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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.04.008 on January 12, 2004

Annals of Surgical Oncology 11:207-212 (2004)
© 2004 Society of Surgical Oncology
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Percutaneous Imaging–Guided Radiofrequency Ablation in Patients With Colorectal Pulmonary Metastases: 1-Year Follow-Up

Karin Steinke, MD, Derek Glenn, FRANCZR, Julie King, MPH, William Clark, FRANCZR, Jing Zhao, MMs, Phillip Clingan, MRACP and David L. Morris, PhD

From the University of New South Wales, Departments of Surgery (KS, JK, JZ, DM), Radiology (DG, WC), and Medical Oncology (PC), The St. George Hospital, Sydney, New South Wales, Australia.

Correspondence: Address correspondence and reprint requests to: David L. Morris, PhD, UNSW Department of Surgery, St. George Hospital, Sydney, NSW 2217, Australia; Fax: 61-2-9350-3997; E-mail: david.morris{at}unsw.edu.au


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We assessed the safety and evidence of efficacy of radiofrequency ablation (RFA) for colorectal lung metastases with follow-up to 1 year.

Methods: Twenty-three patients had percutaneous RFA for 52 colorectal pulmonary metastases under fluoro-computed tomography (CT). Patients received intravenous conscious sedation and local analgesia with routine hospitalization and monitoring for 24 hours after RFA. Patients had CT scanning at 1 month and then every 3 months, with serum carcinoembryonic antigen assessment monthly and every 3 months.

Results: All ablations were technically successful. Tumor diameter ranged from .3 to 4.2 cm. Pneumothorax occurred in 43% (10 of 23) of patients. Six patients required intercostal chest drain placement. Six patients had a second RFA, four for new lesions and two for re-treatment of a previously treated lesion. The median admission was 2.0 days (range, 1–9 days). The median follow-up was 428 days (range, 173–829 days); data are reported to 1 year in this article. Five patients died at 5, 6, 8, 8, and 12 months after RFA from extrapulmonary (n = 1) or widespread (n = 4) disease. One patient developed a malignant pleural effusion at 6 months after RFA. Cavitation was seen in nine treated lesions (17%); all resolved with scar tissue contraction by 12 months. Eighteen patients with CT scan follow-up at 1 year have 40 lesions classified as disappeared (n = 17), decreased (n = 5), stable/same size (n = 4), or increased (n = 14).

Conclusions: Percutaneous imaging–guided RFA of multiple colorectal pulmonary metastases is a minimally invasive treatment option with modest morbidity. A significant proportion of patients show good evidence of successful local control at 1 year.

Key Words: Percutaneous • Radiofrequency ablation • Lung • Metastasis • Colorectal carcinoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer (CRC) is the second most common visceral malignancy in industrialized countries; the highest incidences are encountered in North America, Australia, New Zealand, Europe, and Japan.1 An increasing incidence of CRC has been observed in most areas of the world during the last few decades.1 Although the recurrence of disease is mainly locoregional, in 20% of patients it will recur at distant sites.2

The lung is the most common site of extra-abdominal disease; isolated pulmonary metastases are rare, with an incidence of 2% to 4%.3 Surgery for lung metastases is the only potentially curative treatment, with survival rates of 40% at 5 years and 30% at 10 years reported in recent publications.3,4 Repeat pulmonary metastasectomy plays a favorable role.5

In patients with liver metastases from CRC, it is now well established that cytoablative methods such as cryoablation and RFA are associated with long-term survival in a proportion of patients. In addition, they have lower morbidity rates and shorter hospitalization times than resection.6–9

We have already reported procedural aspects and early outcomes of percutaneous imaging–guided radiofrequency ablation (RFA) of pulmonary metastases in 20 patients.10 The purpose of this study was to study the radiological and tumor marker outcome of percutaneous computed tomography (CT)-guided RFA of lung metastases from CRC at a minimum of 12 months.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From November 2000 until February 2003, we treated 46 patients with 59 treatments for 111 metastases from different primary tumors. We treated 52 lesions in 23 patients with CRC pulmonary metastases that were judged to be inoperable because of the distribution (multiple lobes), the number, bilateral site of the lesions, comorbidity, or the patient’s refusal to accept surgery. Suitability for surgical resection was assessed at a weekly seminar of oncologists, oncological surgeons, and radiologists. Although bilateral disease does not usually preclude resection, especially in the setting of colorectal metastases, 22 of 23 of our reported patients had liver metastases previously treated. Fourteen of the patients were concurrently treated with some form of chemotherapy at the time of diagnosis of their lung metastases. The patients were judged by the treating clinicians as being unsuitable for surgery.

Study inclusion criteria were a colorectal primary tumor, a maximum of six lesions per hemithorax, a maximum lesion diameter of 4.2 cm, and age 18 to 85 years. Study exclusion criteria were uncorrectable coagulopathy (prothrombin time >1.5 and platelets <100 x 109) and significantly compromised lung function. The latter criterion did not affect our reported patient group, because they were exclusively patients treated for colorectal lung metastases and did not have compromised lung function. Any patient with severe clinical respiratory impairment normally has spirometry to assess lung function, and the degree of respiratory impairment and suitability for RFA are assessed by respiratory physicians.

CT imaging alone was considered sufficient for the diagnosis of pulmonary metastases. The patients were continuously monitored for their CRC with abdominal and chest CT scans, and if either new or increasing lung lesions were seen, the CT scans were reviewed at the oncology/radiology meeting. One patient, who had had breast cancer before her CRC, had a percutaneous biopsy performed to assess the metastatic origin.

The study had hospital ethics committee approval, and signed, informed consent was obtained for all patients. Pre- RFA treatment assessment included clinical assessment, CT scans, serum carcinoembryonic antigen (CEA), and the standard SF-36v2TM quality-of-life questionnaire (Quality Metric, Lincoln, RI).11 Informed consent was obtained at least 24 hours before the intervention.

All procedures were performed with the RITA 1500 generator (RITA Medical, Mountain View, CA) with real-time recording and display of temperature, power, and impedance. The probe used was the RITA Starburst XL (Fig. 1), which has a diameter of 14 gauge, with nine deployable electrodes, and is available in three lengths—10, 15, and 25 cm. It is able to create a maximal lesion of 5 cm in diameter. Because of the space limitations caused by the CT gantry, we used 10- and 15-cm probes.



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  		FIG. 1. Starburst XL device with nine retractable hooks.

 
All patients were provided with an intravenous access. The patients were positioned according to the location of the lesion or lesions. Prone and supine positions were preferred to the decubitus position.

Two grounding pads were placed in the correct position, one on each thigh, with the wider part facing the coagulated site to provide a large leading edge of the pad to lessen the risk of skin burns. Anesthesia consisted of generous local anesthesia (Xylocaine 1%) and intravenous conscious sedation (meperidine/midazolam on demand). Oxygen was administered through a mask at a flow rate of 4–5 L/min.

Probe placement was performed under sterile conditions and was fluoro-CT guided (Xpress SX; Toshiba, Tokyo, Japan). An ablation algorithm with staged deployment, a target temperature of 90°C, and a maximum power of 150 W was used. The target temperature was maintained for 15, 20, and 27 minutes for final ablations of 3, 4, and 5 cm, respectively. Track ablation, which is routinely performed, cauterizes the access track on the way out at completion of each lesion ablation.

Patients were monitored for oxygen saturation, pulse rate, blood pressure, and temperature during the treatment and for 4 to 6 hours after treatment. All patients were observed in hospital at least overnight, and a chest radiograph was performed after RFA treatment and before discharge the following morning to exclude pneumothorax.

Patients with a small asymptomatic pneumothorax were observed; in symptomatic patients or those with large pneumothoraces or effusions, a chest drain was inserted. All patients were observed clinically, with CT monitoring performed at 1 week, 1 month, and every 3 months thereafter.

Serum CEA (<5 ng/mL) was measured monthly, and the SF-36v2 quality-of-life questionnaire was repeated at 1 month and every 3 months. Statistical analysis was performed with Fisher’s exact test. Statistical significance was accepted at P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Twenty-three patients entered the study (14 men and 9 women) with a mean age 63 years (range, 29–79 years). Twenty patients had liver metastases, which had been surgically resected and/or treated with regional chemotherapy. One patient had prior pneumonectomy, and one patient had previous radiotherapy for lung metastases; these two patients were treated outside the study guidelines, together with one patient whose maximum tumor diameter was 4.2 cm and four patients with metastases close to central vessels. The mean number of CRC lung metastases treated with RFA was 2.17 (SE, .3).

Four patients had bilateral tumors treated within the same session, and six patients had a second procedure for new metastases—the outcomes of these subsequent treatments were not studied for this article because of the more limited follow-up. An additional three patients had re-treatment for recurrent disease at the site of previous ablation. The median number of days of hospitalization was 2.0 (range, 1–9 days; SE, .4 days).

The median follow-up was 428 days (range, 173–829 days). Five patients died—four from progressive metastatic disease at multiple sites at 6, 8, 8, and 12 months and one from surgery for local recurrence at 5 months with no visible lung metastases.

All patients tolerated the procedure well. There were no deaths within 30 days of the intervention or, indeed, any deaths that could be attributed to the procedure of RFA.

Ten (43%) of the 23 patients developed a pneumothorax, which was identified either during the procedure or within 24 hours on postprocedural chest x-rays. Five patients required chest tube placement—four for pneumothorax and one for hydropneumothorax. The mean duration with the chest tube was 1.35 days (SE, .57 days). Pneumothorax occurred more often with multiple procedures. In patients who developed a pneumothorax, an average of 2.6 lesions were treated, compared with 1.4 lesions treated in those without pneumothorax after RFA (P = .07; 95% confidence interval, .077–1.053).

Nine lesions (17%) cavitated but resolved uneventfully, with no superinfection noted. One patient with a cavitating lesion coughed up desiccated tissue. Cavitation was seen significantly more frequently when the size of the lesion at 1 week after treatment exceeded the size of the pretreatment lesion by 200% or more (P = .0001; 95% confidence interval, .32–.83).

During RFA, five patients developed radiological evidence of intrapulmonary hemorrhage (Fig. 2A and B), which was asymptomatic and self-limiting (Fig. 2C). One patient developed pneumonia, which was treated with antibiotics (cephalosporin 1 g/day orally) for 7 days.



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  		FIG. 2. (A) Lung metastasis (->) adjacent to a large pulmonary artery ({downarrow}) and a large bronchus (dashed arrow). (B) On insertion of the probe, a sudden opacification occurred surrounding the probe, consistent with hemorrhage. The dark circular rim around the probe end indicates the dissected area within the hemorrhagic lung parenchyma. (C) Complete resolution of the hemorrhage at 1 month.

 
One malignant pleural effusion was evident at 6 months, but a causal relationship to RFA is not clear because the patient underwent percutaneous biopsy before RFA. All patients complained of chest pain of variable severity for approximately 1 week; in five patients, this persisted for 1 month, and some patients experienced dyspnea occasionally for a few days after ablation. Fifteen patients reported episodes of increased temperature up to 1 week.

The change in treated lesion size over time, radiologically assessed through measurements of the lesions on axial CT scans in the lung window setting, is shown in Table 1. At 12 months, 40 of 52 pre-RFA lesions in 18 of the initial 23 patients were assessed radiologically: 17 lesions (42.5%) had disappeared, 5 (12.5%) had decreased in size, 4 (10%) were the same size, and 14 (35%) were larger than at baseline.


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  		TABLE 1. Change in treated lesion size over time
 
Of the 23 patients, 5 were dead; 7 had no evidence of disease; 3 had stable disease; 2 had local recurrence of previously treated lung metastases; 3 had generalized metastatic spread, lung included; 2 had new lung deposits (also treated by RFA) with no evidence of tumor elsewhere; and 1 had only distant (hepatic) recurrence at 12 months.

Serum CEA data is shown in Fig. 3. Of the 23 patients, 15 patients had an increased baseline serum CEA. At 1 month, five had returned to the normal value; three showed a decrease, and seven had an increase in serum CEA. Three of these had an increase <10%. One patient with a normal baseline CEA showed an increase at 1 month. Eight patients had a normal baseline CEA; of these, seven had normal CEA at 12 months, and one patient showed an increase.



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  		FIG. 3. Percentage changes of carcinoembryonic antigen (CEA) to 12 months. N, number of patients. The baseline CEA value was set to 0; the changes after radiofrequency ablation are expressed as percentage changes from baseline.

 
The quality-of-life questionnaire comprised eight subscales, both physical and mental. At 1 month, there was a statistically significant decrease from baseline for bodily pain (P = .0005) and physical functioning (P = .0025). At 3 months, there was no statistically significant change from baseline for any of the subscales. The reduced physical functioning at 1 year was not statistically significant (P = .01).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
RFA is an electrosurgical technique with a variety of current indications. It is well established as the treatment of choice for many symptomatic cardiac arrhythmias because of its ability to produce localized necrotic lesions, and it is evolving to a therapeutic means equivalent to surgery in the treatment of primary and secondary liver tumors. Many publications to date cover indications, technique, imaging modalities, complications, outcome, and follow-up.9,12–15

Pulmonary metastases complicate the course of as many as 40% of patients dying of malignant tumors and can represent the only site of distant disease.16 Unlike with many other cancers, the presence of distant metastases from CRC does not preclude curative treatment.17

It has been shown with limited pulmonary resections that patients may live longer than those treated conservatively.18 Intensive follow-up for lung metastases after resection of the colorectal primary tumor and aggressive resection of these metastases has been shown to improve the postoperative survival rate.19

Surgical resection of lung metastases is an established therapy for many primary tumors, but there is some controversy about prognostic factors for long-term survival. The long-term results and prognostic analysis based on 5206 cases of the International Registry of Lung Metastases showed that complete resection is the principal prognostic index, with an actuarial survival after complete metastasectomy of 36% at 5 years, 26% at 10 years, and 22% at 15 years.20

Jaklitsch et al.21 reported on 56 patients who underwent sequential metastasectomies with a minimum of 2 and a maximum of 6 separate lung resections. They concluded that multiple attempts to re-establish intrathoracic control of metastatic disease are justified in carefully selected patients but that the magnitude of benefit decays with each subsequent attempt.

Mineo et al.22 showed in a prospective randomized study that the type of resection did not significantly affect the survival of 85 patients who underwent pulmonary metastasectomy by either conventional resection (22 patients), with minimal resection (diathermy dissection and suture lines, 34 patients) or laser ablation (29 patients).

Pulmonary RFA has been used for the treatment of lung primary and metastatic tumors for almost 5 years, and the previously scarce literature on this topic is just recently being added to by new promising publications.23–26 This study focused on the treatment of metastatic CRC to the lung. We already have reported early results and quality-of-life analysis.10

One of our major concerns at the study outset was the potential for intraprocedural complications, such as needle displacement caused by coughing or respiration, and the potential for serious morbidity to occur, such as pain, pneumothorax, or bleeding into lung, airway, or pleura. Pneumothorax is a frequent complication after lung RFA and occurs in 30% to 50% of the patients. The rate of pneumothorax for ordinary lung biopsies reported in the literature ranges from 19% to 60%,27 and chest drain rates range from 3%28 to 50%.27

Cavitation at the ablation site sometimes occurs but seems to resolve mostly uneventfully. In our experience, only one patient expectorated ablated lung particles, without any clinical signs of pneumonia or abscess. The clinical state of the patient, rather than the radiological features, is mandatory for treatment and patient care. The role of prophylactic antibiotics in lung RFA would be interesting to correlate. Intraparenchymal lung tumors seem well suited to RFA because the surrounding air in adjacent normal lung parenchyma provides an insulative effect that may concentrate the radiofrequency energy.29

Lung RFA in this study was used for unresectable tumors, for patients not amenable to surgery because of comorbidities, or for those not wishing to undergo thoracic surgery. At 1 year, 42.5% of the treated tumors had disappeared, 12.5% were smaller than baseline, and 10% were the same size as baseline. The remaining 35% that were larger than baseline still showed a decreasing tendency (Table 1). Taking into account that the size of the ablated region is supposed to exceed the diameter of the initial tumor by at least 2 cm, encompassing not only the tumor, but also a surrounding 1-cm safety margin, and knowing that almost 50% of the treated lesions are larger than baseline at 6 months after RFA (unpublished data), we can conclude that of those 35% larger than baseline, most lesions were still shrinking at 1 year.

The interpretation of CEA is very complex and has to be performed separately. CEA changes do not reflect the pulmonary situation alone but express the metastatic spread within the entire body. One third of the patients with ablated lung lesions were having concomitant chemotherapy, and not all patients with CRC excrete CEA. A more detailed interpretation concerning the correlation of the CEA with the pulmonary status is in progress.

Evaluation of the quality-of-life questionnaire showed that the procedure was associated with a minor decrease in life quality at 1 month that returned to baseline at 3 months. The reduced physical functioning at 1 year was not statistically significant and was related to the general worsening of the patients’ condition rather than to the RFA procedure.

We cannot yet claim that percutaneous RFA will have results equivalent to those of resection. The aim of this treatment modality is, however, to achieve complete tumor ablation without the additional factors and complications inherent with a surgical procedure—general anesthesia, chest tube drainage, more prolonged hospital stay, and substantial loss of healthy pulmonary tissue. We would suggest that if long-term results parallel those of liver RFA treatment, it might also be a new alternative to lung surgery or radiation.

The well-established data on survival after pulmonary surgery make us confident enough to suggest that if we are able to completely ablate the lung tumors by RFA, we may achieve survival rates comparable to those of surgical tumor removal. Lower morbidity and mortality, as well as a better life quality, additionally accompany this treatment, with the possibility that patients may be treated on an overnight or even outpatient basis.


   ACKNOWLEDGMENTS
 
The acknowledgments are available online in the fulltext version at www.annalssurgicaloncology.org. They are not available in the PDF version.


   FOOTNOTES
 
Percutaneous imaging–guided radiofrequency ablation of multiple colorectal pulmonary metastases is a safe and efficient treatment modality with encouraging follow-up at 1 year.

Received for publication April 8, 2003. Accepted for publication September 22, 2003.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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