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Interact CardioVasc Thorac Surg 2009;9:640-644. doi:10.1510/icvts.2009.202598 © 2009 European Association of Cardio-Thoracic Surgery
Pulmonary resection for metastases from colorectal carcinoma
a Division of Thoracic Surgery, Matsue Red Cross Hospital, 200 Horomachi, Matsue, Shimane 690-8506, Japan Received 12 January 2009; received in revised form 29 June 2009; accepted 7 July 2009
*Corresponding author. Tel.: +81-852-24-2111; fax: +81-852-31-9783.
A pulmonary resection of metastatic colorectal carcinoma is an accepted method of treatment. The purpose of this study was to confirm the role of resections for pulmonary metastases from colorectal carcinoma, and to determine the clinical course, outcome, and prognostic factors after surgery. A retrospective analysis was conducted of the records of all patients with pulmonary metastases from colorectal carcinoma who underwent a surgical resection between 1995 and 2008, at a single surgical center. The overall 5-year survival rate was 74%. Multivariate Cox analysis demonstrated that the number of pulmonary metastases (HR: 9.40, 95% confidence interval (CI): 1.08–82.2, P=0.0428) and prethoracotomy carcinoembryonic antigen (CEA) level (HR: 9.79, 95% CI: 1.11–86.8, P=0.0404) were statistically significant predictors of survival after the first pulmonary metastasectomy. In addition, a second resection for recurrent metastases was performed in eight patients, and a third resection was done in one patient. There were no major postoperative complications among the patients who underwent second or third resections. Pulmonary resections are considered to be a safe and effective treatment in selective patients.
Key Words: Colorectal carcinoma; Lung metastases; Surgical resection
The lung is one of the most frequently affected metastatic sites in patients with colorectal carcinoma. Many reports suggest a role for a pulmonary metastasectomy in managing metastatic colorectal carcinoma [1–9], but inconsistencies among reports has led to confusion. The experience at one institution was reviewed to clarify the role of pulmonary metastasectomy.
From 1995 to 2008, 30 patients underwent 39 curative resections of pulmonary metastases from colorectal carcinoma. All 30 patients received curative pulmonary resections, and all resected specimens pathologically demonstrated tumor-free margins. The selection criteria for a pulmonary resection were: cardio–respiratory fitness for lung resection; no local recurrence of primary colorectal carcinoma; no extra-pulmonary metastases with the exception of associated prior or simultaneous resectable liver metastases; and the feasibility of a radical lung metastasectomy. Preoperative evaluation was performed using chest roentgenogram and chest computed tomographic (CT) for pulmonary nodules. All patients were retrospectively analyzed for gender, age, primary site, prethoracotomy carcinoembryonic antigen (CEA) level, a prior resection of liver metastases, the number and largest diameter of pulmonary metastases, tumor laterality (bilateral or hemilateral), the disease-free interval (DFI) between the colorectal resection and the first pulmonary resection, the surgical method, Dukes' stage of the primary tumor, histological differentiation of the primary tumor, and the administration of postoperative chemotherapy after the pulmonary resection. The end point was overall survival and disease-free survival after the first pulmonary metastasectomy. Disease-free survival was defined as the duration from the resection of the primary tumor to the initial diagnosis of the metastatic pulmonary tumor. For univariate analyses, all cumulative survival were estimated using the Kaplan–Meier method, and differences in variables were determined by the log–rank test. Multivariate analyses were performed using Cox's proportional hazards regression model. Forward and backward stepwise procedures were used to determine independent predictors. All P-values reported were two-sided, and the significance level was set at <0.05. The analyses were performed with the SPSS 11.0 statistical software program (Dr. SPSS II for Windows, standard version 11.0, SPSS Inc, Chicago, IL) and GraphPad Prism statistical software program (Prism for Windows, Version 5.02, GraphPad Software, Inc, La Jolla, CA) [3].
3.1. Patient characteristics (Table 1) The cohort consisted of 17 males and 13 females. The age ranged from 45 to 87 years with a median of 70 years. The maximum tumor size ranged from 0.7 cm to 6.5 cm with a median 2 cm. Because of a clinical lack of evidence of lymph node involvement, no lymph node dissection was performed in 23 patients. No pulmonary or mediastinal lymph node metastases were found in the remaining 7 patients who underwent lymph node dissection.
The DFI ranged from 0 to 133 months, and the median DFI was 20 months. The surgical procedures were: 23 wedge resections; 3 lobectomies (of which 1 was a sleeve lobectomy); 4 segmentectomies. Of the 23 wedge resections, 17 were performed by video-assisted thoracic surgery (VATS). There were no relevant intra-operative complications. The peri-operative mortality was 0%. There were two postoperative morbidities (pneumonia, drug induced hepatocellular injury). The median follow-up was 26 months (range, 3–157 months). A summary of the patient characteristics is outlined in Table 1. 3.2. Overall and disease-free survival and prognostic factor (Table 2) The overall 5-year survival was 73.9%, and the median survival was 19 months (Fig. 1). The disease-free survival rate at five years after pulmonary resection was 46.1%. Fifteen patients are currently alive without evidence of disease, and five patients are alive with disease. Six patients died of disease, and four patients with disease were lost to follow-up.
The 5-year survival for the 12 patients with normal prethoracotomy CEA levels was 91.7%, and that for the 18 patients with elevated prethoracotomy CEA levels were 42.6% (Fig. 2). Patients with normal CEA levels had a better prognosis than those with elevated CEA levels (P=0.00430).
Twenty-one patients had a solitary lesion, whereas nine had multiple lesions. The 5-year survival rate was 91.7% for those with solitary metastasis, and 41.7% for those with multiple metastases. The prognosis of patients with a solitary metastasis was considerably better than with two or more (P=0.00330). The 5-year survival rate in patients who received postoperative chemotherapy was 83.5%, but there was no significant difference (P=0.397). In addition, there was no difference of prognosis based on age, gender, size of tumor, DFI, tumor laterality and histological differentiation of primary colorectal carcinoma. Two prognostic factors for the overall survival after pulmonary resection were determined to be significant by a univariate analysis: the CEA (P=0.00430) and number of pulmonary metastases (P=0.00330). A multivariate analysis was conducted using all of the variables tested by the univariate analysis. The results showed that the CEA level (HR: 9.79, 95% confidence interval (CI): 1.11–86.8, P=0.0404) and number of pulmonary metastases (HR: 9.40, 95% CI: 1.08–82.2, P=0.0428) were independent prognostic predictors (Table 2). A second resection for recurrent metastases was done in eight patients, and a third resection was done in one patient. There were no major postoperative complications. The interval between the first thoracotomy and second thoracotomy ranged from 2 to 39 months, and the median interval was 12 months. The interval between second thoracotomy and third thoracotomy was 8 months.One patient died of disease 13 months after the second thoracotomy. The median survival of the remaining six patients who underwent a second thoracotomy was 10 months (range, 3–35 months) after the second resection, and one patient is still alive 30 months after the third resection.
Colorectal carcinoma is one of the most frequent causes of death. It ranks second after lung cancer in men and after breast cancer in women, with an increasing incidence in the past 20 years [8]. The lung is one of the most frequently affected metastatic sites in patients with colorectal carcinoma and after a resection of the primary carcinoma, 10% of the patients develop lung metastases [10]. Many reports suggest the role for a pulmonary metastasectomy in managing metastatic colorectal carcinoma [1–9]. Non-resected patients with pulmonary metastases from colorectal carcinoma have a markedly poorer median survival, of about 10 months [11]. Therefore, a pulmonary resection in metastatic colorectal carcinoma is an accepted method of treatment. The objective of this study was to confirm the role of resections of pulmonary metastases for colorectal carcinoma. Several studies concerning surgery for pulmonary metastases from colorectal carcinoma have been published, and the 5-year survival rates recently reported ranged from 27% to 57% [1–9]. In the current study, the 5-year overall and disease-free survival rates were 73.9% and 46.1%, respectively. Although the number of patients was limited in this single institutional experience, the study suggested that the current therapy for the pulmonary metastases from colorectal carcinoma might be justified. Various prognostic indicators have been suggested in previous articles. As indicated by others, neither age nor sex nor the location of the primary carcinoma (colon or rectum) nor the tumor size influenced prognosis [2, 4, 6]. This is consistent with the current study. In the literature, one of the most common prognostic factors is the number of pulmonary metastases. Many authors reported a significantly longer survival was observed for patients with single metastasis [2–9]. The current study also found a significantly, better survival of patients with solitary metastasis. CT imaging has recently been improved and is able to detect a tiny nodule allowing for preoperative knowledge of the exact number of pulmonary metastases. Therefore, an accurate preoperative evaluation of the nodule number, which may affect the prognosis, is therefore considered to be important. A significantly longer survival is reported for patients with a normal prethoracotomy CEA level in most of the large series [3–9]. In the current study, the prethoracotomy CEA was also an independent prognostic factor. CEA itself participates in intracellular recognition and attachment and may promote adhesion of tumor cells to each other or to host cells. Therefore, the prethoracotomy CEA level is taken into account when selecting patients for a pulmonary resection. No statistically significant correlation was found between the DFI and the postthoracotomy survival in this study. These findings are consistent with those of most other studies [2–6, 8, 9]; however, they did not correlate with the results of Yedibela et al. and Rena et al. [2, 7]. Iizasa et al. [3] reported that patients with lymph node metastases in the hilum or mediastinum have poor prognoses. Although many reports emphasize the significance of a lymph node dissection, the value of lymph node dissection thus remains unclear. To predict prognosis, lymph node dissection is important, but no surgeon believes that systematic lymph node dissection as part of surgery for metastatic lung tumors improves prognosis. In the current study, wedge resection is performed for a small peripheral metastasis without the inclusion of lymph node dissection and a regional lymphadenectomy is not routinely performed. Although there was no significant difference in disease-free survival between the patients who underwent lymph node dissection and those who did not undergo it, the current study was inadequate for the analysis of lymph node status. Sakamoto et al. [9] reported that no considerable differences in survival rate were found among patient groups for solitary, ipsilateral multiple, and bilateral multiple metastases. Iizasa et al. [3] reported that a multivariate analysis revealed that tumor location and not metastatic number was the most powerful and independent prognostic factor and patients with bilateral metastases will gain no surgical benefit. This point requires further confirmation in a large cohort. The optimal surgical access for a pulmonary metastasectomy remains under discussion. In the 1970s and 1980s the use of a thoracotomy prevailed and, rarely, a sternotomic approach was preferred, whereas in the last 10 years, the improvement of thoracoscopic techniques brought about the predominant use of the mini-invasive videothoracoscopy approach, without loss of surgical radicality. In a study by Landreneau et al. [12], a therapeutic VATS resection was efficacious in improving survival in 80 cases of pulmonary metastases from colorectal carcinoma. In the current study, disease-free survival of pulmonary metastasectomy through thoracoscopy was not significantly different from that of pulmonary metastasectomy through conventional open thoracotomy. The VATS approach, which was technically feasible in 17/30 (63.3%) of all the patients who underwent first lung metastasectomy, was satisfactory and effective. It is generally considered to reduce the length of hospitalization while also being correlated with a low postoperative morbidity [12].
If liver metastases are present (both synchronous and metachronous), but these are suitable for resection or can be treated by another effective method such as radiofrequency ablation or cryotherapy, a lung metastasectomy is still indicated [13, 14]. A combined resection of colorectal carcinoma metastases of the lung and liver has been performed with success, and has been shown to yield an Recently, the validity of various new chemotherapeutic agents for metastatic colorectal carcinoma was reported [15]. In the current study, 23/30 (68.9%) patients received postoperative chemotherapy, and 5-year survival for those who received postoperative chemotherapy was 83.5%. This limited experience suggests that combined pulmonary resection and postoperative chemotherapy might be considered for the patients who undergo a pulmonary resection of colorectal carcinoma. These data also suggested that aggressive treatment, including repeated resections, might thus be considered for such recurrent patients, since there were no major postoperative complications and patients with a recurrence after a pulmonary metastasectomy showed long-term survival.
The low mortality rate and, at present, the lack of an established effective systemic chemotherapy are thus considered to justify an aggressive approach to a surgical resection. Good surgical candidates for pulmonary resection are those showing a prethoracotomy normal CEA level and solitary metastasis. Repeated resections for recurrent lung metastases are therefore considered to be an effective and safe treatment based on our above described.
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Abstract
1. Introduction
30% 5-year survival 
