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10.1245/s10434-006-9100-2
Annals of Surgical Oncology 13:1538-1544 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Surgical Management of Pulmonary Metastases from Colorectal Cancer in 153 Patients

Süleyman Yedibela, MD1, Peter Klein, MD1, Karsta Feuchter, MD1, Martin Hoffmann, MD1, Thomas Meyer, MD1, Thomas Papadopoulos, MD2, Jonas Göhl, MD1 and Werner Hohenberger, MD1

1 Department of General Surgery, University of Erlangen-Nuremberg, Krankenhausstrasse 12, D-91054 Erlangen, Germany
2 Institute of Pathology, University of Erlangen-Nuremberg, Krankenhausstrasse 8-10, 91054 Erlangen, Germany

Correspondence: Address correspondence and reprint requests to: Süleyman Yedibela, MD; E-mail: suleyman.yedibela{at}chir.imed.uni-erlan-gen.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Surgery has become a recognized therapeutic means in selected patients with pulmonary metastases from colorectal origin. We reviewed our experience in the surgical treatment of 153 patients with pulmonary colorectal metastases and investigated factors affecting survival.

Methods: A retrospective analysis of the records of all patients (n = 153) with pulmonary metastases from colorectal cancer who underwent thoracotomy between 1978 and 2003 at a single surgical center was performed.

Results: One hundred fifty-three patients with pulmonary metastases from colon (n = 61) or rectal (n = 92) cancer underwent 180 thoracotomies. The 2- and 5-year probabilities of survival after the first thoracotomy were 64% and 37%, respectively. Sex, age, site, International Union Against Cancer stage of the primary tumor, prethoracotomy carcinoembryonic antigen level, size of metastases, and previous resection of hepatic metastases were not found to be statistically significant prognostic factors. Number of metastases (solitary vs. multiple), mode of operation (wedge vs. anatomical resection), disease-free interval (DFI; >36 months), negative hilar or mediastinal lymph node status, resection margin >10 mm, and administration of intraoperative blood substitution were predictors of a longer survival duration by univariate analysis, but only number of metastases (P = .019), mode of operation (P = .004), DFI (P = .027), and intraoperative blood substitution (P = .002) were identified as independent prognostic factors by multivariate analysis.

Conclusions: Pulmonary resection for metastases from colorectal cancer is safe and results in long-term survival in selected patients. Single metastases, anatomical resection, intraoperative blood substitution, and DFI >36 months seem to be the most reliable predictors of survival.

Key Words: Pulmonary metastases • Colorectal cancer • Surgical resection • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal carcinoma (CRC) is one of the most frequent malignant tumors in Western countries. Several prognostic determinants influence local and distant recurrence after surgical therapy. After a curative resection of colon carcinoma, a recurrence rate of 21% was observed in patients treated in our institution. In 18% of them, there were distant metastases; in 11%, they were isolated in the liver.1 Nevertheless, 10% of patients with CRC will develop lung metastases. Treatment options include chemotherapy and surgery. Only 2% to 4% of these metastases are isolated in the lung, and only half of these patients will be candidates for resection.2–5 Surgical therapy has been attempted for metastatic lung tumors since Thomford et al.6 published the principles for resection of metastatic lung tumors in 1965. Several prognostic factors have been reported; indeed, they are discussed in part controversially. Although resection of solitary lung metastases has been widely accepted, pulmonary resection for multiple or bilateral metastases is still under discussion. This mono-centric retrospective study analyzed data after surgical treatment of pulmonary metastases from CRC.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This study was based on data from the Erlangen Registry of Colorectal Carcinoma with prospective collection of data since 1964. The medical records of all patients between 1978 and 2003 who underwent a pulmonary resection for pulmonary metastases from CRC at the Surgical Department of the University of Erlangen were reviewed. The indication for surgery was based on a routine follow-up after resection of the primary tumor. All patients were evaluated for local recurrence and distant metastases by a chest and abdominal computed tomographic scan. Furthermore, bronchoscopy, pulmonary function tests, and endoscopic evaluations were performed, and carcinoembryonic antigen (CEA) levels were assessed before operation.

One hundred eighty resections were performed in 153 patients during this period. Forty-three (28%) patients had previously undergone resection of hepatic metastases. Eight (5%) patients in whom a thoracotomy was previously performed in another institution were excluded from the following analysis, as were patients with residual tumor in histological examinations (R1; n = 4). Thus, the analysis of this study was based on 141 patients with curative resection of pulmonary metastases (R0).

There were 84 (59%) men and 57 (41%) women, with a median age of 59 years (range, 32–82 years) at the time of the first pulmonary resection. The primary tumor was located in the rectum in 85 (60%) cases, whereas colonic cancer in the history was diagnosed in 56 (40%) patients. Lymph node involvement (pN1/2) resulting from the primary tumor was three times more frequent in patients with rectal carcinoma (Table 1Go).


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  		TABLE 1. UICC stage and pTNM classification of the primary tumor regarding location
 
The surgical approach was chosen according to the location and number of pulmonary nodules. In six patients, a video-assisted thoracoscopic resection was performed. In all, pulmonary metastases were removed by wedge resection (n = 61), segmental resection (n = 26), lobectomy (n = 44), bilobectomy (n = 7), and pneumectomy (n = 3) (Table 2Go). For univariate and multivariate analysis, all patients except these who underwent wedge resection were subsummarized as undergoing anatomical resection. Seven (5%) patients received neoadjuvant chemotherapy. Adjuvant chemotherapy was applied in nine (6%) patients. Twenty-three patients (15%) received a second thoracotomy for pulmonary metastases a median time of 15 months (mean, 21 months; range, 2–96 months) after the first metastasectomy. Three patients underwent a third and one patient a fourth thoracotomy. The mean follow-up was 59 months (range, 0–300 months; median, 35 months). At the end of the follow-up, 42 (29%) patients were alive.


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  		TABLE 2. Charateristic of 141 patients who underwent curative pulmonary resection of colorectal metastases
 
Seventy (46%) patients did not undergo resection for their primary tumor in our department. All patients with unknown pathologic tumor-node-metastasis classifications had previously undergone operation in another hospital for their primary tumors (Table 1Go). The median disease-free interval (DFI) for metachronous pulmonary metastases after resection of the primary tumor was 29 months (range, 2–114 months). Nine (6%) patients had synchronous lung metastases at the time of resection of the primary tumor. None of them underwent a pulmonary resection simultaneously. In all, 40 patients developed lung lesions within 12 months of treatment of the primary tumor. From the remaining 101 patients, 72 developed pulmonary metastases between 12 and 36 months, and 29 did so beyond 36 months after resection of the colorectal primary tumor.

Patients were evaluated for age, sex, primary tumor site, prethoracotomy CEA level, extent of resection, number and size of metastatic lesions, involvement of hilar lymph nodes, tumor-free interval, morbidity, mortality, and long-term survival. The cutoff value for CEA was set at 5 ng/mL. A curative resection (R0) was defined as a histologically con-firmed removal of all tumor lesions. An infiltration of the resection margin with tumor cells in the histological examination was defined as an R1 resection. All cases in which a lymph node dissection was not performed because of clinically (macroscopic and preoperative imaging) undetectable lymph node involvement (metastases) were classified as cN0.

All statistical analyses were calculated by using SPSS for Windows (version 11.5; SPSS Inc., Chicago, IL). The patients were followed up to January 1, 2003, or to the time of their death of any cause. Postoperative death was not excluded from the survival analysis. Observed survival rates were estimated according to the Kaplan-Meier method.7 Ninety-five percent confidence intervals were calculated by using the Greenwood method. Statistical differences were tested for significance with the log-rank test.8 Statistical significance was set at P < .05. For multivariate analysis of prognostic factors, the Cox regression model9 was used.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
One patient (.7%) died after rethoracotomy from a pulmonary embolism with no tumor remnant at autopsy. Postoperative complications occurred in 17 (12%) patients: pleural effusion (n = 6), respiratory insufficiency (n = 2), wound abscess (n = 4), wound necrosis (n = 1), myocardial infarction (n = 1), transient ischemic attack (n = 1), and pneumonia (n = 2). Four patients required reoperation. There were no patients with macroscopically residual tumor (R2) in our series. Extended pulmonary resection was performed in 14 patients (10%): pleura (n = 6), diaphragm (n = 5), chest wall (n = 2), and pericardia (n = 1). The median operating time was 120 minutes (range, 20–375 minutes). Intraoperative blood loss was <200 mL in 71 (49%), between 250 and 1000 mL in 26 (18%), and >1100 mL in 10 (7%) patients (unknown in 36 patients). An intraoperative substitution of packed red blood cells was not necessary in 99 (68%) patients.

The maximum number of lung metastases was eight. One hundred one patients (71%) had solitary metastases, whereas in 40 patients multiple metastases were detected. The median size of the metastases was 18.5 mm (range, 3–130 mm).

The overall 2- and 5- year survival rates for all patients (n = 153) were 64% and 37%, with a median survival time of 39 months. After a curative resection (R0), 2- and 5-year survival was 68% and 39%; the median survival time was 43 months. In univariate analysis, survival was not influenced by age, sex, tumor location, or International Union Against Cancer stage of the primary tumor (Table 3Go). Likewise, 5-year survival for tumors with a diameter <20 mm (n = 82) did not differ significantly from that for tumors >20 mm (n = 59; 34 % vs. 38%).


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  		TABLE 3. Survival and univariate analysis of prognostic factors of 141 patients who underwent curative metastasectomy
 
A history of hepatic metastases was not an unfavorable prognostic factor. The 38% 5-year survival observed for the 43 patients with hepatic metastases resected before thoracotomy did not differ significantly from the 42% survival observed in the remaining patients without hepatic metastases. No significant difference in long-term survival was found in patients with a histology of adenocarcinoma compared with patients with mucinous differentiation of the pulmonary metastases (P = .934).

The number of pulmonary metastases significantly influenced survival (Table 3Go; Fig. 1Go). The cumulative survival for patients with solitary metastases was 44% at 5 years, whereas that for 40 patients with multiple pulmonary metastases was 24% (median survival, 47 vs. 36 months; P = .048).


Figure 1
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  		FIG. 1. Observed survival depending on disease-free interval.

 
Wedge resection was performed to preserve respiratory function, especially in patients with multiple metastases and in patients compromised because of right heart failure (n = 9) and pulmonary hypertension (n = 5). Mode of operation was a significant prognostic factor in this series (P = .001). The best results were achieved after anatomical resections (Table 3Go).

DFI significantly correlated with survival (P = .004). For analysis, patients were divided into three groups according to DFI (Table 3Go). Figure 2Go shows a significant advantage of patients who developed pulmonary metastases beyond 3 years after treatment of their primary tumor.


Figure 2
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  		FIG. 2. Observed survival regarding the number of pulmonary metastases.

 
Prethoracotomy CEA levels were documented in the records of 105 patients. Univariate analysis showed no difference in survival for patients with CEA levels less than or more than 5 ng/mL (P = .572).

The resection margin was <10 mm in 63 patients. In 78 patients, a histological resection margin of >10 mm was measured. Univariate analysis showed a significantly poorer survival in patients with a resection margin <10 mm (P = .038; Table 3Go).

The intraoperative administration of packed red blood cells was necessary in 32 patients. This was a significant prognostic factor in univariate and multivariate analysis, with a 5-year survival rate of 21%. In contrast, 44% of the patients without intraoperative administration of packed red blood cells were alive after 5 years (P = .002; Table 4Go).


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  		TABLE 4. Multivariate analysis of prognostic factors according to the Cox proportional hazards regression model
 
Hilar and mediastinal lymph node metastases were found in 7 patients (pN1/2), whereas 75 patients had no histological evidence of lymph node metastases (pN0). Because of a clinical lack of evidence of lymph node involvement (cN0), lymph node dissection was not performed in 59 patients. Nodal status significantly influenced survival (Table 3Go).

In this series, univariate analysis identified six favorable prognostic factors (shown in Table 3Go): mode of operation, number of pulmonary metastasis, DFI, status of hilar or mediastinal lymph nodes, resection margin, and intraoperative blood transfusion. In multivariate analysis, mode of operation, number of pulmonary metastases, DFI, and intra-operative blood substitution were independent prognostic factors (Table 4Go).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The prognosis of patients with CRC is determined by either local or distant recurrence after resection of the primary tumor. As we have shown recently, rectal carcinoma preoperative chemoradiotherapy significantly reduces local relapse compared with postoperative chemoradiotherapy.10 However, distant recurrence remains unaffected by this procedure. Nevertheless, the development of isolated pulmonary metastases after curative resection of CRC is rare. The objective of this study was to evaluate prognostic factors for patients who underwent pulmonary metastasectomy after curative resection for CRC.

The data so far available suggest that lung metastasectomy is able to significantly improve the overall and disease-free survival with acceptable morbidity and mortality. The overall 5-year survival ranges between 24% and 62%.3,11–17 In this study, the overall survival for 180 thoracotomies in 153 patients was 37% after 5 years. After curative resection (R0), the 5-year survival rate was 39%, with a median survival time of 43 months.

Various prognostic indicators for patients who undergo thoracotomy for lung metastases from CRC have been suggested in previous articles. As indicated by others, neither age nor sex nor the location of the primary carcinoma (colon or rectum) influenced prognosis.5,12,17,18 We also reported previously that the site of origin of CRC, i.e., colon versus upper rectum, did not influence the incidence of lung metastasis or the outcome after metastasectomy.19 Okumura et al.11 and Inoue et al.16 reported a significantly better survival of patients with Dukes’ stage A in comparison with Dukes’ B or C CRC. Vogelsang et al.20 recently identified International Union Against Cancer stage as a variable that significantly affected prognosis after resection of pulmonary metastases in univariate analysis. In our study, neither the location of the primary tumor nor the International Union Against Cancer stage influenced survival significantly (Table 3Go).

In the literature, one of the most common prognostic factors is the number of pulmonary metastases. In three of the largest monocentric studies and in one multicenter study, a significantly longer survival was observed for patients with single metastases.11,12,17,21 In accordance with these results, but in contrast to others,3,16,18 we also found a significantly better survival of patients with solitary metastases (Tables 3Go and 4Go).

A significantly longer survival was reported for patients with a normal prethoracotomy CEA level in most of the large series.12,16–18,21,22 Surprisingly, prethoracotomy CEA was not an independent prognostic factor in our analysis. The 5-year survival rate for patients with increased prethoracotomy CEA (>5 ng/mL) was 27% and was only marginally poorer than for those with normal prethoracotomy CEA levels (33%; Table 3Go). Therefore, the indication for thoracotomy in pulmonary metastases is not based on preoperative CEA levels in our institution.

Regarding DFI, we subdivided our patient cohort into three groups by following the methods described by the International Registry of Lung Metastases.23 In univariate as well as in multivariate analysis, patients with a DFI >36 months had a significantly better prognosis. Considering the results of studies with large patient numbers (≥100 patients), in none of them was DFI a prognostic factor. Rena et al.23 and Zink et al.21 recently reported on 80 and 96 patients with significantly improved survival with a DFI >36 months.

Although in nearly all large series wedge resection is considered as the procedure of choice, whereas lobectomy should be avoided whenever possible, our data indicate that an anatomical resection is accompanied by a significant better prognosis. In our institution, we advocate wedge resection in peripheral lesions or in patients with compromised pulmonary function. Wedge resection should not be forced in centrally located lesions with uncertain resection margins. In these cases, we prefer an anatomical resection together with a dissection of suspicious lymph nodes, if necessary.

Although in many reports the significance of lymph node dissection is underlined,12,18,19,22 we could not observe a difference in patients with and without positive lymph nodes in multivariate analysis. In our opinion, the value of lymph node dissection remains unclear, so we do not routinely perform regional lymphadenectomy.

Resection margins were not analyzed in relation to pulmonary metastasectomy. In accordance with our results for resection of colorectal liver metastases,25 we separately analyzed patients with a resection margin of less than and more than 10 mm. In univariate analysis we observed a significantly longer survival for patients with resection margins >10 mm, but in multivariate analysis this difference did not reach statistical significance. This may partly explain the better prognosis for anatomically resected metastases.

Our data indicate that patients with packed red blood cells administered during surgery had a significantly shorter survival if the cutoff value of two units packed red blood cells was exceeded. No published study had analyzed this variable previously.

In summary, the long-term follow-up data after curative resection for pulmonary CRC metastases indicate satisfying survival rates and, therefore, support an aggressive surgical approach for this particular metastatic disease. In view of the low perioperative morbidity and mortality and the lack of appropriate treatment alternatives, we therefore recommend that metastasectomy should be performed whenever the metastatic lesions can be resected completely.

Received for publication February 4, 2006. Accepted for publication May 19, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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