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10.1245/s10434-006-9101-1
Annals of Surgical Oncology 13:1529-1537 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Percutaneous Radiofrequency Ablation of Pulmonary Metastases from Colorectal Carcinoma: Prognostic Determinants for Survival

Tristan D. Yan, BSc (Med), MBBS1, Julie King, MPH1, Adrian Sjarif, MBBS1, Derek Glenn, FRACR2, Karin Steinke, MD1,2 and David L. Morris, MD, PhD1

1 Department of Surgery, University of New South Wales, St. George Hospital, Sydney, New South Wales 2217, Australia
2 Department of Radiology, University of New South Wales, St. George Hospital, Sydney, New South Wales 2217, Australia

Correspondence: Address correspondence and reprint requests to: Tristan D. Yan, BSc (Med), MBBS; E-mail: Tristan.Yan{at}unsw.edu.au


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Preliminary results have shown that percutaneous radiofrequency ablation (RFA) may play a useful role in patients with inoperable lung tumors. This series evaluated the prognostic features for survival in nonsurgical candidates who underwent percutaneous RFA of pulmonary metastases from colorectal carcinoma.

Methods: Fifty-five patients not suitable for surgery underwent percutaneous RFA for colorectal pulmonary metastases. All clinical and treatment-related data were collected prospectively. The primary end point of the study was overall survival, defined from the time of RFA intervention. Univariate and multivariate analyses were performed to identify statistically significant prognostic parameters for overall survival.

Results: The overall median survival was 33 months (range, 4–40 months), with actuarial 1-, 2-, and 3-year survival of 85%, 64%, and 46%, respectively. Univariate analysis demonstrated that largest size of lung metastasis (P < .001), location of lung metastases (P = .032), and repeat percutaneous RFA for pulmonary recurrence (P = .024) were statistically significant for overall survival. Multivariate analysis demonstrated that largest size of lung metastasis >3 cm was independently associated with a reduced overall survival (P = .003).

Conclusions: Percutaneous lung RFA may play a useful role in nonsurgical candidates with colorectal pulmonary metastases. However, the survival benefit of this interventional procedure for patients with a pulmonary metastasis >3 cm was limited.

Key Words: Radiofrequency ablation • Pulmonary metastases • Colorectal carcinoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The lung is a frequent site of colorectal metastases. Pulmonary resection can achieve 5-year survival rates of 20% to 40%, but is only indicated in a relatively small percentage of carefully selected patients.1–12 Resectability depends on the number of lesions present, their location, and the presence or absence of other systemic metastases.9–12 If surgery is not indicated, these patients would normally receive palliative systemic chemotherapy. In recent years, newer chemotherapeutic regimens, mainly 5-fluorouracil and leucovorin combined with oxaliplatin and/or irinotecan, have demonstrated greater response rates in patients with metastatic colorectal cancer. Despite this, long-term survival is still poor.13–18

We have previously reported the preliminary results of percutaneous radiofrequency ablation (RFA) for a group of 20 patients with inoperable colorectal pulmonary metastases, which showed promising perioperative outcomes and local disease control.19,20 However, in the current literature, the survival benefit of percutaneous RFA remains unclear, and it is also unknown whether this interventional procedure is indicated for all patients or only selected patients. With a median follow-up of 2 years, the present study critically evaluated 10 clinical and 10 treatment-related prognostic parameters for survival in 55 non-surgical candidates who underwent percutaneous lung RFA for colorectal pulmonary metastases.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From November 2000, a total of 55 patients underwent percutaneous RFA for colorectal pulmonary metastases. All patients were followed prospectively. The study was approved by the institution ethics committee.

Patient Selection
The inclusion criteria of this study consisted of the following: (1) patient age between 18 and 85 years; (2) patients with colorectal pulmonary metastases who were considered nonsurgical candidates because of previous metastases to the liver or lung, >3 lesions in either lung, multiple lobar metastases, bilateral disease involvement, or poor performance status; (3) patients refusing to undergo surgery; (4) complete resection of colorectal primary tumor and any liver metastases before the entry onto the study; and (5) signed informed consent.

The exclusion criteria included the following: (1) more than six lesions per hemithorax; (2) diameter of metastases >5 cm; (3) lesions immediately adjacent to major pulmonary vessels; (4) lesions immediately adjacent to major bronchi; (5) bleeding diatheses (prothrombin time >1.5 and platelets <100 x 109); (6) extrapulmonary systemic metastases; and (7) greatly compromised lung function. The last criterion did not affect this reported patient group because they were patients treated exclusively for colorectal lung metastases and did not have compromised lung function. However, any patients with a history of impaired respiratory function were assessed by a hospital respiratory physician to determine the suitability for RFA. The consensus on treatment plans for these patients with colorectal pulmonary metastases was obtained from a group of surgical oncologists, medical oncologists, and radiologists at weekly meetings.

Preprocedural Management
All patients underwent pre-RFA physical examinations; abdominal, pelvic, and chest computed tomography (CT); and bone scans. Measurements of carcinoembryonic antigen levels were also obtained. Positron emission tomography was not routinely performed in these patients.

Percutaneous RFA Treatment Protocol
All procedures were conducted by two experienced interventional radiologists. Two rectangular dispersive electrode pads were placed onto the patients’ shaved thighs with the larger edge facing the RFA site. For lesions located in the anterior part of the lung field, an anterior approach was used with the patient in the supine position; for lesions located in the posterior part of the lung field, a posterior approach was used with the patient in the prone position. Percutaneous lung RFA techniques have been described previously.19 In short, percutaneous RFA procedures were performed under local anesthesia (Xylocaine 1%) and conscious sedation (meperidine-midazolam), with fluoro-CT guided imaging (Xpress SX; Toshiba, Japan) with the Rita 1500 generator (Rita Medical, Mountain View, CA) with real-time recording and display of temperature, power, and impedance. A Rita Starburst XL probe, with a length of either 10 or 15 cm, a diameter of 14 gauge, and nine deployable tines, was used. The probe is available in three lengths—10, 15, and 25 cm—and is able to ablate lesions of 5 cm in diameter. Because of the space limitations caused by the CT gantry, however, only 10- and 15-cm probes were used.

The probe was inserted percutaneously into the lung and positioned so that the deployable tines surrounded the lesion. The ablation algorithm consisted of a staged deployment where the initial power setting was 35 W and then gradually increased to 150 W. Power was increased with incremental probe deployment to enhance the rate at which the temperature increased. The target temperature was 90°C, and when this temperature was reached, it was maintained for 15, 20, or 37 minutes to achieve a complete tumor ablation of 3, 4, or 5 cm in size, respectively.

For lesions >3 cm in diameter, overlapping ablations were performed to ensure a complete ablation. To minimize the incidence of developing pneumothorax in these cases where additional ablation was required, the position of the electrode within the tumor was changed by withdrawing it into superficial lung tissue along its major axis, changing its angle, and then reinserting the electrode into the target without a complete withdrawal of the needle out of the pleura. For the purpose of this study, lesions that were 3 cm from the pulmonary hilum were considered hilar lesions, and lesions located more than 3 cm away from the pulmonary hilum were considered peripheral lesions. Track ablation was routinely performed with cauterizing the access tract on the way out at the completion of each lesion ablation. For a complete RFA procedure, all radiologically identified lesions were ablated according to the treatment protocol. The patients’ vital signs were monitored continuously during the lung RFA and for 6 hours after the procedure.

Postprocedural Management
All patients were observed in the hospital at least overnight after lung RFA, with chest x-rays performed 1 hour after RFA and again just before discharge to check for pneumothorax. Patients with small pneumothoraxes were observed in the hospital; otherwise, chest drains were inserted for larger or symptomatic pneumothoraxes. Antibiotic or anti-fungal agents were not administered prophylactically, unless a specific organism was identified. All patients were reviewed at 1 week, 1 month, and then every 3 months thereafter with chest CTs to monitor the progression of disease (Fig. 1Go).


Figure 1
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  		FIG. 1. Sequential computed tomographic (CT) images demonstrating the usual stages after a successful lung radiofrequency ablation (RFA) treatment. (a) Pre–lung RFA CT image showing a solitary pulmonary metastasis. (b) Opacification during lung RFA treatment with typical rarefraction surrounding ablation field. (c–f) Sequential post–lung RFA CT images at 1 month, 3 months, 6 months, and 12 months, respectively, demonstrating post–lung RFA changes of the ablation field, from a zone of consolidation to a small scar.

 
After RFA, patients with increased carcinoembryonic antigen or radiological evidence of colorectal metastases were referred to a hospital medical oncologist for systemic chemotherapy with 5-fluoro-uracil and, more recently, combined with oxaliplatin or irinotecan. Patients were then followed once every 3 months thereafter, unless they became symptomatic.

Statistical Analysis
The institutional review board granted permission to analyze the data of this study. The clinical and treatment-related data of all patients were collected prospectively and entered into a computerized database. The primary end point of this study was overall survival, determined from the time of RFA intervention. Univariate analysis was computed by the Kaplan-Meier method and compared by log rank test. Multivariate analysis was performed by a Cox regression model (Cox proportional hazard model). All statistical analyses were performed using SPSS for Windows (version 11.5; SPSS GmbH, Munich, Germany). A significant difference was assumed for P values <.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Clinical Data
Fifty-five nonsurgical candidates underwent percutaneous RFA for colorectal pulmonary metastases at the St George Hospital, Sydney. Thirteen patients underwent repeat RFA, and 2 patients underwent RFA for a third time for pulmonary recurrence. A number of selection factors (inclusion and exclusion criteria) influenced this study population. Although bilateral disease did not usually preclude resection, particularly in the setting of colorectal metastases, 30 of the 55 reported patients already had colorectal liver metastases previously treated by hepatectomy. All patients had their extrapulmonary metastases surgically treated before being entered into this study. The median interval of hepatectomy and lung RFA was 14 months (range, 3–80 months).

Sixteen patients had more than three pulmonary metastases; 7 of these 16 patients had three or more lobes involved, and 11 of these 16 patients had bilateral pulmonary metastases; 12 patients refused to have surgery; and 4 patients had poor performance status. It should be noted that in some cases more than one factor influenced the decision to perform RFA. Twenty patients received some form of systemic chemotherapy before lung RFA. Twelve patients were being treated concurrently with some form of systemic chemotherapy at the time of lung RFA. Forty-two patients received some form of systemic chemotherapy after RFA.

The median follow-up period was 24 months (range, 6–40 months), and the follow-up was complete. There were 33 male patients (60%). The mean age at the time of lung RFA was 62 ± 11 years. The mean number of pulmonary metastases ablated per patient was 2 ± 2. The median number of pulmonary metastases ablated per patient was 2 (range, 1–6). The mean size of the largest pulmonary metastasis was 2.1 ± 1.1 cm in diameter. All RFA procedures were completed in a single session. The median duration of the entire RFA procedure was 2.5 hours (range, 1.0–4.5 hours).

Perioperative Outcomes
There was no periprocedural mortality. The overall periprocedural morbidity was 42% (n = 23). Five patients had intrapulmonary bleeding around the ablation site, none of which caused any symptoms and all of which were self-limiting, as shown by CT at 1 week. Post-RFA adverse events included pneumothorax (n = 16), fever (n = 6), pleural effusion (n = 4), and pleuritic chest pain (n = 2). Some patients experienced more than one adverse event. Nine patients with pneumothoraxes and one patient with a pleural effusion required chest drain insertion. The mean duration of chest drain required in these patients was 2 ± 2 days. The pneumothoraxes in the remaining seven patients were small and self-limiting. No patients experienced adverse events severe enough to warrant surgical intervention or intensive care unit support. The median length of hospital stay was 1 day (range, .5–11 days).

Recurrence Results
At the time of last follow-up, 21 patients (38%) developed disease progression at an original RFA site, and the local progression-free survival was not reached. Thirty-six patients (66%) developed disease progression at a systemic site; the overall median progression-free survival was 15 months (range, 3–40 months).

Survival Results
The overall median survival was 33 months (range, 4–40 months), with 1-, 2- and 3-year actuarial survival rates of 85%, 64%, and 46%, respectively (Fig. 2Go).


Figure 2
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  		FIG. 2. Actuarial overall survival of 55 nonsurgical candidates who underwent percutaneous radiofrequency ablation for colorectal pulmonary metastases at St George Hospital, Sydney.

 
Table 1Go provides univariate analysis of 10 clinical factors for overall survival, and Table 2Go provides univariate analysis of 10 treatment-related factors for overall survival. The following three factors were found to be prognostically significant in univariate analysis: largest size of lung metastasis (P < .001) (Fig. 3Go); location of lung metastasis (P = .032) (Fig. 4Go); and repeat percutaneous RFA for pulmonary recurrence (P = .024) (Fig. 5Go). The remaining 17 parameters did not have any statistically significant effect on overall survival.


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  		TABLE 1. Univariate analysis of 10 clinical factors
 

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  		TABLE 2. Univariate analysis of 10 treatment-related factors
 

Figure 3
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  		FIG. 3. Actuarial survival after percutaneous radiofrequency ablation for nonsurgical candidates with pulmonary metastases from colorectal carcinoma. Prognostic significance of largest size of pulmonary metastasis was P < .001.

 

Figure 4
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  		FIG. 4. Actuarial survival after percutaneous radiofrequency ablation for nonsurgical candidates with pulmonary metastases from colorectal carcinoma. Prognostic significance of location of pulmonary metastases was P = .032.

 

Figure 5
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  		FIG. 5. Actuarial survival after percutaneous radiofrequency ablation for nonsurgical candidates with pulmonary metastases from colorectal carcinoma. Prognostic significance of repeat percutaneous RFA for lung recurrence was P = .024.

 
In the multivariate analysis, one factor was found to be independently associated with a reduced overall survival: largest size of lung metastasis >3 cm (hazard ratio, 4.456; 95% confidence interval, 1.664–11.932; P = .003).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Pulmonary metastases are common in patients with colorectal cancer. Resection can achieve 5-year survival rates of 20% to 40%, but only in a small proportion of carefully selected patients.1–12 Non-surgical candidates are usually managed with systemic chemotherapy. Recently, some newer systemic chemotherapeutic regimens for metastatic colorectal cancer have shown improved response rates, but the long-term survival is still poor.13–18

RFA is a new locoregional ablative technique that has been used in focal destruction of hepatic tumors.21 Application of RFA to lung tumors is a more recent development, and preliminary studies have shown some promising perioperative outcomes and local disease control.19–20,22–28 However, the survival benefit of percutaneous RFA remains unclear. With a median follow-up of 2 years, this current series reported the perioperative and survival outcomes of 55 nonsurgical candidates who underwent RFA for colorectal pulmonary metastases. The overall median survival was 33 months (range, 4–40 months), with 1-, 2-, and 3-year survival of 85%, 64%, and 46%, respectively. It was our intention to identify important prognostic factors to improve patient selection.

Patients with bilateral pulmonary metastases are poor candidates for surgery.3,9–11 Saito et al.11 reported that the 5-year survival rates of patients who underwent unilateral pulmonary metastasectomy and bilateral metastasectomy were 42% and 16%, respectively (P = .048). The present series demonstrated similar survival outcomes between patients with unilateral and bilateral disease. In addition, the number of lesions did not seem to have a marked impact on survival. It suggests that percutaneous RFA may play a useful role in selected patients with inoperable colorectal pulmonary metastases, especially because it avoids bilateral thoracotomies and their associated long hospitalization.

However, in patients with larger pulmonary metastases, percutaneous RFA did not seem to be effective. In fact, 70% of patients with lesions of >3 cm died of their disease within the first 14 months. The size of pulmonary metastases is usually not prognostic for survival after lung resection. This is probably because in resection, a solitary tumor can be removed en bloc, whereas in lung RFA, there is a physical limitation of ablation size. The risk of local treatment failure of lung RFA therefore needs to be considered in large pulmonary lesions.29

In this study, all radiologically identified lesions were ablated according to the treatment protocol. For lesions >3 cm, overlapping ablations were performed by repositioning the electrode to ensure an adequate margin. However, we did not resect or perform biopsy after lung RFA; therefore, we cannot prove complete tumor necrosis histologically. Some lesions were adjacent to the hilum, which produces a "heat sink" effect by diminishing thermal energy. Consequently, this would potentially result in inadequate ablation. In this series, 10 patients with hilar lesions had a greatly reduced overall survival.

Five patients had intrapulmonary bleeding, usually appreciated immediately after the commencement of ablation on fluoro-CT as an area of enhancement around the ablation probe. In our study, these patients remained asymptomatic after RFA and the bleeding was self-limiting, as shown on follow-up CT scans at 1 week. However, Dupuy et al.23 reported one death among 27 patients as a result of pulmonary hemorrhage after RFA, attributed to platelet dysfunction. Vaughn et al.24 also recently reported a severe hemorrhagic adverse event after lung RFA. Sixteen patients developed pneumothoraxes, and 9 of these 16 patients required insertion of a chest drain. Often the diagnosis of a pneumothorax was not a clinical but rather a radiological diagnosis because all patients had chest x-rays scheduled after the procedure. Recently, the authors have shown that there is a learning curve in percutaneous lung RFA, and the incidence of pneumothorax and chest drain insertion can be reduced with experience.30

The results of percutaneous lung RFA for colorectal pulmonary metastases should be interpreted cautiously because the number or patients and length of follow-up in most studies may not be adequate to confidently predict long-term survival. Also, the results of this interventional procedure versus systemic chemotherapy should be interpreted with the knowledge that these treatment strategies have not been compared directly. A randomized, controlled study comparing systemic chemotherapy alone versus percutaneous lung RFA and systemic chemotherapy would be ideal.

In conclusion, the present study reported the survival outcomes of 55 nonsurgical candidates who underwent percutaneous lung RFA for colorectal pulmonary metastases. This interventional procedure may play a useful role in selected patients. In patients with multiple or bilateral pulmonary metastases, it may have the advantage of avoiding bilateral thoracotomies and associated long hospitalization. However, the survival benefit of patients with pulmonary metastases >3 cm was limited.


   ACKNOWLEDGMENTS
 
The authors thank Jing Zhao for her diligent and meticulous work in maintaining the RFA database and David Change for his expertise in statistical analysis.

Received for publication May 25, 2006. Accepted for publication May 25, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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