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Ann Thorac Surg 2006;81:448-454
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Nodal Involvement at the Time of Pulmonary Metastasectomy: Experiences in 245 Patients

Department of Surgery, Thoraxklinik Heidelberg, Heidelberg University, Germany

Accepted for publication August 25, 2005.

^_* Address correspondence to Dr Pfannschmidt, Department of Surgery, Thoraxklinik Heidelberg, Amalienstr 5, Heidelberg D-69126, Germany (Email: joachim.pfannschmidt{at}thoraxklinik-heidelberg.de).

	Abstract

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BACKGROUND: Although routine systematic mediastinal and hilar lymph node dissection contemporary with pulmonary metastasectomy has not been uniformly performed in many thoracic surgical centers, the value of this procedure needs to be investigated.

METHODS: Between 1996 and 2001, 245 patients (157 men, 88 women) underwent pulmonary resection of metastatic colorectal carcinoma, sarcoma, and renal cell carcinoma. Generally, systematic mediastinal and hilar lymph node dissection was performed concurrently with pulmonary metastasectomy. Patients were assessed for patterns of lymph node metastases. The frequency of lymph node involvement was determined. Patients and tumor characteristics were assessed to ascertain whether certain factors were likely to predict lymph node spread.

RESULTS: Of the 245 patients (328 primary thoracic procedures), 165 had no lymph node involvement, 45 had pulmonary and hilar metastases, 22 had pulmonary, hilar, and mediastinal metastases, and 13 had only mediastinal involvement without pulmonary and hilar spread. Patients with more than one pulmonary metastasis or metachronous disease were more likely to have thoracic lymph node metastases. The risk for mediastinal lymph node involvement was even more likely for patients who had already pulmonary or hilar lymph node spread; the odds ratios (with 95% confidence intervals) were 1.30 (0.71 to 2.36), 1.32 (0.59 to 2.99), and 5.87 (2.73 to 12.6), respectively. Median survival for the group of patients after complete resection was 54.8 months (95% CI: 40.9 to 68.7); and for the patients with no lymph node involvement, it was 63.9 months (95% CI: 45.3 to 82.6); with N1 disease, 32.7 months (95% CI: 9.2 to 56.2); and with N1 + N2 disease, 20.6 months (95% CI: 5.1 to 36.1). The log-rank test revealed significance between N0 and N1 (p = 0.018) and N0 versus N1, 2 (p = 0.001).

CONCLUSIONS: We conclude that systematic mediastinal and hilar lymph node dissection contemporary with pulmonary metastasectomy offers a further understanding of metastatic disease and provides important information for complete surgical staging.

	Introduction

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Surgical resection remains an important form of treatment for pulmonary metastases from a variety of solid tumors. Many tumors may involve the lung as the unique site of distant spread. The presence or absence of lymph node metastasis is discussed as a single important factor for estimating the prognosis in pulmonary metastasectomy for most extrapulmonary malignancies [1–4]. Routine systematic mediastinal and hilar lymph node dissection contemporary with pulmonary metastasectomy has not been uniformly performed in many thoracic surgical centers. In adopting the recommended procedures in surgical oncology and especially for lung cancer we, like others, [5] have performed systematic lymph node dissection as a standard procedure for pulmonary metastasectomy since 1985. Kamiyoshihsra and colleagues [6], in a retrospective study of 28 patients undergoing pulmonary metastasectomy, suggested that local recurrence seemed to be decreased when a mediastinal lymph node dissection was performed.

Although several studies regarding pulmonary metastasectomy have been published during the last few years, the exact incidence, the pattern of lymph node involvement, the clinical significance, and the pathologic and oncologic interpretation of thoracic lymph node metastases remain to be clarified.

This study was conducted on a series of patients after pulmonary metastasectomy with concurrently systematic hilar and mediastinal lymph node dissection. It focuses on the pattern of lymph node metastases, outcome, long-term results, and factors associated with thoracic lymph node metastases in different tumor entities.

	Patients and Methods

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We retrospectively analyzed 245 patients (157 men and 88 women) who underwent resection of pulmonary metastases in metastatic colorectal cancer (n = 114), renal cell cancer (n = 62), and sarcoma (soft tissue sarcoma, n = 48, and osteosarcoma, n = 21) from January 1996 to December 2001.

After submission of the study to the Institutional Review Board (Ethics Committee, University Hospital of Heidelberg), the chairman approved the study and waived the need for informed consent.

Median age was 58.2 years (range, 32 to 73) for patients with primary renal cell cancer, 60.5 years (range, 31 to 79) for patients with colorectal carcinoma, and 39.8 years (range, 10 to 68) for patients with sarcoma. Primary sarcoma histology is presented in Table 1.

Cases were included only if the histologic features of the pulmonary metastases were compatible with the histology of the primary lesion and characteristic for pulmonary metastases. The pathologic specimens were assessed for patterns of tumor spread at pulmonary/hilar (N1) and mediastinal (N2) lymph node stations according to the International System for Staging Lung Cancer [7]. The N1 lymph node status was confirmed in most cases from the dissected pulmonary lymph nodes by the pathologist. Thus, information about the spread in N1 and N2 lymph nodes was gathered by the surgeon in addition to the pathology report and lymph node dissection.

All patients were retrospectively analyzed for age and sex, primary tumor location, number of pulmonary metastases, and disease-free interval to ascertain whether certain factors were likely to predict lymph node metastases. The endpoint for the assessment of survival was death.

In total, 328 primary thoracic procedures were performed in 245 patients who underwent surgical resection. The surgical approach was chosen according to the location and number of pulmonary nodules. To facilitate a systemic lymph node dissection and for more centrally located metastases, nearly all patients were treated by a sequential approach with lateral thoracotomy. Sternotomies were performed in 4 patients and clamshell incisions in 3 patients for a bilateral approach. The type of lung resection for metastasectomy ranged from wedge resection to various types of anatomic lung resections in selected cases (Table 2). When in doubt of the histology between the primary bronchial adenocarcinoma and metastases of colorectal origin in frozen sections, we performed a lobectomy if the patient was an operable candidate for lobectomy.

Statistical Analysis
The data were analyzed by SPSS for Windows software (Statistical Package for Social Science; SPSS Inc, Chicago, Illinois). Critical values of prognostic factors differentiating between patient groups with good and poor prognosis were determined by the critical level procedure described by Abel and colleagues [9]. The best cut-off value was defined as the value that best discriminated between good and poor prognosis. Probability of survival was then analyzed by the Kaplan-Meier method using the date of pulmonary resection as the starting point [10]. For patients who underwent bilateral sequential metastasectomy, the date of the second operation was used as the starting point. The significance of differences between subgroups was calculated using the log-rank test. Odds ratios with 95% confidence intervals (CI) were calculated for each characteristic [11].

	Results

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There was no operative death. The mean follow-up period of surviving patients (censored patients) was 42.4 months (95% CI: 38.7 to 45.9). Of 201 patients (82.0%) who underwent complete resection, 92 patients (81%) with colorectal cancer, 55 patients (88.7%) with renal cell cancer, and 54 patients (78.3%) with sarcoma had complete resections.

After resection of the pulmonary metastases of extrapulmonary primaries, the following lymph node characteristics were determined on histologic evaluation in 328 procedures. There were 91 lymph node compartments involved with at least one metastatic lymph node. Of all patients (n = 245), 165 had no involvement of lymph nodes, 45 had only pulmonary and hilar involvement, 22 had pulmonary, hilar and mediastinal involvement, and 13 had only mediastinal involvement without pulmonary and hilar involvement.

Of the overall group of 80 patients with lymph node metastases, 13 patients (16.3%) had mediastinal noncontiguous lymph node spread.

The median disease-free interval for patients with and without lymph node involvement was 33.2 months, and 26.6 months, respectively.

Next, a review of patients and tumor characteristics was made to determine whether certain characteristics predicted a higher prevalence of lymph spread. Odds ratios were calculated to determine whether certain characteristics were associated with a higher rate of thoracic lymph node spread (Table 3).

The lymph node involvement according to the number of patients with tumor location in different pulmonary lobes was studied (Figs 1, 2, and 3). Analysis of the spreading to intrapulmonary lymph nodes and then to hilar ones revealed, for lymphatic metastatases of sarcomas, a quota of 49% with noncontiguous involvement of mediastinal lymph nodes, 51% with N1 involvement, and no patient with lymph node involvement in N1 and mediastinal sites together. On the contrary, lymphatic drainage from colorectal metastases showed a pattern of distribution with a proportion of 44.1% metastatic N1 sites, 35.6% N1 and N2 sites, and 20.3% noncontiguous N2 lymph node metastases. In renal cell cancer metastases, we found 66.7% isolated N1 involvement, 10.4% N1 and N2 disease, and 22.9% noncontiguous mediastinal disease (Figs 1, 2, and 3).

View larger version (37K): [in this window] [in a new window]   Fig 1. Number of patients with metastases of renal cell cancer in different lobes and pattern of lymphatic spread.

View larger version (38K): [in this window] [in a new window]   Fig 2. Number of patients with metastases of colorectal carcinoma in different lobes and pattern of lymphatic spread.

View larger version (37K): [in this window] [in a new window]   Fig 3. Number of patients with metastases of sarcoma in different lobes and pattern of lymphatic spread.

Although survival was not a major endpoint of this evaluation, overall survival was assessed for the studied group of patients: patients with N0 disease, N1 disease, N1 disease with N2 disease, and N2 disease without N1 disease. Expectedly, the nodal status significantly influenced survival for the overall group of patients and the group of patients after complete resection. Survival data for the group of 245 patients are presented in Table 4 and Figure 4. Median survival for the group of patients after complete resection was 54.8 months (95% CI: 40.9 to 68.7); and for the patients with no lymph node involvement it was 63.9 months (95% CI: 45.3 to 82.6), for N1 disease, 32.7 months (95% CI: 9.2 to 56.2), and for N1 plus N2 disease, 20.6 months (95% CI: 5.1 to 36.1). The log-rank test revealed significance between N0 and N1 (p = 0.018) and N0 versus N1, 2 (p = 0.001).

View larger version (27K): [in this window] [in a new window]   Fig 4. Survival curves with respect to lymph node involvement. Zero time on the abscisse represents the date of pulmonary resection (log-rank test). (Black solid line: no lymph node involvement; black dotted line: N1 lymph node involvement; gray solid line: N1 + N2 lymph node involvement; gray dotted line: N2 lymph node involvement.)

	Comment

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The role of thoracic lymph node metastases in the treatment of pulmonary metastases is controversial, as metastatic lymphatic spread is considered an ominous prognostic sign [1–3]. In the present series, thoracic lymph node involvement was less often seen in sarcomas (20.3%) than in colorectal (31.3%) and renal carcinoma (42.4%) metastases. More recently, Ercan and colleagues [1] found thoracic lymph node metastases in 28.6% in a study of 70 nonsarcoma patients with concurrently systemic lymph node dissection [1]. Saito and associaites [15] reported on 165 patients with pulmonary metastases of colorectal origin and found 14.9% lymph node involvement. We have found in earlier studies, metastatic colorectal carcinoma in 19.2% and renal carcinoma in 27.5% of patients' thoracic lymph node metastases [3, 4].

The pattern of metastasis of most primary sarcomas is hematogenous; lymph node metastases are uncommon, except for angiosarcomas, synovial sarcomas, and embryonal rhabdomyosarcomas [16]. In our study, sarcoma cell types with a tendency for lymphatic spread are seen, but they form a small subgroup.

Noteworthy, the quota of noncontiguous mediastinal lymph node spread in sarcomas was exceptionally high (49% of thoracic lymph node metastases) compared with 22.9% in renal cell cancer and 20.3% in colorectal cancer in our present series.

The role of noncontiguous N2 lymph node metastases in metastatic disease is not well understood. It is possible that patients with involvement of N2 lymph nodes but not N1 lymph nodes would form a different subgroup. In the current study, however, survival with patients with N2 disease without N1 disease was found to be somewhat worse than that of the patients with involvement of N1 and N2 lymph nodes, but the subgroups were small.

For nonsmall-cell lung cancer, Riquet and coworkers [17] discussed the finding that direct lymphatic channels exist between the lung parenchymal and mediastinal lymph node stations. If this were true, one might hypothesize that pulmonary metastases metastasize to mediastinal lymph nodes. Putnam [18] suggested that mediastinal lymph node metastases rarely occur from pulmonary metastases; however, his report deals exclusively with metastatic sarcoma. We found a high probability of mediastinal lymph node spread, if N1 lymph nodes are involved (odds ratio 5.87). Contrarily, mediastinal lymph node involvement through the spread from abdominal (namely, celiac, portal) lymph node metastases is discussed for colorectal and renal cell carcinoma [19–21]. In the case of pulmonary or hilar lymph node involvement (which is the drainage of the lung), these lymph node metastases are believed to be the result of metastases from the pulmonary metastases [22].

We found an increased risk for thoracic lymph node (N1/2) involvement for patients with metachronous disease and more than one pulmonary metastasis. The occurrence of thoracic lymph node metastases in approximately 20.3% to 42.4% of patients in this study with resectable pulmonary metastases of extrapulmonary malignancies has important implications for long-term survival. Univariate analysis showed a statistically significant difference in survival between patients with lymph node involvement and those without lymph node metastases.

If pulmonary and lymph node metastases are clinically important because they serve as a source of ongoing disease dissemination, early removal of such lesions may interrupt the cascade of metastatic cells derived from metastatic sites. Thus, surgery may be an important form of systemic therapy [6].

In a nonrandomized comparison for patients with bronchial carcinoma, there is some evidence that complete mediastinal lymph node dissection may be associated with improved survival, when compared with systematic lymph node sampling [23]. In the reports by Keller and colleagues [23] and others [24], systematic sampling was as efficacious as complete mediastinal lymph node dissection in staging patients with nonsmall-cell lung cancer. One might speculate whether that may be also true for pulmonary metastasectomy.

In 16 of 72 patients with a preoperative solitary pulmonary nodule suspected of metastases, lymph node involvement was detected by systematic lymph node dissection. Thus, pulmonary resection of a single nodule by video-assisted endoscopic surgery without systematic mediastinal and hilar lymph node dissection is not recommended.

Faries and associates [25] discussed in a retrospective review of 76 patients lymphatic mapping and sentinel lymphadenectomy for primary and metastatic pulmonary neoplasms. Although technically challenging, the results demonstrated the feasibility of successful lymphatic mapping and sentinel lymphadenectomy in all patients [25]. Other novel methods of lymph node analysis, for example, thoracoscopic lymph node staging [26], immunohistochemical assays [27], percutaneous needle cytology [28], and transthoracic needle biopsy [29] are in evaluation for lung cancer but data for pulmonary metastasectomy are pending. The value of positron emission tomography [30] staging in pulmonary metastasectomy has evolved as an imaging modality that further improves detection of metastatic disease [31].

In our current approach, the histologic evaluation of enlarged mediastinal lymph nodes must always be performed, because the finding of metastatic nodal involvement would determine inoperability or indicate systemic chemotherapy. In a patient with a history of colorectal cancer or sarcoma and multiple pulmonary nodules and significant mediastinal enlargement detected in the CT scan or positron emission tomogram, we perform a mediastinoscopy (or other invasive diagnostics, for example, transbronchial needle aspiration). In case of positive nodes, we do not suggest pulmonary metastasectomy for patients with primary colorectal cancer or sarcoma. If we detect positive lymph nodes during sequential metastasectomy on one side, we postpone the contralateral operation and suggest systemic chemotherapy. In patients with primary renal cell cancer, we only postpone the operation when the surgical procedure is limited owing to functional or technical reasons.

We advocate for pulmonary metastasectomy a concurrent systemic mediastinal and hilar lymph node dissection for accurate staging of patients for clinical trials, potentially beneficial adjuvant treatment, frequency of follow-up studies, and determination of individual prognosis. The practice of sparing the patient a systemic mediastinal and hilar lymph node dissection if presurgical clinical assessment reveals no involvement of these lymph nodes may potentially nullify the chance for cure, if thoracic lymph node metastases indeed occurred and treatment strategies are evolved.

Finally, we may have demonstrated that systemic hilar and mediastinal lymph node dissection offers a further understanding of pulmonary metastases and remains a significant prognostic factor that may have an impact on future adjuvant treatment strategies. The paucity of data regarding systematic lymph node dissection in pulmonary metastasectomy makes further evaluation of this procedure necessary.

	Online Discussion Forum

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Each month, we select an article from the The Annals of Thoracic Surgery for discussion within the Surgeon's Forum of the CTSNet Discussion Forum Section. The articles chosen rotate among the six dilemma topics covered under the Surgeon's Forum, which include: General Thoracic Surgery, Adult Cardiac Surgery, Pediatric Cardiac Surgery, Cardiac Transplantation, Lung Transplantation, and Aortic and Vascular Surgery.

Once the article selected for discussion is published in the online version of The Annals, we will post a notice on the CTSNet home page ( http://www.ctsnet.org ) with a FREE LINK to the full-text article. Readers wishing to comment can post their own commentary in the discussion forum for that article, which will be informally moderated by The Annals Internet Editor. We encourage all surgeons to participate in this interesting exchange and to avail themselves of the other valuable features of the CTSNet Discussion Forum and Web site.

For February, the article chosen for discussion under the Pediatric Cardiac Dilemma Section of the Discussion forum is:

Hypothermic Low-Flow Cardiopulmonary Bypass Impairs Pulmonary and Right Ventricular Function More Than Circulatory Arrest

Jess M. Schultz, MD, Tara Karamlou, MD, Julia Swanson, BA, Irving Shen, MD, and Ross M. Ungerleider, MD

Tom R. Karl, MD

The Annals Internet Editor

UCSF Children's Hospital

Pediatric Cardiac Surgical Unit

505 Parnassus Ave, Room S-549

San Francisco,CA 94143-0118

Phone: (415) 476-3501

Fax: (212) 202-3622

e-mail: mailto:karlt{at}surgery.ucsf.edu

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Joachim Pfannschmidt Hendrik Dienemann Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Pfannschmidt, J. Articles by Hoffmann, H. Search for Related Content PubMed PubMed Citation Articles by Pfannschmidt, J. Articles by Hoffmann, H. Related Collections Lung - other