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Eur J Cardiothorac Surg 2007;31:536-544. doi:10.1016/j.ejcts.2006.12.002
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

An audit of surgical outcomes of esophageal squamous cell carcinoma

Yih-Gang Goana,b,c,*, Huang-Chou Changa,d, Hon-Ki Hsua, Yi-Pin Choua

a Division of Thoracic Surgery, Department of Surgery, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan, ROC
b Department of Surgery, National Yang-Ming University, Taipei, Taiwan, ROC
c Department of Healthcare Administration, Tajen University, Pingtung, Taiwan, ROC
d Intensive Care Unit of Department of Surgery, Kaohsiung Veterans General Hospital, Taiwan, ROC

Received 7 September 2006; received in revised form 30 November 2006; accepted 4 December 2006.

* Corresponding author. Address: Department of Surgery, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan 813, ROC. Tel.: +886 7 342 2121x3044; fax: +886 7 3477618. (Email: goan{at}seed.net.tw).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 
Objective: Esophageal squamous cell carcinoma and adenocarcinoma were increasingly recognized as two entities with different biologic behaviors and prognosis. Surgical risks and oncologic benefits of transthoracic and transhiatal esophagectomy for esophageal squamous cell carcinoma patients are not confessed. Methods: Between 1994 and 2005, 216 esophageal squamous cell carcinoma patients underwent esophagectomy were enrolled and analyzed retrospectively. Results: One hundred sixty-six patients underwent transthoracic esophagectomy and 50 patients underwent transhiatal esophagectomy. The overall hospital mortality and postoperative complication rates were 9.7 and 49%, respectively. The amount of intra-operative blood loss or transfusion, postoperative complication rate, lengths of hospital stay and hospital mortality rate were not significantly different between both groups. However, shorter operative time was noticed in transhiatal group (p < 0.001). The overall 5-year survival rate was 16.8%. ESCC patients underwent either transthoracic or transhiatal esophagectomy had comparable long-term survival. The pTNM stage was independent prognostic factor for patients underwent transthoracic esophagectomy. However, location of tumor (p = 0.009) and pathologic tumor length (p = 0.012) were predictors of prognosis for patients underwent transhiatal esophagectomy. Conclusions: For esophageal squamous cell carcinoma patients, no significant differences in postoperative mortality or morbidity rates were observed between transthoracic and transhiatal esophagectomy. However, traditional pTNM staging system might underestimate the severity of esophageal squamous cell carcinoma patients who underwent transhiatal esophagectomy. The information of dissimilar prognostic factors for transhiatal or transthoracic esophagectomies will be helpful in tailoring more individualized adjuvant therapy to optimize esophageal squamous cell carcinoma patient's outcome.

Key Words: Esophagus • Squamous cell carcinoma • Esophagectomy • Prognostic factors


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 References
 
Esophageal cancer is a serious malignancy of digestive system with a fatal outcome in majority of cases [1]. Despite various beneficial effects of different therapeutic modalities have been reported, surgery remains the mainstay of treatment for esophageal cancer patients throughout the world. In the past decades, advances of surgical techniques have remarkably improved the outcomes of a substantial number of esophageal cancer patients. Up to 50% of 5-year survival rate and lower than 5% of surgical mortality rate could be achieved in selected centers [2]. However, such encouraging results are not always observed in published database and the long-term survival rate of esophageal cancer patients underwent surgical resection remains unsatisfactory [3–5].

Transthoracic esophagectomy (TTE) and transhiatal esophagectomy (THE) are the two most commonly utilized techniques for resection of esophageal cancers in the world [6]. One is intended to improve long-term survival by extended lymph-node dissection. Another aims at decreasing early postoperative risk by using limited cervicoabdominal approach without formal lymphadenectomy. The appropriateness and long-term effects of TTE and THE for esophageal cancer patients are debating between different expert centers in Asia and Western countries [6–8]. Although several previous nonrandomized studies endeavored to clarify the long-term benefits of both procedures on esophageal cancer patients, the results were conflicting and not always convictive [9,10]. Besides the different opinions on lymph-node dissection, such controversies might result from the recognition of esophageal squamous cell carcinoma and adenocarcinoma as two entirely different entities with different prognosis after surgical treatment [11,12] and various proportions of patients with different cell entities were pooled together to analyze the outcomes of patients underwent esophagectomy in previous trials [9,10].

Avoiding the influence of histological diversities on the benefits of esophagectomy, only ESCC patients were enrolled in this work to evaluate whether TTE with lymphadenectomy would provide sufficient improvement on overall survival rate and whether THE will result in lesser morbidity and mortality than TTE dose. More importantly, in addition to evaluating which patients will profit from TTE or THE approach, we also intend to identify useful independent indicators for scheduling more individualized adjuvant strategies to improve the dismal outcomes of ESCC patients underwent esophagectomy.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 References
 
2.1 Patients
Between February 1994 and January 2005, 573 consecutive ESCC patients were admitted to Division of Thoracic Surgery, Kaohsiung Veterans General Hospital. All patients had detailed preoperative diagnostic assessments consisting of chest roentgenogram, barium contrast study, UGI endoscopy with biopsy and histologic examination, Tc-99m whole body bone scan, computed tomography scan of the thorax and abdomen, and bronchoscopy if tumor ingrowth in the upper airway was suspected. The preoperative pulmonary function test, electrocardiograph, hematological and biochemistry tests were performed routinely. Among 573 patients, 246 patients (43%) underwent potentially curative surgical resection for esophageal cancers. After excluding those patients who received preoperative chemoradiotherapy or had the history of other nonesophageal tumors, a total of 216 ESCC patients underwent esophagectomies (81.8%) were subjects of this study. This study was approved by ethics committee of Kaohsiung Veterans General Hospital and all patients gave informed consent before surgery.

2.2 Surgical technique
Selection of operative procedure was decided by attending surgeon. No formal department policy existed at the time of the study. Right transthoracic subtotal esophagectomy and upper abdominal mid-line laparotomy with an extensive two-field dissection of regional lymph nodes was the standard procedure for resection of esophageal cancer in this hospital. However, transhiatal esophagectomy was usually performed in patients with limited cardio-pulmonary reserve who were unfit for thoracotomy. The extent of two-field lymphadenectomy included superior mediastinal, infracarinal, periesophagus, perigastric region and celiac axis lymph nodes. Only accessible mediastinal lymph nodes were dissected for transhiatal esophagectomy. Reconstruction of gastrointestinal tract continuity was usually restored with a gastric conduit. Left colon was used in patients who underwent gastrectomy previously. The substernal route was used for reconstruction in most instances. All anastomoses of esophagus and conduit were located in the neck. Hand-sewn cervical anastomosis was constructed by two-layer interrupt technique with absorbable monofilament suture materials. Percutaneous epidural analgesia (PCEA) was provided for pain relief in the first 3 days after surgery. Feeding jejunostomy was performed for postoperative nutritional support and steam inhalation with mucolytic agent was given for postoperative bronchial hygienic maintenance, routinely. The postoperative adjuvant radiotherapy or chemotherapy was administered in patients with evidence of extramural tumor invasion or regional mediastinal lymph node metastasis.

2.3 Follow-up
After hospital discharge, all patients were regularly seen at the outpatient department at interval of 3 months during the first 2 years and every 6 months thereafter. The contents of routine checkup consisted of physical examination, hematological tests, serum biochemistry, and chest roengenography. Computed tomography of thorax, ultrasonography of upper abdomen and Tc-99m whole body bone scan were performed yearly. Other studies were done only in symptomatic patients. All information of follow-up was compiled from medical records. An update inquiry about the present status of all surviving patients was conducted by telephone or letter contact in December 2005.

2.4 Statistics
The standard {chi} 2 test or Fisher's exact test was used for analysis in the case of categorical data. Student's t-test was used for comparing continuous data. The overall survival was constructed by Kaplan–Meier method and evaluated by log-rank test. Survival time was defined as the period between date of operation and date of death. The date and cause of death were confirmed either by telephone inquiry or by medical records. Both cancer-specific and noncancer-specific deaths were included in the analysis because the majority of patients died of cancer-related causes. Patients who died within 30 days after operation or the death happened at the same hospitalization of operation were excluded for survival analysis.

Only factors significant in univariate analysis were included for further Cox proportional hazard analysis in a forward stepwise procedure. A 0.10 level of probability was the significant value used for adding and deleting a co-variable from the model. All reported probabilities and their values were two-tailed and the p values less than 0.05 were considered as statistical significance. All statistical analyses were performed using the SPSS statistical software program package (SPSS version 10.0 for Windows, SPSS Inc., Chicago, IL).


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 References
 
A total of 216 ESCC patients underwent esophagectomy with cervical anastomoses were enrolled in this study. There were 206 males (95.4%) and 10 female (4.6%) patients. The average age of these patients was 64 years (range from 33 to 83 years). Among 216 patients, 166 patients (76.9%) underwent transthoracic esophagectomy and 50 patients (23.1%) underwent transhiatal esophagectomy.

3.1 Clinicopathologic characteristics
The demographic characteristics between patients underwent TTE and THE were listed in Table 1 . There were no significant differences in tumor lengths, depth of tumor invasion and tumor differentiation between two groups. However, patients in THE group were older (70 years vs 62 years; p < 0.001) and had poorer pulmonary function (FEV1, 1.9 vs 2.4 l/min; p < 0.001) as when compared with those in TTE group. Based on the TNM classification of the American Joint Commission on Cancer (1987), a significant number of patients in the TTE group had advanced pTNM stage (p < 0.05) and lymph node metastases (p < 0.05) than those in THE group. A significant number of patients underwent TTE were mid-esophageal tumors in contrast to a predominance of lower esophageal tumors in patients underwent THE (p < 0.001). A significant more number of lymph nodes were harvested by TTE than by THE (17 vs 8.7, p < 0.001).


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  		Table 1 Demographic characters of patients
 
3.2 Mortality and morbidity
There was no intraoperative death in this study. The overall hospital mortality rate was 9.7 and 9.6% (16/166) in TTE and 10.0% (5/50) in THE group without a significant difference. Pulmonary associated events were the major cause of postoperative mortalities in patients underwent TTE (p < 0.001) (Table 2 ).


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  		Table 2 Hospital mortality
 
The intraoperative factors and postoperative complications of TTE and THE groups were shown in Table 3 . The mean operative time was 5.3 ± 1.2 h for the THE group and 8.1 ± 1.5 h for the TTE group (p < 0.001). There was no difference in the amount of intraoperative blood loss and blood transfusion between the two groups.


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  		Table 3 Surgical outcomes and complications
 
The overall postoperative morbidity rate was 46.9% (106/226), and 50% in TTE group and 46% in THE group without significant difference (p = 0.620). The patterns and incidences of postoperative complications between these two groups were similar. The incidence of anastomotic leakage was 27.7 and 28% for TTE and THE groups, respectively. A trend of higher incidence of postoperative pulmonary complications was observed in patients underwent TTE (15.7%) as compared with those underwent THE (8%), but without statistical significance (p = 0.17) (Table 3).

3.3 Long-term survival
The follow-up was completed for all patients and ended at December 2005. The mean follow-up period was 25 months (range, 1 month to 11.2 years). One hundred ninety-five of 216 patients (90.3%) left hospital alive. At the end of follow-up, 38 patients (19.5%) still lived, 31 patients (20.7%) in TTE group and seven patients (15.6%) in THE group. Overall median survival was 511 days. The median survival of TTE and THE groups was 493 and 587 days, respectively. The overall 5-year survival rate was 16.8% in our present series. The estimated 3-, 5-, and 10-year survival rates in the TTE group were 25.4, 17.4, and 10.1%, respectively, whereas those in the THE group were 31.1, 15.7, and 13.1%, respectively (p = 0.702; Fig. 1 ).


Figure 1
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  		Fig. 1. Kaplan–Meier survival curve of patients underwent transthoracic and transhiatal esophagectomy. The 3-, 5-, and 10-year survival rates were 25.4, 17.4, and 10.1 for patients underwent TTE and 31.1, 15.7, and 13.1% for patients underwent THE (p = 0.702).

 
3.4 Analysis of risk factors
The clinicopathological variables that affect patient survival after esophagectomy were assessed with univariate and multivariate analyses (Table 4 ). In univariate analysis, advanced stage (IIb/III/IV), depth of tumor invasion (beyond muscularis), lymph node metastasis (N1) and pathologic tumor length (≥5 cm) were found to be significant risk factors for all patients underwent esophagectomies (p = 0.004, p = 0.006, p = 0.002, p = 0.037, respectively). The overall 5-year survival rate for stage 0/I was 27%, for stage IIA was 19%, for stage IIB was 17%, for stage III was 13% and for stage IV was 0% (Fig. 2 ). The overall cumulative survival curves in terms of depth of tumor invasion, lymph node involvement, and tumor size are shown in Fig. 2B, C and D, respectively.


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  		Table 4 Significant prognostic factors of survival
 

Figure 2
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  		Fig. 2. Prognostic factors of survival for all patients underwent esophagectomies. (A) Overall 5-year survival rates were 27, 19, 17, and 13% for stage 0/I, IIA, IIB, and III, respectively. There was no 5-year-survival for stage IV patients. (B) The estimated 5-year survival rates were 25.5, 18.6, and 16.5% for T0/1, T2, and T3 tumors, respectively. (C) Patients had poorer 5-year survival rate when lymph node was involved (13.7 vs 21.6%). (D) The 5-year survival rate of ESCC patients became worse when tumor was longer than 5 cm (20.2 vs 12.1%, p = 0.0131).

 
In patients underwent TTE, the pTNM stage, and depth of tumor invasion and lymph node metastatic status were significant factors influencing survival of patients. The 5-year survival rate of patients underwent TTE were 44, 20, 19, 12.7, and 0% for stage 0/I, IIA, IIB, III, and IV, respectively. Better long-term survival rate was observed in TTE patients with early-staged disease, superficial tumors, and negative lymph node involvement (Table 4 and Fig. 3 ).


Figure 3
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  		Fig. 3. Prognostic factors of survival for patients underwent transthoracic esophagectomy. (A) Overall 5-year survival rates were 44, 20, 19, and 13% for stage I, IIA, IIB and III, respectively. There was no 5-year-survival for stage IV patients. (B) The estimated 5-year survival rates were 36.5, 19.0, and 16.3% for T1, T2 and T3 tumors. (C) Patients had poorer 5-year survival rate when lymph node involved (14.1 vs 24.1%).

 
The traditional staging system did not provide a significant predicting effect of survival in THE group (p = 0.6231). However, tumor location and tumor size were significant factors influencing survival of patients underwent THE (Fig. 4 ). The 5- and 10-year survival rates of THE patients with tumor length less than 5 cm were 19.6 and 15.7%, respectively. The 5- and 10-year survival rates of THE patients with tumor located at upper/lower esophagus were 21.7 and 18%, respectively. Surprisingly, no 5-year survival could be observed in THE patients whose tumor was longer than 5cm or whose tumor located at mid-esophageal region (Fig. 4). A trend of better survival was observed in THE patients with tumors confining within the muscularis layer of esophagus (p = 0.0577).


Figure 4
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  		Fig. 4. Prognostic factors of survival for patients underwent transhiatal esophagectomy. (A) The pTNM staging system could not provide predictive vale for patients who underwent THE (p = 0.6231). (B). Patients whose tumor located at middle portion had poorer survival after transhiatal esophagectomy (p = 0.0085). (C) The 3-, 5-, and 10-year survival rates of patients having tumor less than 5 cm were 41.4, 22.6, and 18.8%, respectively. The 3-year survival rate of patients with longer tumor length was 12.5%.

 
In further multivariate analysis, depth of tumor invasion (beyond vs within muscularis, HR = 1.501, 95%: 1.062–2.123) and lymph node status (positive vs negative, HR = 1.565, 95% CI: 1.119–2.190) were independent prognostic factors for all patients underwent esophagectomies. However, only pTNM stage (IIb/III/IV vs 0/I/IIa, HR: 1.774, 95% CI: 1.176–2.675) was significant determinant of survival for patients underwent TTE. Noticeably, tumor location (middle vs upper/lower, HR: 3.509, 95% CI: 1.618–7.608) and tumor length (≥5 vs <5 cm, HR: 2.599, 95% CI: 1.253–5.392) were the significant prognostic factors for patients underwent transhiatal esophagectomy (Table 4).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
References
 
In this retrospective study of 216 ESCC patients, the postoperative morbidity and mortality rates were comparable between TTE and THE groups. Such finding consisted with the experiences of many previous reported results of esophagectomies [10,13,14]. Although lower than 5% postoperative mortality rate has been reported by several expert centers [15], our 9.7% overall hospital mortality rate is in line with the commonly published results of less than 10% [16]. Sepsis caused by pulmonary complications or cervical anastomotic leakage was the major cause of hospital death for patients underwent TTE. However, no predominant cause of death was observed in patients underwent THE in present series. The approximate 49% overall postoperative morbidity rate for both procedures considered in our study is also within the limit of less than 50% of recent surveys of esophagectomies [10,17]. Cervical anastomotic leakage was the most commonly encountered complication for all patients underwent esophagectomy in our series. The techniques of esophagectomy did not correlate with the risk of cervical anastomotic leakage.

Our approximate 28% leakage rate is similar to the result of 26% leakage rate for neck anastomoses reported by Chasseray et al. in a previously published randomized study [18]. Our result is also comparable with the experience of 23% leakage rate for manually suture neck anastomoses reported by Singh et al. [19], recently. The etiology of cervical esophageal anastomotic leaks is mutifactorial. However, there is no uniformly accepted explanation for this apparent high incidence of leakage up to now. The surgical experience, technique, the length of esophageal reconstruction, the tension of anastomoses, the compression of the conduit at the narrow thoracic inlet, the adequacy of gastric conduit vascularity, and impairment in oxygen delivery may be parts of the explanation [20,21]. The substernal route also has been supposed to be a potentially lethal factor for anastomosis leakage as it is longer and might result in more tension in the cervical anastomoses causing adverse effect on wound healing [22]. Accordingly, the uniform manner of positioning almost all the esophageal conduits in substernal route might be an important factor of the high risk of cervical leakage rate in present series. Besides, we found that the increased perioperative blood loss significantly correlated with the risk of cervical anastomotic leakage (486 vs 600 ml, p = 0.045).

Although more than 40% of 5-year survival rate after esophagectomy has been reported [23], the long-term results of esophageal cancer patients underwent esophagectomies still varies. The commonly reported five-year survival rates in modern series rarely exceed 30% and approximate 20% of 5-year survival rate is the most commonly observed result world-widely [4,5,24]. From a limited number of patients, our results of 68, 83, 64, 43, and 20% of 1-year survival rates for stage 0/I, IIA, IIB, III and IV diseases as well as the 45, 33, 39, 17, and 0% of 3-year survival rates for stage IIA, IIB and III diseases, respectively, were comparable with the recent results reported by Kukreja et al. [25]. The dismal 16.8% overall 5-year survival rate in present series is also comparable with previously reported results of 17–21.8% 5-year survival rates of only ESCC patients underwent esophagectomies [5,6,8]. Such unsatisfactory long-term survival might indicate that the ESCC is an insidiously progressed malignancy, and it was usually diagnosed and treated in more late-staged disease [25] just as seen in our patients. However, we cannot exactly provide the valid reason for a poor outcome of our clearly early-staged patients. This poor result might result from the patient number is small (N = 18) and approximate 30% (4/12) of non-cancer specific deaths were occurred in these early-staged patients.

In this more than 10 years’ experience of surgically resected ESCC patients, the result of comparable survival benefits between TTE and THE approaches corroborated the findings of several prospective randomized studies comparing the effectiveness of TTE and THE [10,24]. The pTNM stages, depth of tumor invasion (pT), lymph node metastasis (pN) and pathologic tumor length were still the significant prognostic factors of survival for all ESCC patients underwent esophagectomy. However, dissimilar independent prognostic factors for patients underwent TTE and THE were observed in our present work. The pTNM staging system was an independent prognostic factor of survival for patients underwent TTE as usual. The median survival of patients with advanced disease underwent TTE was significantly shorter than patients with earlier disease (11 vs 25 months, p = 0.006). Unexpectedly, the traditional pTNM staging system did not provide predictive effect on survival for patients underwent THE in our work. Such counterintuitive result might result from significantly fewer lymph nodes were harvested by THE than by TTE (8.5 vs 17, p < 0.001) which will lead to underestimating the existence of N1 diseases. The inadequate lymph node staging in THE group might erroneously down-staged the disease and confounded the result. Accordingly, it might be the explanation of why more patients with earlier stage disease in THE group did not present significantly higher long-term survival than patients underwent TTE and the trend of better survival was noticed in patients underwent TEE than those patients who underwent THE in early-staged 0-IIA patients (26.1 vs 14.9% 5-year survival rate). Noticeably, a poorer 5-year survival was observed in mid-esophageal cancer patients underwent THE than patients with upper or lower third tumors underwent THE in our series (p < 0.05), which is consisted with the experiences of Orriger et al. [12] and Chu et al. [24]. In the further analysis of 120 patients with mid-esophageal tumors, the 60, 28, and 19% of 1-, 3-, and 5-year survival rates of 106 patients underwent TTE also were significantly better than that of 42, 8, and 0% of 1-, 3-, and 5-year survival rates of 14 patients underwent THE (p = 0.004). The intra-thoracic metastases with or without evidence of local recurrences were the commonly encountered events for mid-esophageal cancer patients underwent THE in present series. It might reflect the possibility that THE might miss more unrecognized disseminated disease for intra-thoracic esophageal tumors [16]. Accordingly, the THE might not be able to provide adequate information of cancer control for intro-thoracic prevalent ESCC. Together with the different epidemiological prevalence and biologic behavior between sqaumous cell carcinoma and adenocarcinoma, our present results at least could partially clarify the doubt why Western surgeons preferred THE could not achieve as satisfactory benefits in Asia as it did in Western Countries.

In conclusion, the postoperative mortality and morbidity rates of TTE with lymphadenectomy were comparable with transhiatal resection for esophageal squamous cell carcinoma patients. Both TTE and THE could provide equivalent benefits of long-term survival for ESCC patients. For the intra-thoracic prevalent ESCC, traditional pTNM system might underestimate the severity of disease of patients underwent THE. The application of THE to mid-esophageal carcinomas requires more experience and selectivity to improve patients’ survival. However, THE would be a feasible technique for esophageal resection for patients with old age or poor pulmonary reserve. Of course, this is a small, nonrandomized and retrospective experience. The results of this study might be affected by historical bias, staging differences, and selective indications for the adopted surgical techniques. There might be also arguments with EUS biopsy or PET scan was not preformed pre-operatively resulting in inadequate LN staging in THE group which might have played as a major cause for the result of our study as well as the limitation of generalization of the conclusions as a single-institutional experience. Therefore, conclusions concerning the beneficial effects of TTE and THE for ESCC patients should be taken with precaution. Certain diagnostic measures such as EUS or PET scan should be recommended for providing more accurate clinical evaluation and further prospective clinical trials comparing groups with more similar risk factors are needed to confirm the long-term effect of esophagectomies for ESCC patients. However, the information of dissimilar prognostic factors for ESCC patients underwent TTE or THE will be helpful for doctors to make more feasible therapeutic decisions and tailor more individualized adjuvant therapy for patients underwent different surgical approaches to optimize outcomes of ESCC patients.


   Acknowledgments
 
This research was supported by grants from National Science Council, Taiwan, Republic of China, NSC-91-2314-B-075B-002 and Kaohsiung Veterans General Hospital, VGHKS- 91-107 (to Yih-Gang Goan).


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 

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