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Ann Thorac Surg 1995;60:896-901
© 1995 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Superficial Esophageal Carcinoma

Departments of Thoracic and Cardiovascular Surgery, Anatomic Pathology, Radiation Oncology, Biostatistics and Epidemiology, and Hematology and Medical Oncology, The Cleveland Clinic Foundation, Cleveland, Ohio

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The detection of superficial esophageal carcinomas by surveillance endoscopy and the downstaging of advanced carcinomas to superficial carcinomas by induction therapy have increased the number of patients with these carcinomas undergoing resection. The natural history of these carcinomas is not well defined.

Methods. To evaluate the results of surgical resection and identify predictors of improved survival, a retrospective review of (1) patients with superficial esophageal carcinoma at presentation (SECP) and (2) patients with advanced carcinomas that were downstaged to no residual carcinoma or superficial esophageal carcinoma after induction therapy (SECD) was conducted.

Results. There were 54 patients with SECP (19 Tis and 35 T1). Survival was significantly better for patients with Tis carcinomas (85.3% at 5 years) and patients with intramucosal T1 carcinomas (79.4%) than for patients with submucosal T1 carcinomas (16.3%) (p = 0.007 and p = 0.045, respectively). Survival at 5 years for the 49 patients without regional lymph node metastases (N0) was 65.2%, whereas none of the 5 patients with regional lymph node metastases (N1) have survived more than 3 years (p = 0.054), and 3 died of recurrent disease. There were 21 patients with SECD (13 T0, 2 Tis, and 6 T1). Survival at 4 years was 58.2%. In this group, survival was not related to depth of tumor invasion (p = 0.76) or regional lymph node status (p = 0.68).

Conclusions. We conclude that (1) patients with Tis and intramucosal T1 SECP have a significantly better survival than those with submucosal T1 SECP, (2) patients with N0 SECP have a significantly better survival than those with N1 SECP, and (3) survival of patients with SECD is not related to depth of tumor invasion or regional lymph node status.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 902.

The survival rate of patients with esophageal carcinoma is dismal, with 6% to 11% of all patients alive 5 years after diagnosis and treatment [1]. The majority of these patients are seen with dysphagia and have advanced stage III or IV carcinomas. Excellent 5-year survival, ranging from 56.7% to 78%, has been reported in patients undergoing surgical treatment of early-stage esophageal carcinoma [2--10]. Most of these patients, who were either asymptomatic or had mild symptoms, were diagnosed by cytologic screening or endoscopic surveillance in high-risk populations. Carcinomas with a good prognosis have been, in general, squamous cell carcinomas and have been classified as either superficial esophageal carcinomas, ie, carcinomas that have not infiltrated beyond the submucosa, or early esophageal carcinomas, ie, a subset of superficial esophageal carcinomas without regional lymph node metastases [11].

A growing appreciation of the malignant potential of Barrett's esophagus and the increasing use of surveillance endoscopy have resulted in more patients being diagnosed with and undergoing esophageal resection for superficial esophageal carcinomas [12]. Unlike the patients in previous studies, however, most of these patients have early-stage adenocarcinomas of the esophagus [13]. The literature contains scant data addressing the aggressive surgical management of these superficial carcinomas.

In addition to patients with superficial esophageal carcinoma at presentation (SECP) is another group of patients with superficial esophageal carcinomas. This group has advanced-stage esophageal carcinomas at presentation but is downstaged to no residual esophageal carcinoma or superficial esophageal carcinoma by induction therapy (SECD). Theoretically, surgical resection in these patients should produce better survival than expected given their initial stage, a survival perhaps similar to that of patients with SECP.

The purposes of this study were to evaluate the results of surgical resection and to identify predictors of improved survival for (1) patients with SECP and (2) patients with SECD.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Patient Selection
The hospital records of all patients who underwent surgical resection of an esophageal carcinoma at The Cleveland Clinic Foundation between September 1985 and October 1994 were retrospectively reviewed. Patients treated only with surgical resection and found to have a superficial esophageal carcinoma by postoperative pathologic staging were included in the study. These patients were classified as the SECP group. Superficial carcinomas were further classified as intraepithelial carcinoma (high-grade dysplasia [Tis]) or invasive carcinomas involving the lamina propria, muscularis mucosa, or submucosa but not invading beyond the submucosa (T1). T1 carcinomas were subdivided into intramucosal carcinomas, ie, those carcinomas invading the lamina propria or muscularis mucosa (intramucosal T1), and submucosal carcinomas, ie, those carcinomas invading the submucosa but not beyond (submucosal T1).

Patients with clinically advanced esophageal carcinomas (stage IIA or greater) treated with preoperative induction therapy followed by surgical resection and found to have superficial esophageal carcinoma or no residual carcinoma by postoperative pathologic staging were also included in the study. This group of patients was classified as the SECD group and included patients whose resection specimen revealed no residual tumor (T0), high-grade dysplasia (Tis), intramucosal T1 carcinoma, or submucosal T1 carcinoma.

Patient Evaluation
Preoperative evaluation included a medical history, physical examination, complete blood count, electrocardiogram, urinalysis, and serum chemistry studies. Pulmonary function tests were routinely obtained, and cardiologic evaluation was done if deemed necessary because of history, physical examination, or electrocardiogram. All patients underwent esophagogastroduodenoscopy with biopsy to verify the presence of high-grade dysplasia or invasive carcinoma of the esophagus. Clinical (pretreatment) staging included computed tomography of the chest and abdomen and, after 1987, endoscopic esophageal ultrasonography [14--16].

Induction Therapy
Induction chemotherapy was offered to all patients with carcinomas in clinical stage IIA or greater who had no evidence of distant metastases at diagnosis and normal renal, hepatic, and hematologic function. All 21 patients received concurrent radiation and chemotherapy with 5-fluorouracil and cisplatin. Seventeen patients were treated as part of an ongoing clinical trial [17]. This treatment regimen consisted of two preoperative courses of 4 days of continuous intravenous infusions of cisplatin (20 mg • m^-3 • d^-1) and 5-fluorouracil (1,000 mg • m^-2 • d^-1) beginning on day 1 and day 21 concurrent with a split course of accelerated fractionated radiation therapy, 1.5 Gy twice daily to a dose of 24 Gy and 21 Gy during cycles 1 and 2, respectively. Subsequently operation was performed followed by a single postoperative course of concurrent chemotherapy and 24 Gy of accelerated fractionated radiation therapy for patients with residual tumor at operation. Four patients were treated in a similar fashion, except with conventional fractionated irradiation. Induction therapy also included the intravenous administration of etoposide in 1 of these patients.

Surgical Therapy
Surgical esophageal resection, lymphadenectomy, and reconstruction using the stomach were performed by three different surgical approaches. Patients judged preoperatively to have high-grade dysplasia or clinical stage I carcinoma (T₁N₀M₀) underwent a transhiatal esophagectomy. One patient underwent resection and reconstruction with intrathoracic anastomosis through a midline laparotomy. Lymph node sampling was performed in all of these patients. Patients in the SECD group and those judged to have a stage IIA or greater carcinoma by clinical staging who refused induction therapy underwent esophageal resection through a left thoracoabdominal approach or a right thoracotomy and upper abdominal midline laparotomy. An extensive lymphadenectomy was performed in these patients. Patients with cervical esophageal carcinomas involving the larynx and pharynx underwent a pharyngolaryngoesophagectomy [18]. The esophagogastric anastomosis was constructed either in the neck or in the chest by a single-layer sutured or stapled technique.

Pathologic Analysis
Esophageal resection specimens were evaluated pathologically using a standardized protocol in which the resection margins, the esophageal body, the gastroesophageal junction, and the regional lymph nodes were extensively sampled. When gross lesions were identified, five sections of each lesion, including the area of deepest penetration of the esophageal wall, were evaluated. When a gross lesion was not identified, at least ten sections of the esophagus were evaluated. All separately resected lymph nodes and all lymph nodes that were grossly identified in the resection specimen were evaluated pathologically. When small enough, the entire lymph node was submitted, and two levels of that node were examined histologically. Larger lymph nodes were bisected, and two levels of each of the two portions of the bisected node were examined.

Statistical Analysis
Categorical factors were summarized using frequencies and percentages. The presenting histories of the SECP and SECD groups were compared using the ² and Fisher exact tests. Survival time was calculated from the date of operation to the time of death or last follow-up. The Kaplan-Meier [19] method was used to estimate survival, and the log-rank test [20] was used to prove differences in survival distributions between subgroups of interest. All tests were performed using a 5% significance level.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Superficial Esophageal Carcinoma at Presentation
From January 1, 1985, to November 1, 1994, at The Cleveland Clinic Foundation, 54 patients were determined by pathologic staging to have an SECP. Forty-nine (91%) were men, and 5 (9%) were women. The mean age was 63.1 years (range, 35 to 83 years). Twenty patients (37%) were in a Barrett's esophagus surveillance program. The presenting complaints and symptoms are listed in Table 1.

The operative approaches are listed in Table 2. Thirty-eight (70%) of the anastomoses were constructed in the neck.

Three patients (5.6%) died in the hospital. One patient with a Tis adenocarcinoma underwent a transhiatal esophagectomy. The postoperative course was complicated by adult respiratory distress syndrome and death. Two patients with T1 carcinomas (one intramucosal T1 and one submucosal T1) underwent left thoracoabdominal resection of the esophagus with the esophagogastric anastomosis in the neck. One of them had development of an anastomotic leak and empyema and died despite adequate drainage. The other died of a severe pneumonia.

Eleven deaths have occurred after discharge from the hospital during follow-up. One patient with high-grade dysplasia in a Barrett's esophagus died of a second primary malignancy (lung). Ten patients with T1 carcinomas have died, 6 (60%) of documented recurrent esophageal carcinoma.

Survival of patients with SECP at 5 years was 59.7%. Survival was not significantly related to age greater than 70 years (p = 0.672), sex (p = 0.270), smoking (p = 0.56), alcohol intake (p = 0.80), or anastomotic leak (p = 0.267). Survival was significantly decreased with increasing depth of tumor invasion (Fig 1), presence of regional lymph node metastases (Fig 2), squamous cell carcinoma, and respiratory complications (Table 3).

View larger version (16K): [in this window] [in a new window]   Fig 1. . Survival of patients with superficial esophageal carcinoma at presentation with reference to depth of tumor invasion.

View larger version (14K): [in this window] [in a new window]   Fig 2. . Survival of patients with superficial esophageal carcinoma at presentation with reference to presence of regional lymph node metastases.

Superficial Esophageal Carcinoma Downstaged
Twenty-one patients were determined by pathologic staging to have an SECD. Seventeen (81%) were men, and 4 (19%) were women. The mean age was 58.1 years (range, 26 to 72 years). The presenting complaints and symptoms are listed in Table 1. Patients with SECD were more likely to have dysphagia, weight loss, and chest pain at presentation than those with SECP. Pretreatment staging was adequate in 18 patients (Table 4).

The operative approaches are listed in Table 2. Seventeen (81%) of the anastomoses were constructed in the neck.

Four patients (19%) had a postoperative anastomotic leak, 1 with an intrathoracic anastomosis (1/4 or 25%) and 3 with a cervical anastomosis (3/17 or 17.6%). Five patients (23.8%) had postoperative respiratory complications.

Three patients (14.3%) died in the hospital. One patient with a T1 adenocarcinoma underwent an intrathoracic esophagogastric anastomosis, and an anastomotic leak and empyema developed. The patient died despite aggressive drainage. One patient with a T0 squamous cell carcinoma and alcohol-related liver disease died of respiratory failure and hepatic failure. The death of another patient with a T0 squamous cell carcinoma was secondary to a postoperative pulmonary embolism.

Three patients have died after discharge from the hospital during follow-up. All had recurrent carcinoma. All recurrences were distant, two in the liver and one in the lung.

Survival of patients with SECD at 5 years was 58.2%. Survival was not significantly related to depth of tumor invasion (p = 0.76), presence of regional lymph node metastases (p = 0.68), or histologic tumor type (p = 0.73). Survival was significantly decreased in patients with a postoperative respiratory complication (p = 0.035). Because of the small size of the SECD subgroups, the relationships of age, sex, history of smoking, alcohol abuse, and anastomotic leak to survival were not investigated. Although comparisons are difficult, the survival of this group is better than expected and is similar to that of the SECP T1 subgroup. The recurrence rate at 4 years was 23.3%.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The prognosis of patients with esophageal carcinoma is related to the stage of the disease at presentation. Most patients remain asymptomatic until the carcinoma has deeply invaded the esophageal wall and has metastasized to regional lymph nodes. The outlook for these patients is bleak despite aggressive surgical management. There is, however, a small percentage of patients who will undergo esophageal surgical intervention for superficial esophageal carcinomas. Most reports of such superficial carcinomas have originated from geographic regions where squamous cell carcinoma is endemic and where mass screening techniques have been implemented. Squamous cell esophageal carcinoma is considerably less common in North America, and screening of high-risk individuals has not been recommended. Thus, the western experience with superficial disease has been limited.

The changing epidemiology of esophageal carcinoma in North America, however, has resulted in the identification of a new high risk population. The awareness of the malignant potential of Barrett's esophagus and the aggressive investigation of patients with gastroesophageal reflux have increased the number of patients seen with superficial carcinoma. Unlike previous reports, however, the majority of these patients have superficial adenocarcinoma of the esophagus.

Previous reports of patients with superficial squamous cell carcinoma have demonstrated results remarkably similar to those in our study of predominantly superficial adenocarcinomas of the esophagus. Sugimachi and colleagues [9] reported a 56.7% 5-year survival rate compared with the 59.7% 5-year survival rate in this report. Similar predictors of reduced survival were also identified and included depth of tumor invasion and regional lymph node metastases. Both Nabeya [10], Sugimachi [9], and their co-workers have reported progressive decreases in 5-year survival in patients with superficial squamous cell carcinoma as invasion progresses from intraepithelial to intramucosal to submucosal, an observation mirrored by our results.

The association of deeper esophageal wall invasion with an increasing likelihood of lymph node metastases has also been reported by Sugimachi [9], Goseki [4], Bogomoletz [5], and their associates. Lymph node metastases were present in 5% to 8% of patients with intramucosal squamous cell carcinoma, an observation identical to our 5.6% incidence in patients with mainly intramucosal adenocarcinomas.

This finding of a small but definite incidence of regional lymph node metastases in patients with intramucosal esophageal carcinomas can be theoretically explained by the anatomy of the esophageal mucosa. Unlike the stomach, the small intestine, and the large intestine, the loose connective tissue of the lamina propria, which separates the esophageal mucosa from the muscularis mucosa, contains numerous vascular and lymphatic vessels [4]. Therefore, there is a definite risk of regional lymph node metastases even in patients with esophageal carcinomas invading the lamina propria and the muscularis mucosa. In the stomach, the vascular and lymphatic vessels are not found in the lamina propria or muscularis mucosa but in the submucosa. Goseki and co-workers [4] have found a similar frequency of lymph node metastases in submucosal gastric carcinomas and intramucosal esophageal carcinomas. Our observation of an increasing incidence of regional lymph node metastases in patients with submucosal as opposed to intramucosal esophageal carcinomas presumably reflects the increased total number of lymphatic vessels to which the submucosal tumor is exposed.

In this report, squamous cell carcinomas represented only 7.4% of cancers in the SECP group. If this study were to comprise solely superficial squamous cell carcinomas, it would have taken more than 120 years to acquire this experience. The difference in survival of patients with squamous cell carcinoma in this study may be an artifact of the size of the squamous cell group. However, if the overall results of our study are compared with others, it appears that regardless of histology, the overall survival of patients with superficial esophageal carcinoma is excellent, with predictors of poor survival being the depth of tumor invasion and the presence of regional lymph node metastases. There is a progressive decrease in survival as the tumor invades deeper into the esophageal wall, and an increasing incidence of regional lymph node metastases accompanies this invasion. Although this progressive decrease in survival with increasing T status may be entirely due to the increasing likelihood of regional lymph node spread, other unidentified factors could be at work. Further study of this entity will require careful stratification of these substages of T1 carcinomas if these predictors are to be identified.

Early identification and prompt surgical management of superficial esophageal carcinomas before dissemination by way of the lymphatics are crucial if survival from this lethal disease is to be improved. This observation reinforces our previous experience [21] with early aggressive management of high-grade dysplasia in patients with Barrett's esophagus. Expectant treatment after the detection of high-grade dysplasia will result in a 40% incidence of undetected intramucosal carcinoma and a 2% incidence of silent regional lymph node metastases in this group thought to have only intraepithelial carcinoma. Aggressive endoscopic monitoring of patients at risk and prompt surgical management of any patient with a diagnosed superficial esophageal carcinoma are mandatory.

The survival of patients with advanced esophageal carcinoma treated with surgical intervention alone has been so poor that multimodality treatment protocols employing chemotherapy, radiation therapy, and surgical resection have been developed. The hope is that neoadjuvant downstaging might be possible and that such downstaging might have a favorable impact on survival. Although theoretically attractive, the value of such induction therapy remains unclear. In an effort to address this question, we evaluated our patients who had experienced a marked response to preoperative induction therapy and whose carcinomas had been pathologically eradicated or downstaged to superficial esophageal carcinomas at the time of resection. These patients had a survival similar to that of patients in the SECP T1 subgroup and considerably better than expected given their initial staging.

Although clearly reflecting the select results of treatment in a responding subgroup, this is a remarkable observation that supports the concept of downstaging and the possibility that neoadjuvant therapy might favorably affect prognosis. An equally remarkable observation was the absence of local recurrences in this group despite advanced local-regional disease at presentation. In our SECD patient group, we were unable to relate patient survival to depth of tumor invasion or presence of lymph node metastases. Perhaps this was due to the small numbers of patients analyzed. However, this absence of an association between survival and depth of tumor invasion or regional lymph node metastases may be the result of the process of downstaging. The response to neoadjuvant therapy (downstaging) does not mirror the mechanism of tumor invasion and thus can result in a postinduction pathologic stage of T0 N1 M0.

Excellent long-term survival has been found in patients with superficial esophageal carcinomas treated by surgical resection. Patients with submucosal invasion or lymph node metastases have a worse prognosis than patients with high-grade dysplasia or intramucosal tumors and no regional lymph node metastases. Patients with advanced esophageal carcinoma that can be downstaged to superficial carcinoma appear to have a survival similar to that of patients with T1 superficial esophageal carcinoma, despite their more advanced stage at presentation.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Thirty-first Annual Meeting of The Society of Thoracic Surgeons, Palm Springs, CA, Jan 30--Feb 1, 1995.

Address reprint requests to Dr Rice, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Joseph F. Sabik Thomas W. Rice Thomas J. Kirby Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Sabik, J. F. Articles by Adelstein, D. J. Search for Related Content PubMed PubMed Citation Articles by Sabik, J. F. Articles by Adelstein, D. J. Related Collections Related Article