The esophagus traverses the neck, mediastinum, and abdomen. Cancer of the thoracic esophagus can metastasize to lymph nodes and locate in any or all of these compartments.¹ The rate of lymph node involvement is very high. Approximately 50% of tumors that invade the submucosa develop lymph node metastases, and the rate increases with increasing depth of invasion. Radical surgery for esophageal cancer therefore requires three-field lymphadenectomy. Our group has been performing three-field lymph node dissections since 1984 for all thoracoesophageal cancers. In this chapter we lay down the principles, describe the procedure, and discuss the outcome of this mode of treatment based on our experience.

The overall 5-year survival rate for squamous cell carcinoma of the esophagus has improved from 20% to 60%. We believe this improvement in survival can be directly related to extensive and meticulous lymphadenectomy.² This view has been corroborated by multivariate analysis. The key to three-field lymphadenectomy therefore is meticulous dissection of the upper mediastinum and cervical nodes that lie along the course of both recurrent laryngeal nerves. Preserving the right bronchial artery and pulmonary branches of the vagus nerve decreases the rate of pulmonary complications. Using this comprehensive approach, we have achieved a postoperative mortality rate of less than 2%.

Esophageal cancer is biologically more aggressive than other gastrointestinal malignancies and has a higher incidence of lymph node metastasis.³ Lymph node metastasis is an important and independent factor for predicting the prognosis of esophageal cancer. The number of metastatic lymph nodes is thought to reflect the aggressiveness of the cancer.⁴ Accurate documentation of the extent of lymph node involvement therefore is essential to determining the appropriate treatment strategy for esophageal cancer.

Histopathologic assessment remains the gold standard for accurate lymph node staging. Proper assessment also requires that an adequate number of lymph nodes be presented to the pathologist. Since 1984, all tumors determined to have invasion of the submucosa or beyond undergo three-field dissection at our institution. Three-field dissection is defined as an extended en-bloc lymph node dissection throughout the cervical, thoracic, and abdominal fields.⁵

A total of 1123 patients underwent transthoracic esophagectomy with extended en-bloc cervicothoracoabdominal (three-field) lymphadenectomy between January 1998 and December 2011 at Juntendo University in Japan for carcinoma of the esophagus. A total of 120,722 lymph nodes were dissected, and the average number of dissected lymph nodes per patient was 108. The lymph nodes removed en bloc with the specimen were dissected and classified into respective lymph node groups immediately after the operation by the surgeons who performed the esophagectomy, as outlined in the Japanese Guidelines for Clinical and Pathologic Studies on Classification of Esophageal Cancer⁶ (Fig. 20-1). This provides a more detailed lymph node classification than the AJCC Cancer Staging Manual.⁷ The pattern of lymphatic spread was investigated in detail, and the final pathologic diagnosis of lymph node metastasis was compared with the preoperative clinical evaluation to assess the accuracy of preoperative diagnosis for each lymph node station and each field.

Rate of Lymph Node Metastasis

Three hundred forty-eight patients did not have any lymph node metastases, whereas 775 patients had one or more metastatic lymph nodes, yielding a metastatic rate of 69.1%. The rate of lymph node metastasis increased with the depth of tumor invasion and was 54.7% for pT1b, 66.4% for pT2, and 81.0% for pT3 or pT4 disease (Fig. 20-2). The TNM classification divides pT1 tumors into two subclasses, pT1a and pT1b. A pT1a tumor invades only mucosa, including muscularis mucosae (mucosal cancer), and pT1b tumor invades the submucosal layer (submucosal cancer). In the normal esophagus, many lymphatic vessels are found in the lamina propria mucosa.⁸ Therefore, lymphatic invasion can develop in comparatively early-stage cancer.

As shown in Figure 20-2, the rate of lymph node metastasis in esophageal cancer is three times higher than that of gastric cancer even for submucosal invasion (pT1b). The mean number of dissected lymph nodes was 41 in the neck, 35 in the mediastinum, and 31 in the abdomen. The mean number of metastatic lymph nodes was 0.7 in the neck, 1.8 in the mediastinum, and 1.6 in the abdomen.

The frequency and distribution of lymph node metastases differ according to the location of the tumor. The rate of lymph node metastasis was 65.6% in the upper thoracic esophagus (n = 163), 69.1% in the middle thoracic esophagus (n = 651), and 70.6% in the lower thoracic esophagus (n = 309) (Fig. 20-3). Upper esophageal tumors had a greater frequency of metastases to cervical lymph nodes than tumors of the middle and lower esophagus. The frequency of metastasis to abdominal nodes was higher with lower esophageal cancer than with tumors of the middle and upper esophagus. However, we did sometimes find abdominal lymph node metastasis in upper esophageal cancer and cervical node metastasis in lower ­esophageal ­cancer. Midesophageal tumors frequently metastasized to lymph nodes in the neck and abdomen. Approximately 90% of cervical node metastases were caudal to the superior belly of the omohyoid muscle (Fig. 20-4).

Which are the Frequently Involved Lymph Node Groups?

Analysis of lymphatic spread revealed that the sites with a metastatic rate of more than 20% (main metastatic sites) were located along the right recurrent laryngeal nerve in the upper mediastinum (106-recR: 23.8%) and along the lesser curvature of the proximal stomach (3: 21.6%) (Fig. 20-5). The sites with a metastatic rate ranging from 10% to 20% (common metastatic sites) were the right supraclavicular area (104: 14.4%), right cervical paraesophageal area along the recurrent laryngeal nerve (101R: 10.1%), along the left recurrent laryngeal nerve in the upper mediastinum (106-recL: 18.8%), the subcarinal area (107: 10.0%), the middle thoracic paraesophageal area (108: 13.0%), the lower thoracic paraesophageal area (110: 11.6%), the posterior mediastinal area (112: 17.0%), along the thoracic duct (TD: 10.0%), the right (1: 14.5%) and left (2: 16.6%) pericardial area, and along the left gastric artery (7: 18.0%). The nodes involved less often by metastases (metastatic rate <5%) were the middle deep cervical nodes (102R: 1.3%, 102L: 2.9%), the diaphragmatic nodes (111: 1.2%), the nodes along the common hepatic artery (8: 4.0%), and the nodes along the splenic artery (11: 4.4%).

As noted earlier, this detailed analysis of the lymphatic spread of esophageal cancer based on pathologic findings revealed two main metastatic sites: one along the recurrent laryngeal nerve in the upper mediastinum, which Haagensen called the recurrent nerve,⁹ and the other along the lesser curvature of the proximal stomach. Unlike other gastrointestinal malignancies, frequent metastases to distant nodes are a distinctive feature of esophageal cancer.

The preoperative diagnostic workup for lymph node metastasis consists of endoscopic ultrasonography, conventional ultrasonography of the neck and abdomen, and CT scan from the neck to the lower abdomen. A PET scan is done as indicated.

Criteria for Preoperative Diagnosis

Mediastinal and abdominal lymph nodes were considered to be metastatic when the largest diameter was greater than 10 mm, the node was almost round, the internal CT density or ultrasound echogenicity was low, and the margin of the node was clear. For cervical lymph nodes, the same criteria were applied, except that the diameter was set at greater than 5 mm. Figure 20-6 shows a metastatic lymph node along the right recurrent nerve in the superior mediastinum at the root of the right subclavian artery.