Patients
This study was approved by the Research Ethics Committee of Shanghai Jiao Tong University School of Medicine and all participants at the Shanghai Chest Hospital gave written informed consent. A total of 112 consecutive pN0 stage ESCC patients who underwent esophagectomy with lymphadenectomy by the same surgical team from January 2004 to December 2010. The inclusion criteria were as follows: (1) routine preoperative esophageal endoscopy, a clear pathology of squamous cell carcinoma, (2) assessment of tumor location by the upper gastrointestinal barium swallow, (3) no evidence of tumescent cervical or supraclavicular lymph node disease was noted on physical examination, and a preoperative computed tomograpy (CT) scan or cervical B ultrasound study indicated no cervical or supraclavicular lymph node metastasis, (4) positron emission tomography to rule out distant metastasis, (5) no preoperative radiotherapy and/or chemotherapy, (6) pathologically confirmed lymph node-negative after operation, (7) all the patients were R0 resection of pathologically confirmed, (8) all the patients did not receive any adjuvant therapy before recurrence. Of all the patients, there were 92 men and 20 women, and the median age of 60.3 years (range: 36–80 years). The tumor location and the TNM classification were determined according to criteria established by the Union for International Cancer Control (UICC) in 2009 [4].
Surgical procedure
At operation the patient was placed in the 90° left lateral decubitus position. After a right posterolateral thoracotomy, the chest was entered through the fifth intercostal space. The azygos vein arch was divided, and the esophagus was dissected from the esophagogastric junction to the apex of the chest. When the tumor invasion obviously extended outside the esophagus, the thoracic duct was routinely ligated above the diaphragm. An upper midline abdominal incision was also made, and the abdomen was explored. During mobilization of the stomach, care was taken to preserve the right gastroepiploic vessels and arcades. The left gastric artery and vein were isolated and doubly ligated at their origin. The hiatus was enlarged and the stomach was pulled into the chest. An end-to-side esophagogastric anastomosis was performed within the apex of the chest (above the azygos vein) and the stomach was secured into the mediastinum (Ivor-Lewis).When the tumor located in upper thoracic, we will pull the stomach to neck by post-sternum tunnel for anastomosis (McKeown).
According to a lymph node mapping system for esophageal cancer (Japanese esophageal oncology group, JEOG) (Figure 1), thoraco-abdominal 2-field lymphadenectomy was undertaken. Some patients were undertaken cervico-thoraco-abdominal 3-field lymphadenectomy based on the positive results of preoperative cervical ultrasonography. The fields of lymph node dissections were as follows: 100, superficial cervical lymph nodes; 101, cervical esophageal lymph nodes; 102, deep cervical lymph nodes; 104, Supraclavicular lymph nodes; 105, upper thoracic esophageal lymph nodes; 106, recurrent laryngeal nerve lymph nodes; 107, subcarinal lymph nodes; 108, middle thoracic esophageal lymph nodes; 109, hilar lymph nodes; 110, lower thoracic esophageal lymph nodes; 111, diaphragmatic lymph nodes; 1, cardial lymph nodes (right); 2, cardial lymph nodes (left); 3, lesser curvature lymph nodes; 7, left gastric lymph nodes.
Follow-up examinations
Patients were routinely accepted the first examination at 3–4 weeks after the operation, examined at 3-month intervals for 1 year and at 6-month intervals thereafter. During each follow-up visit, the patient underwent a clinical evaluation, blood biochemistry examination including tumor markers, and chest radiography. Endoscopy, ultrasonography (US) of the neck and abdomen, and computed tomography (CT) of the neck, thorax, and abdomen were performed at least once a year. More selective investigations such as positron emission tomography (PET), bone scintigraphy, and Head-enhanced magnetic resonance imaging (MRI) were carried out based on specific symptomatology, clinical examination, and biochemical profile. Detection of a suspected recurrence at any one site was followed by a thorough detailed investigation to confirm or refute the occurrence and to examine every other site.
Definition of locoregional and hematogenous recurrence
The first recurrence was noted, and any additional recurrence found within one month was considered to have occurred simultaneously. These lesions were classified as locoregional (at the remaining esophagus, the anastomotic site, or the mediastinum, cervical, supraclavicular and celiac axis lymph nodes) and hematogenous (in the distant organs such as liver, lung, bone and pleura, peritoneum) recurrence. Simultaneous locoregional and hematogenous recurrence was classified as a hematogenous recurrence.
Statistical analysis
The SPSS 16.0 software package was used for data analysis. Data were expressed as median with ranges (minimum-maximum) or as percentages. The chi-square test was used to evaluate differences in clinicopathologic features. The Cox proportional hazards model was used to determine the independent risk factors for recurrence within 3 years after the operation. Estimation of recurrence was calculated with the Kaplan-Meier method, and the statistical differences were analyzed with the log-rank test. A p value of < 0.05 was considered statistically significant for all procedures.