Improved Surgical Palliation of Advanced Carcinoma of the Esophagus Zwi Steiger, MD, Detroit, Michigan Warren 0. Nickel, MD, Detroit, Michigan Robert F. Wilson, MD, Detroit, Michigan Agustin Arbulu, MD, Detroit, Michigan
Far-advanced, obstructing carcinoma of the esophagus poses a challenging surgical problem. If not treated, it causes the patient a miserable existence until his death. It seems that in many institutions the fate of the patients with carcinoma of the esophagus is dismal [l-4]. In our institution the five year survival for carcinoma of the esophagus in the past fourteen years is 0.52 per cent (l/190). This may be a reflection of the patient population we encounter, because the patients we see with carcinoma of the esophagus have almost uniformly far-advanced disease when first seen. The resectability rate for cure in our institution in the past three years is only 1.8 per cent (l/55). The universal presenting complaint of our patients was dysphagia. The goal of any procedure for dysphagia should be restoration of the swallowing mechanism [3]. At present, we do not see any logic in extensive palliative resection to restore the swallowing mechanism. Also, our present concept in the treatment of far-advanced carcinoma of the esophagus is that it remains a surgical problem and is best treated by bypassing the lesion, using the stomach whenever possible [5]. We arrived at our present policy after reviewing our results between the years 1971 and 1973. In those three years we tried a variety of methods to achieve the goal of palliation of far-advanced carcinoma of the esophagus. Treatment of thirty-five patients with far-advanced carcinoma of the esophagus included gastrostomy and esophagostomy (10 patients), Celestin tube (8), colon bypass (2), palliative resection (8), and radiotherapy (7). In addition, six patients with surgical procedures and locally nonresectable lesions also had radiotherapy. The mortality rate at one month was 31.4 per cent (11/35), and only 51.4 per cent (18/35) lived three From tha Department of Sur&y. Wayne State UniversitySchool of Medicine, Detroit. and the Surgical Service, VA Hospital, Allen Park, Michigan. Reprint requests should be addressed to Zwi Steiger, MD, Chief, Thoracic Section, Surgical Service (112). VA Hospital, Allen Park, Michigan 48101.
782
months or longer. All of them were dead within eleven months after the diagnosis was made except for one patient who lived for fourteen months. He had palliative resection of an adenocarcinoma of the distal esophagus. The average survival of these patients was three and a half months. Many of these patients were not truly palliated after the operation or the radiotherapy. Since 1974 we have changed our approach in the treatment of advanced carcinoma of the esophagus. As mentioned, the principle is to leave the tumor with the esophagus in situ and bypass it using the stomach. The rationale is that when the lesion has extensive local invasion or the patient has distant metastases, then resection appears to be illogical and carries a high mortality. Material and Methods
Between 1974 and 1976 fifty-five patients underwent operation, of whom fifty-four (98.2 per cent) were considered to have a noncurable lesion. This series of fifty-four patients (52 male, 2 female; 28 black, 26 Caucasian) included those with lesions of the gastroesophageal junction. The disability is the same as for more cranial lesions in the esophagus and the aim at surgery is identical. This number of noncurable lesions is considerably higher than in most reported series (6,7]. Average age was 57.1 years (range, 39 to 83 years). Reasons for Nonresectability. There were thirty-one patients with extensive locally invasive lesions infiltrating the vertebrae or aorta or firmly attached to the bronchi without obvious invasion preoperatively. On barium swallow the extent of the lesion was from 7 to 12 cm. Twenty-four patients had metastatic nodes beyond the chest cavity, five patients had liver metastases, three patients had vagal and recurrent laryngeal nerve involvement, four patients had trachea- and bronchoesophageal fistulas, one patient had an esophagopleural fistula, eight patients had a previous full course of radiotherapy and, despite this, were unable to swallow, and two patients had bone metastases. Some of the groups were overlapping. Location of the Lesion. Two patients (3.7 per cent) had cervical lesions, ten (18.5 per cent) had upper third lesions,
The American Journal of Surgery
thirty-three (61.1 per cent) had middle third lesions, and nine (16.6 per cent) had lower third lesions. There were forty-seven squamous cell carcinomas, six adenocarcinomas, and one small cell carcinoma. Possible Etiologic Factors. Thirty-eight patients had a long history of alcoholism and smoking, two had achalasia, one had a long-standing lye stricture, five had previous pulmonary tuberculosis, and three had hiatal hernias, a disputed factor [8]. The specific preoperative workup consisted of barium swallow, esophagoscopy, and bronchoscopy. The preoperative preparation was usually brief and entailed hydration, occasional transfusion of blood, and a futile attempt to improve oral hygiene. Operative Technic. With the patient in the supine position, the abdomen was explored through an upper midline incision, celiac nodes were biopsied, and if possible the resectability of the tumor was assessed by palpating it through the incised right crus of the hiatus [3,9,10]. The presence of metastatic abdominal nodes and/or extensive local invasion by the tumor were indications for palliative bypass [6]. The stomach was mobilized by dividing the gastrocolic ligament, the short gastric vessels, and the left gastric vessels. The gastroepiploic and the right gastric vessels were carefully preserved. Pyloromyotomy or pyloroplasty was performed and the duodenum mobilized. When there were no metastases in the abdomen and the resectability of the lesion could not be properly assessed, then the abdomen was closed. The patient was then turned on his left side and the right chest prepared and entered through the bed of the fourth or fifth rib [II]. When the lesion was found to be nonresectable, the gastroesophageal junction was divided after pulling the freed stomach into the right chest. The divided ends were closed. The esophagus above the lesion was now freed, usually after division of the azygos vein. The esophagus was divided above the lesion and the distal end closed. The proximal end was anastomosed to the fundus of the stomach into an excised area measuring approximately 2 cm in diameter. The anastomosis was done with interrupted 4-O silk. The anastomosis was then wrapped around with stomach wall in an “inkwell” fashion [IL’]. In twenty-one patients the bypass was performed in this fashion in the right chest. Four patients had the bypass performed in the left chest. We entered the left chest because of previous right thoracotomy in two of these patients. The other two had lesions of the gastroesophageal junction. In twenty-eight patients, who had lesions obviously not resectable and lesions of the upper third of the esophagus, the following bypass technic was applied [13]: After mobilization of the stomach, the gastroesophageal junction was divided and both sides closed. A Foley catheter was inserted into the esophagus through an opening in the anterior wall and secured with a pursestring suture. The catheter was brought out in the right subcostal area. The cervical esophagus was then exposed and divided, closing the distal end. The left sternoclavicular junction was then exposed and resected. A retrosternal tunnel was
Volume 135. June 1979
developed and the isolated stomach passed through it into the neck. The fundus was anchored to the prevertebral fascia and an anastomosis performed between the esophagus and the fundus of the stomach using the same technic described previously. The abdomen and the neck were then closed. The Foley catheter, which was left in place, usually drained for two to three weeks and was then removed. (In 1 patient who had a previous partial gastrectomy, the right colon was used for the bypass.) In this technic, we stress the following points: (1) The supine position, which allows the stomach to be mobilized with ease and the right gastric and gastroepiploic vessels to be well preserved; this is considerably difficult in the lateral position into which the patient is positioned for a thoracoabdominal incision. (2) The sequential opening of the chest in the patients in whom the anastomosis was done in the chest [ll]; our patients were usually in poor physical condition, and opening of two cavities simultaneously was not tolerated well in our past experience. (3) No aggressive attempt was made to resect a nonresectable tumor. (4) The “inkwell” anastomosis seems to reinforce the anastomosis and prevents reflux [14].
Results Four patients (7.4 per cent) died within thirty days after the operation. One of the patients with vagal nerve involvement died three weeks after the operation because of aspiration. The second mortality was from an empyema. The barium swallow performed one week after the operation showed an intact anastomosis. The third patient had a stroke two weeks after the operation and died from a partial bowel obstruction in the fourth week after the operation. He refused surgery for the bowel obstruction. In the two patients with cervical lesions the operative result was not good. These patients had vagal nerve involvement. Also, the other patient with vagal nerve involvement had an unsatisfactory result. Despite healed anastomoses in all three, they had difficulty swallowing and they should not have undergone the operation. CompZications. (Table I. ) Anastomotic leaks occurred only in the patients who had cervical esophagogastrostomy. All the leaks healed within three weeks when the neck wound was drained and the patients were placed on hyperalimentation. In the patient who had a partial necrosis of the fundus, the anastomosis was taken down and esophagostomy and gastrostomy performed. The one month mortality in this group was 7.4 per cent compared with 31.4 per cent in the first group. The average survival was five months compared with three and a half months. The quality of survival is reflected in the 92 per cent (46/50) surviving patients who were able to assume
783
Steiger et al
TABLE I
Complications Comolication _ Anastomotic leak (in neck) Empvema Lung abscess Bronchopneumonia Wound infections Abdominal dehiscence Partial necrosis of fundus Tracheostomy Respiratory insufficiency Splenectomy Transient dumping Accidental pneumothorax Cerebrovascular accident Aspiration Total
Summary Number 6 2 1 3 9 1 1 2 3 8 10 6 1 1 1a/54 (33 %)
a near-normal diet soon after surgery. The reason for improvement in survival was attributed to the simplicity of the procedure. Futile attempts to resect the tumor were not made. When the bypass was performed in the chest, it was done in sequence [II]. The stomach was always mobilized with the patient in the most favorable position and the vascular supply never compromised. There is no need to anastomose the distal esophagus into the gastrointestinal tract. Comments
There is considerable controversy as to the optimal treatment of nonresectable, obstructing carcinoma of the esophagus. Esophagostomy-gastrostomy carries a small risk but is cumbersome for the patient to manage and many times only reluctantly accepted by the patient. Palliative intubation requires a change in diet. The gastroesophageal junction is made incompetent and patients tend to aspirate. The various tubes will get obstructed with food and overgrown tumor. The tubes may perforate and migrate. Use of colon requires three anastomoses, and a slight stretch on the mesentery may jeopardize the vascular supply. Radiotherapy is contraindicated in the patients with complicating fistulas. The treatment is relatively long for a patient who has a short life expectancy. The aim of restoring the ability to swallow is not always achieved. In our series eight patients received radiotherapy and could not swal1_._~
LOW.
We believe that a simple one-stage bypass of the esophagus using the stomach is an effective way of achieving palliation with an acceptable morbidity and mortality in a high risk patient group.
784
Fifty-four patients with far-advanced carcinoma of the esophagus were operated on between the years 1974 and 1976. No attempts were made to resect the lesion. The stomach was used fifty-three times to bypass the lesion and the right colon was used once. In twenty-eight patients the stomach was placed substernallv and the anastomosis was done in the neck. Twenty-five patients had the anastomosis to the esophagus done in the chest. The thirty day operative mortality was 7.4 per cent and the average survival was five months. These figures compared favorably with a group of thirty-five patients with far-advanced carcinoma of the esophagus seen between the years 1971 and 1973 and handled with a variety of modalities. In this group the thirty day mortality was 31.4 per cent (11/35) and the average surival was three and a half months. ”
References 1. Leon W, Strug LH, Brickman JD: Carcinoma of the esophagus-a disaster. Ann Thorac Surg, II: 583. 1971. 2. Lawler MR Jr, Gobbel WG, Killen DA, Daniel RA: Carcinoma of the esophagus. J Thorac Cardiovasc Surg 58: 609, 1969. 3. Plested WG, Tildon TT, Hughes RK: A philosophy of treatment of esophageal carcinoma. Am Surg 34: 650, 1968. 4. Proctor DSC: Carcinoma of the esophagus: a review of 523 cases. S Afr J Surg 6: 137, 1968. 5. Wilson SE, Plested WG, Carey JS: Esophagogastrectomyversus radiation therapy for midesophageal carcinoma. Ann Thorac Surg 10: 195, 1970. 6. Just-Viera JO, Silva JE: Esophageal carcinoma. Ann Thorac Surg 19: 688, 1975. 7. Gunnlangsson GH, Wychulis AR, Roland C, Ellis FH Jr: Analysis of the records of 1,657 patients with carcinoma of the esophagus and cardia of the stomach. Surg Gynecol Obstet 130: 997.1970. 8. Michel JO, Olsen AM, Docherty MB: The association of diaphragmatic hiatal hernia and gastroesophageal carcinoma. Surg Gynecol Obstet 124: 585, 1967. 9. MacManus JE: Combined left abdominal and right thoracic approach to resection of esophageal neoplasms. Surgery 24: 9, 1948. 10. Ong GB: Resection and reconstruction of the esophagus. Curr Probl Surg Chicago, Year Book Medical, September 1971, P 1. 11. Parker EF, Gregorie HB Jr: Carcinoma of the esophagus. Curr Probl Surg Chicago, Year Book Medical, April 1967, p 1. 12. Procter DSC: The “inkwell” anastomosis in esophageal reconstruction. S Afr Med J 41: 187, 1967. 13. Orringer MB, Sloan H: Substernal gastric bypass of the excluded thoracic esophagus for palliation of esophageal carcinoma. J Thorac Cardiovasc Surg 70: 836, 1975. 14. Pearson FG, Henderson RD. Parish RM: An operative technique for the control of reflux following esophagogastrostomy. J Thorac Cardiovasc Surg 58: 668, 1969. 15. Girardet RE, Ransdell HT. Wheat MW Jr: Palliative intubation in the management of esophageal carcinoma. Ann Thorac Surg ia:417, 1974.
The American Journal of Surgery
Far-advanced, obstructing carcinoma of the esophagus poses a challenging surgical problem. If not treated, it causes the patient a miserable existence until his death. It seems that in many institutions the fate of the patients with carcinoma of the esophagus is dismal [l-4]. In our institution the five year survival for carcinoma of the esophagus in the past fourteen years is 0.52 per cent (l/190). This may be a reflection of the patient population we encounter, because the patients we see with carcinoma of the esophagus have almost uniformly far-advanced disease when first seen. The resectability rate for cure in our institution in the past three years is only 1.8 per cent (l/55). The universal presenting complaint of our patients was dysphagia. The goal of any procedure for dysphagia should be restoration of the swallowing mechanism [3]. At present, we do not see any logic in extensive palliative resection to restore the swallowing mechanism. Also, our present concept in the treatment of far-advanced carcinoma of the esophagus is that it remains a surgical problem and is best treated by bypassing the lesion, using the stomach whenever possible [5]. We arrived at our present policy after reviewing our results between the years 1971 and 1973. In those three years we tried a variety of methods to achieve the goal of palliation of far-advanced carcinoma of the esophagus. Treatment of thirty-five patients with far-advanced carcinoma of the esophagus included gastrostomy and esophagostomy (10 patients), Celestin tube (8), colon bypass (2), palliative resection (8), and radiotherapy (7). In addition, six patients with surgical procedures and locally nonresectable lesions also had radiotherapy. The mortality rate at one month was 31.4 per cent (11/35), and only 51.4 per cent (18/35) lived three From tha Department of Sur&y. Wayne State UniversitySchool of Medicine, Detroit. and the Surgical Service, VA Hospital, Allen Park, Michigan. Reprint requests should be addressed to Zwi Steiger, MD, Chief, Thoracic Section, Surgical Service (112). VA Hospital, Allen Park, Michigan 48101.
782
months or longer. All of them were dead within eleven months after the diagnosis was made except for one patient who lived for fourteen months. He had palliative resection of an adenocarcinoma of the distal esophagus. The average survival of these patients was three and a half months. Many of these patients were not truly palliated after the operation or the radiotherapy. Since 1974 we have changed our approach in the treatment of advanced carcinoma of the esophagus. As mentioned, the principle is to leave the tumor with the esophagus in situ and bypass it using the stomach. The rationale is that when the lesion has extensive local invasion or the patient has distant metastases, then resection appears to be illogical and carries a high mortality. Material and Methods
Between 1974 and 1976 fifty-five patients underwent operation, of whom fifty-four (98.2 per cent) were considered to have a noncurable lesion. This series of fifty-four patients (52 male, 2 female; 28 black, 26 Caucasian) included those with lesions of the gastroesophageal junction. The disability is the same as for more cranial lesions in the esophagus and the aim at surgery is identical. This number of noncurable lesions is considerably higher than in most reported series (6,7]. Average age was 57.1 years (range, 39 to 83 years). Reasons for Nonresectability. There were thirty-one patients with extensive locally invasive lesions infiltrating the vertebrae or aorta or firmly attached to the bronchi without obvious invasion preoperatively. On barium swallow the extent of the lesion was from 7 to 12 cm. Twenty-four patients had metastatic nodes beyond the chest cavity, five patients had liver metastases, three patients had vagal and recurrent laryngeal nerve involvement, four patients had trachea- and bronchoesophageal fistulas, one patient had an esophagopleural fistula, eight patients had a previous full course of radiotherapy and, despite this, were unable to swallow, and two patients had bone metastases. Some of the groups were overlapping. Location of the Lesion. Two patients (3.7 per cent) had cervical lesions, ten (18.5 per cent) had upper third lesions,
The American Journal of Surgery
thirty-three (61.1 per cent) had middle third lesions, and nine (16.6 per cent) had lower third lesions. There were forty-seven squamous cell carcinomas, six adenocarcinomas, and one small cell carcinoma. Possible Etiologic Factors. Thirty-eight patients had a long history of alcoholism and smoking, two had achalasia, one had a long-standing lye stricture, five had previous pulmonary tuberculosis, and three had hiatal hernias, a disputed factor [8]. The specific preoperative workup consisted of barium swallow, esophagoscopy, and bronchoscopy. The preoperative preparation was usually brief and entailed hydration, occasional transfusion of blood, and a futile attempt to improve oral hygiene. Operative Technic. With the patient in the supine position, the abdomen was explored through an upper midline incision, celiac nodes were biopsied, and if possible the resectability of the tumor was assessed by palpating it through the incised right crus of the hiatus [3,9,10]. The presence of metastatic abdominal nodes and/or extensive local invasion by the tumor were indications for palliative bypass [6]. The stomach was mobilized by dividing the gastrocolic ligament, the short gastric vessels, and the left gastric vessels. The gastroepiploic and the right gastric vessels were carefully preserved. Pyloromyotomy or pyloroplasty was performed and the duodenum mobilized. When there were no metastases in the abdomen and the resectability of the lesion could not be properly assessed, then the abdomen was closed. The patient was then turned on his left side and the right chest prepared and entered through the bed of the fourth or fifth rib [II]. When the lesion was found to be nonresectable, the gastroesophageal junction was divided after pulling the freed stomach into the right chest. The divided ends were closed. The esophagus above the lesion was now freed, usually after division of the azygos vein. The esophagus was divided above the lesion and the distal end closed. The proximal end was anastomosed to the fundus of the stomach into an excised area measuring approximately 2 cm in diameter. The anastomosis was done with interrupted 4-O silk. The anastomosis was then wrapped around with stomach wall in an “inkwell” fashion [IL’]. In twenty-one patients the bypass was performed in this fashion in the right chest. Four patients had the bypass performed in the left chest. We entered the left chest because of previous right thoracotomy in two of these patients. The other two had lesions of the gastroesophageal junction. In twenty-eight patients, who had lesions obviously not resectable and lesions of the upper third of the esophagus, the following bypass technic was applied [13]: After mobilization of the stomach, the gastroesophageal junction was divided and both sides closed. A Foley catheter was inserted into the esophagus through an opening in the anterior wall and secured with a pursestring suture. The catheter was brought out in the right subcostal area. The cervical esophagus was then exposed and divided, closing the distal end. The left sternoclavicular junction was then exposed and resected. A retrosternal tunnel was
Volume 135. June 1979
developed and the isolated stomach passed through it into the neck. The fundus was anchored to the prevertebral fascia and an anastomosis performed between the esophagus and the fundus of the stomach using the same technic described previously. The abdomen and the neck were then closed. The Foley catheter, which was left in place, usually drained for two to three weeks and was then removed. (In 1 patient who had a previous partial gastrectomy, the right colon was used for the bypass.) In this technic, we stress the following points: (1) The supine position, which allows the stomach to be mobilized with ease and the right gastric and gastroepiploic vessels to be well preserved; this is considerably difficult in the lateral position into which the patient is positioned for a thoracoabdominal incision. (2) The sequential opening of the chest in the patients in whom the anastomosis was done in the chest [ll]; our patients were usually in poor physical condition, and opening of two cavities simultaneously was not tolerated well in our past experience. (3) No aggressive attempt was made to resect a nonresectable tumor. (4) The “inkwell” anastomosis seems to reinforce the anastomosis and prevents reflux [14].
Results Four patients (7.4 per cent) died within thirty days after the operation. One of the patients with vagal nerve involvement died three weeks after the operation because of aspiration. The second mortality was from an empyema. The barium swallow performed one week after the operation showed an intact anastomosis. The third patient had a stroke two weeks after the operation and died from a partial bowel obstruction in the fourth week after the operation. He refused surgery for the bowel obstruction. In the two patients with cervical lesions the operative result was not good. These patients had vagal nerve involvement. Also, the other patient with vagal nerve involvement had an unsatisfactory result. Despite healed anastomoses in all three, they had difficulty swallowing and they should not have undergone the operation. CompZications. (Table I. ) Anastomotic leaks occurred only in the patients who had cervical esophagogastrostomy. All the leaks healed within three weeks when the neck wound was drained and the patients were placed on hyperalimentation. In the patient who had a partial necrosis of the fundus, the anastomosis was taken down and esophagostomy and gastrostomy performed. The one month mortality in this group was 7.4 per cent compared with 31.4 per cent in the first group. The average survival was five months compared with three and a half months. The quality of survival is reflected in the 92 per cent (46/50) surviving patients who were able to assume
783
Steiger et al
TABLE I
Complications Comolication _ Anastomotic leak (in neck) Empvema Lung abscess Bronchopneumonia Wound infections Abdominal dehiscence Partial necrosis of fundus Tracheostomy Respiratory insufficiency Splenectomy Transient dumping Accidental pneumothorax Cerebrovascular accident Aspiration Total
Summary Number 6 2 1 3 9 1 1 2 3 8 10 6 1 1 1a/54 (33 %)
a near-normal diet soon after surgery. The reason for improvement in survival was attributed to the simplicity of the procedure. Futile attempts to resect the tumor were not made. When the bypass was performed in the chest, it was done in sequence [II]. The stomach was always mobilized with the patient in the most favorable position and the vascular supply never compromised. There is no need to anastomose the distal esophagus into the gastrointestinal tract. Comments
There is considerable controversy as to the optimal treatment of nonresectable, obstructing carcinoma of the esophagus. Esophagostomy-gastrostomy carries a small risk but is cumbersome for the patient to manage and many times only reluctantly accepted by the patient. Palliative intubation requires a change in diet. The gastroesophageal junction is made incompetent and patients tend to aspirate. The various tubes will get obstructed with food and overgrown tumor. The tubes may perforate and migrate. Use of colon requires three anastomoses, and a slight stretch on the mesentery may jeopardize the vascular supply. Radiotherapy is contraindicated in the patients with complicating fistulas. The treatment is relatively long for a patient who has a short life expectancy. The aim of restoring the ability to swallow is not always achieved. In our series eight patients received radiotherapy and could not swal1_._~
LOW.
We believe that a simple one-stage bypass of the esophagus using the stomach is an effective way of achieving palliation with an acceptable morbidity and mortality in a high risk patient group.
784
Fifty-four patients with far-advanced carcinoma of the esophagus were operated on between the years 1974 and 1976. No attempts were made to resect the lesion. The stomach was used fifty-three times to bypass the lesion and the right colon was used once. In twenty-eight patients the stomach was placed substernallv and the anastomosis was done in the neck. Twenty-five patients had the anastomosis to the esophagus done in the chest. The thirty day operative mortality was 7.4 per cent and the average survival was five months. These figures compared favorably with a group of thirty-five patients with far-advanced carcinoma of the esophagus seen between the years 1971 and 1973 and handled with a variety of modalities. In this group the thirty day mortality was 31.4 per cent (11/35) and the average surival was three and a half months. ”
References 1. Leon W, Strug LH, Brickman JD: Carcinoma of the esophagus-a disaster. Ann Thorac Surg, II: 583. 1971. 2. Lawler MR Jr, Gobbel WG, Killen DA, Daniel RA: Carcinoma of the esophagus. J Thorac Cardiovasc Surg 58: 609, 1969. 3. Plested WG, Tildon TT, Hughes RK: A philosophy of treatment of esophageal carcinoma. Am Surg 34: 650, 1968. 4. Proctor DSC: Carcinoma of the esophagus: a review of 523 cases. S Afr J Surg 6: 137, 1968. 5. Wilson SE, Plested WG, Carey JS: Esophagogastrectomyversus radiation therapy for midesophageal carcinoma. Ann Thorac Surg 10: 195, 1970. 6. Just-Viera JO, Silva JE: Esophageal carcinoma. Ann Thorac Surg 19: 688, 1975. 7. Gunnlangsson GH, Wychulis AR, Roland C, Ellis FH Jr: Analysis of the records of 1,657 patients with carcinoma of the esophagus and cardia of the stomach. Surg Gynecol Obstet 130: 997.1970. 8. Michel JO, Olsen AM, Docherty MB: The association of diaphragmatic hiatal hernia and gastroesophageal carcinoma. Surg Gynecol Obstet 124: 585, 1967. 9. MacManus JE: Combined left abdominal and right thoracic approach to resection of esophageal neoplasms. Surgery 24: 9, 1948. 10. Ong GB: Resection and reconstruction of the esophagus. Curr Probl Surg Chicago, Year Book Medical, September 1971, P 1. 11. Parker EF, Gregorie HB Jr: Carcinoma of the esophagus. Curr Probl Surg Chicago, Year Book Medical, April 1967, p 1. 12. Procter DSC: The “inkwell” anastomosis in esophageal reconstruction. S Afr Med J 41: 187, 1967. 13. Orringer MB, Sloan H: Substernal gastric bypass of the excluded thoracic esophagus for palliation of esophageal carcinoma. J Thorac Cardiovasc Surg 70: 836, 1975. 14. Pearson FG, Henderson RD. Parish RM: An operative technique for the control of reflux following esophagogastrostomy. J Thorac Cardiovasc Surg 58: 668, 1969. 15. Girardet RE, Ransdell HT. Wheat MW Jr: Palliative intubation in the management of esophageal carcinoma. Ann Thorac Surg ia:417, 1974.
The American Journal of Surgery
