- Email: [email protected]
The use of circular myotomy to facilitate resection and end-to-end anastomosis of the esophagus
The use of circular myotomy to facilitate resection and end-to-end anastomosis of the esophagus An experimental study Segmental resection of the thoracic esophagus with end-to-end anastomosis carries a lower mortality rate than esophagogastrostomy or colon interposition. However, if more than a few centimeters is resected, the anastomosis fails because of tension. An experimental study is presented in which circular myotomy was utilized to reduce tension and thereby increase the amount of esophagus which could be resected successfully. Sixteen dogs were first subjected to end-to-end anastomosis without myotomy after resection of segments varying from 4 to 7 em. in length and comprising 20 to 40 per cent of the esophagus. In other dogs, circular myotomy was performed 3 em. proximal to the anastomosis after resection of 40 to 50 per cent of the esophagus. However, initial attempts failed because of ischemia leading to anastomotic breakdown. The myotomy interrupted important vessels running longitudinally in the deeper layers of the muscularis. Subsequently, we determined that partial circular myotomy afforded just as great a reduction in tension without compromising the blood supply. Our studies show that this technique permits successful resection of much longer segments than would otherwise be possible.
Jesada Muangsombut, M.D. (by invitation), John R. Hankins, M.D. (by invitation), G. Robert Mason, M.D., Ph.D., and Joseph S. McLaughlin, M.D., Baltimore, Md.
Restoration of the luminal continuity of the esophagus by end-to-end anastomosis can be performed successfully only when short segments of the esophagus are resected." 5, 7, s, 11, 16 If more than a few centimeters is resected, the anastomosis fails because of tension and necrosis at the anastomotic site. Livaditis;'? working with piglets, used the technique of circular myotomy to reduce tension and thereby facilitate endto-end anastomosis after segmental resection. With this technique he was able to perform primary anastomosis with 100 per cent From the Department of Surgery, Division of Thoracic and Cardiovascular Surgery, University of Maryland School of Medicine and Hospital, Baltimore, Md. Read at the Fifty-fourth Annual Meeting of The American Association for Thoracic Surgery, Las Vegas, Nevada,
April 22, 23, and 24, 1974.
522
success following resection of 36 per cent of the thoracic esophagus. As a preliminary step toward applying this technique in man, we wished to determine if circular myotomy would be as successful in dogs as it was found to be in piglets. An experimental study is presented in which circular myotomy was utilized to reduce tension and thereby increase the length of the dog esophagus which could be resected and still allow successful primary anastomosis. Material and methods Mongrel dogs weighing between 13 and 23 kilograms were used for these experiments. Intravenous Nembutal anesthesia was given in standard doses, an endotracheal tube was introduced, and positive-pressure ventilation was maintained with a Harvard
Volume 68
Circular myotomy
Number 4
523
October, 1974
respirator. A right thoracotomy through the sixth intercostal space was performed. The esophagus was mobilized over a length which was 5 to 6 em. longer than the segment to be resected. The vagus nerves were preserved. After resection of a segment of the desired length, noted in percentage of the total length for purposes of comparison, the approximation force required to bring the ends together was measured by dynamometers attached by stay sutures (Fig. 1). The dynamometers were aligned with the esophagus and the tension on each was adjusted until the readings were equal. The approximation force was measured again after the myotomy; in cases in which both proximal and distal myotomies were performed, the force was measured after each. Next, an end-to-end anastomosis was performed with interrupted 3-0 silk sutures in two rows-an inner mucosal row with the knots tied within the lumen and an outer row in the muscularis which inverted the first row. The chest was closed without drainage, with a small catheter in place to aspirate air after the deeper layers of the chest incision were approximated. Antibiotics were not administered. The dogs were allowed to drink water from the first postoperative day to the third and then milk and water from the third to the seventh days. Thereafter they were fed a soft diet until the tenth day, after which they were given regular kennel food. All dogs were observed when they were fed to see whether there was evidence of dysphagia. In 2 dogs barium swallows and cine-esophagograms were performed to evaluate esophageal morphology and function. All surviving animals were observed for a minimum of 1 month and in some cases for 2 to 3 months. Then they were put to death and autopsied. The esophagus was dissected out and examined thoroughly. The dogs that failed to survive were also subjected to a complete autopsy. The first 16 dogs served as control subjects to determine the length of esophagus that could be resected and still allow successful anastomosis. They were subjected to two-
350 400 450 500
/
oOsll----Dynamometer ose
001' OSE: ODE:
osz OOZ OSI
001 OS
Fig. 1. Measurement of the approximation force. Stay sutures were inserted through each end of the esophagus and connected to dynamometers. The ends were brought into apposition by traction on the dynamometers, and the tension was varied until the readings were equal. This reading was recorded as approximation force (in gram force).
layer, end-to-end anastomosis without myotomy, after resection of segments varying from 4 to 7 em. in length and comprising 20 to 40 per cent of the esophagus. Complete circular myotomy. Complete circumferential division of both muscle layers was performed in the proximal segment 2 to 3 em. from the resected end in 12 dogs. Partial circular myotomy (Fig. 2). Partial myotomy was performed by making a small transverse incision in the outer, longitudinal muscle layer at a level 3 em. above or be-
524
The Journol of Thoracic and Cardiovascular Surgery
Muangsombut et at.
9
o
8
Sunl... 6
5
,g o
z
4 3
2 1
o
3.
Fig. 3. Survival and mortality rates in the control group (base line).
12 10
Submucosal Plexus \
I: Fig. 2. Method of performing partial circular myotomy. 1, Esophagus after mobilization. 2, Injection of saline into the muscular layers of the esophagus. 3, The longitudinal muscle layer was transected by sharp dissection. 4, The circular muscle layer and the submucosal arterial network remain intact.
low the divided ends. The injection of a small amount of saline into the longitudinal and circular muscles allowed the muscle layers to be separated readily. The longitudinal layer was transected circumferentially. The vascular network could be seen through the circular muscle layer which was left intact. Usually a few bleeding vessels in the free edges of the divided longitudinal muscle required ligation with fine silk. Results Control group: 16 dogs (Fig. 3). Of the 9 animals in which less than a third of the esophagus was resected, 6 survived. Of 7 animals in which more than 33 per cent was
8
D
Survive
6
4
~ Dead
2
o 39-56 % Resection in % of Thorac.Esoph. Fig. 4. Results of myotomy Group I: Complete circular myotomy.
resected, only 3 survived. All nonsurviving animals died of anastomotic breakdown. Group I: Complete circular myotomy proximal to anastomosis (Fig. 4). The length resected varied from 39 to 56 per cent of the thoracic esophagus (mean 49 per cent). The reduction in approximation force varied from 23 to 50 per cent (mean 35 per cent). Only 2 of 12 dogs survived. Death occurred between the first and the fourth postoperative day and was caused by ischemic necrosis leading to anastomotic breakdown. The 2 survivors were healthy when they were put
Volume 68
to death, 39 and 65 days following the operation. A latex injection study of the arterial network in the esophageal wall indicated that complete circular myotomy interrupts the deep longitudinal vessels, which tend to adhere to the circular muscle layer. For this reason the technique for subsequent experiments was modified as previously described: myotomy of only the outer longitudinal layer was performed. Group II: Partial circular myotomy proximal to anastomosis (Fig. 5) . The resected length varied from 47 to 50 per cent of the thoracic esophagus (mean 49.5 per cent). The reduction in approximation force produced by partial myotomy varied from 28 to 50 per cent (mean 40 per cent). The difference between this value and the per cent reduction of approximation force in the group in which complete myotomy was performed was not significant. One of the 6 dogs in this group died from an anastomotic leak on the fourth postoperative day. The remaining 5 survived without complication. Group III: Partial circular myotomy distal to anastomosis (Fig. 5). The resected length varied from 44 to 50 per cent of the thoracic esophagus (mean 48 per cent). The approximation force was reduced by 25 to 60 per cent (mean 44 per cent). This value was not significantly different from the means of Groups I and II. Of the 6 dogs in this category, I died from aspiration on the second postoperative day. The remaining 5 were healthy when they were put to death. Group IV: Combined partial circular myotomy proximal and distal to anastomosis (Fig. 6). The resected length varied from 50 to 61 per cent (mean 56 per cent). The two myotomies combined afforded a reduction of tension varying from 43 to 83 per cent (mean 58 per cent). This was significantly greater (p < 0.01) than the reduction produced by either proximal or distal partial myotomy alone. In 3 of the 8 dogs the reduction in approximation force was measured after each myotomy. After proximal myotomy in these 3 dogs, the tension
525
Circular myotomy
Number 4 October, 1974
Proximal
6
Distal Survive
5
D
4 Ill)
0
~
z0
3
Dead
~
2
o Fig. 5. Results of myotomy Groups II and III: Partial circular myotomy (proximal and distal). 7
0
6
5
.gOIl 0
:z:
Survive
4
~
3
Dead
2 1 o
52-61X
Resection in X of Thoracic Esophaaus Fig. 6. Results of myotomy Group IV: Combined partial circular myotomy (proximal and distal).
was reduced by 12, 33, and 38 per cent, and after distal myotomy the tension was reduced by an additional 41, 20, and 25 per cent, respectively. Of the 8 dogs in this group, 2 died from anastomotic leaks on the third and fourth postoperative days. A third died from hemothorax within 24 hours of operation. The anastomosis in this animal was found to be intact at postmortem examination, and this dog is excluded from statistical analysis. The 2 animals that died from anastomotic leaks had resections of 52 and 56 per cent. The 5 long-term survivors were healthy and without dysphagia when they were put to death. In summary, of 9 animals in the control group having less than a third of the esoph-
The Journal of
526
Muangsombut et al.
Thoracic and Cardiovascular
Surgery
CD
CD Fig. 7. Canine esophagus at autopsy, 77 days after resection of 53 per cent of the thoracic esophagus and circular myotomy (proximal and distal) with end-to-end anastomosis. A, External aspect. B, Luminal aspect (bisected). There is no stricture or dilatation (arrows indicate the myotomy sites).
Table I. Results of circular myotomy of all types Resection of thoracic esophagus (per cent) Type of myotomy
No. of dogs
Range
Complete proximal Partial proximal Partial distal Partial proximal and distal
12 6 6 7
39-56 47-50 44-50 52-61
I
Reduction of approx. force (per cent)
Mean
Range
49 49.5 48 56
23-50 28-50 25-60 43-83
I
Mean
Death
35 40 44 57.9
10 1
I" 2
• Death from aspiration.
agus resected (mean 27 per cent) 6 or 67 per cent survived; by contrast, of the 19 dogs that had a partial myotomy in all groups, with an average of 51 per cent of the esophagus resected, 15 or 79 per cent survived (Table I). Thus myotomy allowed the length of esophagus resected to be increased from 27 to 51 per cent, with no significant difference in mortality rate (p > 0.1). Considering the 12 dogs which under-
went single myotomy, the reduction in approximation force afforded by myotomy was highly significant (p < 0.0001). However, no direct correlation could be shown between the per cent reduction of approximation force produced by the myotomy and the success or failure of the anastomosis. All dogs that survived were healthy when they were put to death. Examination of the esophagus at autopsy revealed a normal
Volume 68 Number 4
Circular myotomy
527
October, 1974
lumen lined with smooth mucosa (Fig. 7). There were no anastomotic strictures, nor was there any stricture, dilatation, or diverticular formation at the myotomy site. One dog each from Groups III and IV underwent cine-esophagography. In both animals this study showed a normally functioning esophagus with no stricture or dilatation at any point (Fig. 8). There was no significant delay of the peristaltic waves at the myotomy site. Discussion
End-to-end anastomosis of the esophagus after segmental resection can be performed successfully if there is minimal tension on the anastomosis and a good blood supply to both remaining ends.v- 15 Parker and Brockington" resected segments of the esophagus varying in length from 4 to 7 em. and performed end-to-end anastomosis in a series of 21 dogs. The average length resected was 5 ern. and comprised approximately 33 per cent of the esophagus. The mortality rate was 33 per cent. There did not appear to be any correlation between death and the length of esophagus resected. Swenson and Clatworthy'> performed resection and end-to-end anastomosis in 30 dogs. Their findings are somewhat at variance with those of Parker and Brockington, in that there were no deaths in animals in which less than 50 per cent of the thoracic esophagus was resected. Our own results are more in agreement with those of Parker and Brockington. However, we did find a definite positive correlation between extent of resection and the mortality rate from anastomotic breakdown. The mucosal layer of the esophagus is only loosely attached to the muscularis, thus permitting the elongation and changing of the position of the mucosal tube.!? The blood supply of the esophagus is located mainly in the submucosal layer. This submucosal vascular network is lax and tortuous and thereby adapts to changes in longitudinal dimension of the esophagus." Livaditis," working with piglets, performed complete circular esophageal myot-
Fig. 8. One frame from a cine-esophagogram 60 days after resection of 56 per cent of the thoracic esophagus and combined partial circular myotomy (proximal and distal) with end-to-end anastomosis. The lumen is normal, with no stricture or dilatation. The cine-esophagogram revealed normal peristaltic function.
omy to reduce tension at the anastomosis after segmental resection. His method of complete circular myotomy did not prove successful in dogs. Perhaps there is a species difference. In dogs the submucosal vascular plexus tends to adhere to the circular muscle layer and is destroyed or damaged by complete myotomy. Partial circular myotomy, in which only the longitudinal muscle layer is transected, preserves this submucosal vascular network and yet is as effective in reducing tension as is complete myotomy. These studies indicate no clinically appreciable esophageal dysfunction following myotomy and segmental resection. At autopsy there was no demonstrable stricture or dilatation at the myotomy sites, and cineesophagograms demonstrated no significant interference with esophageal peristalsis. Peristalsis is initiated in the central nervous system and is carried down by the vagus nerves, which were preserved in these experiments. The continuity of the muscularis of the esophagus is not necessary for peristaltic function.': 9 No reflux esophagitis was observed at autopsy in any of the dogs that were subjected to myotomy. Burford' con-
The Journal of
528
Muangsombut et al.
Thoracic and Cardiovascular Surgery
~ m
.. " " " I
SPECI MEN
I
1
.
" · "1
'
I
2
3
I
4
I
5
D ATE_
Fig. 9. A human cadaver esophagus injected with latex shows preservation of the submucosal arterial network after partial circular myotomy (arrows).
trasted the absence of reflux esophagitis after resection and end-to-end anastomosis with the high incidence of this complication after esophagogastrostomy. We plan to apply this work in man. A review of the literature has failed to disclose the use of circular myotomy in connection with resection and anastomosis of the esophagus in man. Davidson" used circumferential myotomy successfully to facilitate the repair of hiatus hernias in patients whose esophaguses were short due to reflux esophagitis. He was able to achieve slight elongation and relaxation of the esophagus. In this way, he was able to make reduction of the hernia easier and presumably the likelihood of recurrence less. Latex injection studies in two human cadavers revealed that the arterial network is located mainly in the submucosal layer (Fig. 9); this fact agrees with the findings of others. n, 12, 14, 17 Thus the human esophagus appears similar to that of the dog in this anatomic respect, and partial myotomy may be feasible. Partial circular myotomy may make it possible to perform successful anastomosis after resecting longer segments of the esophagus for benign strictures than has heretofore been possible. This procedure may prove useful in facilitating end-to-end anasto-
mosis in cases of esophageal atresia in which there is a long gap between the two ends. Lastly, myotomy may increase the applicability of palliative resection with end-to-end anastomosis for esophageal carcinoma in which lateral spread precludes curative resection. REFERENCES
2
3 4
5
6
7
8
Burford, T. H., Webb, W. R., and Ackerman, L.: Caustic Burns of the Esophagus and Their Surgical Management, Ann. Surg. 138: 453, 1953. Davidson, J. S.: Resection of Squamous Cell Carcinoma of the Oesophagus With End-toEnd Anastomosis, Br. J. Surg. 54: 63, 1967. Davidson, J. S.: Circumferential Oesophageal Myotomy, Br. J. Surg, 59: 938, 1972. Davenport, H. W.: Physiology of the Digestive Tract, ed. 3, Chicago, 1971, Year Book Medical Publishers, Inc. Gross, R. E.: Treatment of Short Stricture of the Esophagus by Partial Esophagectomy and End-to-End Esophageal Reconstruction, Surgery 23: 735, 1948. Herman, J. D., and Murugasu, J. J.: The Blood Supply of the Oesophagus in Relation to Oesophageal Surgery, Aust. N. Z. J. Surg. 35: 195, 1966. Hopkins, S. M., and Vandenberg, H. J.: Segmental Resection for Carcinoma of Esophagus, Arch. Surg, 96: 939, 1968. Kunkel, W. M., and Kunkel, P. A.: Resection of Carcinoma of the Mid-thoracic Esophagus
Volume 68 Number 4
Circular myotomy
529
October, 1974
With Primary Anastomosis, J. THORAC. SURG. 36: 49, 1958. 9 Livaditis, A., Bjorck, G., and Kangstrorn, L. E.: Esophageal Myectomy, Scand. J. Thorac. Cardiovasc. Surg. 3: 181, 1969. 10 Livaditis, A., Radberg, L., and Odensjo, G.: Esophageal End-to-End Anastomosis, Scand. J. Thorac, Cardiovasc. Surg. 6: 206, 1972. 11 Parker, E. F., and Brockington, W. S.: Esophageal Resection With End-to-End Anastomosis, Ann. Surg. 129: 588, 1949. 12 Potter, S. E., and Holyoke, E. A.: Observation on the Intrinsic Blood Supply of the Esophagus, Arch. Surg. 16: 944, 1950. 13 Swenson, 0., and Clatworthy, H. W., Jr.: Partial Esophagectomy With End-to-End Anastomosis in the Posterior Mediastinum, Bull. Am. ColI. Surg. 32: 235, 1947. 14 Swigart, L. L., Siekert, R. G., Hambley, W. C., and Anson, B. J.: The Esophageal Arteries, Surg. Gynecol. Obstet. 90: 234, 1950. 15 Shek, J. L., Prietto, C. A., Tuttle, W. M., and O'Brien, E. J.: An Experimental Study of the Blood Supply of the Esophagus and Its Relation to Esophageal Resection and Anastomosis, J. THORAC. CARDIOVASC. SURG. 19: 523, 1950. 16 Tuttle, W. M., and Day, J. C.: The Treatment of Short Esophageal Strictures by Resection and End-to-End Anastomosis, J. THoRAc. SURG. 19: 534, 1950. 17 Yeoh, G. S., and Cohen, Y.: Carcinoma of the Supra-aortic Part of the Thoracic Oesophagus, Aust. N. Z. J. Surg, 28: 18, 1959.
Discussion DR. CLEMENT A. HIEBERT Portland. Maine
This was a nice presentation of an attractive idea. It seems that in addition to facilitating resections of short segments of esophagus, a circular myotomy might also be useful when the lower esophageal sphincter cannot be lowered to the abdomen because of esophagitis. Several years ago we became interested in this problem. We used the opportunity afforded by resections of upper and mid-esophageal cancers to operate on the adjacent normal esophagus about to be discarded. We did circular and helical myotomies, and from this work have emerged three conclusions. First, it is necessary to divide the vagus nerves. Second, it is difficult to operate with precision on the back side of the esophagus. Third, and perhaps most important, the amount of potential slack in the inner lining of the human esophagus is somewhat less than that in the dog.
My question is this: How soon and exactly for what pathology can this attractive idea be translated from the animal laboratory to the operating room? DR. DAVID J. DUGAN Oakland, Calif.
I have had no experience in the laboratory for some time and I cannot reinforce my comments with any data. However, having dealt with thoracic and esophageal surgeries as a T-I surgeon for many years, I feel that this perhaps is one of the most important papers of the meeting. If this procedure can be applicable to man, the thoracic surgeon will certainly be helped with a problem which I feel is our greatest difficulty in general surgery. The cardiac surgeons have everything solved, and pulmonary surgery is pretty well established. However, judging from the character and the amount of discussion and papers today on general thoracic surgery, the esophagus is still a very difficult organ on which to operate. I want to congratulate the authors on their very fine presentation, and I hope the group from Baltimore will return with an application that we can use in the field. DR, McLAUGHLIN (Closing) We thank Drs. Hiebert and Dugan for their comments. In the late 1940's and early 1950's, Drs. Thomas Burford and Robert Gross, both past Presidents of this Association, described the technique of segmental resection and primary anastomosis of the human esophagus. Since that time, this technique has been used to resect short segments with success. It has been found that 2 cm. can be removed and primary anastomosis performed with consistency. However, with removal of between 2 and 4 cm., anastomotic breakdown begins to appear. Resecting more than 4 cm. makes the procedure hazardous, If breakdown occurs, the patient often is left with a condition more grave than the primary abnormality. Circular myotomy may add a new dimension in segmental resection. If only 1.5 em. can be gained proximally and distally, a total of 3 em. will be added to a safe resection and thereby will double the amount of esophagus safely removed. As noted in the paper, our present plans are to continue this work in cadavers and as a primary step in resection of the esophagus for cancer, the myotomy being resected after its potential and adequacy have been assessed. If these studies pan out, the technique will be applied to segmental resection in man.
Jesada Muangsombut, M.D. (by invitation), John R. Hankins, M.D. (by invitation), G. Robert Mason, M.D., Ph.D., and Joseph S. McLaughlin, M.D., Baltimore, Md.
Restoration of the luminal continuity of the esophagus by end-to-end anastomosis can be performed successfully only when short segments of the esophagus are resected." 5, 7, s, 11, 16 If more than a few centimeters is resected, the anastomosis fails because of tension and necrosis at the anastomotic site. Livaditis;'? working with piglets, used the technique of circular myotomy to reduce tension and thereby facilitate endto-end anastomosis after segmental resection. With this technique he was able to perform primary anastomosis with 100 per cent From the Department of Surgery, Division of Thoracic and Cardiovascular Surgery, University of Maryland School of Medicine and Hospital, Baltimore, Md. Read at the Fifty-fourth Annual Meeting of The American Association for Thoracic Surgery, Las Vegas, Nevada,
April 22, 23, and 24, 1974.
522
success following resection of 36 per cent of the thoracic esophagus. As a preliminary step toward applying this technique in man, we wished to determine if circular myotomy would be as successful in dogs as it was found to be in piglets. An experimental study is presented in which circular myotomy was utilized to reduce tension and thereby increase the length of the dog esophagus which could be resected and still allow successful primary anastomosis. Material and methods Mongrel dogs weighing between 13 and 23 kilograms were used for these experiments. Intravenous Nembutal anesthesia was given in standard doses, an endotracheal tube was introduced, and positive-pressure ventilation was maintained with a Harvard
Volume 68
Circular myotomy
Number 4
523
October, 1974
respirator. A right thoracotomy through the sixth intercostal space was performed. The esophagus was mobilized over a length which was 5 to 6 em. longer than the segment to be resected. The vagus nerves were preserved. After resection of a segment of the desired length, noted in percentage of the total length for purposes of comparison, the approximation force required to bring the ends together was measured by dynamometers attached by stay sutures (Fig. 1). The dynamometers were aligned with the esophagus and the tension on each was adjusted until the readings were equal. The approximation force was measured again after the myotomy; in cases in which both proximal and distal myotomies were performed, the force was measured after each. Next, an end-to-end anastomosis was performed with interrupted 3-0 silk sutures in two rows-an inner mucosal row with the knots tied within the lumen and an outer row in the muscularis which inverted the first row. The chest was closed without drainage, with a small catheter in place to aspirate air after the deeper layers of the chest incision were approximated. Antibiotics were not administered. The dogs were allowed to drink water from the first postoperative day to the third and then milk and water from the third to the seventh days. Thereafter they were fed a soft diet until the tenth day, after which they were given regular kennel food. All dogs were observed when they were fed to see whether there was evidence of dysphagia. In 2 dogs barium swallows and cine-esophagograms were performed to evaluate esophageal morphology and function. All surviving animals were observed for a minimum of 1 month and in some cases for 2 to 3 months. Then they were put to death and autopsied. The esophagus was dissected out and examined thoroughly. The dogs that failed to survive were also subjected to a complete autopsy. The first 16 dogs served as control subjects to determine the length of esophagus that could be resected and still allow successful anastomosis. They were subjected to two-
350 400 450 500
/
oOsll----Dynamometer ose
001' OSE: ODE:
osz OOZ OSI
001 OS
Fig. 1. Measurement of the approximation force. Stay sutures were inserted through each end of the esophagus and connected to dynamometers. The ends were brought into apposition by traction on the dynamometers, and the tension was varied until the readings were equal. This reading was recorded as approximation force (in gram force).
layer, end-to-end anastomosis without myotomy, after resection of segments varying from 4 to 7 em. in length and comprising 20 to 40 per cent of the esophagus. Complete circular myotomy. Complete circumferential division of both muscle layers was performed in the proximal segment 2 to 3 em. from the resected end in 12 dogs. Partial circular myotomy (Fig. 2). Partial myotomy was performed by making a small transverse incision in the outer, longitudinal muscle layer at a level 3 em. above or be-
524
The Journol of Thoracic and Cardiovascular Surgery
Muangsombut et at.
9
o
8
Sunl... 6
5
,g o
z
4 3
2 1
o
3.
Fig. 3. Survival and mortality rates in the control group (base line).
12 10
Submucosal Plexus \
I: Fig. 2. Method of performing partial circular myotomy. 1, Esophagus after mobilization. 2, Injection of saline into the muscular layers of the esophagus. 3, The longitudinal muscle layer was transected by sharp dissection. 4, The circular muscle layer and the submucosal arterial network remain intact.
low the divided ends. The injection of a small amount of saline into the longitudinal and circular muscles allowed the muscle layers to be separated readily. The longitudinal layer was transected circumferentially. The vascular network could be seen through the circular muscle layer which was left intact. Usually a few bleeding vessels in the free edges of the divided longitudinal muscle required ligation with fine silk. Results Control group: 16 dogs (Fig. 3). Of the 9 animals in which less than a third of the esophagus was resected, 6 survived. Of 7 animals in which more than 33 per cent was
8
D
Survive
6
4
~ Dead
2
o 39-56 % Resection in % of Thorac.Esoph. Fig. 4. Results of myotomy Group I: Complete circular myotomy.
resected, only 3 survived. All nonsurviving animals died of anastomotic breakdown. Group I: Complete circular myotomy proximal to anastomosis (Fig. 4). The length resected varied from 39 to 56 per cent of the thoracic esophagus (mean 49 per cent). The reduction in approximation force varied from 23 to 50 per cent (mean 35 per cent). Only 2 of 12 dogs survived. Death occurred between the first and the fourth postoperative day and was caused by ischemic necrosis leading to anastomotic breakdown. The 2 survivors were healthy when they were put
Volume 68
to death, 39 and 65 days following the operation. A latex injection study of the arterial network in the esophageal wall indicated that complete circular myotomy interrupts the deep longitudinal vessels, which tend to adhere to the circular muscle layer. For this reason the technique for subsequent experiments was modified as previously described: myotomy of only the outer longitudinal layer was performed. Group II: Partial circular myotomy proximal to anastomosis (Fig. 5) . The resected length varied from 47 to 50 per cent of the thoracic esophagus (mean 49.5 per cent). The reduction in approximation force produced by partial myotomy varied from 28 to 50 per cent (mean 40 per cent). The difference between this value and the per cent reduction of approximation force in the group in which complete myotomy was performed was not significant. One of the 6 dogs in this group died from an anastomotic leak on the fourth postoperative day. The remaining 5 survived without complication. Group III: Partial circular myotomy distal to anastomosis (Fig. 5). The resected length varied from 44 to 50 per cent of the thoracic esophagus (mean 48 per cent). The approximation force was reduced by 25 to 60 per cent (mean 44 per cent). This value was not significantly different from the means of Groups I and II. Of the 6 dogs in this category, I died from aspiration on the second postoperative day. The remaining 5 were healthy when they were put to death. Group IV: Combined partial circular myotomy proximal and distal to anastomosis (Fig. 6). The resected length varied from 50 to 61 per cent (mean 56 per cent). The two myotomies combined afforded a reduction of tension varying from 43 to 83 per cent (mean 58 per cent). This was significantly greater (p < 0.01) than the reduction produced by either proximal or distal partial myotomy alone. In 3 of the 8 dogs the reduction in approximation force was measured after each myotomy. After proximal myotomy in these 3 dogs, the tension
525
Circular myotomy
Number 4 October, 1974
Proximal
6
Distal Survive
5
D
4 Ill)
0
~
z0
3
Dead
~
2
o Fig. 5. Results of myotomy Groups II and III: Partial circular myotomy (proximal and distal). 7
0
6
5
.gOIl 0
:z:
Survive
4
~
3
Dead
2 1 o
52-61X
Resection in X of Thoracic Esophaaus Fig. 6. Results of myotomy Group IV: Combined partial circular myotomy (proximal and distal).
was reduced by 12, 33, and 38 per cent, and after distal myotomy the tension was reduced by an additional 41, 20, and 25 per cent, respectively. Of the 8 dogs in this group, 2 died from anastomotic leaks on the third and fourth postoperative days. A third died from hemothorax within 24 hours of operation. The anastomosis in this animal was found to be intact at postmortem examination, and this dog is excluded from statistical analysis. The 2 animals that died from anastomotic leaks had resections of 52 and 56 per cent. The 5 long-term survivors were healthy and without dysphagia when they were put to death. In summary, of 9 animals in the control group having less than a third of the esoph-
The Journal of
526
Muangsombut et al.
Thoracic and Cardiovascular
Surgery
CD
CD Fig. 7. Canine esophagus at autopsy, 77 days after resection of 53 per cent of the thoracic esophagus and circular myotomy (proximal and distal) with end-to-end anastomosis. A, External aspect. B, Luminal aspect (bisected). There is no stricture or dilatation (arrows indicate the myotomy sites).
Table I. Results of circular myotomy of all types Resection of thoracic esophagus (per cent) Type of myotomy
No. of dogs
Range
Complete proximal Partial proximal Partial distal Partial proximal and distal
12 6 6 7
39-56 47-50 44-50 52-61
I
Reduction of approx. force (per cent)
Mean
Range
49 49.5 48 56
23-50 28-50 25-60 43-83
I
Mean
Death
35 40 44 57.9
10 1
I" 2
• Death from aspiration.
agus resected (mean 27 per cent) 6 or 67 per cent survived; by contrast, of the 19 dogs that had a partial myotomy in all groups, with an average of 51 per cent of the esophagus resected, 15 or 79 per cent survived (Table I). Thus myotomy allowed the length of esophagus resected to be increased from 27 to 51 per cent, with no significant difference in mortality rate (p > 0.1). Considering the 12 dogs which under-
went single myotomy, the reduction in approximation force afforded by myotomy was highly significant (p < 0.0001). However, no direct correlation could be shown between the per cent reduction of approximation force produced by the myotomy and the success or failure of the anastomosis. All dogs that survived were healthy when they were put to death. Examination of the esophagus at autopsy revealed a normal
Volume 68 Number 4
Circular myotomy
527
October, 1974
lumen lined with smooth mucosa (Fig. 7). There were no anastomotic strictures, nor was there any stricture, dilatation, or diverticular formation at the myotomy site. One dog each from Groups III and IV underwent cine-esophagography. In both animals this study showed a normally functioning esophagus with no stricture or dilatation at any point (Fig. 8). There was no significant delay of the peristaltic waves at the myotomy site. Discussion
End-to-end anastomosis of the esophagus after segmental resection can be performed successfully if there is minimal tension on the anastomosis and a good blood supply to both remaining ends.v- 15 Parker and Brockington" resected segments of the esophagus varying in length from 4 to 7 em. and performed end-to-end anastomosis in a series of 21 dogs. The average length resected was 5 ern. and comprised approximately 33 per cent of the esophagus. The mortality rate was 33 per cent. There did not appear to be any correlation between death and the length of esophagus resected. Swenson and Clatworthy'> performed resection and end-to-end anastomosis in 30 dogs. Their findings are somewhat at variance with those of Parker and Brockington, in that there were no deaths in animals in which less than 50 per cent of the thoracic esophagus was resected. Our own results are more in agreement with those of Parker and Brockington. However, we did find a definite positive correlation between extent of resection and the mortality rate from anastomotic breakdown. The mucosal layer of the esophagus is only loosely attached to the muscularis, thus permitting the elongation and changing of the position of the mucosal tube.!? The blood supply of the esophagus is located mainly in the submucosal layer. This submucosal vascular network is lax and tortuous and thereby adapts to changes in longitudinal dimension of the esophagus." Livaditis," working with piglets, performed complete circular esophageal myot-
Fig. 8. One frame from a cine-esophagogram 60 days after resection of 56 per cent of the thoracic esophagus and combined partial circular myotomy (proximal and distal) with end-to-end anastomosis. The lumen is normal, with no stricture or dilatation. The cine-esophagogram revealed normal peristaltic function.
omy to reduce tension at the anastomosis after segmental resection. His method of complete circular myotomy did not prove successful in dogs. Perhaps there is a species difference. In dogs the submucosal vascular plexus tends to adhere to the circular muscle layer and is destroyed or damaged by complete myotomy. Partial circular myotomy, in which only the longitudinal muscle layer is transected, preserves this submucosal vascular network and yet is as effective in reducing tension as is complete myotomy. These studies indicate no clinically appreciable esophageal dysfunction following myotomy and segmental resection. At autopsy there was no demonstrable stricture or dilatation at the myotomy sites, and cineesophagograms demonstrated no significant interference with esophageal peristalsis. Peristalsis is initiated in the central nervous system and is carried down by the vagus nerves, which were preserved in these experiments. The continuity of the muscularis of the esophagus is not necessary for peristaltic function.': 9 No reflux esophagitis was observed at autopsy in any of the dogs that were subjected to myotomy. Burford' con-
The Journal of
528
Muangsombut et al.
Thoracic and Cardiovascular Surgery
~ m
.. " " " I
SPECI MEN
I
1
.
" · "1
'
I
2
3
I
4
I
5
D ATE_
Fig. 9. A human cadaver esophagus injected with latex shows preservation of the submucosal arterial network after partial circular myotomy (arrows).
trasted the absence of reflux esophagitis after resection and end-to-end anastomosis with the high incidence of this complication after esophagogastrostomy. We plan to apply this work in man. A review of the literature has failed to disclose the use of circular myotomy in connection with resection and anastomosis of the esophagus in man. Davidson" used circumferential myotomy successfully to facilitate the repair of hiatus hernias in patients whose esophaguses were short due to reflux esophagitis. He was able to achieve slight elongation and relaxation of the esophagus. In this way, he was able to make reduction of the hernia easier and presumably the likelihood of recurrence less. Latex injection studies in two human cadavers revealed that the arterial network is located mainly in the submucosal layer (Fig. 9); this fact agrees with the findings of others. n, 12, 14, 17 Thus the human esophagus appears similar to that of the dog in this anatomic respect, and partial myotomy may be feasible. Partial circular myotomy may make it possible to perform successful anastomosis after resecting longer segments of the esophagus for benign strictures than has heretofore been possible. This procedure may prove useful in facilitating end-to-end anasto-
mosis in cases of esophageal atresia in which there is a long gap between the two ends. Lastly, myotomy may increase the applicability of palliative resection with end-to-end anastomosis for esophageal carcinoma in which lateral spread precludes curative resection. REFERENCES
2
3 4
5
6
7
8
Burford, T. H., Webb, W. R., and Ackerman, L.: Caustic Burns of the Esophagus and Their Surgical Management, Ann. Surg. 138: 453, 1953. Davidson, J. S.: Resection of Squamous Cell Carcinoma of the Oesophagus With End-toEnd Anastomosis, Br. J. Surg. 54: 63, 1967. Davidson, J. S.: Circumferential Oesophageal Myotomy, Br. J. Surg, 59: 938, 1972. Davenport, H. W.: Physiology of the Digestive Tract, ed. 3, Chicago, 1971, Year Book Medical Publishers, Inc. Gross, R. E.: Treatment of Short Stricture of the Esophagus by Partial Esophagectomy and End-to-End Esophageal Reconstruction, Surgery 23: 735, 1948. Herman, J. D., and Murugasu, J. J.: The Blood Supply of the Oesophagus in Relation to Oesophageal Surgery, Aust. N. Z. J. Surg. 35: 195, 1966. Hopkins, S. M., and Vandenberg, H. J.: Segmental Resection for Carcinoma of Esophagus, Arch. Surg, 96: 939, 1968. Kunkel, W. M., and Kunkel, P. A.: Resection of Carcinoma of the Mid-thoracic Esophagus
Volume 68 Number 4
Circular myotomy
529
October, 1974
With Primary Anastomosis, J. THORAC. SURG. 36: 49, 1958. 9 Livaditis, A., Bjorck, G., and Kangstrorn, L. E.: Esophageal Myectomy, Scand. J. Thorac. Cardiovasc. Surg. 3: 181, 1969. 10 Livaditis, A., Radberg, L., and Odensjo, G.: Esophageal End-to-End Anastomosis, Scand. J. Thorac, Cardiovasc. Surg. 6: 206, 1972. 11 Parker, E. F., and Brockington, W. S.: Esophageal Resection With End-to-End Anastomosis, Ann. Surg. 129: 588, 1949. 12 Potter, S. E., and Holyoke, E. A.: Observation on the Intrinsic Blood Supply of the Esophagus, Arch. Surg. 16: 944, 1950. 13 Swenson, 0., and Clatworthy, H. W., Jr.: Partial Esophagectomy With End-to-End Anastomosis in the Posterior Mediastinum, Bull. Am. ColI. Surg. 32: 235, 1947. 14 Swigart, L. L., Siekert, R. G., Hambley, W. C., and Anson, B. J.: The Esophageal Arteries, Surg. Gynecol. Obstet. 90: 234, 1950. 15 Shek, J. L., Prietto, C. A., Tuttle, W. M., and O'Brien, E. J.: An Experimental Study of the Blood Supply of the Esophagus and Its Relation to Esophageal Resection and Anastomosis, J. THORAC. CARDIOVASC. SURG. 19: 523, 1950. 16 Tuttle, W. M., and Day, J. C.: The Treatment of Short Esophageal Strictures by Resection and End-to-End Anastomosis, J. THoRAc. SURG. 19: 534, 1950. 17 Yeoh, G. S., and Cohen, Y.: Carcinoma of the Supra-aortic Part of the Thoracic Oesophagus, Aust. N. Z. J. Surg, 28: 18, 1959.
Discussion DR. CLEMENT A. HIEBERT Portland. Maine
This was a nice presentation of an attractive idea. It seems that in addition to facilitating resections of short segments of esophagus, a circular myotomy might also be useful when the lower esophageal sphincter cannot be lowered to the abdomen because of esophagitis. Several years ago we became interested in this problem. We used the opportunity afforded by resections of upper and mid-esophageal cancers to operate on the adjacent normal esophagus about to be discarded. We did circular and helical myotomies, and from this work have emerged three conclusions. First, it is necessary to divide the vagus nerves. Second, it is difficult to operate with precision on the back side of the esophagus. Third, and perhaps most important, the amount of potential slack in the inner lining of the human esophagus is somewhat less than that in the dog.
My question is this: How soon and exactly for what pathology can this attractive idea be translated from the animal laboratory to the operating room? DR. DAVID J. DUGAN Oakland, Calif.
I have had no experience in the laboratory for some time and I cannot reinforce my comments with any data. However, having dealt with thoracic and esophageal surgeries as a T-I surgeon for many years, I feel that this perhaps is one of the most important papers of the meeting. If this procedure can be applicable to man, the thoracic surgeon will certainly be helped with a problem which I feel is our greatest difficulty in general surgery. The cardiac surgeons have everything solved, and pulmonary surgery is pretty well established. However, judging from the character and the amount of discussion and papers today on general thoracic surgery, the esophagus is still a very difficult organ on which to operate. I want to congratulate the authors on their very fine presentation, and I hope the group from Baltimore will return with an application that we can use in the field. DR, McLAUGHLIN (Closing) We thank Drs. Hiebert and Dugan for their comments. In the late 1940's and early 1950's, Drs. Thomas Burford and Robert Gross, both past Presidents of this Association, described the technique of segmental resection and primary anastomosis of the human esophagus. Since that time, this technique has been used to resect short segments with success. It has been found that 2 cm. can be removed and primary anastomosis performed with consistency. However, with removal of between 2 and 4 cm., anastomotic breakdown begins to appear. Resecting more than 4 cm. makes the procedure hazardous, If breakdown occurs, the patient often is left with a condition more grave than the primary abnormality. Circular myotomy may add a new dimension in segmental resection. If only 1.5 em. can be gained proximally and distally, a total of 3 em. will be added to a safe resection and thereby will double the amount of esophagus safely removed. As noted in the paper, our present plans are to continue this work in cadavers and as a primary step in resection of the esophagus for cancer, the myotomy being resected after its potential and adequacy have been assessed. If these studies pan out, the technique will be applied to segmental resection in man.