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Treatment Failure After Percutaneous Radiofrequency Ablation for Nonsurgical Candidates With Pulmonary Metastases From Colorectal Carcinoma

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: David L. Morris, MD, PhD, E-mail: david.morris{at}unsw.edu.au

	ABSTRACT

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Background: This study critically evaluated the local and overall treatment failure rates after percutaneous radiofrequency ablation (RFA) of pulmonary metastases from colorectal carcinoma.

Methods: Fifty-five nonsurgical candidates underwent RFA of colorectal pulmonary metastases. The primary end points of this study were local progression-free survival (PFS) and overall PFS. Univariate and multivariate analyses were performed to identify significant prognostic parameters for local and overall PFS.

Results: The local recurrence rate was 38%. For local PFS, univariate analysis demonstrated that the largest size of lung metastasis, the location of lung metastases, the post-RFA carcinoembryonic antigen level at 1 month, and the post-RFA carcinoembryonic antigen level at 3 months were significant prognostic indicators. In multivariate analysis, a largest size of lung metastasis of >3 cm and a post-RFA carcinoembryonic antigen level of >5 ng/mL at 1 month were independently associated with a reduced local PFS. The overall recurrence rate was 66%. For overall PFS, univariate analysis demonstrated that sex and the largest size of lung metastasis were significant prognostic indicators. In multivariate analysis, a largest size of lung metastasis of >3 cm was independently associated with a reduced overall PFS.

Conclusions: RFA of colorectal pulmonary metastases may have a useful role in local disease control for nonsurgical candidates, but its efficacy in patients with a lung metastasis of >3 cm is limited.

Key Words: Radiofrequency ablation • Pulmonary metastases • Colorectal carcinoma

	INTRODUCTION

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Approximately 10% of patients with colorectal cancer develop pulmonary metastases. Surgical resection is indicated in carefully selected patients, and this achieves 5-year survival rates of 20% to 40%.^1–12 Resectability is dependent on the number of lesions present, their location, and the presence or absence of extrapulmonary metastases. Most patients are considered nonsurgical candidates and therefore are treated with systemic chemotherapy. The newer chemotherapeutic regimens for colorectal metastases have improved response rates, but the long-term survival remains limited.^13–18 Since the early 1990s, an increasing number of minimally invasive techniques have been introduced into clinical practice in the treatment of lung tumors. Image-guided interventional and video-assisted thoracoscopic approaches have become attractive alternatives to open thoracic surgical resection. Other minimally invasive therapies using thermal energy sources to destroy tumors include radiofrequency ablation (RFA), cryoablation, focused ultrasonography, laser, and microwave. Percutaneous RFA is a relatively new treatment option for nonsurgical candidates with colorectal pulmonary metastases. RFA delivers a high frequency of 400 to 500 kHz through a needle electrode into the targeted tissue, causing ionic agitation, tissue heating, and cell death. Currently, four generator and electrode systems from four different manufacturers are available: the Boston Scientific RF-3000 generator with LeVeen and Concerto multitined expandable needle electrodes; the RITA system with a 1500X electrosurgical generator and StarBurst SDE, Semi-flex, XL, and XLi multitined expandable electrodes; the Valleylab Cool-tip RF Ablation System with internally cooled single and clustered needle electrodes; and the Berchtold Elektrotom 106 HiTT with open-perfused electrodes. Preliminary reports have shown that percutaneous RFA can be performed safely and that it may have a promising role in local disease control.^19–29 Some studies have found that larger lesions are associated with higher local recurrence rates.^25–29 However, to date, treatment failure rates after this interventional procedure have not been adequately addressed, and the criteria for patient selection are not well defined. The primary end point of this prospective study was progression-free survival (PFS), determined from the time of RFA intervention. Prognostic indicators for local and overall PFS were also statistically analyzed.

	PATIENTS AND METHODS

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The inclusion criteria of this study consisted of (1) age between 18 and 85 years; (2) patients who were considered nonsurgical candidates as a result of previous metastases to the liver or lung, more than three lesions in either lung, multiple lobar metastases, bilateral disease involvement, or poor performance status; (3) complete resection of primary colorectal cancer and any hepatic metastases before entry onto the study; (4) patients refusing to accept surgery; and (5) signed informed consent. The exclusion criteria included (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 not responding to medical therapy (pro-thrombin time international normalized ratio >1.5 and platelets <100 x 10⁹); (6) presence of extrapulmonary metastasis; (7) emphysematous bullae, previous surgery, or previous radiotherapy to the affected lung; and (8) significantly 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 any significant compromise in 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 the treatment plans for patients with colorectal pulmonary metastases was obtained from a group of surgical oncologists, medical oncologists, and radiologists at weekly meetings.

Preprocedural Investigations
All patients had physical examinations; abdominal, pelvic, and chest computed tomography (CT; with contrast); and bone scans. Measurements of carcinoembryonic antigen (CEA) levels were also obtained. Positron emission tomography was not available.

Percutaneous RFA Procedure
All procedures were conducted by two experienced interventional radiologists. Two rectangular dispersive electrode pads were placed on the patient’s shaved thighs with the large 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 RFA procedures were performed with patients under local anesthesia (lidocaine 1%) and conscious sedation (meperidine/midazolam), with CT-guided imaging (Xpress SX; Toshiba, Japan) using the RITA 1500 generator (RITA Medical, Mountain View), with real-time recording and display of temperature, power, and impedance. A RITA Starburst XL probe, either 10 or 15 cm, with a 14-gauge diameter and nine deployable tines, was used. The probe was available in three lengths (10, 15, and 25 cm) and was able to create a maximal lesion of 5 cm in diameter. Because of the space limitations caused by the CT gantry, 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 target lesion. The ablation algorithm consisted of a staged deployment in which 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, respectively. All patients with bilateral or multiple lesions were treated in a single session. For lesions >3 cm in diameter, overlapping ablations were performed to ensure a complete ablation. To minimize the incidence of developing pneumothorax in the cases in which additional cycles of ablation were 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 as hilar lesions, and lesions located >3 cm away from the pulmonary hilum were considered to be peripheral lesions. Track ablation was routinely performed with cauterizing the access tract on the way out at completion of each lesion ablation. For a complete RFA procedure, all radiologically identified lesions were ablated according to the treatment protocol.

Postprocedural Management
All patients were observed in the hospital for a minimum overnight stay after lung RFA. Chest radiographs were performed at 1 hour after RFA and just before discharge to exclude pneumothorax. Patients with small pneumothoraxes were observed in the hospital; for large pneumothoraxes, a chest drain was inserted. Antibiotic or antifungal agents were not administered prophylactically unless a specific organism was identified.

Patient Characteristics
Fifty-five nonsurgical candidates underwent percutaneous RFA for colorectal pulmonary metastases. All patients had their extrapulmonary metastases surgically treated before entering this study. 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 patients had two-organ metastases where their colorectal liver metastases previously treated by hepatectomy. The median interval of hepatectomy and lung RFA was 14 months (range, 3–80 months). The median interval of primary cancer surgery to lung RFA was 25 months (range, 2–84 months). Sixteen patients had more than 3 pulmonary metastases; 7 of these 16 patients had 3 or more lobes involved; and 11 of these 16 patients had bilateral pulmonary metastases. Twelve patients refused to have surgery, and four patients had poor performance status. It should be noted that in some cases, more than one factor influenced the decision to perform RFA.

There were 33 (60%) male patients. 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. Forty-two patients had lesions 3 cm. Twenty-one of the 42 patients had multiple lesions, and the other 21 patients had solitary lesions. Thirteen patients had lesions >3 cm. Four of these patients had multiple lesions, and the remaining nine patients had solitary lesions. Twenty-eight patients had a CEA level >5 ng/mL before the RFA intervention. 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).

Adjuvant systemic chemotherapy was not used as a component of the treatment protocol, because 20 patients had just completed their systemic chemotherapy before lung RFA and 12 patients were being treated concurrently with some form of systemic chemotherapy at the time of lung RFA. However, after RFA, patients with increased CEA or radiological evidence of colorectal metastases were referred to a hospital medical oncologist for systemic chemotherapy with 5-fluorouracil and, more recently, combined with oxaliplatin or irinotecan. Forty-two patients received some form of systemic chemotherapy after RFA; 13 patients underwent repeat RFA, and 2 patients underwent third-time RFA for pulmonary recurrence.

Follow-Up and Study Methods
All patients were reviewed at 1 week, 1 month, and every 3 months thereafter with chest CT (contrast) and serum CEA to monitor the progression of their disease, unless they became symptomatic. At the time of each follow-up review, all prior CT scans were required for comparative assessment. All CT findings were evaluated by two experienced interventional radiologists. The primary end points of this study were local PFS and overall PFS, determined from the time of percutaneous lung RFA intervention. Disease progression was defined as at least a 20% increase in the largest diameter of the target lesion. Local disease progression was referred to disease progression at an original lung RFA site. Overall progression was referred to disease progression at any systemic site.

All the clinical and treatment-related data were prospectively collected and entered into a computerized database. Univariate analysis was performed by using the Kaplan-Meier method and compared by using the log-rank test. Multivariate analysis was performed by using a Cox regression model (Cox proportional hazards model). All statistical analyses were performed with SPSS for Windows (version 11.5; SPSS GmbH, Munich, Germany). A significant difference was defined as P < .05.

	RESULTS

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Morbidity and Mortality Data
There was no hospital mortality. The periprocedural morbidity rate was 42% (n = 23), including intrapulmonary bleeding (n = 5), pneumothorax (n = 16), pleural effusion (n = 4), and persistent pleuritic chest pain for more than 1 week (n = 2). Some patients experienced more than one adverse event. All five cases of intrapulmonary bleeding were self-limiting, as shown on CT scans at 1 week. Nine patients with pneumothoraxes required chest drain insertion, and the other seven patients with pneumothoraxes were asymptomatic and discharged home after 24 hours of in-hospital observation. The mean duration of chest drain required in these patients was 2 ± 2 days. The median length of hospital stay was 1 day (range, .5–11 days).

Overall Survival and PFS
The median follow-up period was 24 months (range, 6–40 months), and the follow-up was complete. The overall median survival was 33 months (range, 4–40 months), with 1-, 2- and 3-year survival rates of 85%, 64%, and 46%, respectively.

Figure 1 illustrates local PFS and overall PFS for these 55 patients. At the time of last follow-up, the local disease progression rate was 38% (n = 21), with actuarial 1- and 2-year local PFS of 74% and 56%, respectively. The median local PFS was not reached. The overall disease progression rate was 66% (n = 36), with actuarial 1- and 2-year overall PFS of 61% and 34%, respectively. The median overall PFS was 15 months (range, 3–40 months).

View larger version (13K): [in this window] [in a new window]   FIG. 1. Cumulative local and overall progression-free survival (PFS) in nonsurgical candidates who underwent percutaneous radiofrequency ablation (RFA) for pulmonary metastases from colorectal carcinoma (n = 55).

View larger version (12K): [in this window] [in a new window]   FIG. 2. Cumulative local progression-free survival (PFS) in nonsurgical candidates who underwent percutaneous radiofrequency ablation (RFA) for pulmonary metastases from colorectal carcinoma. The prognostic significance of the largest size of lung metastasis was P < .001.

View larger version (12K): [in this window] [in a new window]   FIG. 3. Cumulative local progression-free survival (PFS) in nonsurgical candidates who underwent percutaneous radiofrequency ablation (RFA) for pulmonary metastases from colorectal carcinoma. The prognostic significance of the post-RFA carcinoembryonic antigen level at 1 month was P < .001.

View larger version (12K): [in this window] [in a new window]   FIG. 4. Cumulative overall progression-free survival (PFS) in nonsurgical candidates who underwent percutaneous radiofrequency ablation (RFA) for pulmonary metastases from colorectal carcinoma. The prognostic significance of the largest size of lung metastasis was P < .001.

	DISCUSSION

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At our institution, 55 patients underwent percutaneous RFA for colorectal pulmonary metastases. There was no procedure-related mortality. The overall morbidity was 42%. Pneumothorax is the most commonly reported postprocedural complication.²¹ In this study, 16 patients were found to have pneumothoraxes on the follow-up chest radiographs. Nine symptomatic patients required chest drain insertion for resolution.

Early in the study period, we experienced five cases of intrapulmonary bleeding during the RFA procedure. In our experience, these adverse events did not cause these patients any symptoms, and the patients did not require any medical treatment for resolution. However, Dupuy et al.³¹ reported 1 death among 27 patients as a result of pulmonary hemorrhage after RFA, attributed to platelet dysfunction. Vaughn et al.³² also recently reported a severe hemorrhagic adverse event after lung RFA. In our series, intrapulmonary bleeding was largely due to probe placement, particularly when placed close to the hilar vessels or other major pulmonary vessels. With increased experience, we found that precise placement of the needle probe was a critical step to avoid intrapulmonary bleeding. In addition, all patients in our study group underwent an extensive preoperative workup, so patients with lesion(s) immediately adjacent to major pulmonary vessels or patients with bleeding diatheses were not considered for RFA. This careful patient selection process may, at least in part, explain why all five cases of intrapulmonary bleeding were self-limiting.

At the last time of contact, 21 patients (38%) were found to have disease progression at an original lung RFA site. In both univariate and multivariate analyses, a largest size of lung metastasis >3 cm was associated with a reduced PFS. In this study, all radiologically identified lesions were ablated according to the treatment protocol. For lesions >3 cm, two or three overlapping ablations were performed to try to achieve larger ablation coverage. However, during an ablation cycle, there is an immediate zone of pneumonitis surrounding the ablated area, and this may obscure the targeted lesion. Therefore, when repositioning the needle electrode for an overlapping ablation, it is sometimes difficult to determine the needle position. Akeboshi et al.²⁹ achieved a lower rate of tumor necrosis in those targeted lesions >3 cm. Steinke et al.²⁷ showed that it was difficult to achieve a complete ablation in large lung lesions. Lee et al.²³ showed that lower rates of local disease control correlated with decreased mean survival rates: 19.7 vs. 8.7 months. However, from our current data, we are unable to analyze survival to determine whether any patients died of local disease alone, which may be influenced by local treatment options, such as RFA.

Persistent increases of post-RFA CEA levels may indicate an incomplete ablation of the lung lesion or undetected metastasis elsewhere. At our institution, we routinely used CT (contrast), compared with all previous scans, to follow up all patients. One of the major limitations of percutaneous lung RFA is the difficulty in monitoring the progression of disease. After RFA, the area of consolidation may appear larger than the original lung lesion, and the resolution of the consolidation may take months. During this period, disease progression may be difficult to assess. Positron emission tomography scans may continue to have positive results, thus making it difficult to assess whether viable tumor or scarring is present. Because the inflammatory changes after RFA often subside by 3 months, the 3-month scan is often more useful as the baseline measurement against which local progression can be judged.

Limiting resection to patients with single-organ metastases may be denying some patients a chance for long-term survival. There are strong, albeit retrospective, data that suggest that synchronous or metachronous liver and lung metastases may be treated surgically with as good an outcome as those achieved for liver alone or lung alone.³³ Surgical resection is the gold standard treatment for colorectal pulmonary metastases, and we do not regard lung RFA as an alternative to surgery, but it may be indicated in non-surgical candidates. In this study, a number of selection factors influenced this patient population. In some cases, more than one factor influenced the decision to perform RFA rather than surgery. The results of percutaneous lung RFA versus systemic chemotherapy should be interpreted with the knowledge that these treatment strategies have not been compared directly. This study suggested that this interventional procedure might have a useful role in nonsurgical candidates with colorectal pulmonary metastases. However, its efficacy is limited for lesions that are >3 cm.

	ACKNOWLEDGMENTS

 
The authors thank David Chang for his expertise in statistical analysis and Jing Zhao for maintaining the RFA database.

Received for publication September 9, 2006. Accepted for publication October 18, 2006.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Yan, T. D. Articles by Morris, D. L. Search for Related Content PubMed PubMed Citation Articles by Yan, T. D. Articles by Morris, D. L.