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Ann Surg. Aug 2000; 232(2): 225–232.
PMCID: PMC1421135

Improvement in the Results of Surgical Treatment of Advanced Squamous Esophageal Carcinoma During 15 Consecutive Years

Nobutoshi Ando, MD, FACS, Soji Ozawa, MD, FACS, Yuko Kitagawa, MD, Yotaro Shinozawa, MD, and Masaki Kitajima, MD, FACS

Abstract

Objective

To document the clinicopathologic characteristics and survival of patients undergoing esophagectomy for squamous carcinoma of the thoracic esophagus, and to examine the factors contributing to improvements in outcome noted in patients with advanced carcinoma.

Summary Background Data

Japanese and some Western surgeons recently have reported that radical esophagectomy with extensive lymphadenectomy conferred a survival advantage to patients with esophageal carcinoma. The factors contributing to this improvement in results have not been well defined.

Methods

From 1981 to 1995, 419 patients with carcinoma of the thoracic esophagus underwent esophagectomy at the Keio University Hospital. The clinicopathologic characteristics and survival of patients treated between 1981 and 1987 were compared with those of patients treated between 1988 and 1995. Multivariate analysis using the Cox regression model was carried out to evaluate the impact of 15 variables on survival of patients with p stage IIa to IV disease. Several variables related to prognosis were examined to identify differences between the two time periods.

Results

The 5-year survival rate for all patients was 40.0%. The 5-year survival rate was 17.7% for p stage IIa to IV patients treated during the earlier period and 37.6% for those treated during the latter period. The Cox regression model revealed seven variables to be important prognostic factors. Of these seven, three (severity of postoperative complications, degree of residual tumor, and number of dissected mediastinal nodes) were found to be significantly different between the earlier and latter periods.

Conclusions

The survival of patients undergoing surgery for advanced carcinoma (p stage IIa to IV) of the thoracic esophagus has improved during the past 15 years. The authors’ data suggest that this improvement is due mainly to advances in surgical technique and perioperative management.

In Japan, surgeons have the primary responsibility for treating patients with carcinoma of the thoracic esophagus. In the past two decades, advances in esophageal cancer surgery have been remarkable. These advances have included more accurate diagnostic and staging techniques, performance of radical esophagectomy with extensive lymphadenectomy, appropriate use of limited surgery, and improvements in perioperative management and adjuvant therapy. Consequently, a 5-year survival rate of more than 50%1 has been reported in patients who underwent three-field dissection. The aim of our study was to analyze the management and outcome of patients with carcinoma of the thoracic esophagus who underwent esophagectomy during a recent 15-year period to identify the factors contributing to the improvement in the management of this tumor.

METHODS

Patients

From 1981 through 1995, 638 patients with carcinoma of the esophagus were referred to the Department of Surgery, Keio University Hospital. Excluding 24 patients who underwent endoscopic mucosal resection for mucosal or submucosal lesions, 469 of 614 patients underwent esophagectomy, with a resectability rate of 73.5%. Forty patients with carcinoma of the hypopharynx and cervical esophagus and 10 patients with carcinoma of the esophagogastric junction were excluded from the study because the oncologic behavior and treatment of these lesions differ from those of carcinoma of the thoracic esophagus. A total of 419 patients thus were included in the series. There were 366 men and 53 women ranging in age from 35 to 83 years (mean age 62 years). The tumor was in the upper third of the thoracic esophagus in 57 of the 419 patients (13.6%), in the middle third in 229 (54.7%), and in the lower third in 133 (31.7%).

Surgery

We selected the surgical approach depending on the clinical assessment of the depth of tumor invasion and the location of the tumor. In patients with T1b (tumor invading the submucosa) 2 to T3 tumors, a total or subtotal thoracic esophagectomy through a right thoracotomy and regional lymphadenectomy were performed with curative intent. Lymphadenectomy was carried out not only in the mediastinum and the abdomen but also in the neck in some patients (so-called three-field dissection). The status of lymph node metastasis was analyzed in 116 patients who underwent three-field dissection between 1987 and 1995 to evaluate the incidence of metastasis more accurately. Esophagectomy with lymphadenectomy was followed by esophageal reconstruction, most commonly using a gastric tube. The colon was used in patients with a history of gastrectomy and in relatively young patients with early-stage lesions. 3 One-layer or two-layer hand-sutured anastomoses were used until 1982, after which stapled anastomoses were favored for esophageal reconstruction.

Because pTis and pT1a (tumor invading the lamina propria) 2 tumors are recognized to be curable by local resection alone without lymphadenectomy, 4 transhiatal esophagectomy without thoracotomy was performed for the patients with Tis and T1a tumors until 1990. Starting in 1991, endoscopic mucosal resection was performed in eligible patients, such as those with lesions smaller than 2 cm in diameter that were not multicentric. Starting in 1994, patients with suspected T4 tumors underwent chemoradiotherapy with the aim of downstaging the lesion. If downstaging was successful, patients underwent an attempt at resection. In rare patients in whom the main lesion was in the abdominal esophagus, a thoracoabdominal incision was favored.

Adjuvant therapy was administered to eligible patients. The modality used (radiation or chemotherapy) depended on protocols of the Japan Esophageal Oncology Group, which conducted four consecutive randomized controlled trials 5–8 during the study period.

Statistical Analysis

Outcome was evaluated at the end of 1998. The median follow-up period of censored patients was 79 months. Survival analysis was performed using the Kaplan-Meier method, and survival curves were compared using the log-rank test. Both cancer-related and noncancer-related deaths were included in the survival analysis. The 15-year duration of this patient series was divided into two periods, 1981 to 1987 and 1988 to 1995, to compare the results of surgical treatment and several other variables related to prognosis. The reason for choosing 1988 as the beginning of the latter period was that this was the time that advances in surgical treatment for esophageal carcinoma were introduced, including more extensive lymphadenectomy.

To evaluate the impact of prognostic factors on survival of patients with advanced esophageal carcinoma (p stage IIa to IV), multivariate analysis using the Cox regression model was carried out. The following variables were examined: age, gender, date of surgery (earlier vs. latter period), location of tumor (upper vs. middle and lower vs. middle), pathology of tumor (squamous cell carcinoma vs. other histologies), depth of tumor invasion (pT1b, T2, T3 or T4), status of lymph node metastasis (pN0, N1a [1–3 nodes involved], N1b [4–7 nodes involved], or N1c [>7 nodes involved]), 2 pathologic staging (p stage IIa, IIb, III, or IV), adjuvant radiation therapy (yes or no), adjuvant chemotherapy (yes or no), adjuvant chemoradiotherapy (yes or no), degree of residual tumor (R0 [negative] vs. R1 [microscopic positive] or R2 [macroscopic positive]), severity of postoperative complications (absent, moderate [complications not related to hospital death], or severe [complications related to hospital death]), and the number of dissected mediastinal nodes. Patients with p stage 0 (pTis N0) or p stage I (pT1 N0) disease, who are regarded as having early-stage carcinoma, were excluded from the analysis. Hence, the Cox regression model was applied to 341 patients. Variables found to be related to prognosis were examined to identify differences between the two time periods using the t test, the chi-square test, and the Mann-Whitney test. P < .05 was considered statistically significant. All calculations were performed with DANS software (Data Analyzing System, Sanwa Kaguku Co. Limited, Nagoya, Japan) on a computer. Clinicopathologic parameters were characterized according to the TNM classification of the International Union Against Cancer (UICC) 9 and its supplement. 2

RESULTS

Pathologic Characteristics

Pathologic T, N, and M category, stage, and pathologic classification of tumors according to the two time periods are summarized in Table 1. The proportion of pT1a and pT1b tumors (32%) in the latter period was approximately two times higher than in the earlier period (17%). The proportion of pT4 tumors (7%) in the latter period was half that in the earlier period (14%). The proportion of pN1 tumors during the entire study period was 62%, and the proportion of pN0 tumors was 38%. In terms of the status of lymph node metastases according to the depth of tumor invasion, all 33 patients with pTis and pT1a tumors were pN0. In 82 patients with pT1b tumors, 45 (55%) were pN0 and 37 (45%) were pN1. (In this series, the designation “pM1” represents pM1 lym detected by cervical lymphadenectomy in the latter period of the study.) The largest number of patients had p stage III disease, and the increased number of p stage IV patients in the latter period was due to the inclusion of pM1 lym patients who underwent cervical lymphadenectomy. The percentages of p stage IIa, IIb, III, and IV among the patients with advanced esophageal carcinoma were 25%, 19%, 52%, and 4% in the earlier period and 22%, 22%, 42%, and 14%, respectively, in the latter period. The number of dissected mediastinal nodes of p stage IIa to IV patients was 14.9 ± 7.9 (mean ± standard deviation) in the earlier period and 20.0 ± 11.7 in the latter period.

Table thumbnail
Table 1. PATHOLOGIC CHARACTERISTICS OF 419 PATIENTS WITH CARCINOMA OF THE THORACIC ESOPHAGUS

The status of lymph node metastases according to the location of the tumor is shown in Figure 1. The most common sites were the cervical and the upper mediastinal nodes in patients with carcinoma of the upper thoracic esophagus, and the lower mediastinal and perigastric nodes in patients with carcinoma of the lower thoracic esophagus. In patients with carcinoma of the middle thoracic esophagus, cancer was more likely to metastasize widely to the lymph nodes located from the neck to the abdomen.

figure 13FF1
Figure 1. Incidence of lymph node metastases according to the location of the tumor.

The pathologic classification was squamous cell carcinoma in 93% of resected specimens. Adenocarcinoma represented 4% of tumors, and in only two patients did the tumor arise from Barrett epithelium. Other histologies included adenoid cystic carcinoma, carcinosarcoma, and basaloid tumor.

Surgical Result

The resectability rate in patients with carcinoma of the thoracic esophagus was 76.2% (419/550). The resectability rate was 73.3% (162/221) in the earlier period and 78.1% (257/329) in the latter period. This analysis excluded patients who underwent endoscopic mucosal resection. An R0 resection was achieved in 149 patients (85.8%) in the earlier period and 241 (93.8%) in the latter period. Resectability according to the location of the tumor was 71.3% (57/80) in the upper thoracic esophagus, 74.8% (229/306) in the middle thoracic esophagus, and 81.1% (133/164) in the lower thoracic esophagus.

Surgical procedures are summarized in Table 2 according to approaches for esophageal resection and reconstruction. Right thoracotomy and laparotomy was the most common procedure. In the latter period, an increase was noted in the proportion of patients who underwent transhiatal esophagectomy without thoracotomy with curative intent for T1a tumors or with palliative intent for other tumors. The position of the conduit most commonly was the retrosternal position, followed by the orthotopic posterior mediastinum and the subcutaneous position. Since 1992, the posterior mediastinum has been the first choice for reconstruction, and it was the most common location in the latter period. The stomach was the most common conduit used for esophageal reconstruction, followed by the colon. Of 56 patients with colon interposition, 25 had a history of gastrectomy or a synchronous gastric cancer. In the remaining 31 patients, the stomach was reserved intentionally. The jejunum was used in a Roux-en-Y fashion in the posterior mediastinum, the abdomen, or the subcutaneous position.

Table thumbnail
Table 2. SURGICAL PROCEDURES FOR ESOPHAGEAL RESECTION AND RECONSTRUCTION

Of 419 patients who underwent resection, 7 died within 1 month of surgery, for a 30-day death rate of 1.7%. Thirty-three patients, including these seven, died in the hospital after surgery, for a hospital death rate of 7.9%. The hospital death rate was 11.7% (19/162) in the earlier period and 5.4% (14/257) in the latter period. Pulmonary complications, namely pneumonia and respiratory failure, and anastomotic leaks were the most common postoperative complications. Pulmonary complications developed in 94 patients (22.4%), 27.2% in the earlier period and 19.5% in the latter period. Anastomotic leaks and fistulas developed in 58 patients (13.8%). These closed spontaneously within 1 month of surgery in 36 patients (8.6%). In the remaining 22 patients (5.3%), closure required longer than 1 month or additional surgery.

Survival

The 1-, 2-, 3-, and 5-year survival rates for all patients were 71.4%, 52.5%, 46.8%, and 40.0%, respectively (Fig. 2). The 5-year survival rate was 52.5% in women and 38.1% in men (P = .0520). The 5-year survival rate was 35.2% in patients with carcinoma of the upper thoracic esophagus, 41.6% in those with carcinoma of the middle thoracic esophagus, and 40.3% in those with carcinoma of the lower thoracic esophagus. There were no significant differences between these groups (Fig. 3). The 5-year survival rate was 80% in patients with Tis, 100% with T1a, 70.8% with T1b, 30.1% with T2, 27.1% with T3, and 0% with T4 lesions. One patient with a Tis tumor died 18 months after surgery with no cancer recognized at autopsy. Significant differences between the groups are shown in Figure 4. The 5-year survival rate was 65.2% in patients with negative nodes (N0) and 24.8% in patients with involved nodes (N1) (P < .0001) (Fig. 5). The 5-year survival rate according to TNM stage was 80% for stage 0, 88.0% for stage I, 44.2% for stage IIa, 42.8% for stage IIb, 17.1% for stage III, and 13.2% for stage IV. Significant differences between the groups are shown in Figure 6. The overall 5-year survival rate was 17.7% in patients with advanced esophageal carcinoma (p stage IIa to IV) treated in the earlier period and 37.6% for those treated in the latter period (P < .001) (Fig. 7).

figure 13FF2
Figure 2. Overall survival curve of all patients who underwent esophagectomy between 1981 and 1995.
figure 13FF3
Figure 3. Survival curves according to the location of the main lesion.
figure 13FF4
Figure 4. Survival curves according to the depth of tumor invasion (T1a vs. T1b, P = .0009; T1b vs. T2, P < .0001; T1b vs. T3, P < .0001; T3 vs. T4, P < .0001).
figure 13FF5
Figure 5. Survival curves according to presence or absence of lymph node metastasis (P < .0001).
figure 13FF6
Figure 6. Survival curves according to TNM p stage (I vs. IIa, P < .0001; I vs. IIb, P < .0001; IIa vs. III, P < .0001; IIb vs. III, P < .0001).
figure 13FF7
Figure 7. Survival curves of p stage IIa to IV patients according to the date of surgery (P < .001).

Of the 15 demographic and clinicopathologic characteristics analyzed by the Cox regression model, 7 were identified as significant prognostic variables. The most important independent variable was the status of lymph node metastasis (P < .0001), followed by the severity of postoperative complications (P < .0001), the degree of residual tumor (P = .0019), the date of surgery (P = .0024), the number of dissected mediastinal nodes (P = .0121), gender (P = .0147), and depth of tumor invasion (P = .0252) (Table 3). Of these seven variables, three were found to be significantly different between the earlier and the latter periods: severity of postoperative complications (P = .0078), degree of residual tumor (P = .0267), and number of dissected mediastinal nodes (P < .0001).

Table thumbnail
Table 3. MULTIVARIATE ANALYSIS OF PROGNOSTIC FACTORS

DISCUSSION

It has been claimed that the prognosis of patients with carcinoma of the thoracic esophagus is dismal. 10 In our study, the 3- and 5-year survival rates for patients undergoing curative and palliative resection were 52.5% and 40.0%, respectively. Akiyama et al 1 have reported similar 3- and 5-year survival rates (52.6% and 42.4%) based on 913 patients treated during a 20-year period, although patients with surgical and hospital deaths were excluded. Orringer 11 has suggested that few Western surgeons have been able to duplicate these survival statistics because of a possible biologic difference between tumors in Japan and the West. Turnbull and Ginsberg 12 also stated that the 5-year survival rate after resection rarely exceeds 20%.

The patients studied were divided into two time periods, with the latter period beginning in 1988. This stratification was chosen because the years 1987 and 1988 marked a transition in the surgical treatment of esophageal carcinoma. Since this turning point, three-field dissections were performed routinely for patients with advanced carcinoma of the thoracic esophagus. When we focused on patients with advanced esophageal carcinoma (p stage IIa to IV), the 5-year survival rate of patients in the latter period was 37.6%, compared with 17.7% in the earlier period. We sought to identify the factors associated with this improvement. The T1 category was subclassified into T1a and T1b according to the TNM supplement in 1993 as a result of the different frequencies of lymph node metastasis. Our experience also revealed remarkable differences between pT1a and pT1b tumors. All pT1a patients were pN0, whereas 45% of pT1b patients were pN1. Therefore, patients with pT1b N1 or more invading tumors (p stage IIa to IV) were analyzed, and patients with pTis, pT1a, or pT1b N0 tumors (p stage 0 or I) were excluded from the Cox regression model.

The most important independent prognostic factor was the status of lymph node metastasis, including not only the presence or absence of involved lymph nodes (pN0/pN1) but also the number of involved nodes. Lerut et al 10 and Baba et al 13 also have shown lymph node metastasis to be a significant prognostic factor using the multivariate analysis, and Roder et al 14 have emphasized the ratio of invaded to removed lymph nodes as an important independent prognostic factor.

The severity of postoperative complications also was shown to be an important independent factor in the present study. Postoperative complications were categorized as none, moderate, or severe (the cause of a hospital death). The degree of residual tumor was also an important factor, as was the number of dissected mediastinal nodes. The average number of dissected mediastinal nodes, from the recurrent nerve node to the lower posterior mediastinal node, is considered an index indicating the extent of surgery. 15 In terms of gender, the Japanese nationwide study 16 revealed a significantly better survival rate for women. This phenomenon was attributed to the endocrine milieu in premenopausal women. 17

Depth of invasion was also an important factor. Skinner et al 18 reported that only the depth of invasion and the number of involved nodes are independent prognostic variables.

Although it was not identified as a significant predictor of outcome, the location of the tumor is usually considered an important factor because of the low survival rate of patients with carcinoma of the upper thoracic esophagus. 19,20 Although this tumor location was associated with the lowest survival rate, we believe that the number of patients in this group was too small to identify tumor location as an important prognostic factor. The distribution of tumor pathology is considerably different between Japan and Western countries. Squamous cell carcinoma represented 93% of the tumors in our series. Adenocarcinoma arising from Barrett epithelium is not common in Japan, and an increasing incidence of this condition has not been recognized. In studies by Orringer et al 21 and McLarty et al, 22 however, adenocarcinoma represented more than 60% of tumors. Holscher et al 23 considered adenocarcinoma of the esophagus to be of particular interest because of an increasing incidence of this tumor. Because this is not the case in Japan, tumor pathology was not identified as an important prognostic factor.

In terms of adjuvant therapy, the randomized controlled trials that took place during our study did not demonstrate a survival benefit, irrespective of treatment modality. The latest randomized trial of the Japan Esophageal Oncology Group comparing surgery alone with surgery plus chemotherapy (CDDP + 5-fluorouracil), however, demonstrated improved disease-free survival. 6

The severity of postoperative complications was different in the earlier and latter periods. A severe complication was defined as a postoperative complication that represented a possible cause of hospital death. The hospital death rate, which was 11.7% in the earlier period, decreased to 5.4% in the latter period. The proportion of pT4 tumors in the latter period was half that in the earlier period. The reason is that the 5-year survival rate in patients with T4 tumors who underwent esophagectomy with palliative intent was only 8.2% in Japanese surgeons’ experience. 16 No patients with a T4 tumor survived in our series. Therefore, palliative resection of T4 esophageal tumors is not warranted based on long-term survival or improved quality of life. Therefore, the R1·R2 resection rate, which was 14.2% in the earlier period, decreased to 6.2% in the latter period. Our philosophy is to avoid palliative esophagectomy for patients with T4 tumors. Since 1993, we have administered preoperative chemoradiotherapy to patients with suspected T4 tumors with the aim of downstaging. Only if downstaging is successful do we proceed with radical esophagectomy.

The average number of dissected mediastinal nodes of p stage IIa to IV patients, which was 14.9 in the earlier period, increased to 20.0 in the latter period. This difference was significant, although the numbers of dissected abdominal nodes in both time periods were not significantly different. Until 1987 to 1988, the right recurrent laryngeal nerve nodes, for example, had been dissected only up to the right subclavian artery as the uppermost point of superior mediastinal dissection, and the left recurrent nerve node dissection was incomplete. Since then, however, bilateral recurrent nerve node dissections have been extended to include the cervical portion as well. Hence, the increase in the number of dissected mediastinal nodes, in particular the superior mediastinal nodes, represents an improvement in the level of lymphadenectomy. 24

Three prognostic factors identified as significantly different between the two time periods were associated with the quality of surgical treatment of patients with advanced carcinoma of the thoracic esophagus: severity of postoperative complications, degree of residual tumor, and number of dissected mediastinal nodes. Our data suggest that this improved survival of patients undergoing surgery for advanced carcinoma (p stage IIa to IV), in particular squamous cell carcinoma, of the thoracic esophagus is due mainly to advances in surgical technique and perioperative management.

Our study was a retrospective analysis, and it had some not negligible issues of case selection bias, such as the content of surgical adjuvant therapy or the phenomenon of stage migration with three-field dissection. For example, tumors that were staged as p stage IV because of positive cervical nodes by three-field dissection in the latter period might have been regarded as p stage III in the earlier period. To prove the survival benefit of extended lymphadenectomy, a well-designed and well-conducted prospective randomized controlled trial is required.

Acknowledgment

The authors thank Norio Sugimoto, PhD, for performing multivariate analysis.

Footnotes

Correspondence: Nobutoshi Ando, MD, Dept. of Surgery, Keio University School of Medicine, 35, Shinanomachi, Shinjukuku, Tokyo 160-8582, Japan.

E-mail: nando@med.keio.ac.jp

Accepted for publication January 4, 2000.

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