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Interact CardioVasc Thorac Surg 2005;4:180-183. doi:10.1510/icvts.2004.105031 © 2005 European Association of Cardio-Thoracic Surgery
Oesophagectomy for squamous cell carcinoma: lessons from a decade of consecutive resectionsThoracic Surgery Unit, Nottingham City Hospital, Hucknall Road, Nottingham NG5 1PB, UK Received 21 December 2004; received in revised form 19 February 2005; accepted 22 February 2005
*Corresponding author. Tel/Fax- +44 115 969 1169.
The aim of this study was to analyse the outcome following oesophageal resection for squamous cell carcinoma (SCC) in a large volume unit. Between 1987 and 1997, 166 patients with SCC underwent oesophagectomy. The outcomes and pathological characteristics of this cohort were then analysed. Operative mortality was 6% (10 patients). Anastomotic leak occurred in 11 (6.6%). A history of previous respiratory disease and anastomotic leak were independent predictors of early mortality (P=0.02). Pathological examination demonstrated the presence of stage I disease in 8, stage IIa in 58, stage IIb in 14 and stage III in 87 patients. Kaplan–Meier survival at 1, 3 and 5 years for all patients was 71.6%, 44.6% and 33.5%. Five-year survival was 87.5% for stage I, 47.1% for stage IIa, 27.4% for stage IIb and 14.5% for stage III. On multivariate analysis, pathological stage (P=0.001) and presence of involved lymph nodes were independent adverse predictors of survival (P<0.0001). In conclusion, oesophagectomy for SCC carries an acceptable risk, which is higher for those having a respiratory disease and those developing an anastomotic leak. The good survival observed in early pathological stages and the presence of long-term survivors amongst those with locally advanced disease are encouraging.
Key Words: Oesophagectomy; Squamous cell carcinoma
Although hospital mortality and long-term survival have improved considerably following oesophageal resection for carcinoma over the last two decades, oesophageal cancer remains one of the most lethal gastrointestinal tumours [1,2]. Despite the apparent consensus that surgery should be performed where possible at high volume centres [3], there exist differing opinions as to whether results can further improve by performing more extensive resections [4–6]. The purpose of this paper was to analyse our evolving experience in the surgical management of squamous cell carcinoma of the oesophagus, and to analyse the short and long-term clinical results obtained.
From 1987 to 1997, a total of 198 patients with histologically proven SCC of the oesophagus with no evidence of metastatic disease on preoperative assessment, who were considered medically fit for operation, underwent surgical exploration with a view to oesophagectomy. In 166 patients (83.8%) the tumour was resected. These patients are the subjects of this report. There were 89 male and 77 female patients with a mean age of 64.4 years (range 37–85 years). 2.1. Preoperative physical and oncological evaluation Preoperative evaluation was by means of a number of techniques including physical examination, haematological and biochemical investigations, chest X-ray, barium meal, abdominal ultrasound, CT scan and oesophago-gastroscopy. Bone scan was performed only if it was specifically indicated. Major airways involvement by tumour was excluded where appropriate by bronchoscopy. Pulmonary function tests and ECG were performed routinely. Exercise tolerance testing was performed in all patients above the age of 70 years; those with lung volumes of less than 60% of predicted value for age and height and those with significant ischaemic changes on the ECG.2.2. Surgery None of the patients received pre- or post-operative chemotherapy or radiotherapy. Patients who underwent a transthoracic oesphagectomy underwent routine mediastinal dissection included excision of all peri-oesophageal tissues with the sub-carinal, paratracheal and parahiatal lymph nodes, both parietal pleurae and the aortic adventitia. In the abdomen the lymph nodes from the left gastric artery pedicle were routinely excised, flush ligation of the left gastric pedicle being achieved by application of a vascular stapler. A nasogastric tube was inserted upon completion of the oesophago-gastric anastomosis. A pyloromyotomy was not performed routinely. The discovery of tumour at stage IV on surgical exploration was considered as a contraindication for resection.2.3. Postoperative management After the operation the patients were transferred to the Intensive Care Unit for a short period to allow elective removal of the endotracheal tube before their return to the ward. Postoperative analgesia was provided by means of continuous infusion of a local anaesthetic (bupivacaine) and an opioid (fentanyl) mixture through an epidural catheter. Fluids were given intravenously (crystalloid solutions, blood or other colloids) in order to maintain adequate hydration, stable haemodynamics and a haemoglobin level greater than 10 g/dl. Parenteral or enteral nutrition was not used. Barium swallow was carried out on the seventh postoperative day to check for anastomotic leakage prior to the removal of nasogastric tube and commencement of oral feeding.2.4. Follow-up The unit policy is for life-long follow-up. Information was obtained from the patients' medical records, the patients' medical practitioners, and the Thoracic Surgery Audit database.2.5. Definitions and statistics Operative mortality includes death within 30 days since the operation or during the same hospital admission. The impact of 18 variables on operative mortality and survival (age, gender, symptom duration, weight loss, previous respiratory disease, cardiovascular disease, diabetes mellitus, tumour site, tumour length, type of operation, year of operation, surgeon, anastomotic leak, respiratory complications, cardiovascular complications, involved lymph nodes, and pathological stage) was assessed with univariate and multivariate analyses. Means were compared with t-test, proportions with Chi-square or Fisher's exact test as appropriate. Survival was calculated with the Kaplan–Meier method and the resulting curves compared with the log-rank test. Multiple logistic regression analysis and Cox proportional hazards regression models were used to identify predictors of operative mortality and overall survival. A P<0.05 was considered significant. Statistical analysis were performed with SPSS PC (version 11.0) (SPSS Inc., Chicago, IL, USA).
3.1. Clinical and pathological features Dysphagia (94%) and weight loss (42%) were the most common presenting symptoms. Sixteen patients (9.6%) had a history of respiratory disease (namely chronic obstructive airways disease, asthma or tuberculosis), 42 patients (25.3%) had history of cardiovascular disease (ischaemic heart disease, hypertension, myocardial infarction, peripheral vascular disease or deep venous thrombosis) and 12 patients (7.2%) had diabetes mellitus. The tumours were situated in the upper third of the oesophagus in 14 patients (8.4%), in the middle third in 90 (54.2%), in the lower third in 50 (30.1%) and in the lower third and gastro-oesophageal junction in 8 patients (4.8%). The mean tumour length was 5.2 cm, ranging from 2.4 to 11 cm. 3.2. Operative data, operative mortality and morbidity The surgical approach to the tumours is shown in Table 1. All nine transhiatal resections were performed in the first four years of this study, but the technique was later largely discontinued. The oesophagogastric anastomosis was performed using a single layer 3/0 non-absorbable suture 26 patients (16%); all of whom underwent resection in the first four years of the study period; whilst anastomosis with a circular stapling device was performed in the remaining 140 patients (84%).
Ten patients died in hospital or within 30 days after their operation giving a hospital mortality of 6%. Causes of death were anastomotic leak complicated by sepsis in 4, pneumonia in 3, myocardial infarction in 1, pulmonary embolus in 1 and aortic rupture intra-operatively in 1 patient. Previous respiratory disease (P=0.02) and occurrence of anastomotic leak (P=0.02) were significant multivariable factors for operative death. Fifty-six patients (33.6%) experienced significant postoperative complications. These were respiratory in 34 (20.4%), cardiovascular in 10 (6%), atrial fibrillation in 35 (20.5%), anastomotic leak in 11 (6.6%) and chylothorax in 8 patients (4.8%). 3.3. Pathological staging The excised lymph nodes were involved by cancer cells in 92 patients (55.4%). Pathological staging (p TNM) was accomplished according to the criteria proposed by the American Joint Committee on Cancer (AJCC) (12). Stage I disease was present in 8 patients (4.8%), stage IIa in 58 patients (34.9%), stage IIb in 14 patients (8.4%) and stage III in 87 patients (52.4%) (12).3.4. Survival Kaplan–Meier, survival at 1, 3 and 5 years for all (n=166) patients, including operative mortality, was 71.6, 44.6 and 33.5% and the median survival was 31 months (95% CI 19.4–42.6 months) (Fig. 1). If the operative mortality was excluded from the analysis the 1, 3 and 5 year survival was 76.1, 46.7 and 35.5%, respectively, and the median survival was 32 months (CI 11.6–52.5 months).
The 1, 3 and 5 years Kaplan–Meier survival in patients with negative lymph nodes was 87.2, 67.4 and 53% and the median survival was 70 months (95% CI 48.5–91.5 months). In the patients who were found to have lymph nodes involved by the disease process the 1, 3 and 5-year survival was 58.6, 22 and 13.7% and the median survival was 15 months (95% CI 10.9–19.1 months), P<0.0001 (Fig. 2).
Survival at 5 years was 87.5% for stage I (median 98 months, 95% CI could not be calculated), 47.1% for stage IIa (median 57 months, CI 35.1–79 months), 27.4% for stage IIb (median 33 months, CI 8.5–57.5 months) and 14.5% for stage III (median 15 months, CI 11.6–18.4 months) (P=0.001) (Fig. 3).
On Cox proportional hazards regression analysis, P TNM stage and presence of involved lymph nodes were independent adverse predictors of survival (P<0.0001). 3.5. Palliation of dysphagia Good palliation of dysphagia amongst the hospital survivors (n=106) was achieved in 86 patients (80.2%). The remaining 20 patients developed following their discharge from the hospital various degrees of dysphagia and required 1–5 oesophageal dilatations.
Although the incidence of oesophageal cancer is rising rapidly in the Western World, the incidence of squamous as opposed to adenocarcinoma has remained static over the last two decades [7]. By contrast, there has been an encouraging trend in reduction of mortality and morbidity following surgical resection. A review of the world literature by Earlam and Cuhna-Melo in 1980 [8] reported a disappointing 30% operative mortality and a further review by Muller et al. in 1990 [1] showed this to have been decreased to 13%. The 6% mortality in these series represents thus a dramatic reduction in comparison with these reports and is close to that of contemporaneous reports from other specialist centres in the USA [9] and Europe [10]. Moreover, the five-year survival of 35.5% in the present series compares favourably with previous reports [9] from centres employing also surgery alone as the standard treatment for oesophageal carcinoma. Not surprisingly, on multiple regression analysis pathological tumour stage and lymph nodal involvement were the only independent predictors of long-term survival. Nevertheless, a significant proportion (13.7%) of our patients with involved lymph nodes survived for more than 5 years, illustrating that surgical resection can provide a realistic hope of cure even in patients with advanced local disease. Although our in-hospital mortality rate was low, it should be noted that over one-third of our patients did suffer from significant post-operative complications. This figure is comparable with previous studies [2] and illustrates the high-risk nature of oesophageal surgery. Of all the complications, respiratory events and anastomotic leaks were the most serious, accounting for the majority of postoperative fatalities. The 4.8% incidence of chylothorax is higher than previously published reports [11], and is almost certainly attributable to the extensive mediastinal dissection carried out routinely in our unit. In three cases of chylothorax, re-operation and ligation of the thoracic duct was needed with the remaining patients being managed conservatively. Within our institution, there appears to be a number of evolving trends. Over the decade, we abandoned our initial interest in trans-hiatal oesophagectomies and standardised our resection technique to include an en bloc resection. The rationale for this approach was to ensure adequate mediastinal clearance and we would like to believe that the encouraging survival observed in the present series is related to the extensive mediastinal resection carried out in our institution. Higher overall 5-year survival rates (ranging from 30% to over 50%) have also been reported from institutions that employ more extensive resections [4,5,12,13], and a recent randomised control trial [14] appears to support our theory that en-bloc lymphadenectomy is associated with an improved long-term survival. In addition, it should be emphasized that during the study period we did not give patient any pre- or post-operative chemotherapy or radiotherapy due to the conflicting evidence of its efficacy. This controversy was recently addressed by the MRC study, which suggested an unequivocal benefit in pre-operative chemotherapy [15], and this has now been incorporated into our practice. We are hopeful that this will be reflected in improved long-term survival in our patients. Similarly, none of our patients underwent pre-operative endoscopic ultrasound as during the study period, its diagnostic value was questionable. With advances in imaging technology, this technique has had a renaissance, and it is hoped that the use of this staging procedure will, in future, reduce our 16% incidence of exploratory procedures.
Oesophagectomy for SCC carries an acceptable operative risk, which is higher for those having a history of respiratory disease and those developing an anastomotic leak. The good survival observed in early pathological stages and the presence of long-term survivors amongst those with locally advanced disease are encouraging. We continue to believe that an aggressive surgical approach is appropriate in all patients with no evidence of metastases on preoperative assessment.
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Abstract
1. Introduction
