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10.1245/s10434-006-9010-3
Annals of Surgical Oncology 13:1588-1595 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Learning Curve for Percutaneous Radiofrequency Ablation of Pulmonary Metastases From Colorectal Carcinoma: A Prospective Study of 70 Consecutive Cases

Tristan D. Yan, BSc (Med) MBBS1, Julie King, MPH1, Adrian Sjarif, MBBS1, Derek Glenn, MBBS2, 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: David L. Morris, MD, PhD; E-mail: david.morris{at}unsw.edu.au


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Percutaneous radiofrequency ablation (RFA) for inoperable colorectal pulmonary metastases is associated with a morbidity rate of 30% to 40%. A learning curve in this treatment approach has not been documented before.

Methods: The clinical and treatment-related data regarding 70 consecutive percutaneous RFA procedures for inoperable colorectal pulmonary metastases were collected prospectively. A comparison between the initial 35 cases (group 1) and the subsequent 35 cases (group 2) was performed. Univariate and multivariate analyses were conducted to identify the significant risk factors for overall morbidity, pneumothorax, and chest drain requirement.

Results: There was no hospital mortality. The overall morbidity rate was 37%. The rate of pneumothorax was 27%. Twelve patients (17%) required chest drain insertion for pneumothorax. There was a significant decline in the incidence of overall morbidity, pneumothorax, and chest drain requirement in group 2 as compared with group 1. Both the number of lung metastases ablated and the RFA treatment period (group 1 vs. group 2) were independent risk factors for overall morbidity, pneumothorax, and chest drain requirement. Distribution of lung metastases (unilateral vs. bilateral) was an independent risk factor for overall morbidity and pneumothorax, but not for chest drain requirement.

Conclusions: There is a learning curve for percutaneous lung RFA. With accumulated experience in this procedure, a low morbidity rate can be achieved.

Key Words: Radiofrequency ablation • Pulmonary metastases • Colorectal carcinoma • Learning curve


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pulmonary metastases in patients with colorectal carcinoma is common. Lung resection can achieve a 5-year survival rate of 20% to 40%, but it is indicated in only a small percentage of patients whose disease is confined to the lung.1–12 Most patients with inoperable colorectal pulmonary metastases are treated with systemic chemotherapy. With the introduction of newer chemotherapeutic regimens, there has been an increased response rate, but the long-term survival remains disappointing.13–18

Percutaneous radiofrequency ablation (RFA) is a relatively new and minimally invasive technique that delivers a high frequency of 400 to 500 kHz through a needle electrode into the targeted tissue, thus causing ionic agitation, tissue heating, and cell death. It has been used in treating unresectable liver tumors.19–22 Percutaneous lung RFA is a more recent treatment intervention. We have previously reported the preliminary results of percutaneous RFA for inoperable colorectal pulmonary metastases.23–26 A recent survey including 493 percutaneous lung RFA procedures from 7 international institutions showed that the rate of pneumothorax was 30% and the rate of chest drain requirement was 10%.27

However, the effect of operator experience in this intervention has not been elucidated. It is important for a physician to recognize and overcome the learning curve associated with a new treatment procedure. This prospective study was conducted when this treatment intervention was initiated at our institution. It was designed to clarify whether there is a learning curve in percutaneous RFA of colorectal pulmonary metastases and to identify the significant risk factors for morbidity.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Percutaneous lung RFA was initiated as a treatment option for patients with inoperable colorectal pulmonary metastases at St. George Hospital, Sydney, in November 2000. A total of 70 consecutive procedures were performed on 55 patients with inoperable colorectal pulmonary metastases. These included 55 initial RFA procedures and 13 repeat and 2 third-time RFA procedures for recurrence. All procedures were conducted by two experienced interventional radiologists who initially had minimal experience with percutaneous lung RFA. The hospital ethics committee approved the study, and signed informed consent was obtained from all patients.

Patient Selection
Percutaneous RFA was considered in patients who had colorectal pulmonary metastases that were inoperable as a result of number, distribution (multiple lobes or bilateral disease), poor performance status, or the patient’s refusal to accept surgery. The exclusion criteria included (1) more than six lesions per hemithorax, (2) diameter of metastases >5 cm, (3) bleeding diathesis (prothrombin time international normalized ratio >1.5 and platelets <100 x 109 g/L), (4) extrapulmonary systemic metastases, and (5) previous radiotherapy to the affected lung and/or significantly compromised lung function. Any patient with a history of impaired respiratory function was assessed by hospital respiratory physicians to determine suitability for surgery. The consensus on the treatment plans for patients with colorectal pulmonary metastases was obtained at weekly meetings by a group of oncological surgeons, medical oncologists, and radiologists.

Pre-RFA Management
All patients had a pre-RFA physical examination; 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 Procedure
Two rectangular dispersive electrode pads were placed on to the patient’s shaved thighs with the larger edge facing the RFA site. Patients were positioned on the scanning table to allow optimal location of the lesion(s). Percutaneous lung RFA procedures were performed with patients under local anesthesia (lidocaine 1%) and conscious sedation (meperidine/midazolam), with fluoro-CT–guided imaging (Xpress SX; Toshiba, Tokyo, Japan), by using the RITA 1500 generator (RITA Medical, Mountain View, CA) with real-time recording and displaying of temperature, power, and impedance. A RITA Starburst XL probe, either 10 or 15 cm, with a diameter of 14-guage and nine deployable tines, was used (Fig. 1Go). The probe is capable of ablating a lesion up to 5 cm in diameter. The ablation algorithm consisted of a staged deployment in which the initial power setting was 35 W and was 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 complete tumor ablation of 3, 4, or 5 cm, respectively. A 360° tumor-free margin must be produced to obtain a successful area of ablation around each lesion. The target diameter for ablation of 2 cm larger than the patients’ tumor diameter was achieved in all patients. The vital signs were continuously monitored during the lung RFA and for 6 hours after the procedure.


Figure 1
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  		FIG. 1. A radiofrequency ablation probe (RITA Starburst XL probe) with nine deployable tines.

 
Post-RFA Management
All patients were observed in the hospital at least overnight after lung RFA, with chest x-rays performed at 1 hour after RFA and just before discharge to exclude pneumothorax. Patients with a small pneumothorax were observed in the hospital; otherwise, a chest drain was inserted. 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 every 3 months thereafter with chest CT scans to monitor the progression of their disease. Some patients were referred to a medical oncologist for adjuvant chemotherapy, including systemic chemotherapy with 5-fluorouracil and, more recently, 5-fluorouracil combined with oxaliplatin or irinotecan. Patients were then followed up at 3-month intervals thereafter unless they became symptomatic.

Study Methods
All the clinical and treatment-related data were prospectively collected and entered into a computerized database. The database was specifically designed to evaluate patients treated with lung RFA. It categorized events into intraprocedural and postprocedural adverse events. The 70 consecutive percutaneous lung RFA procedures in 55 patients with inoperable colorectal pulmonary metastases over a 3-year period formed the basis of this study. The institutional review board granted permission to analyze and report the data. For the purpose of this study, the 70 RFA procedures were divided into 2 groups. Group 1 consisted of the initial 35 procedures, and group 2 consisted of the subsequent 35 procedures.

The clinical and treatment-related data were compared between the two groups. The main outcome measures of this study were overall morbidity and the incidence of pneumothorax and chest drain requirement for pneumothorax. Pneumothorax and chest drain requirement were individually evaluated in this study because they contributed to the most postprocedural morbidity.

Statistical Analysis
Categorical variables were compared by using {chi}2 analysis or Fisher’s exact test, as appropriate. Multivariate analysis of risk factors for morbidity was performed by using a binary logistic regression 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
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Seventy consecutive percutaneous RFA procedures were performed in 55 patients with inoperable colorectal pulmonary metastases by 2 experienced interventional radiologists. The mean age of the study group was 63 ± 11 years. The mean number of pulmonary metastases ablated in each patient was 2 ± 1. The mean size of the largest pulmonary metastasis was 2 ± 1 cm. The mean size of the ablated area achieved for each lesion was 4 ± 1 cm.

Table 1Go demonstrates the comparison of clinical and treatment-related data between the initial 35 procedures (group 1) and the subsequent 35 procedures (group 2). It shows that there were no significant statistical differences between these groups in terms of number, distribution, size, location, or proximity to major pulmonary vessels. In this study, a major pulmonary vessel was defined as a main pulmonary vessel or its secondary and tertiary branches.


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  		TABLE 1. Comparison of clinical, operative, and postoperative data between the initial 35 procedures (group 1) and the subsequent 35 procedures (group 2)
 
Perioperative Outcomes
There was no hospital mortality. The mean length of hospital stay was 1 ± 2 days. The overall morbidity rate was 37%. The intraprocedural morbidity rate was 9%. The intraprocedural adverse events included intrapulmonary bleeding (7%), coughing, and pleuritic chest pain. The postprocedural morbidity rate was 33%. The postprocedural adverse events included pneumothorax (27%), pleural effusion (10%), and persistent pleuritic chest pain (6%). Most patients were asymptomatic and were observed for 24 hours before being discharged from the hospital. Thirteen patients (19%) required a chest drain, including 12 patients with pneumothorax and 1 patient with pleural effusion. Four patients who developed severe pleuritic chest pain after RFA required opioid analgesia for adequate pain control.

Table 2Go demonstrates the differences in the incidence of intraprocedural and postprocedural adverse events between the two groups. It shows a decline in overall morbidity and reduced intraprocedural and postprocedural adverse events in group 2 when compared with group 1. No intrapulmonary bleeding was recorded in group 2 (P = .027). The overall incidence of pneumothorax detected on a postprocedural chest x-ray was 40% in group 1, as compared with 14% in group 2 (P = .030). A chest drain was required in 10 patients (29%) with pneumothorax in group 1, as compared with 2 patients (6%) in group 2 (P = .023). Figure 2Go shows the decline in the incidence of pneumothorax (P = .023) and chest drain requirement (P = .017), year by year over the study period.


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  		TABLE 2. Comparison of the morbidity data between the initial 35 procedures (group 1) and the subsequent 35 procedures (group 2)
 

Figure 2
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  		FIG. 2. Significant decline in the incidence of pneumothorax (P = .023) and chest drain requirement (P = .017) after percutaneous radiofrequency ablation (RFA) for inoperable colorectal pulmonary metastases year by year over the study period.

 
Risk Factors for Overall Morbidity
Both univariate and multivariate analyses were performed to evaluate the association of 10 clinical and treatment-related factors with the rates of overall morbidity, pneumothorax, and chest drain requirement for pneumothorax. Three factors were significantly associated with overall morbidity in the univariate analysis: number of lung metastases ablated (P = .011), distribution of lung metastases (P = .012), and RFA treatment period (P = .025) (Table 3Go). In the multivariate analysis, the number of lung metastases ablated (odds ratio, 5.128; 95% confidence interval, 1.483–13.841; P = .008) and RFA the treatment period (odds ratio, .248; 95% confidence interval, .081–.757; P = .014) were the two independent risk factors for overall morbidity.


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  		TABLE 3. Univariate analysis of potentially significant risk factors for morbidity
 
Risk Factors for Pneumothorax
Three factors were significantly associated with pneumothorax in the univariate analysis: number of lung metastases ablated (P = .001), distribution of lung metastases (P = .033), and RFA treatment period (P = .030) (Table 3Go). In the multivariate analysis, the number of lung metastases ablated (odds ratio, 9.225; 95% confidence interval, 2.459–34.616; P = .001) and the RFA treatment period (odds ratio, .191; 95% confidence interval, .050–.734; P = .016) were the two independent risk factors for pneumothorax.

Risk Factors for Chest Drain Requirement
Two factors were significantly associated with a chest drain requirement for pneumothorax in the univariate analysis: number of lung metastases ablated (P = .002) and RFA treatment period (P = .023) (Table 3Go). In the multivariate analysis, the number of lung metastases ablated (odds ratio, 11.143; 95% confidence interval, 2.413–51.463; P = .002) and the RFA treatment period (odds ratio, .112; 95% confidence interval, .019–.661; P = .016) were the two independent risk factors for chest drain requirement.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
There was a significant reduction in morbidity in the more recent 35 cases when compared with the initial 35 cases of percutaneous lung RFA. This suggests that there is a learning curve associated with this interventional procedure. A learning curve has been found in a number of other relatively recent surgical techniques, such as laparoscopic surgery, RFA of the cardiac accessory pathways, and RFA of liver tumors.20,28,29

A recent international survey from seven institutions reported that the most common adverse event after percutaneous lung RFA was pneumothorax (30%) and that approximately 10% of cases required a chest drain.27 When the study was first initiated at our institution, the two interventional radiologists who were responsible for all the procedures had minimal experience in lung RFA, and the preliminary report at 1 year showed that the pneumothorax rate was 43% and that a chest drain was required in 26% of the cases.23 Several other studies also reported the short-term results of lung RFA.24–26,30,31 However, the importance of operator experience in this treatment approach has not been previously elucidated.

In this study, a comparison of clinical and treatment-related factors between the two study groups was performed. It showed that the overall rate of morbidity decreased from 51% to 20%, the intraprocedural complication rates decreased from 17% to 0%, and the postprocedural complication rates decreased from 46% to 20%. Early in the study period, we experienced five cases of intrapulmonary bleeding during the procedure. In our experience, these adverse events did not cause these patients any symptoms and were self-limiting, as was evident on the follow-up CT scans at 1 week. However, Dupuy et al.30 reported 1 death among 27 patients as a result of pulmonary hemorrhage after RFA; this was attributed to platelet dysfunction. Vaughn et al.31 also recently reported a severe hemorrhagic adverse event after lung RFA.

In our series, intrapulmonary bleeding was largely due to probe placement, particulary when placed close to hilar or any major pulmonary vessels. Early in the study period, we used fluoroscopic imaging guidance, but this was soon discontinued because fluoro-CT imaging enabled superior precision of probe placement.32 Axial images also provided better anatomical information for detection of the needle tip and tine location, particularly when these were adjacent to other structures, such as the heart and pulmonary vessels. Precise placement of the needle probe is a critical step to avoid intrapulmonary bleeding. In addition, all patients in our study group underwent extensive preoperative workup, so that patients with coagulopathy unresponsive medical therapy were excluded from the study. This careful patient-selection process may, at least in part, explain why none of the five cases of intrapulmonary bleeding required any medical treatment.

Pneumothorax was the most common postprocedural complication.23,27 In this study, pneumothorax was not a clinical, but a radiological, diagnosis, because all patients had follow-up chest x-rays 1 hour after the RFA procedure and just before discharge. The high reported rate of pneumothorax might also be a reflection of a prospective study. Only patients who were symptomatic required a chest drain. Ten patients required a chest drain in the first 35 cases, as compared with 2 patients in the second 35 cases. This series also demonstrated that both the number of lung metastases ablated and the RFA treatment period were independently associated with pneumothorax and chest drain requirement. Understandably the more punctures made when the RFA probe is inserted, the more likely will pneumothorax develop. However, there was no statistically significant difference in the number of lung metastases ablated between the two groups. This suggests that operator experience may be a more important contributon to the reductions of the incidence of pneumothorax and chest drain requirement over the study period.

Patients with emphysematous bullae, previous thoracic surgery, or lung radiation to the affected lung should be carefully evaluated, together with consideration of other selection factors, such as the expected survival and the size, number, and location of the pulmonary metastases, before acceptance for lung RFA. Not only are these patients more likely to develop pneumothorax, but also lung RFA may compromise their residual lung function.

Generous local analgesia infiltration at the planned puncture site and an appropriate dosage of intravenous sedation is necessary to minimize the irritation to the parietal pleura, especially in patients with peripheral lesions. In patients with cough as a presenting symptom, sufficient antitussive medications or intravenous sedation must be given, because one of our patients had a persistent cough during the procedure, and this resulted in pneumothorax. These important steps in the preparation will help avoid the patient’s making sudden respiratory movements that might cause trauma to the affected lung.

After the first 25 lung RFA procedures, with increased experience, the 2 radiologists decided that all patients should have conscious intravenous sedation routinely and that positive-pressure ventilation should be avoided when possible. In addition, special efforts were made to reduce the number of unnecessary needle tracts with careful planning of the angle of insertion and accurate placement of the needle into the desired position within the tumor before deployment of the tines. Increased operator experience in percutaneous lung RFA has contributed to the reduction in the incidence of pneumothorax and chest drain requirement at our institution (Fig. 2Go).

Percutaneous RFA may have a role in patients with inoperable colorectal pulmonary metastases, as it has in the treatment of inoperable liver tumors.19–22 Improving prognosis is not the only goal in cancer treatment. Because lung tumors cause debilitating symptoms, such as cough, hemoptysis, and pain, percutaneous lung RFA may also have a role in improving the quality of life of these patients. This study demonstrates that there is a learning curve in percutaneous lung RFA and that this interventional procedure can be performed safely with accumulated experience.


   ACKNOWLEDGMENTS
 
The authors thank David Chang for his expertise in statistical analysis and Jing Zhao for her maintenance of the RFA database.

Received for publication December 15, 2005. Accepted for publication February 20, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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