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Ann Thorac Surg 2001;72:225-229
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Value of systematic mediastinal lymph node dissection during pulmonary metastasectomy

Accepted for publication March 1, 2001.

Address reprint requests to Dr Loehe, Department of Surgery, University of Munich, Marchioninistr 15, D-81377 Munich, Germany
e-mail: floehe{at}hotmail.com

	Abstract

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Background. Systematic mediastinal lymph node dissection is the accepted standard when curative resection of bronchial carcinoma is performed. However, mediastinal lymph node dissection is not routinely performed with pulmonary metastasectomy, in which only enlarged or suspicious lymph nodes are removed. The incidence of malignant infiltration of mediastinal lymph nodes in patients with pulmonary metastases is not known.

Methods. Sixty-three patients who underwent 71 resections through a thoracotomy for pulmonary metastases of different primary tumors were studied prospectively. Selected patients showed no evidence of tumor progression or extrathoracic metastases and pulmonary metastasectomy was planned with curative intent. All patients underwent preoperative helical computed tomography (CT) scanning. Only patients with no evidence of suspicious mediastinal lymph nodes on the CT scan (less than 1 cm in the short axis) were included in this study. A mediastinal lymph node dissection was performed routinely with metastasectomy.

Results. In 9 patients (14.3%) at least one mediastinal lymph node revealed malignant cells in accordance with the resected metastases. When compared with the preoperative CT scan, additional pulmonary metastases were detected in 16.9% of performed operations. There was a trend toward an improved survival rate in patients without involvement of the mediastinal lymph nodes. The number of pulmonary metastases had no influence on survival.

Conclusions. On a patient-by-patient basis, the frequency of misdiagnosed mediastinal lymph node metastases is about the same as compared with non–small cell bronchial carcinomas. Systematic mediastinal lymph node dissection reveals a significant number of patients, who otherwise are assumed free of residual tumor. The knowledge of metastases to mediastinal lymph nodes after complete resection of pulmonary metastases could influence the decision for adjuvant therapy in selected cases.

	Introduction

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Pulmonary metastases are often best treated by resection if the primary tumor is under control and metastatic disease at other sites is absent [1]. The most consistent prognostic factor predicting survival is complete surgical removal of all metastases [2, 3]. It has been reported that thoracotomy and palpating the deflated lung during resection of pulmonary lesions presumed to be metastases often reveals additional pulmonary lesions, which were not detected on the preoperative computed tomography (CT) chest scan. When compared with preoperative CT chest scans, additional malignant pulmonary lesions were found in up to 30% of patients by thoracotomy [4, 5].

Thoracotomy and systematic nodal dissection performed in curative resection of bronchial carcinoma revealed metastases to mediastinal lymph nodes in 10% to 36%, which appeared to be of normal size on the preoperative CT scan [6, 7]. Because dissection of mediastinal lymph nodes is usually not performed routinely during metastasectomy, no studies have reported on additional lymph node metastases when the CT chest scan shows only normal-sized mediastinal lymph nodes (less than 1 cm in short axis).

Therefore, the purpose of the present study was to investigate the incidence of malignant mediastinal lymph nodes when compared with preoperative CT chest scans in patients with pulmonary metastases.

	Material and methods

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During a 33-month period (January 1996 to September 1998) a total of 71 pulmonary resections and ipsilateral mediastinal lymph node dissections through a thoracotomy were performed on 63 consecutive patients with pulmonary metastases. In 41 patients (65.1%) lung metastases were the first site of metastatic disease; 22 patients (34.9%) had a history of surgically treated metastases at other locations.

In this study only patients with no evidence of extrathoracic metastases and residual or local recurrent disease at the site of primary tumor were included. The 24 women and 39 men had a mean age of 59.3 ± 12.5 years (range 22.2 to 82.7 years). In 8 patients (12.7%) pulmonary metastases were bilateral. Pulmonary metastases were discovered on chest radiographs or CT scans performed during routine follow-up. The mean interval between surgical therapy of the primary tumor and appearance of pulmonary metastases was 33.8 ± 39.8 months (range 1 to 204 months). The distribution of primary tumors is shown in Table 1.

Procedure
Wedge or segmental resections of the pulmonary nodules were the operative procedures of choice. A lobectomy was performed when either a solitary metastasis was located deeply and centrally in the lobe or when multiple nodules were confined to one lobe. Pneumonectomy was performed if no other choice was available to achieve radical metastasectomy.

The surgical approach was a standard anterolateral thoracotomy. Only monolateral procedures were performed. Patients with bilateral metastases (8 of 63 cases) underwent delayed sequential contralateral thoracotomy within 8 weeks. After mobilization of the lung by dissecting the pulmonary ligament and adhesions, the lung was palpated in atelectasis and every suspicious nodule was resected. Wedge resection was the preferred procedure, but—when necessary—extended resections were performed to achieve an R0-resection (no microscopic or macroscopic malignant disease left after metastasectomy).

Mediastinal lymph nodes were dissected systematically at the following locations according to the American Thoracic Society [8]: L1 through L4 (superior and inferior pre- and paratracheal), L5 (subaortic), L6 (paraaortic), L8 (paraesophageal), L9 (pulmonary ligament), and L10 (hilar).

Statistical analysis
Differences between the groups were compared with the ² test. A Kaplan–Meier analysis of cumulative survival was calculated and difference in survival was compared using the log rank test. Differences were considered significant when p was less than 0.05.

	Results

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The mean disease-free interval (DFI) until the occurrence of pulmonary metastases was 32.2 ± 33.4 months (range 0 to 146 months). We performed 71 pulmonary resections (right side = 41; left side = 30) in 63 patients. Table 2 lists types of operative procedures for radical resection of all palpable metastases. No intraoperative complication developed. Three patients (4.8%) had postoperative minor complications (1 had superficial wound infection and 2 had pneumonia) that were treated successfully. Major complications developed in 3 patients (4.8%): a Mallory–Weiss gastric bleeding was treated successfully by endoscopic intervention, a postoperative pleural empyema had to be drained operatively, and 1 patient with a postoperative myocardial infarction died. Therefore, the total mortality rate was 1.6%. The average hospital stay was 10.8 ± 5.9 days (range 1 to 43 days).

In all 71 pulmonary resections, histologic examination proved lung metastases in accordance with the primary tumor. There was a discrepancy between the number of identified pulmonary lesions on the preoperative CT scan and the findings on digital palpation of the deflated lung during the operation in 19 resection procedures (26.8%) involving 19 different patients (30.2%). In one case, the number of manually palpated lesions was less than those identified on the preoperative CT scan. Depending on the primary tumor, the incidence of additional pulmonary lesions, which were found during the operation, differed between 0% and 42.8% (Table 1). The histologic examination revealed a total number of 22 additional metastases after 71 pulmonary resections (16.9%) involving 12 different patients (19%).

None of the performed preoperative CT chest scans suggested malignant alteration by enlargement of the mediastinal lymph nodes. Macroscopically the collected mediastinal lymph nodes were not suspicious, but histologic examination gave evidence of malignant cells in at least one mediastinal lymph node in accordance with the resected lung metastases in 9 cases (12.7%) involving 9 patients (14.3%) (Table 3). The incidence of positive mediastinal lymph nodes depending on the primary tumor ranged between 5.6% (colon/rectum) and 33.3% (gynecological malignancies), but the difference was not significant. There was only a tendency (p = 0.49) toward an increasing incidence of nodal involvement between patients with a solitary pulmonary metastasis (9.7%) and patients with two or more pulmonary metastases (17.6%).

View larger version (16K): [in this window] [in a new window]   Fig 1. Kaplan–Meier cumulative survival for patients after pulmonary metastasectomy with positive mediastinal lymph nodes (+) and without nodal involvement (-), log rank p = 0.37.

The mean DFI in the group of survivors was 37.6 ± 37.2 months (range 0 to 146 months) and did not differ significantly from the mean DFI of the patients who died (22 ± 21.9 months; range 0 to 88 months).

	Comment

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Almost 30% of patients who have curative resection of a malignancy will develop pulmonary metastases [9]. Therefore, all newly detected pulmonary lesions after a history of malignant disease are strongly suspicious for metastases. Only histologic examination of the resected pulmonary nodule provides the correct diagnosis and may influence further therapeutic approaches.

Complete surgical resection of pulmonary metastases is now an accepted treatment for improving the overall and disease-free survival and is performed routinely in selected patients. The overall survival rate after complete pulmonary metastasectomy is 36% at 5 years and 26% at 10 years [3]. Survival in patients operated on for solitary metastasis compared with patients with two or more metastases is considered to be significantly higher [5, 9, 10]. In contrast, the number of pulmonary metastases and DFI had no influence on survival in our study. Nevertheless, there is general agreement that a complete resection of all pulmonary metastatic lesions is crucial for long-term survival. Incomplete resection decreases survival significantly [2, 3, 5, 9].

In our study, the overall incidence of intraoperatively detected additional pulmonary lesions as compared with the preoperative CT scan was 26.8%, revealing additional pulmonary metastases in 16.9% of performed operations. In 1997, Girard and colleagues [5] observed in a study of 346 patients with pulmonary metastases an overall incidence of additional metastases in 30%. Again our data suggest the recommendation that complete surgical exploration by thoracotomy and palpating the lung should remain the procedure of choice in patients undergoing therapeutic pulmonary metastasectomy [11].

In our study the frequency of wedge and segmental resections (70%) was the same as reported from an analysis of 5,206 cases of pulmonary metastasectomy [3]. Other investigations also showed that a pneumonectomy was necessary in up to 8% of patients for achieving radical metastasectomy [2, 12]. To evaluate the incidence of metastatic involvement of macroscopically unsuspicious mediastinal lymph nodes, we performed a mediastinal lymph node dissection also in patients undergoing wedge resections for pulmonary metastasectomy. There was no difference when comparing the perioperative morbidity and mortality in our study with the results reported by other investigations about pulmonary metastasectomies without mediastinal lymph node dissection [2, 3].

Systematic nodal lymph node dissection must be performed routinely in patients undergoing pulmonary resection of lung cancer for accurate intrathoracic staging, because the sensitivity of CT scans to correctly predict lymph node involvement is only 73% [13, 14]. Several studies have already shown that metastatic involvement of lymph nodes in patients with bronchial carcinoma is frequently misdiagnosed by preoperative CT scan, revealing a false-negative prediction between 14% and 18% [15–17]. All these studies were based on the assumption that 1 cm in the short axis in the transversal plane represents the upper limit of a normal mediastinal lymph node [18, 19].

However, routine mediastinal lymph node dissection accompanying pulmonary metastasectomy is not an accepted standard curative concept in patients with pulmonary metastases. An analysis of the International Registry of Lung Metastases based on 5,206 cases revealed in 5% metastases to hilar or mediastinal lymph nodes, but only suspicious lymph nodes were removed and lymph node dissection was performed in less than 9% of patients [3]. Another study suggested that local recurrence after complete pulmonary metastasectomy seemed to be decreased when a mediastinal lymph node dissection was performed simultaneously [20]. Factors predicting the incidence of mediastinal lymph node involvement in patients with pulmonary metastases are not known. In addition, our investigation, because of the small sample size, does not allow a valid statistical analysis to identify risk factors or predictors for the possibility of nodal involvement or clinical outcome. In our study, we performed routine mediastinal lymph node dissection and found metastases to mediastinal lymph nodes in 12.7% of pulmonary resections; 70% of the pulmonary metastasectomies were performed as wedge and segmental resections in our study. Collecting L11 through L14 lymph nodes could have raised the operative complication rate in these cases. Furthermore, routine dissection of L7 lymph nodes involves an extension of the lymph node dissection to the contralateral mediastinum and could have increased the operative morbidity in our preliminary study. Therefore, routine evaluation L7 and L11 through L14 was not included in our preliminary investigation.

The incidence of malignant infiltration of unsuspicious mediastinal lymph nodes in patients undergoing pulmonary metastasectomy is not known. The assessment of L7 and L11 through L14, which is required for a complete systematic node dissection, would have raised the frequency of nodal involvement documented on a patient-by-patient basis.

The findings of our preliminary study suggest that long-term survival of patients with metastases to mediastinal lymph nodes could be impaired when compared with patients without metastatic lymph node infiltration, whereas DFI and number of pulmonary metastases had no influence on survival.

In accordance with other studies, we found additional pulmonary metastases when compared with the number predicted on the preoperative CT scan in up to 17%. Therefore, thoracotomy and digital palpation of the lung should remain the standard operative procedure to achieve curative metastasectomy. Furthermore, based on our results, we suggest that a routine mediastinal lymph node dissection for histologic examination performed with complete metastasectomy provides useful information to assess the state of tumor progression, permitting more accurate oncologic staging.

	References

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