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J Thorac Cardiovasc Surg 1994;107:1073-1078
© 1994 Mosby, Inc.
GENERAL THORACIC SURGERY |
Tokyo, Japan
Supported by grants-in-aid for cancer research (No. 1-34) from the Ministry of Health and Welfare, Japan.
Received for publication June 14, 1993. Accepted for publication Aug. 19, 1993. Address for reprints: Toshiki Matsubara, MD, Department of Surgery, Cancer Institute Hospital, 1-37-1 Kami-Ikebukuro, Toshima-Ku, Tokyo 170, Japan.
Abstract
From 1985 to 1992, 171 patients with cancer of the thoracic esophagus underwent esophagectomy with systematic dissection of regional lymph nodes including cervical nodes. The hospital mortality rate was 5.3%. The dissected nodes were classified into four groups: the deep cervical (C), upper mediastinal and cervical paratracheal (U), middle and lower mediastinal (L), and upper perigastric (G) groups. The U group mainly consisted of nodes beside the recurrent laryngeal nerves. The phase of cancer infiltration of lymph nodes was evaluated by the total number and the distribution of involved nodes. Of cases with nodal involvement, only 37% were in the late phase, in which more than seven nodes or in which the U, L, and G groups were all involved. Of cases in the earliest phase in which only one node was involved, 93% had either the U or G group involved. The C group of nodes was infrequently involved until the late phase. Cancer had metastasized to the U and G groups across a considerable anatomic distance even in earlier phases. Outcomes of the cases with nodal involvement not in the late phase were satisfactory; the cumulative survival was 60% at 3 years and 54% at 5 years. Systematic nodal dissection would benefit even cases with nodal involvement, unless the disease is in the late phase. Nodes beside the recurrent nerves and upper perigastric nodes should be dissected with higher priority, though they are located anatomically distant. (J THORACCARDIOVASCSURG1994;107:1073-8)
The adequate extent of lymph node dissection in operation for squamous cell carcinoma of the thoracic esophagus is a topic of controversy. Some surgeons regard an esophageal cancer with nodal involvement as a systemic disease and advocate transhiatal esophagectomy. 
1 Some others advocate aggressive operation with wide lymph node dissection. 2,3 To select a dissecting approach, it is essential to know the exact anatomic sites of regional lymph nodes commonly involved and to evaluate the benefit derived from dissecting them. We reported in 1976 the clinical significance of lymph nodes located along the recurrent laryngeal nerves at the thoracocervical junction 4 and have incorporated bilateral lower neck dissection into our routine operation to perform a thorough dissection of nodes at the thoracocervical junction.
The purpose of this paper was to elucidate the distribution pattern of involved lymph nodes and to analyze the correlation between the nodal state and survival after dissection on the basis of clinical results of our cases involving systematic lymph node dissection. This could form the basis for adjusting the anatomic ranges of lymph node dissection in standard, extensive, and compromised operations according to the disease stage and patient's operative risk.
MATERIALS AND METHODS
From 1985 to 1992, 207 patients with squamous cell carcinoma of the thoracic esophagus underwent esophagectomy with systematic dissection of regional lymph nodes including cervical nodes. Dissection was done through cervical incision, laparotomy, and right thoracotomy. In this patient group, 171 cases were analyzed in terms of lymph node involvement, excluding patients who had previously undergone perigastric dissection because of stomach cancer and patients who had undergone preoperative therapy, mainly for infiltration of the aorta or tracheobronchial tree.
We classified the dissected regional lymph nodes into four groups: the inferior deep cervical lymph nodes, the C group; the upper mediastinal and cervical paratracheal lymph nodes, the U group; the middle and lower mediastinal lymph nodes, the L group; and upper perigastric lymph nodes, the G group (Fig. 1). The C group consisted of nodes located posterior and lateral to the bilateral internal jugular veins. The U group mainly consisted of lymph node chains beside the bilateral recurrent laryngeal nerves and the esophagus. The U-group nodes are located in a continuous region ranging from the base of the neck to the upper mediastinum. We dissected the upper part of the U group of nodes through the cervical approach followed by dissection of the lower part through a right thoracotomy, preserving the continuity of the dissection layer. Though the region above the upper edge of the sternum is usually classified in the neck, 5 we did not differentiate the cervical part of the U group (cervical paratracheal nodes) from the mediastinal part to avoid ambiguity, because it was difficult to define a precise boundary in an anatomically continuous range at operation. A great proportion of involved nodes were definitely located above the upper edge of the sternum. The L group included lymph nodes around the left main bronchus, nodes at the tracheal bifurcation, middle and lower paraesophageal nodes, nodes beside the thoracic duct, and nodes in the pulmonary ligaments. The thoracic duct was removed in continuity with the specimen. The G group consisted of not only nodes at the gastric cardia and the lesser curvature, but also lymph nodes around the celiac artery.
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The degree of wall penetration of the primary lesion was classified according to the T categorization in the International Union Against Cancer (UICC) TNM system 5: T1, tumor invading lamina propria or submucosa; T2, muscularis propria; T3, adventitia; and T4, adjacent structure. The thoracic esophagus was divided into three portions also according to the UICC TNM system: the upper, middle, and lower thoracic portions, and each of these was further subdivided into oral and anal halves.
In the analysis of survival, 10 cases in which definite cancer foci were macroscopically left at operation were excluded. All patients were followed up between February and April 1993. Survival curves were made by the Kaplan-Meier method, and the difference in survival was evaluated by the generalized Wilcoxon method. Cause of death was not distinguished in the survival analysis. All censored cases are those in which the patient was living at the follow-up time.
Patterns of cancer recurrence were examined in 54 cases in which recurrent lesions were clinically detected. Distributions of recurrent lesions were evaluated on findings of clinical examinations at the time cancer recurred: physical examination, plain roentgenography, computed tomography, echography, and scintigraphy. Recurrence in the neck and mediastinum was categorized as local recurrence. Lymph node recurrence in the abdominal cavity was found only at the paraaortic region and was categorized as distant recurrence along with hematogenous metastasis and pleural and pericardial recurrence.
RESULTS
Pattern of involvement.
Lymph node involvement was found in 70% of cases: 44% in T1, 67% in T2, and 84% in T3 and T4. Of cases with lymph node involvement (n[+] cases), a quarter had only one positive node and another quarter had more than seven (Fig. 2). The deeper the cancer invaded the esophageal wall, the more lymph nodes were involved (Table I). The prevalence of metastasis to C-, U-, L-, and G-group nodes was 11%, 49%, 41%, and 46%, respectively. Of 19 cases having C-group involvement, 15, 17, and 19 cases, respectively, also had G-, L-, and U-group involvement. The distribution of involvement of three main regions (U, L, and G groups) is shown in Fig. 3.
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Results in cases with only one positive node (N1 group) were favorable: 3- and 5-year survival was 75% and 68%, respectively (Fig. 6). The difference in survival between N0 and N1 groups was not significant, whereas the N1 group had more favorable outcomes than the N2a group (p < 0.03). In the group with two to seven positive nodes (N2), no subgroup was significantly different in survival from the rest. The N3 group had poorer outcomes than the N2b group (p < 0.02). Although no patient with more than seven positive nodes survived 4 years after operation, two of five patients with seven positive nodes were alive 4 years after operation.
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The pattern of cancer recurrence was local in 17 cases, distant in 33 cases, and mixed in four cases, when the recurrence was first detected. The prevalence of cervical and/or upper mediastinum recurrence was similar to that of middle and/or lower mediastinal recurrence (Table II). The proportion of local recurrence was 19% (4 of 21) in N0, N1, and N2a cases and was 39% (13 of 33) in N2b and N3 cases.
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To maximize the surgical effect with the least surgical invasion, surgeons should know which lymph nodes are more frequently involved. It is natural to suppose that cancer metastasizes to nearer nodes in the early phase. Some authors have referred to the special importance of thorough dissection of the middle and lower mediastinum (L-group nodes) along with the upper perigastric nodes (G-group nodes). 2 However, metastasis to upper mediastinal and cervical paratracheal nodes (U-group nodes) was no less common than metastasis to the L-group nodes in our series. Moreover, U- and G-group nodes were involved much more frequently than the L-group nodes in the earliest phase of cancer metastasis. In addition, cancer had metastasized to the U- and G-group nodes across a considerable anatomic distance even in earlier phases of lymphatic invasion. For example, metastasis to the U-group nodes from cancer limited to the lower one third of the esophagus was not uncommon.
These results strongly suggest that the paratracheal lymph nodes (especially nodes beside the recurrent laryngeal nerves) and perigastric lymph nodes should be given higher priority than the middle and lower mediastinum in the early phase of metastasis. Apparently, distantly located nodes have higher priority than nodes nearer to the primary lesion. We suppose that this is because of abundant lymph flow in the esophageal wall in the longitudinal directions. 6
Recently, several authors emphasized the importance of cervical dissection for cancer of the thoracic esophagus. 3,7 In the analysis of metastasis to cervical nodes, the deep cervical node group should be precisely distinguished from the cervical part of the U group. The classification between them is anatomically definite. 8 They are much different from each other in clinical significance. As mentioned earlier, metastasis to the cervical parts of the U group was common. We frequently found involvement of lymph nodes located around the inferior thyroid arteries. We take the cervical approach mainly for thorough dissection of U-group lymph nodes. Compared with this group, the deep cervical group has little clinical significance. The overall incidence of metastasis to the deep cervical nodes was 11% in our series, and most of the positive cases were in a phase too advanced for complete cure.
But dissection of the deep cervical group is not completely meaningless. The operative risk is not increased much by dissecting them, and cervical incision is necessary anyway for thorough dissection of the upper part of the U-group nodes. Accidental metastasis to this regional group may be possible even in earlier phases. In one of our cases with this group involved the patient was alive more than 5 years after operation. Cancer recurrence to this region was commonly found in our former cases in which cervical dissection was not done: of 131 cases with cancer recurrence, 64 had neck or upper mediastinum recurrence or both (neck, 37; upper mediastinum, 35). 9 In three cases with deep cervical recurrence the patient survived more than 5 years after recurrent lesions were removed. The incidence of neck recurrence was much decreased in this series in which cervical dissection was done.
The total number of positive nodes is a good index for predicting outcome after operation. 10 Outcomes were unfavorable in our series when the total was more than seven. This group accounted for about a quarter of the n(+) cases. Cases with only one positive node also amounted to about a quarter of the n(+) cases. The survival of this group was significantly favorable. These special groups should be treated discriminatively from other n(+) cases in the clinical evaluation after operation.
Surgical outcomes were also greatly influenced by the anatomic distribution of involved nodes. In cases having only G-group involvement, the outcome was as favor able as the outcome in n(-) cases. Therefore perigastric involvement is not always a sign of unfavorable outcome. Cases having U-group involvement presented less favorable outcomes. However, complete cure is still expected, unless all of the U, L, and G groups are involved.
Many surgeons regard an esophageal cancer that infiltrates regional lymph nodes as a systemic disease. 11 However, we have many long-time survivors who had nodal involvement. If metastatic lesions had not been removed, they would have had little chance of long-term survival. Our results suggest that the disease is probably still localized in a considerable portion of n(+) cases: the cases having less than eight involved nodes and not having involvement of all of the U, L, and G groups. Such cases amounted to more than 60% of n(+) cases. Systematic nodal dissection with special emphasis on the U and G regions would benefit the patients in such cases.
References
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  S. Komatsu, Y. Ueda, D. Ichikawa, H. Fujiwara, K. Okamoto, S. Kikuchi, A. Shiozaki, K. Imura, R. Ohsawa, T. Ochiai, et al. Prognostic and Clinical Evaluation of Axillary Lymph Node Metastasis in Esophageal Cancer Jpn. J. Clin. Oncol., April 1, 2007; 37(4): 314 - 318. [Abstract] [Full Text] [PDF]
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 D. W. Gee and D. W. Rattner Management of Gastroesophageal Tumors Oncologist, February 1, 2007; 12(2): 175 - 185. [Abstract] [Full Text] [PDF]
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K. Hayashi, N. Ando, H. Watanabe, H. Ide, K. Nagai, N. Aoyama, W. Takiyama, K. Ishida, K. Isono, H. Makuuchi, et al. Phase II Evaluation of Protracted Infusion of Cisplatin and 5-Fluorouracil in Advanced Squamous Cell Carcinoma of the Esophagus: a Japan Esophageal Oncology Group (JEOG) Trial (JCOG9407) Jpn. J. Clin. Oncol., September 1, 2001; 31(9): 419 - 423. [Abstract] [Full Text] [PDF]
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 C.-H. Shih, S. Ozawa, N. Ando, M. Ueda, and M. Kitajima Vascular Endothelial Growth Factor Expression Predicts Outcome and Lymph Node Metastasis in Squamous Cell Carcinoma of the Esophagus Clin. Cancer Res., March 1, 2000; 6(3): 1161 - 1168. [Abstract] [Full Text]
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 C. G. Bremner Invited Commentary Arch Surg, July 1, 1996; 131(7): 713 - 713. [Abstract] [PDF]
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 T. Matsubara, M. Ueda, T. Nakajima, K. Nakagawa, T. Yamashita, N. Horikoshi, and A. Yanagisawa Can Esophagectomy Cure Cancer of the Thoracic Esophagus Involving the Major Airways? Ann. Thorac. Surg., January 1, 1995; 59(1): 173 - 177. [Abstract] [Full Text]
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