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Eur J Cardiothorac Surg 2007;31:167-172. doi:10.1016/j.ejcts.2006.11.004
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Prognostic impact of lymph node involvement in pulmonary metastases from colorectal cancer

Stefan Weltera,*, Jan Jacobsa, Thomas Krbeka, Christoph Poettgena,b, Georgios Stamatisa

a Department of Thoracic Surgery, Ruhrlandklinik Essen, Tüschener Weg 40, 45239 Essen, Germany
b Department of Radiology, University of Duisburg-Essen, Hufelandstraße 55, 45122 Essen, Germany

Received 28 July 2006; received in revised form 23 October 2006; accepted 6 November 2006.

* Corresponding author. Tel.: +49 201 4334012; fax: +49 201 1969. (Email: Stefan.We{at}t-online.de; Stefan.Welter{at}ruhrlandklinik.de).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Objective: The purpose of this study was to identify the prognostic impact of unexpected lymph node metastases in patients undergoing resection of pulmonary metastases from colorectal cancer and specify the influence of pulmonary and mediastinal nodal involvement according to the modified Narukes lymph node mapping [Mountain CF, Dresler CM. Regional lymph node classification for lung cancer. Chest 1997;111(6):1718–23.]. Methods: From January 1993 to December 2003, 175 patients were diagnosed and resected for pulmonary metastases of colorectal cancer. Follow up informations were collected for 169 patients and an analysis of prognostic factors was performed. Ninety-six men (56.8%) and 73 women (43.2%) with a median age of 62 (range 34–81) were identified, 28 (16.7%) patients were found to have lymph node metastases, five of them were identified during a recurrent procedure. Probability of survival was calculated according to the method of Kaplan–Meier. The prognostic influence of lymph node metastases on survival was analyzed with the log-rank test. Results: Median survival was 47.2 months after first metastasectomy. Ten patients with intrapulmonary nodal involvement had a median survival of 86 months whereas 12 patients with hilar and six patients with mediastinal lymph node metastases had a median survival of 24.5 and 34.7 months. The survival difference between pulmonary and hilar/mediastinal metastases was statistically significant (p = 0.008/p = 0.07). Five year survival with pulmonary, hilar, and mediastinal metastases was 78.5, 0, and 0%, respectively. Perioperative mortality was 0%. Conclusions: Resection of pulmonary metastases secondary to colorectal cancer is safe and indicated in highly selected patients. Because tumor involvement of lymph nodes has a strong impact on survival; depending on their location, at least a lymph node sampling should always be performed. Adjuvant chemotherapy in case of proven lymph node metastases might be a good option to improve prognosis.

Key Words: Metastasectomy • Lymph nodes • Survival analysis • Cancer


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Colon cancer is still one of the leading courses of cancer death in western countries. After initial diagnoses more than two-thirds of these patients undergo primary curative resection. Nonetheless more than half of the resected patients eventually die from the underlying disease [2]. Tumor recurrence is usually due to distant metastases [3]. Patients with untreated metastatic disease have a 5-year survival of less than 5% [4]. Fluorouracil-based chemotherapy is still the standard treatment in this situation. But despite stage IV disease, some highly selected patients with only few pulmonary metastases still have a curative option. Many published retrospective studies could show encouraging results of resections of isolated or few colorectal pulmonary metastases, yielding 5-year survival rates up to 60%. The results of 5206 cases assessed in the International Registry of Lung Metastases showed that lung metastasectomy in general is a safe and potentially curative procedure [5]. Depending on tumor size, number of metastases and performance status, surgical resection can be offered. Well-established prognostic factors are the number of metastases, the disease free interval, performance status and accompanying lymph node involvement [5–8]. Especially the treatment of suspected lymph node metastases is unclear.

In this retrospective study, we reviewed our experience with pulmonary metastases from colorectal cancer and focused on the prognostic impact of intrathoracic, unexpected lymph node metastases.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Conclusion
 References
 
From January 1993 to December 2003, 175 patients with colorectal lung metastases were surgically treated in our hospital. During the study, period 169 could be further examined and six were lost to follow up. Twenty-eight (16.6%) of them were found to have unexpected lymphatic spread. There were 96 men (56.8%) and 73 women (43.2%) with a median age of 62 (range 34–81). The initial tumor site was the colon in 73 (43.2%), the rectum in 96 (56.8%) and the initial tumor stage was stage I (19), II (37), III (68) and IV (37) according to UICC (1997) classification. Eight patients had no information about the initial TNM-stage. Two patients had their lung tumor removed and due to the histologic finding of adenocarcinoma of intestinal origin, bowel resection was done in a second step. The median disease free interval from colorectal resection to pulmonary metastasectomy was 31.4 months, ranging from 0 to 168 months (Table 1 ).


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  		Table 1. Patient characteristics
 
Thirty-seven patients (21.9%) had prior complete resection of liver metastases. All 169 patients had an open procedure that allowed palpation of the whole lung, no thoracoscopic procedure was performed.

All together 527 metastases had been removed with up to 18 metastases in one staged bilateral thoracotomy in one patient. At the time of first lung resection 81 patients had one single metastasis, 88 had multiple. The greatest diameter of the metastasis was 0.6 up to 10.0 cm according to the pathologist's measurement, 150 had a diameter of 5 cm or less, 19 had a diameter of more than 5 cm.

All palpable nodules were removed in a total of 266 unilateral and bilateral operations in 169 patients, 45 interventions were recurrent procedures in 31 patients (Table 2 ).


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  		Table 2. Treatment and pathologic results
 
Operative mortality included patients who died within 30 days after thoracotomy or during the same hospital stay and was 0%. The rate of major complications were 15.4% including relevant arrythmias, pneumonia, pulmonary embolism, prolonged ventilation, bronchopleural fistula, empyema and gastric ulcer bleeding. Lymph nodes were visually evaluated and sampled if suspicious. At least a regional lymphadenectomy was done always in the last cases. All resection of pulmonary metastases were finished even when intrathoracic lymph nodes appeared suspicious for metastatic involvement. Interlobar, hilar, or mediastinal lymph nodes were removed in 171 of 266 interventions and the pathologist described up to 14 lymph nodes in one patient. In 95 operations no lymph node had been removed, in 133 interventions 1 up to 5 nodes and in 43 resections between 6 and 14 lymph nodes had been removed. In 28 patients lymph nodes were positive, in 23 of them during first intervention, and in five during a recurrent thoracotomy (Table 3 ).


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  		Table 3. Patients with lymph node metastases (n = 28)
 
2.1 Definitions
Initial TNM stage was extracted from external medical reports. Preoperative selection criteria were as follows: completely resectable lesions in the lung, less than 10 seen on CT scan, no evidence of metastasis other than in the lung, resected primary colorectal tumor, no suspicion of mediastinal lymph node metastases, good performance score (WHO 0–2), sufficient lung function and no contraindication due to concomitant disease. Previous liver metastases had to be completely resected before pulmonary intervention was planned. If new nodules had evolved a minimum of 6 months after the last procedure, re-operation was defined as ‘recurrent’ operation. Resection was considered curative if all pulmonary nodules could be completely removed. Lymph nodes were classified according to the modified Narukes lymph node mapping [1].

2.2 Data collection
Preoperative, operative and pathological data were collected from review of medical records. The investigated variables were age, sex, type and extent of resection, diameter and number of metastatic lesions, tumor free interval, morbidity and mortality. Involved lymph nodes were classified pulmonary, hilar, or mediastinal. In case of multiple metastases in one patient only the largest diameter was counted. Tumor free interval was calculated from the date of the original resection to the date of first pulmonary metastasectomy. Staged operations on both lungs were counted as one resection and the number of metastases from each side were added together.

2.3 Follow-up
Follow-up information like date of death, tumor recurrence and location were gathered by written inquiries to the general practitioner, the oncologists or (if otherwise impossible) the registry offices respectively. Some patients were directly contacted by phone call. Six Patients were lost to follow up after discharge and were excluded from this study. Finally 169 cases could be completely worked up. All histologic reports of pulmonary metastases were reviewed and confirmed adenocarcinoma of intestinal origin.

2.4 Staging
The preoperative staging in our hospital consisted of abdominal ultrasound, CT-scan of the thorax and upper abdomen, fiberoptic bronchoscopy and clinical examination. Brain and bone scans were only done if there was clinical suspicion for metastases. Barium enema or colonoscopy to rule out local recurrence was accepted if not older than 6 months. Patients presenting with obvious mediastinal metastases had transtracheal needle biopsy or mediastinoscopy and were excluded from metastasectomy and this study. As far as possible, wedge resection or segmentectomy was the procedure of choice, if necessary even pneumonectomy was performed. Lymph nodes were sampled if suspicious.

2.5 Statistical analysis
The data were analyzed using the program SPSS 11.5 for Windows (SPSS Inc., Chicago, IL). Probability of survival was calculated according to the method of Kaplan–Meier [9] using the date of the first pulmonary resection and the date of last follow-up or death of the patient as start and end points. The prognostic influence of variables on survival was analyzed using the log-rank test [10]. Cox proportional hazards model [11] was used to perform a multivariate analysis of prognostic factors. Variables with a p-value of less than 0.15 were included into the stepwise regression model. A probability value of 0.05 or less was considered significant. Stepwise regressions of parameters due to highest p-value were achieved with the likelihood quotient method (LR-method).


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Conclusion
 References
 
All pulmonary resections were performed in the department of thoracic surgery, Ruhrlandklinik Essen. The initial abdominal resections were all done in external hospitals.

3.1 Survival
The actuarial overall survival was 47.2 (95%—CI 39.8; 54.5) months. Overall survival at 5 and 10 years was 39.1 and 20.0% (Fig. 1 ). At the end of the study 76 patients were alive, 93 had died, 88 of them with proven tumor recurrence. All together 123 (76.3%) from 161 patients faced tumor recurrence, eight cases are unknown and only 38 patients are free of tumor yet. No significant age related mortality was found.


Figure 1
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  		Fig. 1. Overall survival after first pulmonary metastasectomy.

 
Median survival time with or without lymph node metastases was 34.7 and 48.7 months, respectively (p = 0.02) and a corresponding 5-year survival rate of 19.2 and 42.0% (Fig. 2 ). No 5-year survivor was found in the group with hilar or mediastinal involvement (n = 18), whereas the 5- and 10-year survival for patients with intrapulmonary (n = 10) lymph node disease only was 78.5 and 13.4% (Fig. 3 ). Lymph node involvement was an independent prognostic factor with p = 0.025 in the univariate (log-rank test) and p = 0.038 in the multivariate (Cox regression) analysis (Table 4 ). Subjects with prior complete resection of liver metastases had a median survival of 47.2 month, which was almost equal to those without prior liver metastases (47.3 months). The number of metastases is a strong predictor of survival in our study as well. Patients with one metastasis and more than 10 metastases had a median survival of 58.6 and 24.0 months, respectively, which was a statistically significant difference (p = 0.002).


Figure 2
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  		Fig. 2. Survival with or without lymph node metastases.

 

Figure 3
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  		Fig. 3. Survival depending on the involved position of lymph nodes. Station 1 = pulmonary, station 2 = hilar, station 3 = mediastinal.

 

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  		Table 4. Univariate analysis (log-rank test)
 
Multivariate analysis of independent prognostic factors was done using the Cox regression method. Covariables without significant values were stepwise excluded. Beginning with age, sex, primary tumor stage, disease free interval, number of metastases, size of metastases, preoperative liver metastases, WHO performance score, complications, comorbidity, and lymph node involvement, nine iteration steps left three independent variables as statistically significant prognostic factors (Table 5 ).


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  		Table 5. Multivariate analysis of prognostic factors
 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Conclusion
 References
 
To date resection of pulmonary metastases from colorectal cancer becomes a more and more accepted method in the treatment of this cancer entity. This investigation was especially focused on the problem of lymph node involvement and was planned to add a single center experience to already existing data. The importance of lymph node metastases as prognostic factor was evaluated and will be further discussed. In our series we identified intrathoracic lymph node metastases, number of pulmonary metastases, and disease free interval as the only variables associated with a significant influence on survival. Others found CEA-level, and size of metastases as independent factors as well [6,12,13]. Survival was not influenced by sex or age in any investigation.

In our series, as well as in others [2,14,15] resected liver metastases were not associated with a decreased survival. The associated 5-year survival ranged from 11% [16], 28% in our series up to 56% [12], respectively.

The number of metastases is also a strong predictor of survival [7,8,12–14,16]. We found a median survival of 58 months in patients with one metastasis and 33 months in those with up to 10 metastases, which is still a good result. The results of 5206 cases of pulmonary metastasectomy including various histologies [5] showed a survival of 43% at 5 years for single metastases and 27% for more than four metastases at 5 years. A cut-off value for denying surgery in this patients is controversial.

The disease free interval is a prognostic factor of low importance in our study. But there is little doubt in other series that synchronous metastases have a minor prognosis than metachronously evolving tumor spread [5,14]. The international registry showed the best prognostic group being those with a single resectable metastasis and a DFI of more than 3 years with no other risk factor. Assuming that all other covariables are constant, a patient with a DFI of 1 month less (n – 1) has a 0.6% (1/0.994) increased hazard (risk of death), the patient with one more metastasis (n + 1) has a 11.3% (1.129-fold) increased risk to die and the patient with lymph node involvement has a 83% (1.829-fold) increased risk to die compared to those without lymph node involvement.

We could show that intrathoracic lymph node metastases are a strong predictor of reduced probability of survival. Furthermore, there is an important difference between intrapulmonary and extrapulmonary lymph node metastases. No 5-years survivor was found in the group with hilar or mediastinal metastases. Taking these facts into account, patients with obvious mediastinal metastases seem to be unsuitable for extensive surgery.

Few articles are written about the need of lymphadenectomy accompanying metastasectomy [7,17]. Performing systematic lymph node dissection Loehe found unexpected metastases in nine patients (14.3%) resulting in a worse survival, which was not significant. We found, as did Okumura et al. [7], a significant prognostic difference in patients with or without lymph node involvement, having performed a sampling only in case of suspicious enlarged nodes. It has to be noted that we do not know how many lymph node metastases we have missed with this strategy. Saito et al. [15] emphasized the need for a prospective study to investigate whether lymph node dissection improves the survival with pulmonary metastases from colorectal carcinoma. As we know from lung cancer, lymph node dissection improves the correct staging of multilevel N2 disease and improves the overall survival in some subgroupes [18]. Okumura et al. [7] reported that systematic dissection of involved mediastinal nodes is not helpful in controlling the systemic disease. This is emphasized by the fact that we found an intrathoracic tumor recurrence alone in 23% of all tumor recurrences only. The recurrence rate was 76.3%, which correlates exactly with other reports [13] and indicates, that colorectal lung metastases are predecessors of further systemic spread. So we think it is more important to offer adjuvant chemotherapy after metastasectomy in case of nodal involvement, than talk about radical or systematic lymph node dissection in a stage IV disease, knowing about the risk for recurrence in extra pulmonary organs.

From the beginning our policy was to perform open procedures allowing the palpation of the whole lung. It was described by other authors [5,17,19] that up to 30% of metastases are missed on CT scan so that palpation is mandatory. McCormack et al. [20] found a success rate of 22% only, in detecting all metastases with video assisted thoracoscopic surgery.

Operative mortality is low regardless of age, 0% in our series and up to 3% in others [13] so that age should not be a selection criterion. The actuarial overall 5-year survival with 39% in our series was well comparable to other series [6,7] but varies up to 56% [12].

Repeated thoracotomy of recurrent pulmonary metastases is a well established procedure with satisfactory survival [13,15,21]. We had 31 patients with a recurrent procedure and found a 46% 5-year survival, which is almost equal to the outcome after the first metastasectomy. On this basis, we did not see any need to exclude the five cases with lymph node metastases diagnosed in a recurrent procedure from the survival analysis.

Finally, alternative treatment options, mainly chemotherapy have to be discussed. A comparison is very difficult because no trial is available that differentiates resectable from irresectable lung involvement prior to chemotherapy. Furthermore the rate of ‘complete response’ which is comparable to a radical metastasectomy is almost zero in most series [22,23], and all series contain different sites of metastases, not only restricted to the lung. Even the best prognostic groups (one tumor site, good performance status) had a median survival of 15 months only [22]. Some recent phase III studies investigated the addition of oxaliplatin [24,25] to standard leucovorine and 5-fluorouracil regimen and could show a change in overall survival from 14.7 to 16.2 months and 19.9–19.4, respectively which was not significant. In addition, we have to point out that our results can be biased by many factors mainly initial TNM stage and adjuvant or palliative chemotherapy. Comparing our results with up mentioned studies about chemotherapy [24,25] seems nevertheless possible, because they included patients with second or third-line chemotherapy as well and which were not selected by initial tumor stage.


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
References
 
Pulmonary metastasectomy in selected patients is a safe and successful treatment. The intraoperative finding of intrathoracic lymph node metastases correlates significantly with a poorer prognosis but the median survival of 34.7 months after surgery in selected cases appear to be encouraging compared to the published results of chemotherapy alone. Though this statement is limited by the small number of cases and the retrospective study design. In our opinion, lymph node sampling during pulmonary metastasectomy is required and sufficient. Adjuvant chemotherapy should be discussed after complete metastasectomy in case of lymph node involvement. We could not find one 5-year survivor when unexpected mediastinal lymph node metastases were found at the resection. So patients with obvious and proven mediastinal metastases are no good candidates for resection.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 

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