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Ann Thorac Surg 1998;65:787-792
© 1998 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Esophageal Carcinoma: Depth of Tumor Invasion Is Predictive of Regional Lymph Node Status

Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
Department of Gastroenterology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
Department of Hematology and Medical Oncology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
Department of Biostatistics and Epidemiology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
Department of Anatomic Pathology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA

Dr Rice, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195 (e-mail: ricet@cesmtp.ccf.org).

Presented at the Forty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Naples, FL, Nov 6–8, 1997.

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Background. The depth of tumor invasion (T) and regional lymph node status (N) are two factors that define the stage of an esophageal carcinoma. However, the arrangement of staging groups assumes that these factors are independent variables. A retrospective review of 359 consecutive patients undergoing esophageal resection was conducted to define the relationship between T and N and to determine whether T is a significant predictor of regional lymph node metastasis (N1).

Methods. Primary treatment was operation without preoperative therapy. There were 295 (82%) adenocarcinomas, 55 (15%) squamous cell carcinomas, and 9 (3%) adenosquamous carcinomas. T status was Tis in 29 (8%) patients, T1 in 65 (18%), T2 in 37 (10%), T3 in 219 (61%), and T4 in 9 (3%). N status was N0 in 161 (45%) patients and N1 in 198 (55%). M status was M0 in 327 (91%) patients and M1 in 32 (9%). Stage was 0 in 29 (8%) patients, I in 58 (16%), IIA in 70 (20%), IIB in 22 (6%), III in 148 (41%), and IV in 32 (9%).

Results. The likelihood of N1 disease occurring with increasing T was tested using the trend test. The percentage of patients with N1 disease is 0% for Tis, 11% for T1, 43% for T2, 77% for T3, and 67% for T4 (p < 0.001). This relationship existed for both adenocarcinoma and squamous cell carcinoma. Multivariable analysis identified increasing T, adenocarcinoma, and lack of well-differentiated histologic features as significant predictors of N1 disease. Compared with a T1 patient, a T2 patient is 6 times more likely to have N1 disease, a T3 patient 23 times, and a T4 patient 35 times.

Conclusions. We conclude that for patients with esophageal carcinoma, T is an important predictor of N and this association should be included with other established factors used in clinical staging and treatment decisions.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
The present staging system for esophageal carcinoma recognizes the importance of depth of tumor invasion (T) and regional lymph node status (N) in defining stage [1]. These factors are assumed to be independent, and the arrangement of staging groups is based on this hypothesis. Because both increasing T and the presence of regional lymph node metastasis (N1) greatly reduce survival, it is important to explore the relationship between these factors and determine their importance in clinical staging and treatment decisions.

The purposes of this study were to define the relationship between depth of tumor invasion and regional lymph node status and to determine whether depth of tumor invasion is a predictor of regional lymph node metastasis.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Patients
All records of patients with esophageal carcinoma who underwent esophagectomy at The Cleveland Clinic Foundation between January 1, 1983, and August 1, 1997, were reviewed. Patients excluded from the study were those who received any treatment of the primary carcinoma before resection and pathologic staging. Patient age, sex, histologic cell type, histologic differentiation, presence of Barrett’s mucosa, presence of signet ring cells, depth of tumor invasion (T), number of regional lymph nodes examined, number of regional lymph nodes with metastasis (N1), regional lymph node status (N), distant metastatic status (M), pathologic stage, and status of the resection margins were recorded.

Surgical Therapy
Esophageal resection, lymphadenectomy, and reconstruction using the stomach were performed by three different surgical approaches. Patients diagnosed preoperatively to have high-grade dysplasia (Tis N0 M0), stage I carcinomas (T1 N0 M0), or a performance status that would not allow thoracotomy underwent a transhiatal esophagectomy. Lymph node sampling was performed in these patients. Patients judged to have T2 N0 M0 or greater stage carcinoma underwent esophageal resection through a left thoracoabdominal approach, or a right thoracotomy and upper abdominal midline laparotomy. An extensive lymphadenectomy was performed in these patients. Patients with cervical esophageal carcinomas that involved the larynx and pharynx underwent a pharyngolaryngoesophagectomy. The esophagogastric anastomosis was constructed either in the neck or chest by a single-layer sutured or stapled technique.

Pathologic Analysis
Esophageal resection specimens were evaluated pathologically using a standardized protocol in which the resection margins, the esophageal body, the gastroesophageal junction, and regional lymph nodes were extensively sampled. When gross lesions were identified, up to five sections of each lesion, which included the area of deepest penetration of the esophageal wall, were evaluated. When a gross lesion was not identified, at least ten sections of the esophagus were evaluated. All separately resected lymph nodes and all lymph nodes that were grossly identified in the resection specimen were evaluated pathologically. When small enough, the entire lymph node was submitted, and two levels of that node were examined histologically. Larger lymph nodes were bisected and two levels of each of the two portions of the bisected lymph node were examined.

Statistical Analysis
Descriptive information is summarized as frequencies and percentages for categorical variables, and as the median and range for continuous variables. Data for the variables studied were available for all patients. A one-sided Cochran-Armitage test was used to determine whether increasing T status is associated with increasing risk of N1 disease, overall and by histologic cell type. Logistic regression analysis was used to identify univariable predictors of N1 disease. Variables that were significant in the univariable analysis at p < 0.05 and that made clinical sense to include in a model to predict N1 disease were considered in a stepwise logistic regression model. Results for the final multivariable model are summarized as the p value, odds ratio, and 95% confidence interval for the odds ratio, along with probability of N1 disease for each combination of variables in the final multivariable model. Patients with Tis carcinomas were excluded from univariable analysis and multivariable analysis because there was a 0% prevalence of N1 disease in this group. All statistical tests were performed using a 5% level of significance.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Three hundred fifty-nine patients were studied. Descriptive information for all patients and for histologic cell types is summarized in Table 1. The frequency of regional lymph node metastasis (N1) for each level of tumor invasion (T) is listed in Table 2. A sufficient number of patients with T1 adenocarcinomas allowed subdivision of T1 adenocarcinomas into two groups: (1) adenocarcinomas that breached the basement membrane but with invasion limited to the lamina propria and muscularis mucosa (T1 intramucosal), and (2) adenocarcinomas invading into the submucosa but not deeper (T1 submucosal). The difference in the prevalance of regional lymph node metastasis between patients with T1 intramucosal adenocarcinomas (2.8%) and patients with T1 submucosal adenocarcinomas (20.8%) was unlikely to be caused by chance (p = 0.033). The prevalance of regional lymph node metastasis significantly increased with increasing depth of tumor invasion for all patients (p < 0.001), for patients with adenocarcinoma (p < 0.001), and for patients with squamous cell carcinoma (p = 0.034).

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

View larger version (75K): [in this window] [in a new window]   The lymphatic anatomy of the esophagus. Lymphatics enter the mucosa to lie just below the basement membrane of the epithelium and drain the lamina propria and muscularis mucosa. The submucosa is richly supplied with an interconnecting network of lymphatic channels that run the length of the esophagus. Lymphatics intermittently pierce the muscularis propria to drain into regional lymph nodes or directly into the thoracic duct. (Reprinted with permission from the Cleveland Clinic Foundation.)

Clinical Staging
Depth of tumor invasion and regional lymph node status are correlated variables in the determination of the stage of an esophageal carcinoma. Because increasing depth of tumor invasion and regional lymph node metastasis greatly reduce survival, clinical (pretreatment) staging should be used for prognostication and to guide therapy. Unfortunately, a perfect clinical staging tool does not exist. Computed tomographic scanners do not allow an accurate assessment of depth of tumor invasion. In this evaluation, computed tomography is most useful in excluding T4 carcinomas by demonstrating the maintenance of fat planes between the tumor and adjacent structures. In the assessment of regional lymph node status, size of the node is the only factor measured, thus limiting the usefulness of computed tomography in this clinical assessment. Endoscopic esophageal ultrasonography is an excellent clinical staging tool and provides the best clinical estimate of depth of tumor invasion. Multiple factors, including size, shape, border, internal echo characteristic, and proximity to the primary carcinoma, are evaluated to determine the status of regional lymph nodes. Most studies, however, lack histologic correlation with esophageal ultrasonographic findings, except those with esophageal ultrasonographic-directed fine-needle aspiration of suspicious regional lymph nodes. Sheathed fine-needle aspiration needles are not available. Therefore, regional lymph nodes located immediately adjacent to the primary tumor, where the needle must traverse the tumor, cannot be accurately assessed. A negative fine-needle aspiration result raises the question of sampling error.

Thoracoscopy allows direct biopsy of regional nodes, but unlike mediastinoscopy in the staging of bronchogenic carcinoma, it is not a simple outpatient procedure. General anesthesia and one-lung ventilation are required. Unilateral sampling is generally the only procedure performed. In most instances the primary tumor must be dissected to gain access to regional lymph nodes. Because this dissection is not confined by definite tissue boundaries, a potential exists for tumor dissemination throughout the pleural space. If laparoscopy is added, this becomes a formidable procedure with operating times approaching that of resection.

Despite the shortcomings of present staging technologies, precise clinical staging of esophageal carcinomas can be obtained. The assessment of depth of tumor invasion (T) by esophageal ultrasonography and the best clinical evaluation of regional lymph node status (N), individualized for each patient, may be augmented by the consideration of the relationship between T and N.

Clinical Predictors of Regional Lymph Node Metastasis
Clinical predictors of regional lymph node metastasis may also be used to complement clinical staging. Of all factors in this study, depth of tumor invasion was the most useful clinical predictor. The likelihood of regional lymph node metastasis increased dramatically with deeper invasion, a clear reflection of an increasing exposure to lymphatics as a tumor grows along and through the esophageal wall. Patients with adenocarcinoma were significantly more likely to present with regional nodal metastases than patients with squamous cell carcinoma. A similar result could not be established for patients with adenosquamous carcinoma because of the small number of patients. However, the prevalence of regional lymph node metastasis was nearly identical between adenocarcinoma and adenosquamous carcinoma. A less well differentiated neoplasm had a greater potential for regional nodal metastasis demonstrated by multivariable analysis.

The presence of Barrett’s esophagus, one of the factors accounting for the increasing prevalence of esophageal adenocarcinoma, was not predictive of regional lymph node metastasis. Although lack of Barrett’s esophagus was a univariable predictor of regional lymph node metastasis, it appeared to be highly associated with the three multivariable predictors, but did not add additional information to the multivariable model. In this series, many patients with Barrett’s esophagus were identified through screening programs and, in general, had early mucosal involvement. Many patients with early Barrett’s associated tumors had more differentiated adenocarcinomas.

Age and sex, so important in the recent epidemic of adenocarcinoma of the esophagus and esophagogastric junction, were not predictive of regional lymph node metastasis.

Postresection Predictors of N1
Although factors identified at pathologic staging are not available for clinical staging, analysis of these data indicates the need for excellent surgical technique in the resection of esophageal carcinoma. Univariable analysis demonstrated that regional lymph node metastases are more common when the surgical margins are positive, a reflection of the intramural extent of the tumor. When a resection is undertaken, patients with regional lymph node metastasis are more likely to have positive resection margins, and vice versa.

The total number of lymph nodes resected was a univariable predictor of regional lymph node metastasis. This suggests that surgical removal of all regional lymph nodes (lymphadenectomy) is important, both prognostically and therapeutically. The relationship between the number of lymph nodes resected and the likelihood of lymph node metastasis must be considered when attempting to assess the role of pathologic staging in this disease.

Conclusions
We conclude that for patients with esophageal carcinoma, the probability of regional lymph node metastasis (N1) can be predicted from an assessment of (1) pathologic diagnosis of adenocarcinoma, (2) a less than well-differentiated histology, and (3) most importantly, increasing depth of tumor invasion (T). This assessment identifies those patients at particularly high risk for regional lymph node metastasis and should be included with other established factors used in clinical staging and treatment decision making.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/annals

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 

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