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Annals of Surgical Oncology 9:65-70 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Paratracheal Lymph Node Metastasis Is Associated With Cervical Lymph Node Metastasis in Patients With Thoracic Esophageal Squamous Cell Carcinoma

Fumiaki Sato, MD, PhD, Yutaka Shimada, MD, PhD, FACS, Zhigang Li, MD, Masato Kano, MD, PhD, Go Watanabe, MD, Masato Maeda, MD, PhD, Atsushi Kawabe, MD, PhD, Junichi Kaganoi, MD, Atsushi Itami, MD, Shiro Nagatani, MD and Masayuki Imamura, MD, PhD, FACS

From the Department of Surgery and Surgical Basic Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Correspondence: Address correspondence and reprint requests to: Yutaka Shimada, MD, FACS, Department of Surgery and Surgical Basic Science, Graduate School of Medicine, Kyoto University, Kawara-cho 54, Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan; Fax: 81-75-751-4390; E-mail: shimada{at}kuhp.kyoto-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We determined which lymph node metastases were associated with cervical lymph node metastases of thoracic esophageal squamous cell carcinoma.

Methods: A total of 6464 lymph nodes derived from 155 consecutive patients with thoracic esophageal squamous cell carcinoma were stained by immunohistochemistry (antibody: AE1/AE3). Lymph node metastases were mapped according to the mapping scheme of the American Thoracic Society, as modified by Casson et al. (Ann Thorac Surg 1994;58:1569–70). Patients were divided into two groups: those with and without cervical lymph node metastasis (CLNM). Mapping data were examined by uni- and multivariate analysis.

Results: Hematoxylin and eosin–positive and AE1/AE3-positive lymph node metastases were found in 59% and 77% of patients, respectively. Twenty-one (55%) of 38 patients in the CLNM(+) group and 30 (26%) of 117 patients in the CLNM(-) group had AE1/AE3-positive lymph node metastasis in the thoracic paratracheal lymph node. Paratracheal lymph node metastasis is only one independent factor for (CLNM), whereas upper thoracic paraesophageal lymph node and pulmonal hilar lymph node status were also significant in univariate analysis. Three (43%) of seven patients with cervical jumping metastasis from the thoracic esophagus had micrometastasis in the paratracheal lymph node.

Conclusions: The paratracheal lymph node is most associated with (CLNM) of thoracic esophageal squamous cell carcinoma.

Key Words: Paratracheal lymph node • Cervical lymph node • Thoracic esophageal squamous cell carcinoma • Immunohistochemistry


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although there have been recent improvements in surgical procedures and technique methods, the overall prognosis for esophageal carcinoma remains poor, with a 5-year survival of 5% to 45% of patients.1–3 Some reports using multivariate analysis reveal that lymph node metastasis is an independent prognostic factor.4,5

Nowadays, the importance of regional lymph node dissection for esophageal cancer has been accepted. With respect to distant lymph nodes, cervical lymph node metastases and cervical recurrences are found in many patients with thoracic esophageal cancer (cervical lymph node metastasis, 16%–436–11; cervical lymph node recurrence after operation, 6%–1612–14). However, the clinical effect of cervical lymphadenectomy for patients with thoracic esophageal cancer remains a subject of controversy. Skinner et al.15 emphasized the selection of surgical procedure on the basis of tumor stage, instead of a standardized procedure. The selection of the best lymphadenectomy field for each patient with thoracic esophageal cancer requires accurate diagnosis and prediction of lymph node metastasis, especially cervical lymph node metastasis. Therefore, the metastatic pathway from the mediastinum to the cervical lymph nodes should be analyzed in detail.

Until now, several authors6–9,16 minutely analyzed the mapping of lymph node metastases in esophageal cancer by use of hematoxylin and eosin (H&E) staining. However, there was no report that analyzed the distribution pattern of lymph node metastases by other techniques with high sensitivity (e.g., immunohistochemistry and polymerase chain reaction).

The purpose of this study was to investigate the pattern of lymph node metastases, including micrometastases, in patients with thoracic esophageal squamous cell carcinoma and to determine which lymph node metastasis is most associated with cervical lymph node metastasis. For this purpose, we retrospectively examined numerous lymph nodes immunohistochemically.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Selection
From January 1988 to June 1997, 258 patients with primary esophageal cancer were admitted to the Department of Surgery and Surgical Basic Science of Kyoto University. Two hundred four consecutive patients underwent resections of primary cancer with systematic lymphadenectomy by the same surgeon17 (M.I.). Forty-nine patients were excluded from this study for the following reasons: 14 patients had esophageal cancer in the cervical esophagus; 9 patients had other types of esophageal cancer that were not squamous cell carcinoma; before the esophagectomy, 16 patients had undergone another operation around the esophagus which could have changed the lymph flow around the esophagus; and 10 patients had a synchronous double cancer in another organ. A total of 155 patients were examined in this study.

Lymphadenectomy
Details of our surgical procedure were described previously.17 We performed two types of systematic lymphadenectomy: two-field lymphadenectomy for 75 patients and three-field lymphadenectomy for 80 patients (Table 1). Our criteria for three-field lymphadenectomy were as follows: there was no major pre- or intraoperative complication; curative (R0) resection was expected by pre- and intraoperative diagnosis; cervical lymph node metastasis was suspected by preoperative imaging; patients had cervical or upper thoracic esophageal cancer; and an intraoperative frozen section of the paratracheal lymph node was positive in patients with middle and lower thoracic esophageal cancer.


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  		TABLE 1. Clinicopathological background of patients in CLNM(-) and CLNM(+) groups
 
Patients who did not satisfy these criteria received two-field lymphadenectomy. We obtained 6464 lymph nodes from 155 patients (mean, 41.7 nodes per patient; range, 6–136 nodes). Formalin-fixed and paraffin-embedded specimens of primary tumors and lymph nodes were studied immunohistochemically. The primary cancers of the esophagus were categorized according to the tumor, node, metastasis classification.18 To analyze lymphatic mapping in detail, lymph nodes were categorized according to the mapping scheme of the American Thoracic Society, modified by Casson et al.19

Grouping of Patients
The purpose of this study was to ascertain the main metastatic pathway from the mediastinum to the cervix and to determine the key lymph node by analyzing the mapping of lymph node metastasis. Because we did not focus on the full extent of cervical metastasis or the timing of detection in this study, we simply determined the incidence of cervical metastasis, including micrometastasis and recurrence, as the end point.

One hundred fifty-five patients were divided into two groups. Cervical lymph node metastases, including micrometastases, were found in 25 patients at the esophagectomy. Cervical lymph node recurrences were developed in 18 patients. Five patients had both cervical lymph node metastasis and recurrence. A total of 38 patients were defined as the CLNM(+) (with cervical lymph node metastasis) group. Patients without cervical lymph node or recurrence after more than 2 years of follow-up were defined as the CLNM(-) group (without cervical lymph node metastasis; n = 117).

Immunohistochemistry
The tissue samples were fixed in 10% buffered formalin and embedded in paraffin. The paraffin sections were dewaxed, hydrated, and treated with an autoclave heating antigen retrieval technique (soaking in a 10 mM citric acid solution, pH 6.0, at 120°C for 5 minutes). The endogenous peroxide activity was blocked with .3% H2O2 in absolute methanol for 30 minutes. Nonspecific staining was eliminated by 30 minutes of incubation with 10% normal horse serum. The excess normal serum was removed and was replaced by anticytokeratin antibody20 cocktail (AE1/AE3; Dako, Carpinteria, CA) and incubated overnight at 4°C. After rinsing the slides, the sections were incubated with a 1/200 dilution of the secondary antibody, followed by avidin-biotin-peroxidase complex (Vecstain Elite ABC Kit; Vector Laboratories, Inc., Burlingame, CA) for 40 and 50 minutes, respectively. Subsequently, the sections were stained with .003% 3,3-diaminobenzidinetetrahydrochloride and .005% H2O2 in .05 M Tris/HCl buffer (pH 7.2) counterstained with Mayer’s hematoxylin, dehydrated, and mounted. We used the normal esophageal epithelium as positive control.

Definition of Lymph Node Micrometastasis
The criteria for micrometastasis were previously described.21 In brief, pathologists in our institute examined dissected lymph nodes by one maximum cross-section with H&E staining in our routine pathological examination. In this study, we stained one extra cross-section as close to the section observed in the routine study as possible. All newly detected lymph node metastases were defined as micrometastases. Two authors (F.S. and Y.S.) judged micrometastasis in a blinded fashion. We consulted pathologists to exclude false-positive cells. AE1/AE3-positive cells in four lymph nodes of two patients were confirmed as macrophages by CD68 staining and excluded.

Statistical Analysis
Statistical calculations were performed with JMP software version 3 for Macintosh (SAS Institute, Inc., Cary, NC). A proportional analysis between the sample groups was performed with Fisher’s exact probability test in 2 x 2 contingency tables and with the {chi}2 test in 2 x n contingency tables.

The presence or absence of cervical lymph node metastasis was used as a response variable for logistical regression analysis. In addition, scoring of metastatic status in each lymph node was as follows: 0, no lymph node metastasis was found, or no lymph node was found in the dissected sample; and 1, lymph node metastasis, including micrometastasis, was found. All tests were two sided, and the results were considered to be significant when P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Detection of Lymph Node Micrometastasis
In 6464 lymph nodes, 612 (9.5%) H&E-positive lymph node metastases and 234 (3.6%) micrometastases were found. When detection rates were expressed as number of patients, 92 (59.4%) of 155 patients had H&E-positive lymph node metastases. Lymph node micrometastases (range, 1 to 5) were detected in 27 (17.4%) patients.

Correlation Between Cervical Lymph Node Metastasis and the Clinicopathological Findings
As listed in Table 1, younger age (P = .025) and a higher pN and M factor (P < .0001) are associated with cervical lymph node metastasis in thoracic esophageal cancer. Sex (male), location of the primary tumor (upper thoracic esophagus), and a higher pT factor had a tendency toward cervical lymph node metastasis, but their P value did not reach statistical significance.

Mapping of Lymph Node Metastasis in Thoracic Esophageal Cancer
Table 2 shows details of lymph node metastasis mapping. Tumors metastasized widely into neck, mediastinal, and abdominal lymph nodes. The most frequent metastatic site of upper and middle esophageal cancer was the thoracic paratracheal lymph node (11 of 19, 57.9%; and 33 of 100, 33%, respectively), whereas metastasis into the lesser curvature and left gastric artery lymph node was most frequent in lower esophageal cancer (26 of 36, 72.2%).


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  		TABLE 2. Location of primary tumor and mapping of lymph node metastasis
 
According to the univariate analysis in Table 3, immunohistochemical detection of thoracic paratracheal lymph node metastasis is most associated with cervical lymph node metastasis in thoracic esophageal cancer (P = .001), followed by upper paraesophageal lymph nodes and pulmonal hilar lymph nodes. However, multivariate analysis (logistical regression analysis) revealed that the thoracic paratracheal lymph node status is only independently associated with cervical lymph node metastasis (odds ratio, 3.32; P = .008)


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  		TABLE 3. Cervical lymph node metastasis and mapping of lymph node metastasis
 
Mapping of Initial Lymph Node Metastasis in Thoracic Esophageal Cancer
Twenty-five of 155 patients had a single lymph node metastasis, including micrometastasis. Mapping of initial lymph node metastasis is listed in Table 4. Locations of initial lymph node metastases from both superficial and advanced esophageal cancers varied not only in the mediastinal lymph node, but also in the cervical or abdominal lymph node.


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  		TABLE 4. Location of initial nodal metastasis
 
Jumping Metastasis to Cervical Lymph Node
In our series, metastases or micrometastases to cervical lymph nodes in the absence of mediastinal H&E-positive metastasis, namely, jumping metastases, were found in seven patients. However, three of seven patients with jumping metastasis had paratracheal lymph node micrometastases.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our data indicate that the paratracheal lymph node (stations 2 and 4) is the key lymph node. Until now, some authors emphasized the importance of the paratracheal lymph nodes because their metastatic rate was highest in the patients with upper and middle thoracic esophageal cancer7,9 or because thoracic recurrent nerve nodal involvement was associated with patients’ prognosis.22,23 In this study, for upper and middle esophageal cancer, the metastasis rate (37%) in the thoracic paratracheal lymph node was highest among the rates of all dissected lymph nodes, whereas metastasis in the lesser curvature and left gastric artery lymph node (station 17) was most frequent (47%) for patients with lower esophageal cancer. This result, with immunohistochemistry, is compatible with some former reports that used H&E staining. In univariate analysis, not only the paratracheal lymph node status, but also the upper thoracic paraesophageal lymph node (station 3p) and pulmonal hilar lymph node (station 10) status, are associated with cervical lymph node metastasis. It is interesting to note that multivariate analysis indicates only paratracheal lymph node status as an independent factor for cervical lymph node metastasis. The result of univariate analysis would be reflected by the indirect association between cervical lymph node metastasis and these two lymph nodes.

Esophageal cancer is characterized by a malignant behavior of skip or jumping lymph node metastasis. The lymphatic route of jumping metastasis has been discussed previously.6,24 In our series, jumping metastases were found in seven patients by H&E staining. However, three of seven patients had micrometastases in the paratracheal lymph node. This finding cannot deny the existence of jumping metastasis via the submucosal pathway, because an anatomical study25 showed a long intramural lymphatic pathway from the thoracic esophagus to the cervical esophagus. Our findings suggest that the cancer cells could metastasize to the cervical lymph node via the paratracheal lymph node in some patients with jumping metastasis.

Does this high metastatic rate in paratracheal lymph nodes mean that cancer cells metastasize to the paratracheal lymph node in an early phase? To answer this question, the location of the initial lymph node metastasis was investigated. Our data indicate that initial lymph node metastases not only from advanced tumors, but also from superficial tumors, were located in various lymph node stations. Two articles6,26 using H&E staining described the initial lymph node metastasis of thoracic esophageal cancer. The current data are similar to these reports by H&E staining, although we used an immunohistochemical technique.

In the fields of other malignancies, the concept of a sentinel lymph node was established, and intraoperative examination27,28 of the sentinel lymph node was applied clinically. In the field of esophageal cancer, however, it is difficult to define a sentinel lymph node because of the complexity in the lymphatic structure of esophageal cancer. According to analysis of the initial lymph node metastasis, Matsubara et al.26 suggested that there were two metastatic pathways (i.e., through the submucosal and extramural network) and that esophageal cancer may have two or more sentinel nodes. Therefore, the association demonstrated in this study between paratracheal lymph node status and cervical lymph node metastasis suggests that the paratracheal lymph node would not always be the sentinel node of thoracic esophageal cancer, but it would be the most proximate pathway to cervical lymph nodes in the extramural metastatic pathway.

Skinner et al.15 emphasized the selection of operative procedure on the basis of tumor stage. Accurate diagnosis and the prediction of cervical lymph node metastasis are required to decide whether or not a patient should receive cervical lymphadenectomy. Results of this study emphasize that much attention should be paid to the thoracic paratracheal lymph node in the preoperative and intraoperative evaluation for the selection of cervical lymphadenectomy.

In this study, we selected two-field lymphadenectomy in 48% of patients, according to patients’ clinical condition and stage. Because exclusion of two-field lymphadenectomy cases from this study would lead to a biased selection of patients, we analyzed 155 consecutive cases that included both two- and three-field lymphadenectomy.

In conclusion, mapping of lymph node metastases in 155 thoracic esophageal squamous cell carcinomas were analyzed in detail by immunohistochemical staining. The thoracic paratracheal lymph node is the key lymph node for cervical lymph node metastasis of thoracic esophageal cancer.


   Acknowledgments
 
The authors thank Professor Yamabe H. and Dr. Sakurai T., Laboratory of Anatomic Pathology, Kyoto University Hospital, for their kind assistance in the histopathological technique. Supported by a grant in aid from the Japanese Ministry of Education, Science, and Culture (Grant 10470241) and from the Japanese Ministry of Health and Welfare.

Received for publication January 31, 2001. Accepted for publication August 23, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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