Esophagogastrostomy in the Treatment of Carcinoma of the Distal Two-Thirds of the Esophagus

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1 Esophagogastrostomy in the Treatment of Carcinoma of the Distal Two-Thirds of the Esophagus Clinical Experience and Operative Methods R. Darryl Fisher, M.D., Robert K. Brawley, M.D., and Richard F. Kieffer, M.D. ABSTRACT Between 1955 and 1971, esophagogastrostomy was used as the primary form of therapy for carcinoma of the distal two-thirds of the esophagus in 31 patients. The operation has provided effective palliation in this group of patients, most of whom were incurable at the time of operation. Postoperative mortality and morbidity were relative1 low following this single-stage procedure, and dysphagia was completely relievedyin all but 2 of the patients who survived o eration. A modified technique for fixation of the gastric fundus within the Jest and for construction of the esophagogastric anastomosis has consistently prevented gastroesophageal reflux. R elief of esophageal obstruction is the primary consideration in managing patients with esophageal carcinoma. Most of these patients are incurable because of invasion of contiguous vital structures or metastases to mediastinal or celiac lymph nodes [7], and treatment of any type usually does not prolong life. Therapy therefore should relieve pain and dysphagia and make the patient comfortable during his remaining days. In addition, the treatment should be simple and expeditious. The surgical treatment of esophageal neoplasms received great impetus more than twenty-five years ago when several surgeons initially described the technique of esophagogastrostomy [l, 11, 131. More recently, a variety of treatment modalities has been advocated ranging from radiotherapy or esophagectomy alone to combined irradiation and operation [3-5, 7, 14-16, 201. In our experience, esophagogastrostomy has proved to be the most satisfactory treatment for carcinoma of the distal esophagus, since the tumor is removed and the dysphagia relieved in a single operation. Moreover, hospitalization has usually been brief, and associated mortality and morbidity have been relatively low. Dysphagia has rarely recurred in these patients, and gastroesophageal reflux has not been observed. From the Departments of Surgery, The Johns Hopkins University School of Medicine and the Loch Raven Veterans Administration Hospital, Baltimore, Md. Supported in part by National Institutes of Health Training Grant 5 TO1 GM Accepted for publication May 16, Address reprint requests to Dr. Fisher, Department of Surgery, The Johns Hopkins Hospital, Baltimore, Md THE ANNALS OF THORACIC SURGERY

2 Carcinoma of the Esophagus The absence of gastroesophageal reflux in the present series of patients is attributed to a modified technique for fixation of the gastric fundus within the chest and for construction of the esophagogastric anastomosis. Several other aspects of management have been refined and adapted as the results of the operation have been evaluated. Our experience with and technique for esophagogastrostomy in the treatment of carcinoma of the distal two-thirds of the esophagus is detailed in this report. Clinical Material Between 1955 and 1971 at the Loch Raven Veterans Administration Hospital in Baltimore, esophagogastrostomy was used in 31 patients as the primary form of therapy for carcinoma of the distal two-thirds of the esophagus. All the patients were men ranging in age from 39 to 76 years. All had dysphagia, and weight loss varied from 10 to 60 pounds. Regurgitation of saliva and vomiting of solid food were distressing symptoms in each man. More than three-quarters of the patients had moderate to severe pain that occasionally necessitated narcotics for relief. The duration of symptoms before the diagnosis was established ranged from two to twelve months. Many patients had tolerated the chest discomfort or pain until it was quite severe, but the onset of dysphagia always caused them to seek medical advice soon. Roentgenographic examination of the barium-filled esophagus was virtually diagnostic in all patients. The characteristic esophageal narrowing seen in the esophagograms is illustrated in Figure 1A. Nevertheless, all patients underwent preoperative esophagoscopy, and in most, this procedure was combined with bronchoscopy to assess the trachea and main bronchi for signs of tumor invasion, fixation, or extrinsic compression. Biopsy of the intraluminal mass established the tumor histology in each patient prior to operation. Squamous carcinoma was found in 28 patients, adenocarcinoma in 3. Operative Met hods Retained food and secretions were removed from the esophagus prior to operation in those patients who had severe obstruction. The esophagus proximal to the obstruction was lavaged and aspirated the evening before operation and immediately prior to induction of anesthesia. Neomycin was then instilled in the proximal esophageal segment in an effort to reduce the bacterial count within the obstructed esophagus. The colon was usually prepared with enemas and nonabsorbable antibiotics in the event that colon interposition or bypass was required. Except for lesions located at the esophagogastric junction, for which a left thoracic or thoracoabdominal approach may be desirable, we prefer a right anterolateral thoracotomy and an upper midline incision for esophago- VOL. 14, NO. 6, DECEMBER,

3 FISHER, BRAWLEY, AND KIEFFER A FIG. 1. Preoperative esophagogram (A) from a patient who had nearly complete occlusion of the esophageal lumen from carcinoma; the obstructing mass is indicated by the arrow. A postoperative barium contrast study (B) was obtained in the same patient two weeks after operation; the esophagogastric anastomosis is marked by the arrow. At this early postoperative time, the previously obstructed proximal esophagus remains slightly dilated but is unobstructed. B gastrostomy. Often it is convenient and efficient for two operating teams to work simultaneously. The patient is placed supine with the right side elevated 30 degrees by cushions positioned beneath the right shoulder and hip (Fig. 2, inset). The right arm is padded and secured to the transverse bar of the anesthesiologist s screen. Braces are applied to the patient on both sides to permit free lateral rotation of the table and so facilitate exposure of each operative field. The neck, entire chest, and abdomen are prepared and included in the operative field. A long anterolateral incision is made in the fourth intercostal space from the sternum to the posterior axillary line. The internal mammary vessels are ligated and divided. Additional exposure can be obtained by excising a segment of the third and sometimes the fourth costal cartilage close to the sternum. The right lung is displaced medially and anteriorly (Fig. 2). The tumor is located, and its mobility and the presence of enlarged nodes in the mediastinum are assessed. On the basis of these findings it can be determined whether the lesion is resectable and possibly curable, resectable but incurable, or unresectable. The posterior trachea, proximal main bronchus, aorta, and pulmonary veins were the most common sites for local extension in this series. Submucosal extension of the tumor for long distances along the esophageal lumen has rarely been observed in our experience. The abdominal exploration is performed simultaneously by the second operating team. Fixation of the intraabdominal esophagus, gastroesophageal 660 THE ANNALS OF THORACIC SURGERY

4 Carcinoma of the Esophagus Division azygos v / Mediastinal pleura incised FIG. 2. A right anterolateral thoracotomy incision in the fourth intercostal space with the thorax rotated 30 degrees (inset) provides access to the posterior mediastinum. Assessment of the extent of invasion of contiguous structures and the possibility of complete removal of the tumor are primary considerations in the initial stage of the procedure. junction, or stomach by the tumor or by enlarged celiac nodes is usually an indication for colon interposition. The greater and lesser gastric curvatures are mobilized, preserving the right gastric artery and the gastroepiploic arcade (Fig. 3). It is often helpful to increase the mobility of the stomach by a Kocher maneuver, which allows the proximal duodenum to be displaced medially and upward. Pyloroplasty or pyloromyotomy may be performed, but we have preferred not to incise the pylorus, which is really a narrow vascular pedicle upon which the blood supply of the mobilized stomach depends. Instead, we have dilated the pylorus digitally by vigorously invaginating the anterior walls of the stomach and duodenum. After this procedure the pylorus becomes patulous. Gastric retention has occurred during VOL. 14, NO. 6, DECEMBER,

5 FISHER, BRAWLEY, AND KIEFFER G L li FIG. 3. The stomach and esophagogastric junction are exposed through a midline laparotomy incision (inset). The stomach is mobilized by dividing its ligamentous attachments from the esophageal hiatus to the pylorus with preseruation of the right gastric artery and the gastroepiploic arcade. Retraction of the left lobe of the liver after division of its triangular ligament facilitates exposure of the esophageal hiatus. the postoperative period in only 1 of our patients. In this man, the obstruction was caused by a large tumor containing celiac lymph nodes. While the gastric mobilization is being performed, the team operating in the chest has dissected the esophagus from its mediastinal attachments. The azygos vein is divided to improve exposure of the mediastinum. The mediastinum is entered through a longitudinal incision in the mediastinal pleura from the apex of the chest to the diaphragm. Mediastinal node metastases or invasion of contiguous structures such as the vertebrae, aorta, trachea, bronchus, or pulmonary veins becomes readily apparent after the mediastinal pleura is incised. If en bloc removal of the tumor and involved structures is 662 THE ANNALS OF THORACIC SURGERY

6 Carcinoma of the Esophagus not possible, blunt and sharp dissection through the tumor and around the vital structures is performed; the electrocautery is particularly useful when it is necessary to cut through a locally invasive tumor. Removal of the tumor bulk in these incurable esophageal carcinomas has not significantly prolonged the operation or added to the postoperative mortality or morbidity. Following removal of the bulk of the tumor, symptoms of chest pain and discomfort have been relieved in most of these patients. One must be careful during retraction of the lung to avoid excess pressure upon the mediastinum, because venous return can be compromised and severe systemic hypotension can develop. When exposure is difficult, the right main bronchus can be mobilized and then occluded with an atraumatic vascular clamp, permitting the lung to collapse. The anesthesiologist can then ventilate the opposite lung without interfering with exposure. Secretions must be aspirated from the previously occluded bronchus upon release of the clamp. If difficulty in exposing the posterior mediastinum is anticipated preoperatively, as in the case of an emphysematous patient, the use of a Carlens tube will allow selective collapse of the right lung and avoid the necessity of dissecting and clamping the right main bronchus. When mobilization of the esophagus is complete, the stomach is drawn through the hiatus (Fig. 4). The esophagogastric junction is divided, and the incision in the gastric fundus is closed with a double row of inverting sutures. The stomach is drawn to the apex of the pleural cavity so that the lesser curvature lies against the mediastinum. The fundus of the mobilized stomach is sutured to the prevertebral fascia behind and medial to the mobilized esophagus above the desired level of anastomosis. The lesser curvature is secured to the prevertebral fascia, and the greater curvature is fixed to the edge of the mediastinal pleura with sutures. These maneuvers prevent tension at the esophagogastric anastomosis, and the tubular fixation prevents gastric dilatation. When fixation of the stomach has been completed, the abdominal team attaches the wall of the stomach to the esophageal hiatus with interrupted sutures. The laparotomy incision is closed. Meanwhile, the esophagogastric anastomosis is performed. The site for the gastric stoma is the anterior wall of the gastric fundus 3 cm. below the uppermost portion of the stomach. With this method of anterior implantation of the esophagus, part of the gastric fundus lies posterior to the remaining distal esophageal segment (Fig. 5); dilatation of the uppermost portion of the gastric fundus, which may occur when the patient reclines, will occlude the esophageal segment anterior to the fundus. The posterior outer suture line of the anastomosis is first performed with interrupted Lembert sutures of 3-0 silk (Fig. 5A). The posterior half of the esophagus is divided, leaving a 1.0-cm. cuff distal to the first row of sutures. A transverse incision corresponding in size to the esophageal lumen is made in the anterior wall of the fundus. The inner posterior row of interrupted sutures is placed, with each suture passing through the full thickness of the walls of both the VOL. 14, NO. 6, DECEMBER,

7 664 THE ANNALS OF THORACIC SURGERY \

8 Carcinoma of the Esophagus Distal esoph. esoph., A. _- Ayt.f lap'zashioned longer \, than post. flap FIG. 5. A two-layer inverting anastomosis is used to construct the esophagogastric stoma. The posterior suture lines are completed before transection of the eso hagus (A). A 1.0-cm. anterior esophageal flap is tailored from the proximal esophagus d A second layer of Lembert sutures on the anterior aspect completes the anastomosis (C). FIG. 4. The esophagogastric junction is closed with inverting sutures, and the mobilized stomach is drawn into the chest through the esophageal hiatus. The right bronchus has been occluded with an atraumatic clamp to allow collapse of the right lung and to improve operative exposure. The stomach is fixed to the fwevertebral fascia high in the thorax and at several other points, to prevent tension at the anastomosis and to give the stomach a tubular configuration which prevents gastric dilatation. The site of the esophagogastric stoma is on the anterior wall of the fundus 3.0 cm. below the tip of the fundus, and not in the uppermost portion of the gastric fundus. VOL. 14, NO. 6, DECEMBER,

9 FISHER, BRAWLEY, AND KIEFFER stomach and the esophagus. At this point the esophagus is transected and the specimen removed. Because of the placement of this anastomosis on the anterior gastric wall, it is important for the esophagus to be divided in such a way that an anterior flap 1.0 cm. longer than the posterior flap is created. The inner row of the anastomosis is completed with interrupted sutures, placed so as to allow the knots to lie within the lumen (Fig. 5B). Just prior to the completion of this row, a nasogastric tube is advanced through the anastomosis into the stomach. An outer row of interrupted Lembert sutures completes the anastomosis (Fig. 5C). A single chest tube is placed, and the intercostal incision is closed in the usual manner. Results All 31 patients survived the operation. Each procedure required four to five hours of anesthesia time, and blood loss was usually less than 2 units. Two patients died in the immediate postoperative period. One died on the fourth postoperative day of overwhelming staphylococcal pneumonia; the other patient died suddenly on the eleventh postoperative day after he aspirated a large quantity of secretions and food that had been entrapped in a redundant intrathoracic segment of stomach. This patient had been operated upon early in the series, before the importance of developing the intrathoracic stomach into a tubular organ was recognized. Another factor contributing to gastric retention in this patient was a large mass of tumor containing celiac nodes. It was not recognized at operation that these nodes were compressing the pylorus after the mobilized stomach had been drawn into the chest. Two other patients died prior to discharge from the hospital. One died ten weeks after operation from a rapidly progressive, undifferentiated carcinoma and widespread metastases. The other death was a result of the only leak that occurred in the group. This leak was not located at the anastomosis, but in the gastric wall at the site of one of the sutures that had been used to attach the greater curvature to the posterior parietal pleura. For this reason, special care must be taken not to place these sutures too deep nor to tie them too tight. Twenty-seven of the 31 patients were discharged from the hospital. Hospitalization in these patients ranged from 14 to 40 days and averaged 25 days. At this writing, 7 of the 31 patients are alive six to twenty-four months after operation. The length of survival in the 24 patients who have died since operation is shown in Figure 6. Five of the 24 patients lived two years or more following their operation, and 1 patient survived five years before dying of distant metastases. The patients were usually able to swallow within 3 or 4 days after operation. By the end of the second postoperative week, most were eating a soft diet. Dysphagia was completely relieved in all but 2 patients. One 666 THE ANNALS OF THORACIC SURGERY

10 Carcinoma of the Esophagus NUMBER PATIENTS ALIVE MONTHS FOLLOWING OPERATION FIG. 6. Length of postoperative suruival following esophagogastrostomy. Seven of the 31 patients are currently surviving six to twenty-four months postoperatively. The graph indicates the suruival rates during the first two postoperative years for the 24 patients who have died since operat ion. required several esophageal dilations in the early postoperative period because the anastomosis had been narrowly constructed. In the other patient, recurrent tumor at the diaphragmatic esophageal hiatus caused dysphagia to reappear in the period immediately prior to his death. Symptoms of gastroesophageal reflux did not occur in any patient. In fact, several patients have described an inability to belch following construction of an esophagogastric anastomosis in this manner. Roentgenographic examination of the anastomosis and intrathoracic stomach was performed in each patient. A typical postoperative barium contrast study is illustrated in Figure 7, which shows the tubular stomach closely resembling a normal A B FIG. 7. Postoperative barium contrast study six weeks after operation showing the esophagogastric anastomosis and intrathoracic stomach. The arrows and metal clips mark the anastomosis. The functioning anastomosis and the tubular form of the intrathoracic stomach are apparent in the anteroposterior (A) and left anterior oblique IB) projections. VOL. 14, NO. 6, DECEMBER, 197' 667

11 FISHER, BRAWLEY, AND KIEFFER esophagus. Attempts to demonstrate esophageal reflux by various maneuvers during fluoroscopy were unsuccessful in all patients. Comment The surgical management of carcinoma of the distal two-thirds of the esophagus has frequently been described as disappointing and difficult because of the very low resectability rate and the rather dismal prospects for long-term cure of malignancies in this area. If one accepts the idea that most patients with carcinoma of the esophagus are incurable at the time of diagnosis [5-71, decisions concerning their management may then be based upon selection of appropriate forms of palliation. Irradiation in the treatment of carcinoma of the esophagus is not innocuous. Erosion of the esophagus, bleeding, persistence of pain, and mucositis are complications of radiotherapy for these tumors. Also, this form of therapy is not particularly suitable for the annular, obstructing lesions which constitute the bulk of esophageal cancers, since effective relief of obstruction cannot be reliably obtained. The length of time required for the completion of radiotherapy often exceeds the period required for recovery from esophagogastrostomy [ZO] and seriously shortens the period of palliation for these incurable patients. However, irradiation often provides effective palliation in patients with esophageal tumors that have not progressed to complete occlusion of the esophageal lumen, especially if there is no circumferential involvement of the esophageal wall. We believe that even in these patients, irradiation should be employed as primary therapy only when cure is precluded by the extent or spread of the tumor or when operation is contraindicated by the patient s condition. Placement of intraluminal tubes through the obstructing tumor mass does have a place in the palliation of the poor-risk patient. However, numerous complications have been reported with the use of such tubes [5, 61; the tubes can produce pressure necrosis of the esophagus, they can result in infection and obstruction, or the tube can migrate beyond the area of obstruction. Colon interposition is an operative procedure of greater magnitude than esophagogastrostomy and requires longer time and two additional intestinal anastomoses. Thus, we do not employ colon interposition unless it is technically impossible to perform an esophagogastrostomy, a rather unusual circumstance. The main advantage of esophagogastrostomy is the fact that it relieves symptoms of esophageal obstruction in a single-stage operation that can be performed with a relatively low operative mortality in these high-risk patients. The operation can be modified to include resection of all the tumor mass if the tumor appears at operation to be contained within the esophagus and there are no intraabdominal metastases. In our experience, removal of 668 THE ANNALS OF THORACIC SURGERY

12 Carcinoma of the Esophagus surrounding tumor that has invaded the less important mediastinal structures has not increased the mortality or morbidity, nor does it significantly extend the duration of the operation. Also, dysphagia can be eliminated and satisfactory palliation accomplished even in patients in whom it is necessary to leave residual tumor because of invasion of vital structures. Almost immediate relief of esophageal obstruction can be anticipated following this procedure, so that by the fourth or fifth postoperative day the patient can swallow liquids with ease and by the end of the second postopera tive week he can tolerate a soft diet well. One objection to esophagogastrostomy has been the reportedly high incidence of reflux of gastric contents across the anastomosis with subsequent development of esophagitis [9, 10, 191. In this series, symptoms of esophageal reflux have not occurred, nor could any discomfort associated with deglutition be elicited except in 2 patients with narrow anastomoses who complained of mild dysphagia. Esophageal reflux was not demonstrated in any patient at the time of fluoroscopic examination in the early and late postoperative period. The absence of clinically detectable esophageal reflux in this series has been attributed to the technique used for construction of the gastroesophageal anastomosis and for fixation of the gastric fundus within the chest, since distention of the intrathoracic stomach by air will result in temporary occlusion of the esophagogastric anastomosis. Numerous variations of a valvular reconstruction of the esophagogastric anastomosis have been studied experimentally [Z, 181, and there have been reports of the successful clinical application of similar ideas for various esophageal lesions [8, 12, 171. Gastroesophageal reflux following esophagogastrostomy for carcinoma of the esophagus can present a distressing management problem if special attention is not given to the construction of the esophagogastric anastomosis. Esophagogastric reconstruction as performed in the patients in this series has prevented this problem. In summary, esophagogastrostomy has provided effective palliation for patients with carcinoma of the distal two-thirds of the esophagus. This type of treatment can be accomplished in a single stage, and postoperative hospitalization is relatively brief. Moreover, if the tumor is localized to the esophagus without invasion of contiguous structures, the operation can be performed for cure. In the present series, hospital mortality and morbidity have been relatively low and the almost immediate restoration of swallowing without esophageal reflux has been gratifying. References 1. Adams, W. E., and Phemister, D. B. Carcinoma of the lower thoracic esophagus: Report of a successful resection and esophagogastrostomy. J. Thorac. Surg. 7:621, Adler, R. H., Firme, C. N., and Lanigan, J. M. Valve mechanism to prevent gastroesophageal reflux and esophagitis. Surgery 44:63, VOL. 14, NO. 6, DECEMBER,

13 FISHER, BRAWLEY, AND KIEFFER 3. Belsey, R. Reconstruction of the esophagus with the left colon. J. Thorac. Cardiovasc. Surg. 49:33, Brooks, V. Right colon bypass for inoperable carcinoma of the esophagus. Br. J. Surg. 53:705, Burdette, W. J. Palliative operation for carcinoma of cervical and thoracic esophagus. Ann. Surg. 173:174, Duvoisin, G. E., Ellis, F. H., Jr., and Payne, W. S. The value of palliative prostheses in malignant lesions of the esophagus. Surg. Clin. North Am. 47: 827, Ellis, F. H., Jr., Jackson, R. C., Krueger, J. T., Moersch, H. J., Clagett, 0. T., and Gage, R. P. Carcinoma of the esophagus and cardia: Results of treatment 1946 to N. Engl. J. Med. 260:351, Flavell, G. The Oesophagus. Washington, D.C.: Butterworth, Pp Hanna, E. A., Harrison, A. W., and Derrick, J. R. Comparative function of visceral esophageal substitutes by cinefluoroscopy. Ann. Thorac. Surg. 3: 173, Hanna, E. A., Harrison, A. W., and Derrick, J. R. Long-term results of visceral esophageal substitutes. Ann. Thorac. Surg. 3: 11 1, Lewis, I. Surgical treatment of carcinoma of the esophagus with special reference to a new operation for growth of the middle third. Br. J. Surg. 34: 18, Lortat-Jacob, J. L., Maillard, J. N., and Fekete, F. Procedure to prevent reflux after esophagogastric resection: Experience with 17 patients. Surgery 50:600, Marshall, S. F. Carcinoma of esophagus. Surg. Clin. No& Am. 18:643, Nakayama, K., Orihata, H., and Yamaguchi, K. Surgical treatment combined with preoperative concentrated irradiation for esophageal cancer. Cancer 20:778, Parker, E. F., and Gregorie, H. B., Jr. Combined radiation and surgical treatment of carcinoma of the esophagus. Ann. Surg. 161:710, Parker, E. F., and Gregorie, H. B., Jr. Carcinoma of the esophagus. Curr. Probl. Surg. April, Pearson, F. G., Henderson, R. D., and Parrish, R. M. An operative technique for the control of reflux following esophagogastrostomy. J. Thorac. Cardiovasc. Surg. 58:668, Redo, S. F., Barnes, W. A., and Della Sierra, A. 0. Esophagogastrostomy without reflux utilizing submuscular tunnel into stomach. Ann. Surg. 151: 37, Ripley, H. R., Olsen, A. M., and Kirklin, J. W. Esophagitis after esophagogastric anastomosis. Surgery 32: 1, Watson, T. A. Radiation treatment of cancer of the esophagus. Surg. Gynecol. Obstet. 117:346, THE ANNALS OF THORACIC SURGERY

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