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Treatment of Carcinoma of the Esophagus or Cardia*

  • F. HENRY ELLIS Jr.
    Correspondence
    Address reprint requests to Dr. F. H. Ellis, Jr., Department of Thoracic and Cardiovascular Surgery, Lahey Clinic Medical Center, 41 Mall Road, Burlington, MA 01805
    Affiliations
    Department of Thoracic and Cardiovascular Surgery, Lahey Clinic, Medical Center, Burlington, Massachusetts, and Division of Thoracic and Cardiovascular Surgery, New England Deaconess Hospital and Harvard Medical School, Boston, Massachusetts
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      Esophagogastrectomy is the best available treatment for patients with carcinoma of the esophagus or cardia and is associated with low hospital morbidity and mortality. It provides better longevity than other types of therapy and an acceptable survival rate. After esophagogastrectomy, 80% or more of the patients have satisfactory palliation of dysphagia. During an 18-year experience (1970 to 1988) with surgical treatment of carcinoma of the esophagus or cardia at the Lahey Clinic, 82.3% of patients with this disease were surgical candidates. Of the 310 patients who were treated surgically, 275 (88.7%) underwent resection, and the 30-day mortality rate was 2.2%. In 196 patients, gastrointestinal continuity was reestablished afterward by intrathoracic esophagogastrostomy. Cervical anastomosis was performed in 61 patients, 53 of whom had transhiatal resection. Major complications that prolonged the hospital stay occurred in 40 patients, and minor complications occurred in 28. The adjusted actuarial 5-year survival rate was 20.8% for all patients and 23.3% when only curative resections were considered. Stage of the disease was the most important determinant of long-term survival. Survival statistics were similar for patients with squamous cell epithelioma, adenocarcinoma of the cardia, or adenocarcinoma in Barrett's esophagus.
      In contrast to its almost endemic incidence elsewhere in the world, carcinoma of the esophagus is an uncommon disease in the United States; yet it remains a persistent therapeutic problem for the physician. If carcinoma of the cardia is included, the total number of patients involved is almost doubled, and the number may be increasing. For example, the incidence of carcinoma of the esophagus is increasing among black men, and the incidence of carcinoma of the cardia has not followed the overall decline of gastric malignant lesions and may, in fact, be increasing. Evidence also suggests that the incidence of adenocarcinoma may be increasing in patients with Barrett's esophagus.
      Because the surgical approaches to carcinoma of the lower esophagus and of the cardia are the same and the results of treatment are similar, management of these two lesions will be discussed together. Emphasis will be on my experience with these lesions during the past 18 years at the Lahey Clinic. Before surgical treatment is discussed, however, other therapeutic options should be mentioned. Table 1 lists the available nonsurgical and surgical therapeutic modalities for patients who have carcinoma of the esophagus or cardia.
      Table 1Carcinoma of the Esophagus or Cardia: Therapeutic Options
      NonsurgicalSurgical
      • Radiotherapy
      • Chemotherapy
      • Pulsion intubation
      • Miscellaneous
        • Bougienage
        • Nd:YAG
          Neodymium:yttrium-aluminum-garnet.
          laser therapy
        • Photoirradiation
        • Brachytherapy
      • Resection
      • Adjuvant therapy
        • Preoperative radiotherapy
        • Preoperative chemotherapy
        • Preoperative chemoradiotherapy
      • Esophagogastrostomy
      • Traction intubation
      • Gastrostomy
      * Neodymium:yttrium-aluminum-garnet.

      NONSURGICAL THERAPY

      Radiotherapy.

      The extraordinarily good results obtained with radiotherapy alone for carcinoma of the esophagus first reported 20 years ago and updated approximately 10 years ago by Pearson
      • Pearson JG
      The present status and future potential of radiotherapy in the management of esophageal cancer.
      (a 17% 5-year survival rate) have not been duplicated. In fact, an extensive review of the literature by Earlam and Cunha-Melo
      • Earlam R
      • Cunha-Melo JR
      Oesophageal squamous cell carcinoma. II. A critical review of radiotherapy.
      disclosed a 5-year survival rate that varied from 1 to 8% (overall mean, 6%). Although not without risk, this type of therapy does provide temporary palliation of dysphagia for an appreciable number of patients who have esophageal obstruction attributable to carcinoma. Unfortunately, the duration of palliation tends to be brief, and the complication of radiation stricture may negate the palliative effects.

      Chemotherapy.

      Chemotherapy alone plays a relatively small role in the primary management of carcinoma of the esophagus or cardia. Single-drug therapy has yielded response rates of 15 to 20%.
      • Kelsen D
      Chemotherapy of esophageal cancer.
      Although multidrug therapy increases the response rate to 33 to 63%,
      • Kelsen D
      • Hilaris B
      • Coonley C
      • Chapman R
      • Lesser M
      • Dukeman M
      • Heelan R
      • Bains M
      Cisplatin, vindesine, and bleomycin chemotherapy of localregional and advanced esophageal carcinoma.
      the duration of response is again brief, and the treatment is associated with considerable toxicity. In multidrug therapy, cisplatin is usually used in conjunction with one or more of the following: vindesine, bleomycin, 5-fluorouracil, and mitomycin.

      Chemoradiotherapy.

      The results of combined radiotherapy and chemotherapy have been somewhat better than those with either therapeutic modality alone—a median survival of 22 months in one report
      • Earle JD
      • Gelber RD
      • Moertel CG
      • Hahn RG
      A controlled evaluation of combined radiation and bleomycin therapy for squamous cell carcinoma of the esophagus.
      and effective palliation of dysphagia.

      Endoprosthesis.

      Various prosthetic devices are currently available for peroral intubation of the area of malignant obstruction. A recent review
      • Van den Brandt-Grädel V
      • den Hartog Jager FCA
      • Tytgat GNJ
      Palliative intubation of malignant esophagogastric obstruction.
      of the use of one of these devices in 400 patients, most of whom had esophageal carcinoma, found a 95% incidence of satisfactory tube function. Such treatment, however, was not without complication. Bleeding occurred in 1% of patients, obstruction of the tube in 6%, perforation in 7%, and migration of the tube in 23%; the mortality rate was 4%.

      Miscellaneous.

      Dilation of malignant esophageal strictures may provide temporary relief of dysphagia, and in some patients, the relief may be surprisingly long-lasting.
      • Heit HA
      • Johnson LF
      • Siegel SR
      • Boyce Jr, HW
      Palliative dilation for dysphagia in esophageal carcinoma.
      Dilation is especially useful in preparing patients with inoperable disease for more definitive palliative therapy, such as peroral pulsion intubation. The use of neodymium:yttrium-aluminum-garnet laser coagulation as palliative therapy for obstructing esophageal carcinoma has aroused considerable interest among endos copists. A recent report
      • Krasner N
      • Barr H
      • Skidmore C
      • Morris AI
      Palliative laser therapy for malignant dysphagia.
      on 76 patients described this treatment as successful in 86% of the patients who became asymptomatic or able to eat most solids. The mortality rate from the procedure was 5%, but the median survival of 19 weeks was no different from that for untreated patients. Another report,
      • Karlin DA
      • Fisher RS
      • Krevsky B
      Prolonged survival and effective palliation in patients with squamous cell carcinoma of the esophagus following endoscopic laser therapy.
      however, showed a tripling of the survival interval after laser therapy in comparison with that in control subjects. Whether laser therapy or bipolar electrocoagulation of the tumor will prove to be preferable remains to be determined.
      • Jensen DM
      • Machicado G
      • Randall G
      • Tung LA
      • English-Zych S
      Comparison of low-power YAG laser and BICAP tumor probe for palliation of esophageal cancer strictures.
      Photoirradiation, in which patients are presensitized with a hematoporphyrin derivative before treatment with light delivered by an argon pumped dye laser, is also being studied with considerable enthusiasm.
      • Thomas RJ
      • Abbott M
      • Bhathal PS
      • St. John DJB
      • Morstyn G
      High-dose photoirradiation of esophageal cancer.
      It has proved to be an effective alternative to other palliative measures. The ultimate role of photoirradiation in the treatment of patients with esophageal carcinoma remains to be determined.
      Intracavitary irradiation (brachytherapy) is another palliative therapeutic modality.
      • Rowland CG
      • Pagliero KM
      Intracavitary irradiation in palliation of carcinoma of oesophagus and cardia.
      Implantation of radioactive iridium directly into the tumor allows administration of a high dose of irradiation with relatively little risk of deep penetration of the rays. This technique should be reserved for patients who are not candidates for surgical treatment.

      SURGICAL THERAPY

      The pessimism of past years about the role of operative management of esophageal carcinoma has persisted, nurtured by an exhaustive review of the literature by Earlam and Cunha-Melo
      • Earlam R
      • Cunha-Melo JR
      Oesophageal squamous cell carcinoma. I. A critical review of surgery.
      that extended back to the early 1970s. In that report, the resectability rate was only 67%, the hospital death rate was 33.3%, and the overall 5-year survival rate was only 4%—no better than the results found in their review of radiation therapy.
      • Earlam R
      • Cunha-Melo JR
      Oesophageal squamous cell carcinoma. II. A critical review of radiotherapy.
      These data do not reflect current results in several large series of patients treated by resection during the past 10 years in various parts of the world (Table 2). Although operability and hospital mortality rates vary considerably, as do the 5-year survivals of patients who undergo successful resection, these values have clearly improved in comparison with those reported by Earlam and Cunha-Melo.
      • Earlam R
      • Cunha-Melo JR
      Oesophageal squamous cell carcinoma. I. A critical review of surgery.
      Other data in Table 2 more closely reflect current practice. Operability and resectability rates are increasing, and hospital mortality rates are decreasing. Thus, more treated patients will have long-term survival now than was true previously. My experience with esophagogastrectomy for carcinoma supports this view; some of these results have been reported previously.
      • Ellis Jr, FH
      • Gibb SP
      • Watkins Jr, E
      Overview of the current management of carcinoma of the esophagus and cardia.
      • Ellis Jr, FH
      • Gibb SP
      Esophagogastrectomy for carcinoma: current hospital mortality and morbidity rates.
      • Ellis Jr, FH
      • Maggs PR
      Surgery for carcinoma of the lower esophagus and cardia.

      Ellis FH Jr, Gibb SP, Watkins E Jr: Esophagogastrectomy: a safe, widely applicable, and expeditious form of palliation for patients with carcinoma of the esophagus and cardia. Ann Surg 198:531–539, 198

      • Ellis Jr, FH
      • Gibb SP
      • Watkins Jr, E
      Limited esophagogastrectomy for carcinoma of the cardia: indications, technique, and results.
      Table 2Summary of Reported Results of Surgical Treatment of Carcinoma of the Esophagus or Cardia
      NS = not stated.
      Rates (%)
      AuthorYearLocationCases (no.)OperabilityResectability
      Percentage of patients who underwent operation.
      Hospital mortality5-year survival
      Percentage of patients who survived resection.
      Van Andel et al
      • Van Andel JG
      • Dees J
      • Dijkhuis CM
      • Fokkens W
      • van Houten H
      • de Jong PC
      • van Woerkom-Eykenboom WM
      Carcinoma of the esophagus: results of treatment.
      1979Holland328426121.021
      Wu and Huang
      • Wu YK
      • Huang KC
      Chinese experience in the surgical treatment of carcinoma of the esophagus.
      1979China66985695.625
      Griffith and Davis
      • Griffith JL
      • Davis JT
      A twenty-year experience with surgical management of carcinoma of the esophagus and gastric cardia.
      1980England513NS4112.015
      Giuli and Gignoux
      • Giuli R
      • Gignoux M
      Treatment of carcinoma of the esophagus: retrospective study of 2,400 patients.
      1980Europe2,400NSNS30.014
      Earlam and Cunha-Melo
      • Earlam R
      • Cunha-Melo JR
      Oesophageal squamous cell carcinoma. I. A critical review of surgery.
      1980Review83,783586733.316
      Akiyama et al
      • Akiyama H
      • Tsurumaru M
      • Kawamura T
      • Ono Y
      Principles of surgical treatment for carcinoma of the esophagus: analysis of lymph node involvement.
      1981Japan354NS591.435
      Skinner
      • Skinner DB
      En bloc resection for neoplasms of the esophagus and cardia.
      1983United States181668011.018
      Xu et al
      • Xu LT
      • Sun ZF
      • Li ZJ
      • Wu LH
      Surgical treatment of carcinoma of the esophagus and cardiac portion of the stomach in 850 patients.
      1983China850NS7810.022
      Orringer
      • Orringer MB
      Transhiatal esophagectomy without thoracotomy for carcinoma of the thoracic esophagus.
      1984United States100NSNS6.017
      Survival at 4 years.
      Ellis et al
      • Ellis Jr, FH
      • Gibb SP
      • Watkins Jr, E
      Overview of the current management of carcinoma of the esophagus and cardia.
      1985United States21980872.116
      Hennessy and O'Connell
      • Hennessy TP
      • O'Connell R
      Carcinoma of the hypopharynx, esophagus and cardia.
      1986Ireland2008710017.520
      Bluett et al
      • Bluett MK
      • Sawyers JL
      • Healy D
      Esophageal carcinoma: improved quality of survival with resection.
      1987United States144467210.013
      Wong
      • Wong J
      Esophageal resection for cancer: the rationale of current practice.
      1987Hong Kong28475826.924
      Survival at 3.5 years.
      King et al
      • King RM
      • Pairolero PC
      • Trastek VF
      • Payne WS
      • Bernatz PE
      Ivor Lewis esophagogastrectomy for carcinoma of the esophagus: early and late functional results.
      1987United States100NSNS3.022.8
      Mathisen et al
      • Mathisen DJ
      • Grillo HC
      • Wilkins Jr, EW
      • Moncure AC
      • Hilgenberg AD
      Transthoracic esophagectomy: a safe approach to carcinoma of the esophagus.
      1988United States104NSNS2.9
      Reported for two groups: 33.2% for patients with squamous cell epithelioma; 7.7% for patients with adenocarcinoma.
      * NS = not stated.
      Percentage of patients who underwent operation.
      Percentage of patients who survived resection.
      § Survival at 4 years.
      Survival at 3.5 years.
      Reported for two groups: 33.2% for patients with squamous cell epithelioma; 7.7% for patients with adenocarcinoma.
      Current interest in extending the operation to a superradical procedure in highly selected favorable patients has thus far resulted in no appreciable improvement in the overall 5-year survival.
      • Skinner DB
      En bloc resection for neoplasms of the esophagus and cardia.
      • DeMeester TR
      • Zaninotto G
      • Johansson KE
      Selective therapeutic approach to cancer of the lower esophagus and cardia.
      Because of this, my associates and I continue to use a standard resection for resectable lesions; the details have been described previously
      • Ellis Jr, FH
      Carcinoma of the distal esophagus and esophagogastric junction.
      • Ellis Jr, FH
      Esophagogastrectomy for carcinoma: technical considerations based on anatomic location of lesion.
      and will be outlined briefly here.
      For lesions at the esophagogastric junction and in the distal lower esophageal area, an esophagogastrectomy is performed through a left thoracotomy, access to the upper abdomen being obtained through a semilunar incision bordering the costal arch. Unless involved by the tumor, neither the omentum and spleen nor the tail of the pancreas is removed. Adequate margins, 5 cm or more on both sides of the tumor, are sought. After resection, gastrointestinal continuity is restored by an end-to-side two layer esophagogastrostomy.
      For lesions in the upper thoracic esophageal area, an Ivor Lewis approach is preferred. An intrathoracic esophagogastrostomy is performed at or above the level of the azygos vein. A third incision in the left side of the neck to accommodate a cervical esophagogastrostomy with uninvolved margins is necessary only when frozen sections show extensive submucosal spread.
      A transhiatal approach is preferred for lesions in the cervical esophagus and at the thoracic inlet, as well as for lesions at other locations, when evaluation by computed tomography and exploration suggest that the lesion is confined to the esophagus proper without extension into the surrounding tissue. I have not used this approach as freely as others have,
      • Orringer MB
      Transhiatal esophagectomy without thoracotomy for carcinoma of the thoracic esophagus.
      who advocate it for lesions at all locations. Although the operation has had no adverse effects on long-term survival, it also has not diminished the rate of postoperative complications as originally expected.
      • Shahian DM
      • Neptune WB
      • Ellis Jr, FH
      • Watkins Jr, E
      Transthoracic versus extrathoracic esophagectomy: mortality, morbidity, and long-term survival.

      Vogel SB: Comparison of esophagogastrectomy and transhiatal esophagectomy: early and late complications. Presented at the meeting of the Society of Surgical Oncology, New Orleans, May 23, 1988

      A colon interposition procedure was used more freely in past years but is now restricted to those patients in whom the amount of stomach available to function as an esophageal substitute is inadequate.

      CASE MATERIAL

      Between January 1970 and January 1988, 310 patients with carcinoma of the esophagus or cardia underwent operation at the Lahey Clinic. Meaningful data on operability were available for only those patients who underwent treatment from July 1974 onward. Patients who had had initial treatment elsewhere and those who refused operation or went elsewhere for treatment were excluded from this analysis. During this latter period, 277 patients had a diagnosis of carcinoma of either the esophagus or the cardia; of these, 228 underwent operation, an overall operability of 82.3%.
      The ages of the 310 surgical patients ranged from 24 to 89 years (mean, 62.7 years). Men predominated over women, 231 to 79. Almost half of the tumors occurred at the esophagogastric junction, and the distribution of lesions in the cervical and upper thoracic esophagus was approximately equal to that in the lower thoracic esophagus (Fig. 1).
      Figure thumbnail gr1
      Fig. 1Anatomic distribution of lesions among 310 patients with carcinoma of the esophagus or cardia. (By permission of Lahey Clinic.)

      Pathologic Findings.

      The most frequently occurring tumors were adenocarcinomas (Table 3), and almost three-quarters of these lesions were located at the cardia. The other adenocarcinomas had developed in a Barrett esophagus. In addition to 108 squamous cell carcinomas, 4 of which developed in patients with achalasia, 12 tumors were classified as miscellaneous. Of the 275 resected tumors, 57 were stage I, 24 were stage II, 175 were stage III, and 19 were stage IV (staging based on criteria from the American Joint Committee on Cancer
      • American Joint Committee on Cancer
      ).
      Table 3Pathologic Findings in 310 Patients With Carcinoma of the Esophagus or Cardia
      FindingNo. of patients
      Adenocarcinoma190
       Cardia141
      One patient had achalasia.
       Barrett's esophagus49
      Squamous cell epithelioma108
      Four patients had achalasia.
      Miscellaneous12
       Adenosquamous carcinoma6
       Mucoepidermoid carcinoma2
       Histiocytic lymphoma2
       Small cell carcinoma1
       Carcinosarcoma1
      * One patient had achalasia.
      Four patients had achalasia.

      Surgical Features.

      Two hundred seventy five of the patients underwent resection, a resectability rate of 88.7% (Table 4). Various surgical approaches were used, depending on the site of the lesion (Table 5). The majority of patients underwent esophagogastrectomy with intrathoracic anastomosis. Six patients died within 30 days after operation, a mortality rate of 2.2%. Three patients died of myocardial infarction, two patients died of respiratory failure, and one patient, who had previously undergone pneumonectomy for carcinoma, died of a pulmonary embolus 1 day after transhiatal resection. Six other patients died after the 30-day postoperative interval without having left the hospital. Respiratory failure accounted for two of these deaths; cardiac arrest, pulmonary embolus, mesenteric thrombosis, and renal failure were responsible for the other deaths.
      Table 4Surgical Features in 310 Patients With Carcinoma of the Esophagus or Cardia
      Overall operability, 82.3%.
      Patients
      Type of procedureNo.%
      Resection27588.7
       30-day mortality62.2
       Hospital mortality62.2
      Exploratory
      Median survival, 5.5 months. Hospital mortality was 14.3% (five patients).
      35
       Celestin's tube17
       Bypass2
       Miscellaneous16
      * Overall operability, 82.3%.
      Median survival, 5.5 months. Hospital mortality was 14.3% (five patients).
      Table 5Surgical Procedures and Mortality in 275 Patients With Carcinoma of the Esophagus or Cardia Who Underwent Esophagogastrectomy
      Overall mortality, 2.2% (six patients).
      ProcedureNo. of patientsMortality (no.)
      Esophagogastrostomy257
       Intrathoracic196
        Left thoracotomy1091
        Ivor Lewis762
        Thoracoabdominal11
       Cervical61
        Transhiatal532
        Ivor Lewis61
        Left thoracotomy2
      Colon interposition17
      Miscellaneous1
      * Overall mortality, 2.2% (six patients).
      The mortality rate for patients whose lesions were nonresectable at the time of operation because of local extension of the growth was higher than that for patients who underwent resection. Of the 35 patients with nonresectable lesions, 5 (14.3%) died within 30 days postoperatively (Table 4). The most common procedure for nonresectable lesions was intraoperative insertion of Celestin's tube; all five deaths occurred in this group. The median survival rate for these patients was not significantly different from that for untreated patients, but satisfactory palliation was provided in most instances.

      Complications.

      Postoperative complications developed in 68 patients (Table 6) and were of major importance in that they prolonged the hospital stay of 40 of them (14.5%). An anastomotic leak developed in 12 patients, occurring at an intrathoracic anastomosis in 3 of them. The leakage in one of these three patients occurred 5 days after operation and was successfully repaired surgically. An empyema necessitating open drainage developed in another patient with an intrathoracic anastomotic leak; this patient later died of a pulmonary embolus while still in the hospital. In the third patient, the leak was contained and successfully treated with conservative therapy, including hyperalimentation and antibiotics. Only one of the nine cervical leaks, most of which occurred at a cervical esoph agocolostomy, necessitated surgical closure.
      Table 6Postoperative Complications Among 275 Patients With Carcinoma of the Esophagus or Cardia
      Patients
      ComplicationNo.%
      Major4014.5
       Anastomotic leak12
        Cervical9
        Thoracic3
       Gastrointestinal obstruction10
       Respiratory failure6
       Subphrenic abscess6
       Miscellaneous6
      Minor2810.2
       Arrhythmia13
       Retained secretions7
       Wound infection3
       Vocal cord paralysis3
       Urinary tract infection2
      Gastrointestinal obstruction was the next most common complication. The gastric outlet at the level of the hiatus was involved in seven patients, all of whom required operative relief. In two patients who had obstruction at the pylorus, pyloroplasty was necessary. One patient required surgical relief for obstruction of the colon.
      Respiratory failure developed in six patients. Six patients with a subphrenic abscess required either surgical drainage or percutaneous needle aspiration. Various miscellaneous complications accounted for the remainder of the patients. Cardiac arrhythmia was the predominant minor complication, and retained secretions, wound infections, temporary vocal cord paralysis, and urinary tract infections accounted for the rest.

      Clinical Results.

      No patient was lost to follow-up, and actuarial 5-year survival data were calculated by the Kaplan-Meier method with adjustment for operative mortality and noncardiac deaths. Satisfactory palliation of dysphagia was achieved in 80% of the patients in whom this information could be obtained, from either the patient or the patient's relatives or personal physician, until the time of late follow-up or death.
      The overall 5-year survival rate was 20.8%, and the median survival time was 17.9 months (Fig. 2). Forty patients underwent resections termed “palliative” in that residual tumor was knowingly present. The difference between the results in patients who underwent curative resection and those who underwent palliative resection was striking: 23.3% of the patients with curative resections survived 5 years (median survival time, almost 2 years), but no patient with a palliative resection survived 5 years (Fig. 3).
      Figure thumbnail gr2
      Fig. 2Adjusted actuarial survival rates for all patients who survived resection of carcinoma of the esophagus or cardia. MST = median survival time; SEM = standard error of the mean.
      Figure thumbnail gr3
      Fig. 3Adjusted actuarial survival rates for palliative resection in comparison with curative resection in patients with carcinoma of the esophagus or cardia. MST = median survival time; SEM = standard error of the mean.
      The stage of the disease influenced long-term survival (Fig. 4). Patients with stage I or II disease were analyzed collectively because each group had relatively few patients. Of the patients with these early stages of disease, 38.4% survived 5 years, and the median survival time was almost 3 years. The outlook for patients with stage III disease is not hopeless; 13.3% of these patients survived 5 years, and their median survival time was 15 months.
      Figure thumbnail gr4
      Fig. 4Adjusted actuarial survival rates among patients with carcinoma of the esophagus or cardia, shown by stage of disease. MST = median survival time; SEM = standard error of the mean.
      When survival data for patients with squamous cell carcinoma were compared with those for patients with adenocarcinoma of the cardia or adenocarcinoma in a Barrett esophagus, the differences were not statistically significant (Fig. 5).
      Figure thumbnail gr5
      Fig. 5Adjusted actuarial survival rates for patients with adenocarcinoma of the cardia (Ca cardia), adenocarcinoma in Barrett's esophagus (Adeno in Barrett's), or squamous cell epithelioma (SCE). MST = median survival time; SEM = standard error of the mean.

      Miscellaneous Surgical Procedures.

      When local extension of the tumor prohibits resection, various surgical options remain. For nonresectable lesions at the cardia, a side-to-side esophagogastrostomy around the tumor, leaving the carcinoma in situ as originally proposed by d'Allaines and associates,
      • D'Allaines F
      • DuBost C
      • Galley J-J
      Oesophagogastrostomies palliatives sans resection dans les cancers de l'oesophage et du cardia.
      can provide excellent palliation in association with a reasonably low mortality rate. At a higher level in the thoracic esophagus, an operation first proposed by Kirschner
      • Kirschner M
      Ein neues Verfahren der Oesophagoplastik.
      provides satisfactory palliation. As modified by Ong,
      • Ong GB
      The Kirschner operation—a forgotten procedure.
      this operation currently consists of thorough mobilization of the stomach, division and closure of the distal part of the esophagus, and substernal placement of the stomach to facilitate a cervical esophagogastrostomy after transection of the cervical esophagus and suture closure of its distal end. The procedure is particularly applicable to patients with a malignant tracheoesophageal fistula, but it is not without risk and should be used only when the patient's condition permits, because the reported associated mortality rate has been high.
      • Orringer MB
      Substernal gastric bypass of the excluded esophagus—results of an ill-advised operation.
      If the lesion proves to be nonresectable, another alternative is intraoperative placement of a plastic prosthesis across the obstruction. This approach is not without risk, as reflected in detail in our aforementioned experience. An even higher mortality rate was reported by Watson,
      • Watson A
      A study of the quality and duration of survival following resection, endoscopic intubation and surgical intubation in oesophageal carcinoma.
      who favors endoscopic intubation over surgical intubation. Complications such as displacement, hemorrhage, and perforation are all potential hazards of the technique, which was accompanied by a hospital mortality rate of 18% in one reported series.
      • Saunders NR
      The Celestin tube in the palliation of carcinoma of the oesophagus and cardia.
      When successful, satisfactory palliation can be provided, but patients must be restricted to a mechanically soft diet, and survival is no different from that for untreated patients.
      A feeding gastrostomy or jejunostomy used for palliation is an unacceptable procedure. No palliation is actually provided in that the swallowing mechanism is not restored, and such a procedure is not without risk. Such an approach might occasionally be justified as a temporizing measure between stages of a reconstructive procedure, such as a colon interposition operation, or in an effort to maintain adequate nutrition in a patient undergoing radiotherapy in anticipation of normal alimentation.

      Adjuvant Therapy.

      Currently, the use of combined therapeutic modalities, such as preoperative radiotherapy, chemotherapy, or chemoradiotherapy, in an effort to improve long-term survival has aroused considerable interest. The impressive results with preoperative radiotherapy reported from Japan
      • Nakayama K
      Pre-operative irradiation in the treatment of patients with carcinoma of the oesophagus and of some other sites.
      • Akakura I
      • Nakamura Y
      • Kakegawa T
      • Nakayama R
      • Watanabe H
      • Yamashita H
      Surgery of carcinoma of the esophagus with preoperative radiation.
      have not been confirmed in the United States.
      • Marks Jr, RD
      • Scruggs HJ
      • Wallace KM
      Preoperative radiation therapy for carcinoma of the esophagus.
      Two recent prospective randomized controlled studies in which operation alone was compared with operation plus preoperative radiotherapy have found no advantage of the combined approach.
      • Launois B
      • Delarue D
      • Campion JP
      • Kerbaol M
      Preoperative radiotherapy for carcinoma of the esophagus.
      • Gignoux M
      • Roussel A
      • Paillot B
      • Gillet M
      • Schlag P
      • Favre J-P
      • Dalesio O
      • Buyse M
      • Duez N
      The value of preoperative radiotherapy in esophageal cancer: results of a study of the E.O.R.T.C..
      Various combinations of drugs have been used before operation in an effort to improve overall results. All these regimens have included cisplatin. Drug toxicity seems to be tolerable, and operative morbidity and mortality remain low. Overall response rates in terms of regression or elimination of the primary tumor have varied from 33 to 63%.
      • Kelsen DP
      Preoperative chemotherapy in esophageal carcinoma.
      • Hilgenberg AD
      • Carey RW
      • Wilkins Jr, EW
      • Choi NC
      • Mathisen DJ
      • Grillo HC
      Preoperative chemotherapy, surgical resection, and selective postoperative therapy for squamous cell carcinoma of the esophagus.
      Although early survival seems to be improved over that in historical control subjects and is better in patients who have had a complete response to chemotherapy, as yet no convincing evidence has shown that long-term survival has been affected beneficially. Similar results have occurred with preoperative chemoradiation, a therapeutic modality used to improve local control of disease while destroying distal micrometastatic lesions.
      • Kelsen DP
      Preoperative chemotherapy in esophageal carcinoma.
      • Poplin E
      • Fleming T
      • Leichman L
      • Seydel HG
      • Steiger Z
      • Taylor S
      • Vance R
      • Stuckey WJ
      • Rivkin SE
      Combined therapies for squamous-cell carcinoma of the esophagus, a Southwest Oncology Group study (SWOG-8037).
      • MacFarlane SD
      • Hill LD
      • Jolly PC
      • Kozarek RA
      • Anderson RP
      Improved results of surgical treatment for esophageal and gastroesophageal junction carcinomas after preoperative combined chemotherapy and radiation.
      The early findings were encouraging but have not been followed by any meaningful influence on long-term survival. Although protocols vary, the duration of treatment is generally prolonged: 3 to 4 weeks of chemotherapy and radiotherapy followed by a 3-week interval before operation is performed. After operation, further chemotherapy or irradiation or both are used in selected patients. Thus, treatment may last for several months, in comparison with the 2 weeks or so necessary for recovery from operation alone. Only time will determine whether this type of therapy will prove to have an appreciable effect on survival rates.

      DISCUSSION

      Although the treatment of patients with carcinoma of the esophagus or cardia still is suboptimal, the overall results have improved steadily since World War II. The data presented in this review support that opinion. Whether increasing the extent of operation or using adjuvant therapy will ultimately improve long-term results remains to be seen.
      That improvement has occurred in the management of this disease is supported by comparison of the operability and resectability rates, the percentage of operative survivors, and the overall 5-year survival rates during three periods: 1946 to 1955, 1956 to 1965, and the current review, 1970 to 1988 (Fig. 6). The first two reviews involved patients treated at the Mayo Clinic and were reported earlier.
      • Ellis Jr, FH
      • Jackson RC
      • Krueger Jr, JT
      • Moersch HJ
      • Clagett OT
      • Gage RP
      Carcinoma of the esophagus and cardia: results of treatment, 1946 to 1956.
      • Gunnlaugsson GH
      • Wychulis AR
      • Roland C
      • Ellis Jr, FH
      Analysis of the records of 1,657 patients with carcinoma of the esophagus and cardia of the stom ach.
      The most recent review was of patients at the Lahey Clinic. Each successive period showed improvements in operability and resectability rates and a decline in hospital mortality; the result was an almost fourfold increase in the overall 5-year survival of all patients, not only those who underwent operation.
      Figure thumbnail gr6
      Fig. 6Comparison of results of treatment of carcinoma of the esophagus or cardia, 1946 to 1988, in three series of patients.
      This progressive improvement is probably a result of several factors, including earlier diagnosis, more aggressive surgical approach, and overall improvement in patient care, which decreased the hospital mortality rate. Future improvement in survival rates probably will depend on techniques to improve early diagnosis rather than on improvement in treatment modalities.

      CONCLUSION

      Surgical procedures remain the mainstay of treatment for patients with carcinoma of the esophagus or cardia. Esophagogastrectomy, usually followed by esophagogastrostomy either intrathoracically or cervically, is the procedure of choice. Currently, this operation can be used in most patients with carcinoma of the esophagus or cardia and is associated with low hospital mortality and morbidity. The duration of treatment is short. This procedure provides excellent palliation of dysphagia and results in the best longevity of any type of treatment currently available. Finally, it is accompanied by an acceptable 5-year survival rate, which approaches 40% in patients with stage I or II disease.

      REFERENCES

        • Pearson JG
        The present status and future potential of radiotherapy in the management of esophageal cancer.
        Cancer. 1977; 39: 882-890
        • Earlam R
        • Cunha-Melo JR
        Oesophageal squamous cell carcinoma. II. A critical review of radiotherapy.
        Br J Surg. 1980; 67: 457-461
        • Kelsen D
        Chemotherapy of esophageal cancer.
        Semin Oncol. 1984; 11: 159-168
        • Kelsen D
        • Hilaris B
        • Coonley C
        • Chapman R
        • Lesser M
        • Dukeman M
        • Heelan R
        • Bains M
        Cisplatin, vindesine, and bleomycin chemotherapy of localregional and advanced esophageal carcinoma.
        Am J Med. 1983; 75: 645-652
        • Earle JD
        • Gelber RD
        • Moertel CG
        • Hahn RG
        A controlled evaluation of combined radiation and bleomycin therapy for squamous cell carcinoma of the esophagus.
        Int J Radiat Oncol Biol Phys. 1980; 6: 821-826
        • Van den Brandt-Grädel V
        • den Hartog Jager FCA
        • Tytgat GNJ
        Palliative intubation of malignant esophagogastric obstruction.
        J Clin Gastroenterol. 1987; 9: 290-297
        • Heit HA
        • Johnson LF
        • Siegel SR
        • Boyce Jr, HW
        Palliative dilation for dysphagia in esophageal carcinoma.
        Ann Intern Med. 1978; 89: 629-631
        • Krasner N
        • Barr H
        • Skidmore C
        • Morris AI
        Palliative laser therapy for malignant dysphagia.
        Gut. 1987; 28: 792-798
        • Karlin DA
        • Fisher RS
        • Krevsky B
        Prolonged survival and effective palliation in patients with squamous cell carcinoma of the esophagus following endoscopic laser therapy.
        Cancer. 1987; 59: 1969-1972
        • Jensen DM
        • Machicado G
        • Randall G
        • Tung LA
        • English-Zych S
        Comparison of low-power YAG laser and BICAP tumor probe for palliation of esophageal cancer strictures.
        Gastroenterology. 1988; 94: 1263-1270
        • Thomas RJ
        • Abbott M
        • Bhathal PS
        • St. John DJB
        • Morstyn G
        High-dose photoirradiation of esophageal cancer.
        Ann Surg. 1987; 206: 193-199
        • Rowland CG
        • Pagliero KM
        Intracavitary irradiation in palliation of carcinoma of oesophagus and cardia.
        Lancet. 1985; 2: 981-983
        • Earlam R
        • Cunha-Melo JR
        Oesophageal squamous cell carcinoma. I. A critical review of surgery.
        Br J Surg. 1980; 67: 381-390
        • Van Andel JG
        • Dees J
        • Dijkhuis CM
        • Fokkens W
        • van Houten H
        • de Jong PC
        • van Woerkom-Eykenboom WM
        Carcinoma of the esophagus: results of treatment.
        Ann Surg. 1979; 190: 684-689
        • Wu YK
        • Huang KC
        Chinese experience in the surgical treatment of carcinoma of the esophagus.
        Ann Surg. 1979; 190: 361-365
        • Griffith JL
        • Davis JT
        A twenty-year experience with surgical management of carcinoma of the esophagus and gastric cardia.
        J Thorac Cardiovasc Surg. 1980; 79: 447-452
        • Giuli R
        • Gignoux M
        Treatment of carcinoma of the esophagus: retrospective study of 2,400 patients.
        Ann Surg. 1980; 192: 44-52
        • Akiyama H
        • Tsurumaru M
        • Kawamura T
        • Ono Y
        Principles of surgical treatment for carcinoma of the esophagus: analysis of lymph node involvement.
        Ann Surg. 1981; 194: 438-445
        • Skinner DB
        En bloc resection for neoplasms of the esophagus and cardia.
        J Thorac Cardiovasc Surg. 1983; 85: 59-69
        • Xu LT
        • Sun ZF
        • Li ZJ
        • Wu LH
        Surgical treatment of carcinoma of the esophagus and cardiac portion of the stomach in 850 patients.
        Ann Thorac Surg. 1983; 35: 542-547
        • Orringer MB
        Transhiatal esophagectomy without thoracotomy for carcinoma of the thoracic esophagus.
        Ann Surg. 1984; 200: 282-287
        • Ellis Jr, FH
        • Gibb SP
        • Watkins Jr, E
        Overview of the current management of carcinoma of the esophagus and cardia.
        Can J Surg. 1985; 28: 493-496
        • Hennessy TP
        • O'Connell R
        Carcinoma of the hypopharynx, esophagus and cardia.
        Surg Gynecol Obstet. 1986; 162: 243-247
        • Bluett MK
        • Sawyers JL
        • Healy D
        Esophageal carcinoma: improved quality of survival with resection.
        Am Surg. 1987; 53: 126-132
        • Wong J
        Esophageal resection for cancer: the rationale of current practice.
        Am J Surg. 1987; 153: 18-24
        • King RM
        • Pairolero PC
        • Trastek VF
        • Payne WS
        • Bernatz PE
        Ivor Lewis esophagogastrectomy for carcinoma of the esophagus: early and late functional results.
        Ann Thorac Surg. 1987; 44: 119-122
        • Mathisen DJ
        • Grillo HC
        • Wilkins Jr, EW
        • Moncure AC
        • Hilgenberg AD
        Transthoracic esophagectomy: a safe approach to carcinoma of the esophagus.
        Ann Thorac Surg. 1988; 45: 137-143
        • Ellis Jr, FH
        • Gibb SP
        Esophagogastrectomy for carcinoma: current hospital mortality and morbidity rates.
        Ann Surg. 1979; 190: 699-705
        • Ellis Jr, FH
        • Maggs PR
        Surgery for carcinoma of the lower esophagus and cardia.
        World J Surg. 1981; 5: 527-533
      1. Ellis FH Jr, Gibb SP, Watkins E Jr: Esophagogastrectomy: a safe, widely applicable, and expeditious form of palliation for patients with carcinoma of the esophagus and cardia. Ann Surg 198:531–539, 198

        • Ellis Jr, FH
        • Gibb SP
        • Watkins Jr, E
        Limited esophagogastrectomy for carcinoma of the cardia: indications, technique, and results.
        Ann Surg. 1988; 208: 354-360
        • DeMeester TR
        • Zaninotto G
        • Johansson KE
        Selective therapeutic approach to cancer of the lower esophagus and cardia.
        J Thorac Cardiovasc Surg. 1988; 95: 42-53
        • Ellis Jr, FH
        Carcinoma of the distal esophagus and esophagogastric junction.
        in: Cohn LH Modern Technics in Surgery: Cardiac-Thoracic Surgery. Futura Publishing Company, New York1979: 13-1-13-10
        • Ellis Jr, FH
        Esophagogastrectomy for carcinoma: technical considerations based on anatomic location of lesion.
        Surg Clin North Am. April 1980; 60: 265-279
        • Shahian DM
        • Neptune WB
        • Ellis Jr, FH
        • Watkins Jr, E
        Transthoracic versus extrathoracic esophagectomy: mortality, morbidity, and long-term survival.
        Ann Thorac Surg. 1986; 41: 237-245
      2. Vogel SB: Comparison of esophagogastrectomy and transhiatal esophagectomy: early and late complications. Presented at the meeting of the Society of Surgical Oncology, New Orleans, May 23, 1988

        • American Joint Committee on Cancer
        Beahrs OH Myers MK Manual for Staging of Cancer. Second edition. JB Lippincott Company, Philadelphia1983
        • D'Allaines F
        • DuBost C
        • Galley J-J
        Oesophagogastrostomies palliatives sans resection dans les cancers de l'oesophage et du cardia.
        J Chir. 1949; 65: 289-301
        • Kirschner M
        Ein neues Verfahren der Oesophagoplastik.
        Arch Klin Chir. 1920; 114: 606-663
        • Ong GB
        The Kirschner operation—a forgotten procedure.
        Br J Surg. 1973; 60: 221-227
        • Orringer MB
        Substernal gastric bypass of the excluded esophagus—results of an ill-advised operation.
        Surgery. 1984; 96: 467-470
        • Watson A
        A study of the quality and duration of survival following resection, endoscopic intubation and surgical intubation in oesophageal carcinoma.
        Br J Surg. 1982; 69: 585-588
        • Saunders NR
        The Celestin tube in the palliation of carcinoma of the oesophagus and cardia.
        Br J Surg. 1979; 66: 419-421
        • Nakayama K
        Pre-operative irradiation in the treatment of patients with carcinoma of the oesophagus and of some other sites.
        Clin Radiol. 1964; 15: 232-241
        • Akakura I
        • Nakamura Y
        • Kakegawa T
        • Nakayama R
        • Watanabe H
        • Yamashita H
        Surgery of carcinoma of the esophagus with preoperative radiation.
        Chest. 1970; 57: 47-57
        • Marks Jr, RD
        • Scruggs HJ
        • Wallace KM
        Preoperative radiation therapy for carcinoma of the esophagus.
        Cancer. 1976; 38: 84-89
        • Launois B
        • Delarue D
        • Campion JP
        • Kerbaol M
        Preoperative radiotherapy for carcinoma of the esophagus.
        Surg Gynecol Obstet. 1981; 153: 690-692
        • Gignoux M
        • Roussel A
        • Paillot B
        • Gillet M
        • Schlag P
        • Favre J-P
        • Dalesio O
        • Buyse M
        • Duez N
        The value of preoperative radiotherapy in esophageal cancer: results of a study of the E.O.R.T.C..
        World J Surg. 1987; 11: 426-432
        • Kelsen DP
        Preoperative chemotherapy in esophageal carcinoma.
        World J Surg. 1987; 11: 433-438
        • Hilgenberg AD
        • Carey RW
        • Wilkins Jr, EW
        • Choi NC
        • Mathisen DJ
        • Grillo HC
        Preoperative chemotherapy, surgical resection, and selective postoperative therapy for squamous cell carcinoma of the esophagus.
        Ann Thorac Surg. 1988; 45: 357-361
        • Poplin E
        • Fleming T
        • Leichman L
        • Seydel HG
        • Steiger Z
        • Taylor S
        • Vance R
        • Stuckey WJ
        • Rivkin SE
        Combined therapies for squamous-cell carcinoma of the esophagus, a Southwest Oncology Group study (SWOG-8037).
        J Clin Oncol. 1987; 5: 622-628
        • MacFarlane SD
        • Hill LD
        • Jolly PC
        • Kozarek RA
        • Anderson RP
        Improved results of surgical treatment for esophageal and gastroesophageal junction carcinomas after preoperative combined chemotherapy and radiation.
        J Thorac Cardiovasc Surg. 1988; 95: 415-420
        • Ellis Jr, FH
        • Jackson RC
        • Krueger Jr, JT
        • Moersch HJ
        • Clagett OT
        • Gage RP
        Carcinoma of the esophagus and cardia: results of treatment, 1946 to 1956.
        N Engl J Med. 1959; 260: 351-358
        • Gunnlaugsson GH
        • Wychulis AR
        • Roland C
        • Ellis Jr, FH
        Analysis of the records of 1,657 patients with carcinoma of the esophagus and cardia of the stom ach.
        Surg Gynecol Obstet. 1970; 130: 997-1005