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Vascular and Interventional Radiology |
1 From the Departments of Radiology (T.H., N.T., H.M., K.Y., H.G., T.M., S.H., H.F., T.I., S.K.) and Cancer and Thoracic Surgery (Y.S., N.S.), Okayama University Medical School, 2-5-1 Shikatacho, Okayama 700-8558, Japan. Received June 28, 2005; revision requested August 23; revision received October 18; accepted November 16; final version accepted May 12, 2006. Address correspondence to T.H. (e-mail: takaoh{at}tc4.so-net.ne.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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Materials and Methods: Institutional review board approval was obtained, with waiver of informed consent. This retrospective study comprised 224 ablation sessions for 392 tumors in 142 patients (92 men, 50 women; mean age, 64.0 years). Multiple variables were analyzed by using the Student t test or the Mann-Whitney U test for numerical values and by using the 
2 test or the Fisher exact test for categorical values in order to assess risk factors for pneumothorax, pleural effusion, and chest tube placement for pneumothorax.
Results: The incidence of pneumothorax, pleural effusion, and chest tube placement for pneumothorax was 52% (117 of 224 sessions), 19% (42 of 224 sessions), and 21% (24 of 117 sessions), respectively. For pneumothorax, risk factors included male sex (P = .030), no history of pulmonary surgery (P < .001), a greater number of tumors ablated (P < .001), involvement of the middle or lower lobe (P = .008), and increased length of the aerated lung traversed by the electrode (P = .014). For pleural effusion, risk factors included the use of a cluster electrode (P = .008), decreased distance to the nearest pleura (P = .040), and decreased length of the aerated lung traversed by the electrode (P = .019). For chest tube placement for pneumothorax, risk factors included no history of pulmonary surgery (P = .002), the use of a cluster electrode (P < .001), and involvement of the upper lobe (P < .001).
Conclusion: Pneumothorax and pleural effusion can occur after RF ablation in patients with lung tumors, and chest tube placement for pneumothorax is sometimes required.
© RSNA, 2006
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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The study comprised 224 consecutive RF ablation sessions that were performed at our institution from June 2001 to February 2005. During these sessions, RF ablation was performed for 392 lung tumors in 142 patients (92 men, 50 women; mean age, 64.0 years ± 10.0 [standard deviation]; age range, 34–88 years) by using computed tomographic (CT) guidance. Eighty-nine patients (63%) underwent a single ablation session, which was defined as one visit to the interventional CT suite during which one or more tumors were treated. Fifty-three patients (37%) underwent repeat ablation sessions (mean number of sessions per patient, 1.6 ± 0.9; range, 1–5). A single tumor was ablated during 126 sessions (56%), and multiple tumors were ablated during 98 sessions (44%) (mean number of tumors ablated per session, 1.8 ± 1.1; range, 1–7).
Tumors were classified as primary lung neoplasms in 30 patients and as metastatic lung neoplasms in 112 patients. Metastatic neoplasms were from colorectal cancer in 40 patients, from lung cancer in 22 patients, from renal cell carcinoma in 10 patients, from esophageal cancer in eight patients, from hepatocellular carcinoma in seven patients, from maxillary cancer in two patients, from breast cancer in two patients, and from other sources (including 10 sarcomas) in 21 patients. The mean long-axis tumor diameter was 21.0 mm ± 15.2 (range, 3–98 mm).
RF Ablation Techniques
All patients underwent chest CT before RF ablation in order to assess the tumor and plan the procedure. Patient positioning for the 224 sessions was determined according to tumor location and included the supine position (108 sessions), the prone position (92 sessions), and a combination of prone and supine positions for ablation of multiple tumors (22 sessions). During two sessions, the lateral decubitus position was used to avoid severe pain in the supine or prone position.
The electrodes that were used for the 224 ablation sessions included a single 17-gauge internally cooled electrode with a 1-, 2-, or 3-cm noninsulated tip (Cool-tip; Radionics, Burlington, Mass) (n = 153), a 17-gauge multitined expandable electrode with a 2- or 3-cm diameter array (LeVeen; Boston Scientific, Natick, Mass) (n = 46), a combination of single internally cooled and multitined expandable electrodes (n = 15), or an internally cooled cluster electrode (Radionics) (n = 10). Until October 2003, only the internally cooled electrode was available at our institution, and thus all ablation procedures were performed with this electrode. Since then, multitined expandable electrodes have become available.
The type of electrode that was used depended mainly on the tumor location, tumor size, and physicians' preference. Generally, a single internally cooled electrode was preferred for tumors located adjacent to the pleura or pulmonary hilum. Multitined expandable electrodes were preferred for tumors smaller than 1 cm but not for tumors adjacent to the pleura or pulmonary hilum because the unpredictable expansion of tines could damage the pleura, large vessels, or bronchi. An internally cooled cluster electrode was used mainly for the ablation of large (>5-cm) tumors. The site and number of electrode insertions into the tumor were determined so that the expected ablation volume would be greater than the entire tumor volume and ablative margin.
For the procedure, the patient was placed in the planned position, and standard steel mesh grounding pads were placed on the patient's thighs. CT images were obtained for targeting prior to the procedure. The procedure was always performed percutaneously with CT fluoroscopy (Asteion; Toshiba, Tokyo, Japan) by two authors (T.H., N.T., H.M., K.Y., H.G., T.M., S.H., H.F., or T.I.), all of whom began performing RF ablation of lung tumors starting in 2001.
After an anesthetic was administered, the electrode was introduced into the tumor and was connected to an RF generator. The CC-1 generator (Radionics) was used for internally cooled electrodes, and the RF 2000 generator (Boston Scientific) was used for multitined expandable electrodes. An impedance-control algorithm was selected for the CC-1 generator. For the RF 2000 generator, RF energy was applied until a dramatic increase in impedance occurred or until automatic shut-off at 15 minutes, which was repeated twice at each site. For the CC-1 generator, RF energy was applied for 12 minutes with the infusion of ice saline into the cooling lumen of the electrode.
Ablation time and the number of RF applications at each site were reduced if the tumor was small (<1 cm), if RF application was performed at multiple sites for overlapping ablation, or if the patient, despite anesthesia and the use of an analgesic, complained of severe pain during RF ablation. Immediately after RF application with the CC-1 generator, the temperature of the tumor at the electrode tip was measured. If the temperature did not reach 60°C, an additional RF application was attempted at the same site. Immediately after the planned procedure was completed, CT images of the entire lung were obtained (5-mm section thickness).
After the procedure, the patient was carried (in the supine position) to the hospital room on a stretcher. Patients were instructed to stay in bed for 4 hours after the procedure. No instructions about posture in bed were provided. An upright posteroanterior chest radiograph was obtained 4 hours after the procedure and again the following morning.
Assessment and Management of Pneumothorax and Pleural Effusion
The presence of pneumothorax and pleural effusion was evaluated on CT images during and immediately after RF ablation and on follow-up chest radiographs by the consensus of the two authors who performed the procedure (T.H., N.T., H.M., K.Y., H.G., T.M., S.H., H.F., or T.I., with 9, 5, 18, 18, 13, 12, 9, 7, and 7 years of experience, respectively, in chest diagnosis at time of the study). Pneumothorax that exceeded an estimated 35%–40% of a hemithorax or symptomatic pneumothorax was treated with chest tube placement. Placement was maintained until air leakage ceased. If air leakage persisted for more than 1 week, further treatments (such as pleurodesis) were considered. Pleural effusion that exceeded an estimated 50% of a hemithorax was also treated with chest tube placement. There were no deaths related to pneumothorax or pleural effusion.
Data Collection and Definition of Variables
Multiple variables were collected by two authors (T.H., N.T.) by means of retrospective review of preoperative and intraoperative CT images, procedure records, and patient charts. Variables included the presence of pulmonary emphysema, history of pulmonary surgery, tumor factors (distance to the nearest pleura and location of tumor), and ablation factors (total ablation time, maximum power, and length of the aerated lung traversed by the electrode).
Pulmonary emphysema was determined to be present if centrilobular or panlobular emphysema, bullae, and blebs were observed in the vicinity of the tumor on CT images obtained with a 5-mm collimation. A patient was considered to have a history of pulmonary surgery if there had been any kind of pulmonary surgery performed on the side of the lung in which RF ablation was performed. Tumor size was measured along the long axis. The distance to the nearest pleura was measured between the nearest pleural surface and the edge of the tumor. Tumor location was defined as either the upper lobe or the middle or lower lobe. Total ablation time was the sum time of all RF applications. Maximum power was the peak power during all RF applications. The length of the aerated lung that was traversed by the electrode was measured from the pleural surface to the edge of the tumor along the electrode trajectory. When multiple electrode insertions were performed, the average length was used.
Statistical Analysis
Repeat ablation sessions were considered to be independent, and analyses were performed by using sessions as the sampling unit (224 sessions). Analyses were also performed by using patients as the sampling unit (142 sessions [first session for each of the 142 patients]). The results of these analyses are shown in the Appendix.
The sessions were divided into groups according to the occurrence of pneumothorax or pleural effusion. All of the sessions that were accompanied by pneumothorax were divided into groups according to the need for chest tube placement. Each factor was compared between groups by using a univariate analysis. Groups were defined as patients with or those without pneumothorax, patients with or those without pleural effusion, and patients with or those without chest tube placement for pneumothorax.
The variables that were evaluated included (a) patient and equipment factors, such as age, sex, the presence of pulmonary emphysema, history of pulmonary surgery, the number of tumors ablated, procedural patient positioning, and electrode type; (b) tumor factors, such as size, distance to the nearest pleura, and location; and (c) ablation factors, such as total ablation time, maximum power, and length of the aerated lung traversed by the electrode. Patient and equipment factors, except for patient positioning and electrode type, were analyzed for all ablation sessions (n = 224).
For the analysis of patient positioning, the 24 ablation sessions that were performed with patients in either the lateral decubitus position or a combination of the prone and supine positions were excluded. For the analysis of electrode type, the 15 ablation sessions that were performed with multiple electrodes (ie, the single internally cooled electrode and the multitined expandable electrode) were excluded. Tumor and ablation factors were analyzed for sessions during which a single tumor was ablated (n = 126) because, in sessions during which multiple tumors were ablated, it could not be determined which tumor or ablation procedure was responsible for the occurrence of pneumothorax and pleural effusion.
Univariate analyses were performed by using the Student t test or the Mann-Whitney U test for numerical values and by using the 2 test or the Fisher exact test for categorical values. Continuous value in the variables with a significant difference was categorized into discrete data. Categories were then compared, and odds ratios were calculated by using the category with the lowest risk as the reference. A P value less than .05 was considered to indicate a statistically significant difference for all analyses. Statistical analyses were performed by using a commercially available software program (SPSS, version 11.0; SPSS, Chicago, Ill).
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RESULTS |
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For the analyses in which the first 142 sessions were involved, different results were obtained. An internally cooled cluster electrode was not a significant risk factor (P = .091), although there still existed a tendency for patients who had undergone RF ablation with an internally cooled cluster electrode to have a higher risk of pleural effusion. Significant risk factors included larger tumor size, longer total ablation time, and higher maximum power (P = .006, .022, and .025, respectively; Table 4) (Appendix).
Chest Tube Placement for Pneumothorax
Of the 117 cases of pneumothorax, 24 (21%) necessitated chest tube placement (Table 1), which was correspondent to 11% (24 of 224 sessions) across all sessions. Of the 24 cases of pneumothorax that required chest tube placement, two required repeat pleurodesis to stop persistent air leakage. One patient underwent surgical repair of the perforated pleura to stop persistent air leakage despite repeat pleurodesis. The other cases resolved without any other intervention. For the analyses in which all 224 sessions were involved, the variables that increased the risk of chest tube placement were no history of pulmonary surgery (P = .002; odds ratio, infinitely higher for patients without a history of pulmonary surgery than for those with a history of pulmonary surgery), use of an internally cooled cluster electrode (P < .001; odds ratio, infinitely higher for internally cooled cluster electrodes than for multitined expandable electrodes), and involvement of the upper lobe (P < .001; odds ratio, 16.2 times higher for involvement of upper lobe than for involvement of middle or lower lobe) (Tables 1, 2).
For the analyses in which the first 142 sessions were involved, similar results were obtained (Appendix).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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No history of pulmonary surgery and an increased length of the aerated lung traversed by the electrode were risk factors for pneumothorax in our study, the results of which are in accordance with those obtained in studies on the risk factors for pneumothorax after lung biopsy (9–17). Previous surgery causes adhesion between the parietal and visceral pleura, and this adhesion works as interference for the occurrence of pneumothorax. Increased length of the aerated lung traversed by the electrode seems to suggest difficulty in maneuvering the electrode into the tumor, thereby requiring more pleural punctures, more redirections of the electrode, and longer procedural times. A greater number of tumors ablated seems to relate strongly to a greater number of pleural punctures, which significantly increases the rate of pneumothorax (15). Men tend to have greater vital capacity, which has been shown to be a risk factor for pneumothorax after lung biopsy (16). Greater vital capacity may allow greater respiratory movement of the lung. The middle or lower lobe may also be related to greater respiratory motion. Greater respiratory motion of the lung may increase the risk of pneumothorax by enlarging the pleural hole through the electrode. Male sex and involvement of the middle or lower lobe are not common risk factors after lung biopsy. In RF ablation, the variables related to respiratory motion may be more influential in the occurrence of pneumothorax because the electrode needs to dwell through the pleura during long RF applications.
Unlike lung biopsy, RF ablation involves not only the insertion of a needle but also the application of thermal energy. We had expected that thermal conduction to the pleura might somewhat affect the incidence or severity of pneumothorax because the ablated pleura might lose resilience and thus lose the ability to recoil or wrap the pleural hole. However, no variables relating to thermal conduction to the pleura, such as distance to the nearest pleura, maximum power, or total ablation time, were indicated as risk factors for pneumothorax or chest tube placement. Thus, pneumothorax after RF ablation of lung tumors is considered to be associated mainly with insertion of the electrode.
The cause of pleural effusion after RF ablation is generally expected to be pleurisy brought on by the heat conducted to the pleura. Our results seem to support this expectation. The distance to the nearest pleura is a substantial factor governing thermal conduction to the pleura. The length of the lung traversed by the electrode seems to be related to the distance to the nearest pleura. Regarding other factors concerning applied thermal energy, including total ablation time and maximum power, there was a tendency for longer total ablation time and higher maximum power in the group with pleural effusion, although these factors were not statistically significant in the analyses in which all sessions were involved. The use of an internally cooled cluster electrode was also a risk factor for pleural effusion. The construction of this electrode, which is a combination of three spaced electrodes, is suggested as a contributor. This electrode has a tendency to involve the pleura between the electrodes while being advanced through the pleura, and the involved pleura was likely ablated together with the tumor, possibly inducing pleurisy. However, pleural effusion was usually small in amount, asymptomatic, and thus clinically insignificant; massive pleural effusion that required chest tube placement was encountered after only three sessions.
Regarding chest tube placement for pneumothorax after RF ablation, no patients with a history of pulmonary surgery required chest tube placement. Induced pleural adhesion may be helpful in the prevention of pneumothorax enlargement. All four cases of pneumothorax that were induced by the internally cooled cluster electrode necessitated chest tube placement. This electrode creates three pleural holes at once and might tear the involved pleura while being advanced. Whereas tumor location in the middle or lower lobe was a risk factor for the occurrence of pneumothorax, tumor location in upper lobe was a risk factor for chest tube placement for pneumothorax. In the upper lobe, increased accumulation of aspirated air may cause alveolar expansion and thus elevate the alveolar to pleura pressure gradient while the patient is in an erect position, thereby allowing massive persistent air leakage through the pleural hole. In this regard, pleural "entry side down" patient positioning after the procedure might be helpful in the prevention of pneumothorax enlargement, as previously shown (12,18).
There are limitations to this study. Analysis of tumor factors and ablation factors was confined to sessions during which a single tumor was ablated. Therefore, the group with pleural effusion and chest tube placement for pneumothorax was small for these analyses. The number of pleural punctures was not recorded in all procedure records and thus was not analyzed, although it might be an important risk factor for pneumothorax (15). The presence of pulmonary emphysema was not indicated as a risk factor for pneumothorax in our study. However, this result was obtained from an analysis in which the severity of pulmonary emphysema was not graded. Severe pulmonary emphysema might increase the risk of pneumothorax. Multiple testing for multiple variables is necessarily associated with an inflated type I error rate. Despite this issue, the variables with a high odds ratio likely represent risk factors, and attention should be given to the patients with such variables.
In conclusion, pneumothorax and pleural effusion are frequently encountered after RF ablation of lung tumors. Performing RF ablation should not, however, be avoided just because of such risks, which require treatment only in limited cases and are not fatal. Attention should be given to the patients with the following risk factors, which for pneumothorax include male sex, no history of pulmonary surgery, a greater number of tumors ablated, involvement of the middle or lower lobe, and increased length of the aerated lung traversed by the electrode and for pleural effusion include decreased distance to the nearest pleura, decreased length of the aerated lung traversed by the electrode, and use of an internally cooled cluster electrode. In particular, patients will have a higher risk of chest tube placement if they experience pneumothorax with no previous history of pulmonary surgery, if they have a tumor in the upper lobe, or if they undergo ablation with an internally cooled cluster electrode.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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ADVANCES IN KNOWLEDGE |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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FOOTNOTES |
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Abbreviations: RF = radiofrequency
Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, T.H.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, T.H., N.T., H.M., H.G., T.M., H.F., T.I., Y.S., N.S., S.K.; clinical studies, all authors; statistical analysis, T.H.; and manuscript editing, T.H., N.T., H.M., K.Y., H.G., T.M., S.K.
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References |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXADVANCES IN KNOWLEDGEReferences |
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This article has been cited by other articles:
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  J. C. Zhu, T. D. Yan, and D. L. Morris A Systematic Review of Radiofrequency Ablation for Lung Tumors Ann. Surg. Oncol., June 1, 2008; 15(6): 1765 - 1774. [Abstract] [Full Text] [PDF]
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 N. A. Durick, P. F. Laeseke, L. S. Broderick, F. T. Lee Jr, L. A. Sampson, T. M. Frey, T. F. Warner, J. P. Fine, D. W. van der Weide, and C. L. Brace Microwave Ablation with Triaxial Antennas Tuned for Lung: Results in an in Vivo Porcine Model Radiology, April 1, 2008; 247(1): 80 - 87. [Abstract] [Full Text] [PDF]
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 C. J.A. Haasbeek, S. Senan, E. F. Smit, M. A. Paul, B. J. Slotman, and F. J. Lagerwaard Critical Review of Nonsurgical Treatment Options for Stage I Non-Small Cell Lung Cancer Oncologist, March 1, 2008; 13(3): 309 - 319. [Abstract] [Full Text] [PDF]
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 T. Hiraki, H. Gobara, T. Iishi, Y. Sano, T. Iguchi, H. Fujiwara, N. Tajiri, J. Sakurai, H. Date, H. Mimura, et al. Percutaneous radiofrequency ablation for clinical stage I non-small cell lung cancer: results in 20 nonsurgical candidates. J. Thorac. Cardiovasc. Surg., November 1, 2007; 134(5): 1306 - 1312. [Abstract] [Full Text] [PDF]
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