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Ann Thorac Surg 1995;59:1085-1090
© 1995 The Society of Thoracic Surgeons

Multimodality Therapy for Adenocarcinoma of the Esophagus

Division of Cardiothoracic Surgery, St. Louis University Health Sciences Center, St. Louis, Missouri

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Few reports exist detailing results of multimodality treatment for adenocarcinoma of the esophagus. We have treated 28 such patients using a preoperative regimen consisting of two courses of cisplatin and 5-fluorouracil with radiation (either 3,000 or 3,600 cGy). There were 25 men and 3 women (mean age, 62.9 years; range, 35 to 86 years), and 16 patients were known to have Barrett's esophagus. Dysphagia was present for a mean of 2.7 months, and the average weight loss was 6.5 kg. Tumors ranged from 2 to 10 cm in length (mean, 5.2 ± 1.8 cm) with American Joint Committee on Cancer clinical stage I in 2 patients, stage II in 19 patients, and stage III in 7. Dysphagia improved in 23 patients (82%), and in 8 (29%) no tumor was detected during radiologic and endoscopic staging after neoadjuvant therapy. Four patients refused operation. Esophagectomy via standard Ivor Lewis approach was accomplished in 20 of 24 patients (87%) undergoing operation. There were no operative deaths, and mean hospital stay was 15.5 ± 11.6 days. Four patients (17%) were complete responders with no tumor in the resected specimen. Actuarial survival in the 28 patients at 1, 2, and 3 years is 71%, 28%, and 20% respectively. Of the 20 esophagectomy patients, 6 are alive with no evidence of disease at 10, 50, 54, 70, 77, and 84 months. Three of these were complete responders. Only 1 of the 8 patients not undergoing resection is alive at 16 months with no evidence of disease after further radiotherapy and chemotherapy. These data suggest that preoperative combined modality therapy for adenocarcinoma of the esophagus is safe and effective treatment. It results in excellent symptomatic improvement, a complete response rate of 17%, and a significant chance for long-term survival.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 1090.

Combined modality therapy for esophageal carcinoma was originally undertaken for tumors of squamous histology. Because of early encouraging results, the utilization of combined modality therapy was broadened to include patients with adenocarcinoma of the esophagus. The purpose of this report is to analyze our results of combined modality therapy in the treatment of esophageal adenocarcinoma.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
From October 1, 1986, through December 31, 1993, 28 patients with esophageal adenocarcinoma believed to be resectable (T1–3, N0–1, M0) were seen at Saint Louis University Health Sciences Center. There were 25 men and 3 women ranging in age from 35 to 86 years (mean age, 62.9 years). All patients underwent a staging workup including barium swallow, computed tomography of the chest and upper abdomen, and esophagoscopy with biopsy. Patients with upper and mid-esophageal lesions underwent bronchoscopy to rule out tracheal involvement. Signs, symptoms, or hematologic values suggestive of musculoskeletal or neurologic involvement were evaluated with bone scan or computed tomographic scan of the head. Both preoperative and pathologic staging was performed according to the criteria outlined by the American Joint Committee on Cancer [1].

Sixteen of the 28 patients (57%) carried a diagnosis of or were discovered to have Barrett's esophagus. One of these patients had undergone a prior Nissen fundoplication. All but 2 of these patients suffered from dysphagia, which varied in duration from 1 to 8 months (mean, 2.7 months). Weight loss was reported in 21 patients (75%) and averaged 6.5 kg (range, 0 to 27 kg) among the entire group. Tumor length could be measured endoscopically in 27 patients, and varied from 2 to 10 cm in length (mean, 5.2 cm). One patient had a totally obstructing tumor, which precluded endoscopic length assessment.

The treatment regimen consisted of preoperative chemotherapy and radiation therapy given in and out of the hospital during a period of 5 weeks. After a 3-week rest period, patients were referred for esophagectomy. The initial chemotherapy regimen consisted of intravenous 5-fluorouracil (5-FU) (1 g • m^-2 • day^-1), given by continuous 24-hour infusion in the hospital on days 1 to 4, plus cisplatin (25 mg • m^-2 • day^-1) administration for 1 hour on days 1 to 4, with vigorous hydration (2.5 L saline solution per day). Patients were discharged on hospital day 6 and referred for an identical course of chemotherapy on days 25 through 34 (week 5). Radiation therapy was delivered by means of an 18 MeV linear accelerator via a 20 x 8-cm port centered on the primary tumor. For tumors in the distal area of the esophagus, this port also included the celiac lymph nodes. Radiation was delivered in anterior and posterior ports in daily fractions of 200 cGy/day, 5 days per week during the first 3 weeks of treatment, for a total delivered dose of 3,000 cGy.

After the first 8 patients, this regimen was changed in an attempt to maximize the radiosensitizing effect of 5-FU. For the last 20 patients, a silicone rubber central venous catheter was inserted and patients received 5-FU continuously for 24 hours at 500 mg • m^-2 • day^-1 for 5 days each week over a 4-week period. Cisplatin was given at a dose of 20 mg • m^-2 • day^-1 administered for 1 hour during weeks 1 and 4 (days 1 to 5 and 22 to 26). The radiation therapy was changed to a daily fractional dose of 180 cGy given on weekdays and continued throughout the 4 weeks of chemotherapy administration, yielding a total delivered dose of 3,600 cGy. It was expected that the simultaneous administration of 5-FU and radiation would take maximal advantage of the proposed synergistic effect of these two modalities. Three weeks after completion of radiation, the patient was restaged. Unless distant metastasis was identified, the patient was referred for esophagectomy.

The esophagectomy was performed using a standard Ivor Lewis approach and encompassed the primary tumor, cardia, and lesser curvature of the stomach. Ten-centimeter proximal and distal margins were obtained whenever possible, and lymph nodes were sampled from the celiac and thoracic areas. All patients had a pyloromyotomy or pyloroplasty. The alimentary tract was reconstructed by advancing the gastric remnant into the posterior mediastinum. A high intrathoracic anastomosis was performed in 27 patients (96%) and a cervical anastomosis in 1. All intrathoracic anastomoses were fashioned with an end-to-end stapling device or hand sewn in two layers consisting of an inner layer of continuous 4-0 polydioxanone sutures and an outer layer of interrupted 3-0 silk sutures. In the majority of patients the anastomosis was wrapped with an omental pedicle based on the right gastroepiploic vessel and fixed in place with interrupted 4-0 silk stitches. The cervical anastomosis was hand sewn with the same two-layer technique with no omental wrap. Before closure, a tube jejunostomy was constructed for enteral alimentation, which began on the second postoperative day. On the seventh postoperative day, barium swallow was performed and oral alimentation begun if no extravasation was noted. The mean operative blood loss was 919 mL (range, 500 to 2,500 mL).

Statistical analysis was performed with a computer software package (Statview 4.0; Abacus Concepts, Inc, Calabasas, CA). The values are expressed as mean ± standard deviation. Continuous variables were compared by Student's t test, and discrete variables were compared with a ² test using the Yates correction. Survival curves were constructed via the method of Pearson and Gage and compared with a Mantel-Haenzel log rank analysis. Values of p less than 0.05 were considered significant.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Chemoradiation Morbidity and Outcome
The preoperative chemoradiation regimen generally was tolerated well. Significant morbidity included nausea in 16 (57%), esophagitis in 13 (46%), vomiting in 10 (36%), neutropenia in 7 (25%), infections requiring antibiotics in 5 (18%), subclavian or superior vena caval thrombosis in 2 (7%), requirement for blood transfusion in 2 (7%), transient elevation of creatinine level in 1 (4%), and a significant bleeding episode in 1 (4%). In 1 patient Candida esophagitis and fungemia developed, which required amphotericin. There were two additional complications. One patient noted the onset of angina during chemotherapy and radiation, and required treatment with percutaneous transluminal coronary angioplasty, which delayed the second cycle of chemotherapy. In 1 patient a perforated duodenal ulcer developed during his neoadjuvant therapy, which necessitated emergency vagotomy and pyloroplasty. Only 7 patients (25%) had an absolute granulocyte nadir less than 1,000/µL, whereas only 2 patients (7%) had a platelet count of less than 100,000/µL. These problems accounted for an overall treatment delay of greater than 7 days in 14 patients (50%).

Dysphagia improved in 23 patients (82%). Ten of 28 patients (36%) maintained their weight or gained weight (up to 4 kg) during the course of preoperative therapy; the remaining patients lost between 1 to 12 kg during treatment. The average weight change in all 28 patients was -2.9 kg (median, -1.5 kg). There was no mortality attributable to preoperative chemoradiation.

Staging undertaken after this preoperative regimen consisted of barium swallow, chest computed tomographic scan, and repeat endoscopy with biopsy. The clinical stage worsened in 1 patient (4%), was stable in 11 (39%), and improved in 16 (57%). Repeat endoscopic biopsy performed at the original tumor site was positive in only 7 patients (25%). All 28 patients were referred for surgical intervention.

Surgical Result and Morbidity
Four of the 28 patients (14%) referred for operation refused because their dysphagia had been relieved. Nonsurgical therapy was strongly recommended, and all 4 agreed to further radiation therapy (between 1,800 and 3,300 cGy) and 2 accepted further chemotherapy (two cycles in each). The remaining 24 patients (86%) agreed to an operation. In 4 of the 24 patients (16%) esophagectomy could not be performed secondary to matted malignant celiac adenopathy in 3 and aortic invasion in 1. Postoperative complications in this unresected group included pneumonia and seizure in 1 patient each. One month after discharge, a small bowel obstruction requiring adhesiolysis occurred in 1 of these patients. All were referred for and underwent postoperative radiation therapy (2,400 to 3,400 cGy) and chemotherapy.

One patient undergoing esophagectomy suffered an intrathoracic anastomotic leak and had development of sepsis, pneumonia, adult respiratory distress syndrome, atrial fibrillation, and prolonged ventilator dependence. Additional complications were as follows:

The mean hospital stay for all operative patients was 15.2 ± 11.5 days (range, 4 to 60 days) with a median of 12 days. No patient died in the hospital or within 30 days of operation. No patient died of an operative complication after discharge.

Pathologic Staging
Lymph nodes were positive for adenocarcinoma in 10 of the 24 patients (42%) undergoing operation. Surgical margins were negative in all 20 resected patients. Pathologic examination of resected specimens found no histologic evidence of cancer in 4 of 24 patients (16%) undergoing surgical procedures. The initial clinical staging in these complete responders demonstrated 3 were in stage II and 1 patient was in stage I. Three of the 4 complete responders were found on pathologic inspection to have concomitant Barrett's mucosal changes. None of these patients were under surveillance for their Barrett's esophagus. Final pathologic staging in the remaining 20 patients undergoing operation revealed 5 in stage I (21%), 5 in stage II (21%), and 10 in stage III (42%).

Survival and Recurrence
Follow-up was obtained from all patients during office visits or telephone interviews in October 1994, yielding a median follow-up time of 50 months. One of the 4 patients who refused surgical intervention is alive at 16 months with no evidence of recurrent disease. The other 3 died of their cancer within 11 months. All 4 patients found to have unresectable disease died of cancer within 15 months. Of the 20 patients undergoing a ``curative'' esophagectomy, 12 had development of recurrent disease and all died within 3 years. Recurrence was local in 4 (33%), distant in 6 (50%), and simultaneous (both local and systemic) in 2 (17%) as follows:

In 2 of the 20 patients with resected disease pneumonia developed; they died of respiratory failure at 12 and 16 months with no recurrence. At the time of follow-up, 21 patients have died, 19 due to persistent or recurrent tumor. There are 7 patients who are alive with no evidence of disease at intervals ranging from 10 to 84 months after the initial diagnosis. This group includes 3 of the 4 complete responders, who are alive at 70, 77, and 84 months.

The actuarial survival for all 28 patients is depicted in Figure 1. Median survival was 18 months with 1-, 3-, and 5-year survivals of 71%, 28%, and 20%, respectively. Figure 2 compares the actuarial survival curves of the 24 operative (nonrefusal) patients stratified into a complete response group (n = 4) and the group of partial and nonresponders (n = 20). Survival was significantly (p = 0.016) better in those patients achieving a complete histologic response. Median survival was 17 months for noncomplete responders, but had not been reached in the complete response group.

View larger version (16K): [in this window] [in a new window]   Fig 1. . Actuarial survival curves for all 28 patients entered into the protocol. Error bars indicate standard error.

View larger version (17K): [in this window] [in a new window]   Fig 2. . Actuarial survival curves for the four complete responders (triangles) and the 20 partial and nonresponders (circles) are depicted. Mantel-Haenzel log rank analysis reveals a significant difference (p = 0.016).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Table 1 depicts results of several phase II trials of combined chemotherapy and radiation therapy for esophageal adenocarcinoma [18–21]. For several of these reports results were sifted from the data, which reported both squamous carcinoma and adenocarcinoma patients [18–20]. Median survivals ranged from 11 to 36 months, with 3-year survivals in the range of 25% to 52%. Nearly all the studies included 5-FU and cisplatin with radiation doses varying from 3,000 to 4,900 cGy.

It is this lack of demonstrable benefit for the entire patient population coupled with the invasive nature of surgical procedures that may dissuade many physicians from considering surgical intervention. Although operation has been regarded as the cornerstone of treatment for many decades, there is little evidence from prospective randomized trials to demonstrate that surgical resection is superior even to radiotherapy alone. The relatively high response rate of combined chemotherapy and radiation therapy has prompted oncologists and radiotherapists to attempt definitive treatment of esophageal carcinoma without including surgical resection as a component of therapy. Whittington and associates [23] reported retrospectively their results using 5-FU and cisplatin plus 6,000 cGy in patients with both early and advanced esophageal carcinoma. Twenty-six of these patients had adenocarcinoma and were treated without operation. The investigators reported good response with a median survival of 9 months and an actuarial survival of 11% at 2 years.

In 1991, Coia and associates [24] reported a subset of 16 patients with early stage I and II disease to whom ``curative'' chemoradiation was administered. The median survival was 20 months with a 3-year actuarial survival of 38%. Herskovic and colleagues [25] also have reported on a nonoperative approach for esophageal carcinoma in a multiinstitutional study carried out by the Radiation Therapy Oncology Group. In this randomized study, the investigators prospectively compared radiation therapy alone to combined radiation and chemotherapy for definitive treatment of esophageal carcinoma. Fourteen patients in the study were identified as having adenocarcinoma, but the results in this small subset were not specified. However, in the group as a whole, patients treated with aggressive chemotherapy and radiation followed up for a median of 38 months were noted to have a 3-year survival of 31% with 14 long-term survivors with no evidence of disease past 3 years. These studies demonstrate that a subset of patients with esophageal carcinoma respond well to combined chemotherapy and radiation therapy, and many oncologists thus believe that esophageal cancer may be treated definitively with these two modalities alone.

In the past, practitioners dealing with this difficult disease have attempted to prove one modality as superior to others for the treatment of esophageal carcinoma. It is becoming increasingly clear that the best prospect for cure lies in a combination of different modalities to forge a treatment regimen and that these modalities should be used in a complementary rather than a competitive fashion. Chemotherapy and radiation therapy when combined do appear to yield a high incidence of tumor shrinkage. The goal in the future will be to identify those patients in whom the addition of surgical resection will provide an added survival advantage versus continued therapy with chemoradiation. Identification of such patients may occur via new diagnostic imaging technology such as endoscopic ultrasound or may be accomplished via more sophisticated testing such as identification of immunologic or genetic markers predictive of beneficial response.

In addition, it is hoped that variations in the three major treatment modalities might prove helpful in producing incremental improvements in survival. Radiation therapists are investigating the use of hyperfractionation and radiosensitizers to improve the efficacy of their therapy. Oncologists continue to seek new, more active anticancer agents and to devise more aggressive yet tolerable regimens. New developments also continue in the surgical field. Controversy continues to exist regarding the extent of the surgical procedure that is most beneficial, because no definitive survival advantage has been demonstrated to result from the radical procedure proposed by Skinner nor with the minimalist transhiatal approach championed by Orringer. Surgeons in Japan and Europe currently are undertaking aggressive three-field lymphadenectomy with encouraging preliminary results. It is clear at this time that the ``magic bullet'' has not been discovered, and that further research with randomized studies are required.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Address reprint requests to Dr Naunheim, Department of Surgery, St. Louis University Health Sciences Center, 3635 Vista Ave at Grand Blvd, St. Louis, MO 63110-0250.

	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 Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Naunheim, K. S. Articles by Baue, A. E. Search for Related Content PubMed PubMed Citation Articles by Naunheim, K. S. Articles by Baue, A. E.