagus with trachcoesophageal tistula. Extraoleural ligation of fistula and endto-end anastomosis of esophagea1 segments. Surg. Gynec. ~7 Obst., 76: 672, 1943. DEBOER, A. and POTTS, W. J. CongenitaI atrcsia of the esophagus with tracheoesophageal listula. Surg. Gynec.
1949. IO. DETTI~GER, G. B. and BOWERS, W. F. Tissue rcsponse to orIon and dacron sutures. Surgery, 42: 325. ‘957. I I. POSTLETHWAIT. R. W.. SCHAUBLE. J. F.. DILLION. M. L. and MORGAN,‘J. An evaldation bf surgical suture material. Surg. Gynec. cv Obst., 108: 555, 1959. 12. OPPENIIEIMER, B. S., OPPENHEIMER, E. T., DANISHEFSKY, I., STOUT, A. P. and &RICH, F. R. Further studies of polymers as carcinogenic agents in animals. Cancer Res., 15: 333, 1955. 13. NARAT, J. K., CANGELOSI, J. P. and BELMONTE, J. V. EvaIuation of Dacron suture for general surgery. S. Forum, 7: 176, 1957.
REFERENCES
I. LEVEN, N. L. Congenital atresia of the esophagus with trachea-esophagea1 fistuta. Report of suc-
849