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Annals of Surgical Oncology 9:807-811 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Frequency of Nodal Metastases to the Upper Mediastinum in Barrett’s Cancer

W. Schröder, MD, S.P. Mönig, MD, S.E. Baldus, MD, C. Gutschow, MD, P.M. Schneider, MD and A.H. Hölscher, MD

From the Departments of Visceral and Vascular Surgery (WS, SPM, CG, PMS, AHH) and Pathology (SEB), University of Cologne, Cologne, Germany.

Correspondence: Address correspondence and reprint requests to: Wolfgang Schröder, MD, Department of Visceral and Vascular Surgery, University of Cologne, Joseph-Stelzmann Str. 9, 50931 Cologne, Germany; Fax: 0049-221-4786258; E-mail: wolfgang.schroder{at}uni-koeln.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In Barrett’s cancer, the frequency of lymph node metastases to the middle and upper mediastinum has rarely been analyzed because it requires a complete mediastinal lymphadenectomy.

Methods: Fifty-one patients with esophageal adenocarcinoma underwent transthoracic en-bloc esophagectomy with two-field lymph node dissection. A meticulous work-up of the resected specimen allowed a specific assignment of each single lymph node to defined groups of the abdominal and mediastinal compartment. Histopathology classified the lymph nodes as metastatic or nonmetastatic.

Results: A total of 1706 lymph nodes were resected, with a mean of 33.5 lymph nodes per patient (range, 13–74). Of 51 patients, 28 (54.9%) were classified as pN1; 7 (25%) of 28 pN1 patients had nodal metastases at the level of the tracheal bifurcation (3 of 28 patients) or in the upper mediastinum (5 of 28 patients). In all 28 pN1 patients, the abdominal compartment was involved. The distribution of nodal metastases demonstrated that the main lymphatic spread occurred close to the primary tumor, along the lesser curvature and the left gastric artery.

Conclusions: Adenocarcinomas of the distal esophagus have a bidirectional lymphatic spread to the mediastinum and the abdomen. Two-field lymphadenectomy seems to be an adequate surgical approach for this tumor entity to achieve a complete nodal clearance.

Key Words: Barrett’s cancer • Esophagectomy • Lymphadenectomy • Nodal metastasis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is well known that adenocarcinomas of the distal esophagus exhibit lymph node metastases close to the primary tumor in the lower mediastinum, along the lesser curvature and the left gastric artery.1–4 However, the frequency of mediastinal lymph node metastases proximal to the tumor in the middle and upper mediastinum is unclear, because in most series, only a lymphadenectomy of the lower mediastinum is performed.5,6 In addition, series with two-field lymphadenectomy, including the upper mediastinum, do not specify the exact frequency of metastases to these lymph node groups,7–9 do not differentiate between true adenocarcinomas of the distal esophagus and other carcinomas of the gastric cardia,1,2,4 or do not include squamous cell carcinomas of the esophagus10,11 in their analysis. Therefore, this study was performed to analyze the exact pattern of nodal metastases to the abdominal and especially the mediastinal compartment on the basis of a series of esophageal adenocarcinomas that were systematically treated by transthoracic en-bloc esophagectomy with complete mediastinal lymphadenectomy.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From February 1997 and September 2001, 52 patients with adenocarcinoma of the distal esophagus underwent surgical resection with curative intention and were included in this prospective study. According to morphological/topographical description, carcinomas of the gastroesophageal junction (type I–III) were designated as those with a tumor center 5 cm oral or aboral of the lower esophageal sphincter. Type I carcinomas were classified as adenocarcinomas of the distal esophagus with the majority developing in Barrett’s esophagus.6,12 In this study, only type I tumors were included. Because of an incomplete work-up of the resected specimen, one patient had to be excluded from further analysis.

Forty-nine (96.1%) of the 51 included patients were male; 2 were female. The median age was 60.9 years (range, 29 to 82 years). The overall distribution of the pathologic T categories was as follows: pT0 (n = 2, 3.9%), pT1 (n = 13, 25.5%), pT2 (n = 11, 21.6%), pT3 (n = 25, 49%), and pT4 (n = 0). Nineteen patients in good general health with locally advanced tumors (cT3/4NxM0) received standardized neoadjuvant radiochemotherapy. Cis-platinum (20 mg/m2/day) was administered as a short-term infusion on days 1 to 5, and 5-fluorouracil (1000 mg/m2/day) was administered as a continuous infusion over 24 hours on days 1 to 5. Radiotherapy was administered by linear accelerators with 10- to 15-MV photons. Radiotherapy was simulated to encompass the tumor volume with 5-cm cephalocaudad margins and 2-cm radial margins, and treatment ports were designed to include enlarged regional nodes on the basis of computed tomographic evaluation and endoscopic ultrasound. Radiation was delivered in daily fractions of 1.8 Gy (days 1–5, 8–12, 15–19, and 22–26), to a total dose of 36 Gy, by using a multiple-field technique. Surgical resection was performed after a 3-week rest after completion of chemoradiation. The ypT category of these patients was as follows: ypT0 (n = 2), ypT1 (n = 1), ypT2 (n = 3), and ypT3 (n = 13).

Surgery
After laparotomy and opening of the esophageal hiatus, the resectability of the primary tumor and the absence of distant metastases were reconfirmed. The duodenum was mobilized by an extensive Kocher maneuver followed by dissection of the gastrocolic and gastrosplenic ligament, with maintenance of the right gastroepiploic artery along the greater curvature. Partial en-bloc lymphadenectomy of compartment II was performed, including a meticulous dissection of lymph nodes along the left gastric artery (group 7), common hepatic artery (group 8), celiac trunk (group 9), and splenic artery (group 11). All lymph node groups were marked with different suture material to identify single groups after complete resection of the specimen. The right gastric artery was preserved. Before closure of the abdomen, gastric tube formation was commenced by one linear stapler (GIA 60, Tyco United States Surgical, US) placed at the lesser curvature between the middle and distal third. After the patient was moved to a left lateral position, an anterolateral thoracotomy through the fifth intercostal space was performed, followed by an en-bloc resection of the esophagus with dissection of the azygos vein and thoracic duct. Lymph node dissection of the upper mediastinum included the right-sided paratracheal nodes without the right recurrent nerve chain. The left paratracheal/recurrent laryngeal nerve chain was also left in situ. Lymph nodes at the tracheal bifurcation (subcarinal group) were dissected separately. The esophagus was transected in the upper mediastinum 3 to 5 cm above the azygos vein, and the stomach was pulled up into the chest. A stapler esophagogastrostomy was performed at the gastric fundus with a circular stapler (Premium plus CEEA 28, Tyco United States Surgical, US). The procedure was completed by resection of the lesser curvature with the adherent esophagus by a linear stapler (TA 90, Tyco United States Surgical, US).

Pathology
The work-up immediately after resection of the specimen followed a standardized protocol and included close cooperation of the operating surgeon and an experienced pathologist. Abdominal lymph nodes were classified according to the Japanese Gastric Cancer Association.13 In addition to the marked lymph node groups of compartment II, lymph nodes of the gastric cardia (group 1), gastric fundus (group 2), and lesser curvature (group 3) were dissected from the specimen and separated. Mediastinal lymph nodes were separated into three groups: lymph nodes of the lower mediastinum, lymph nodes at the level of the tracheal bifurcation (carinal, left, and right bronchial lymph nodes), and lymph nodes of the upper mediastinum (paratracheal lymph nodes).

All lymph nodes, as well as representative sections of the primary tumor, were fixed in 5% formaldehyde and embedded in paraffin. After equatorial sectioning of the lymph nodes at six levels, routine staining with hematoxylin and eosin, as well as periodic acid–Schiff, was performed to histologically examine the presence or absence of metastatic disease. The number and site of all lymph node metastases were recorded. Histopathological findings were classified according to International Union Against Cancer tumor-node-metastasis guidelines.14

Statistical Analysis
Descriptive analysis was used to characterize data. The prevalence of lymph node metastases was analyzed by the Wilcoxon test, and ordinal data, by the {chi}2 test. P < .05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Lymph Node Dissection
A total of 1706 lymph nodes were resected from 51 patients (mean, 33.5 lymph nodes per patient; range, 13–74). A total of 733 lymph nodes were dissected from the mediastinal compartment (mean, 14.4 lymph nodes per patient; range, 3–55), and 973 lymph nodes were dissected from the abdominal compartment (mean, 19.1 lymph nodes per patient; range, 3–32). The number of resected lymph nodes was similar for compartment I and II of the abdomen (compartment I, 473 lymph nodes, average 9.3; compartment II, 500 lymph nodes, average 9.8). Twenty-eight (54.9%) of 51 patients had lymph node metastases to the abdominal and mediastinal compartment and were classified as pN1. Only this patient group was subjected to further analysis. A total of 983 lymph nodes were resected in these patients (mean, 35.1 lymph nodes per patient; range, 17–74). Of these lymph nodes, 21.9% (n = 216) showed histological evidence of metastatic infiltration. Differences between 19 patients with neoadjuvant radiochemotherapy and 32 patients without preoperative radiochemotherapy are summarized in Table 1.


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  		TABLE 1. Differences between 19 patients with neoadjuvant radiochemotherapy and 32 patients without preoperative radiochemotherapy
 
Pattern of Nodal Metastases
The distribution of metastatic lymph nodes to single node groups is displayed in Table 2. The majority of metastatic lymph nodes were located in the abdomen (158 metastatic lymph nodes [73.1%] in the abdominal compartment vs. 58 metastatic lymph nodes [26.9%] in the mediastinal compartment). The prevalence of positive nodes was 27.9% in the abdomen (158 of 566 resected nodes) and was significantly higher (P < .0001) compared with the mediastinal compartment (58 metastatic of 417 resected lymph nodes; 13.9%). The majority of lymph node metastases were located in close proximity to the primary tumor in the lower mediastinum (33 of 141 resected lymph nodes; 23.4%), at the lesser curvature at node group 1 (40 of 117 resected lymph nodes; 34.2%) and node group 2 (19 of 52 resected lymph nodes; 36.5%), and along the left gastric artery (42 of 111 resected lymph nodes; 37.8%). At the level of the tracheal bifurcation and in the upper mediastinum, only a small portion of the resected lymph nodes were metastatic (10.6% and 6.9%, respectively).


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  		TABLE 2. Pattern of nodal metastases of 28 pN1 patients with adenocarcinoma of the distal esophagus
 
In all 28 patients with metastatic lymph nodes, the abdominal compartment was involved; in 9 patients (32.1%), the abdominal compartment alone was involved, and in 19 patients (67.9%) it was involved in combination with the mediastinal compartment. The most frequently involved lymph node group was group 1, with 64.3% (18 of 28) of the pN1 patients. At least 12 (42.9%) of 28 patients could be classified as having pM1 lymph for esophageal carcinoma because of metastatic lymph nodes located at the celiac trunk (n = 8), the common hepatic artery (n = 5), and the splenic artery (n = 1). In case of metastatic lymph nodes in the mediastinum, 15 of 19 patients showed metastatic infiltration of lymph nodes in the lower mediastinum. In 3 of 28 pN1 patients (10.7%) and in 5 of 28 pN1 patients (17.9%), infiltrated lymph nodes were found at the level of the tracheal bifurcation or in the upper mediastinum, respectively. Summarizing these two lymph node groups, 7 (25%) of 28 pN1 patients had lymph node metastases proximal to the primary tumor. Six of these seven patients had locally advanced primary tumors (pT3, n =3; ypT3, n =3) (Table 3). Only one of the seven patients had an early esophageal carcinoma (pT1).


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  		TABLE 3. Correlation of T stage and location of mediastinal lymph node metastases in 19 patients with mediastinal lymph node metastases
 
Only 3 (23.1%) of 13 patients with early adenocarcinoma (pT1) had nodal metastases. In all three patients, the abdominal compartment showed evidence of metastatic infiltration. In two patients, the mediastinal compartment was also involved.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The surgical approach, the extent of resection, and, in particular, the extent of lymphadenectomy are still matters of controversy in adenocarcinoma of the gastroesophageal junction. Radical transhiatal resection is advocated as standard procedure for adenocarcinoma of the distal esophagus,5,6,15 but there is increasing evidence that favors transthoracic resection.3,4 Both procedures offer an adequate proximal and distal resection margin to perform a complete resection of the primary tumor, but they differ in terms of mediastinal lymphadenectomy. Whereas transhiatal resection can clear only the lower mediastinal lymph nodes, the transthoracic approach is associated with a complete two-field lymphadenectomy, including the lymph nodes at the level of the tracheal bifurcation and the upper mediastinum. On the basis of these considerations, the crucial questions have to be whether adenocarcinomas of the distal esophagus metastasize to lymph nodes of the middle and upper mediastinum and whether an extended lymphadenectomy of this region results in a prognostic benefit in terms of decreased locoregional recurrence and increased survival. The last two issues can not be addressed in this study, but the rate of lymph node metastasis in the middle and upper mediastinum could favor the transthoracic en-bloc esophagectomy.

In patients with squamous cell carcinoma of the esophagus, a bidirectional lymphatic spread to the abdominal and cervical compartment could be demonstrated in several studies, including our own.16–19 Even in submucosal carcinomas of the thoracic esophagus, cervical lymph node metastases were observed in 17% of all patients.20 Consequently, several authors performed a three-field lymphadenectomy for squamous cell cancer of the thoracic esophagus. This radical lymph node dissection resulted in an increased 5-year survival compared with that of patients with two-field lymphadenectomy who served as historical controls.21–23

The pattern of lymphatic spread in adenocarcinoma of the distal esophagus has not been as extensively and systematically investigated as that of squamous cell carcinoma. Only a few articles have been published regarding a two-field1,3,4,7–9 or three-field10,11 lymphadenectomy for adenocarcinoma of the distal esophagus. Despite this extended lymphadenectomy, the crucial question of lymph node metastasis to the middle and upper mediastinum cannot be completely answered in most of these studies. A few authors do not give a distinct and detailed description of lymphatic spread for type I adenocarcinoma to different lymph node groups in the mediastinum.7,9 Other studies include adenocarcinomas of the distal esophagus and also the gastric cardia in their analysis, so it is not possible to exactly characterize the lymphatic spread for single tumor entities of different locations.1,4 Other authors analyze adenocarcinoma and squamous cell carcinomas in the same series,10,11 and we consider these to be two different biological tumor entities.

Despite these disadvantages, most published studies demonstrate a predominantly abdominal spread along the lesser curvature and left gastric artery of the stomach to the celiac trunk.1–4,8 This corresponds to our results. Therefore, this pattern of nodal spread requires an adequate lymphadenectomy of compartment I (lymph node groups 1–3) and compartment II (lymph node groups 7–9). Because the rate of positive lymph nodes along the splenic artery (lymph node group 11) is very low, lymphadenectomy of this region cannot be generally recommended.

Although most previous studies do not exactly specify the location of mediastinal lymph node metastases, the results of this study and other studies clearly demonstrate that adenocarcinomas of the distal esophagus do metastasize to mediastinal lymph nodes that are located proximal of the primary tumor. In the first article of Clark et al.,1 1 of 42 patients with adenocarcinoma of the distal esophagus and cardia had lymph node metastases at the level of the tracheobronchial system. Altorki and Skinner10 performed a three-field lymphadenectomy in 15 patients with adenocarcinoma of the esophagus and demonstrated metastases to the cervical nodes (recurrent or/and deep cervical nodes) in 4 patients. Dresner et al.3 performed a two-field lymphadenectomy in 104 patients with adenocarcinoma of the esophagus. The prevalence of nodal metastases to the right and left bronchus was approximately 15%; paratracheal nodes in the upper mediastinum were involved in <10%. Hulscher et al.4 found that subcarinal nodes and paratracheal nodes in the upper mediastinum were positive in 19% and 8% of the patients, respectively. In this series, the authors did not differentiate between tumors of the tubular esophagus and the esophagogastric junction.

This study consists of 51 patients with an adenocarcinoma of the esophagus who underwent a two-field en-bloc lymphadenectomy, including a complete clearance of the lower and upper mediastinum. A meticulous work-up of all resected specimens proved a high prevalence of 25% (7 of 28 pN1 patients) with metastatic lymph nodes located at the level of the tracheal bifurcation or in the upper mediastinum. Most of these patients had locally advanced tumors. Therefore, at least 25% of pN1 patients would have had an incomplete resection in terms of lymph node clearance in case of a transhiatal resection. In addition, the immunohistochemical work-up of the resected lymph nodes might detect tumor cell microinvolvement, or micrometastases, thereby increasing the prevalence of involved lymph nodes in the upper mediastinum.24 Compared with squamous cell carcinoma of the lower third of the esophagus, the prevalence of metastatic lymph nodes in the subcarinal or paratracheal region is similar. In addition, because the same mediastinal lymph node groups are involved, the pattern of dissemination seems to be the same for both histological subtypes. Therefore, it seems to be justified to use the same surgical approach and resection for both esophageal carcinomas.

Currently, there are no studies that investigate the influence of neoadjuvant radiochemotherapy on the pattern of lymphatic spread. Because for squamous cell carcinoma and adenocarcinoma the number of resected lymph nodes is lower in patients who receive preoperative treatment,25 the incidence of upper mediastinal lymph node metastases before treatment can be expected to be even higher than the reported 25%.

In conclusion, whether removal of positive mediastinal nodes decreases the incidence of locoregional recurrence and might improve long-term survival is beyond the scope of this analysis. However, these data clearly demonstrate that adenocarcinomas of the distal esophagus have a bidirectional lymphatic spread and, in particular, that lymph node metastases in the middle and upper mediastinum are a frequent event. To achieve a complete clearance of metastatic nodes, a two-field lymphadenectomy seems adequate preferentially for locally advanced tumors. Because the rate of nodal metastases is more than 20% for submucosal carcinomas,26 even this type of early carcinoma should be considered for an extended lymphadenectomy.


   Footnotes
 
Adenocarcinomas of the distal esophagus demonstrate a bidirectional lymphatic spread to the abdominal and mediastinal compartment. Twenty-five percent of pN1 patients with Barrett’s cancer have metastatic lymph nodes at the level of tracheal bifurcation and upper mediastinum.

Received for publication January 7, 2002. Accepted for publication June 4, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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