DOI: 10.1148/radiol.2433060157
(Radiology 2007;243:877-884.)
© RSNA, 2007
Vascular and Interventional Radiology |
Percutaneous Radiofrequency Ablation of Hepatic Tumors against the Diaphragm: Frequency of Diaphragmatic Injury1
Hayden W. Head, MD,
Gerald D. Dodd, III, MD,
Neal C. Dalrymple, MD,
Srinivas R. Prasad, MD,
Fadi M. El-Merhi, MD,
Michael W. Freckleton, MD, and
Linda G. Hubbard, RN
1 From the Department of Radiology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, Mail Code 7800, San Antonio, TX 78229. From the 2003 RSNA Annual Meeting. Received January 26, 2006; revision requested March 27; revision received June 29; accepted August 2; final version accepted October 4.
Address correspondence to H.W.H. (e-mail: headh{at}uthscsa.edu).
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ABSTRACT
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Purpose: To retrospectively determine the frequency of diaphragmatic injury when percutaneous hepatic radiofrequency (RF) ablation is performed adjacent to the diaphragm.
Materials and Methods: Institutional Review Board approval was obtained for our HIPAA-compliant study. Informed consent for the ablation procedure and for use of related data for future research was obtained from each patient. A retrospective review was conducted of 215 patients undergoing percutaneous RF ablation of hepatic tumors. Twenty-nine patients (21 men and eight women; age, 41–89 years) were identified with tumors abutting the diaphragm. Episodes of right shoulder pain were recorded. A panel of radiologists blinded to the patients' clinical histories reviewed their imaging for evidence of diaphragmatic injury and ablation success. A generalized estimating equation model and the Fisher exact test were used for statistical analysis.
Results: The 29 patients had a total of 33 tumors abutting the diaphragm. Tumor size was 1.3–5.5 cm (mean, 3.2 cm ± 1.1). After ablation, five (17%) patients reported right shoulder pain. In four, pain was mild or moderate, with symptoms lasting 2–14 days (median, 5.5 days). Three of these showed diaphragmatic thickening on postablation computed tomographic (CT) scans. One patient had severe pain lasting 2 weeks, followed by milder pain for 2 months. This patient's postablation CT images showed focal nodular diaphragmatic thickening. This patient was treated with a multitined device; the other four, with straight-needle devices. Local tumor progression was seen in 14 tumors (42.4%). Tumors 3 cm or smaller had a much lower local progression rate than tumors larger than 3 cm (12.5% vs 70.6%).
Conclusion: Of 29 patients who had ablation of hepatic tumors adjacent to the diaphragm, five (17%) had diaphragmatic injury, which was clinically apparent with right shoulder pain.
© RSNA, 2007
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INTRODUCTION
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Radiofrequency (RF) ablation is the most widely used thermal ablation technique for minimally invasive therapy of hepatic tumors. Benefits include low morbidity, few complications, outpatient use, and repeatability for recurrence. Numerous studies have established the effectiveness of RF ablation in treating primary and metastatic hepatic tumors. Two recent studies reported the complication rate as approximately 2%–6% for major complications and 5%–36% for minor complications, depending on how complications were defined (1,2). A recent article designed to standardize terminology and reporting criteria in tumor ablation distinguished between major complications, minor complications, and side effects (3). Major complications are those that if untreated might lead to death, substantial morbidity and disability, or a lengthened hospital stay; all other complications are called minor. Side effects are expected but undesired consequences of the procedure, including pain, that although occurring frequently, rarely if ever result in substantial morbidity. Side effects are not true complications because they do not lead to an unexpected increase in level of care.
A pervasive idea among practitioners and equipment vendors is that RF ablation of tumors adjacent to the diaphragm poses a substantial risk of diaphragmatic injury. Consequently, some have concluded that RF ablation adjacent to the diaphragm is contraindicated or that special interventional techniques are necessary to separate the diaphragm from the liver (4–6). Although this thinking is supported by human and animal studies (7–21), to our knowledge no human studies have addressed the frequency of diaphragmatic injury after RF ablation. We have treated a number of tumors abutting the diaphragm. Thus, the purpose of our study was to retrospectively determine the frequency of diaphragmatic injury when percutaneous hepatic RF ablation is performed adjacent to the diaphragm.
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MATERIALS AND METHODS
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Institutional Review Board approval was obtained for our Health Insurance Portability and Accountability Act–compliant study. Informed consent for the ablation procedure and use of related data for future research was obtained from each patient before the procedure.
Patients
Between June 1996 and September 2003, we performed percutaneous RF ablation on hepatic tumors in 215 patients. A corresponding database of patient information was compiled, including data on imaging performed before and after ablation procedures (with all follow-up imaging) and all medical records pertaining to the work-up, ablation procedure, periprocedural course, and follow-up of every ablation patient. One author (H.W.H.) searched this database to identify patients with tumors in the upper half of the liver. Of the patients identified, this author reviewed preablation computed tomography (CT) or magnetic resonance (MR) images to include only patients with tumors in direct contact with the diaphragm, then reviewed the corresponding medical records to identify any instances of right shoulder pain. Severity and duration of pain were recorded, and the type of electrode used was noted. Patients' medical records were also reviewed for tumor type, tumor size, tumor location by Couinaud segment, number of tumors that were reablated, number of ablation sessions, number of ablations per session, and complications. We identified 29 patients (21 men and eight women; mean age at time of first ablation, 60.4 years ± 12.1; range, 41–89 years).
Radiofrequency Ablation Systems
Two main RF systems were used. A model 500 50-W generator with a model 30 3-cm multitined expandable electrode (RITA Medical Systems, Mountain View, Calif) was used from 1996 to 1999. A model CC-1 200-W generator with various internally cooled single and cluster straight-needle electrodes (Valleylab, Boulder, Colo) was used from 1999 to 2003. A single procedure in 2002 utilized a model 1500 150-W generator with a StarBurst XLi 2.5-cm multitined expandable electrode (RITA Medical Systems). All ablations included in this study were performed percutaneously with ultrasonographic (US) guidance and employed the manufacturers' recommended energy deposition algorithms. Aseptic technique was observed.
Ablation Procedure
The aim of RF ablation was complete destruction of the tumor and to achieve ablation of a 5–10-mm circumferential cuff of adjacent normal hepatic parenchyma. All RF ablation was performed after patients fasted overnight. Conscious sedation and local anesthesia were used every time. All procedures were performed by one of the authors (G.D.D., 9 years experience with interventional procedures).
Over the course of our 7-year experience with RF ablation, we modified our technique for ablating tumors adjacent to the diaphragm. After the electrode is positioned in the tumor and the ablation cycle is started, the patient is monitored during the procedure for right shoulder pain. If any is experienced, the needle is pulled back 1–2 mm. If pain persists, additional withdrawals of the needle are carried out in 1–2 mm increments until the patient experiences minimal or no pain. This technique has been used since 1999, coinciding with our conversion to straight-needle electrodes.
All patients underwent ablation as outpatients and were observed for complications for 4–6 hours afterward. No antibiotics were administered before or after ablation. A three-phase CT scan (see below) was routinely performed immediately after ablation for three reasons: to assess completeness of ablation, to obtain a baseline image of the ablation zone, and to detect any immediate complications. All patients were followed-up by means of telephone by a designated clinical research nurse (since 1998, L.G.H.; previously, two nurses who are not authors) for 1 week or until remission of symptoms. All symptoms during the recovery and follow-up periods, including any focal pain and location of pain (including right shoulder pain), were documented. The patients were asked to rate their shoulder pain on a scale of mild, moderate, or severe.
Imaging
Our standard imaging protocol for patient assessment and follow-up begins with CT or MR of the abdomen either at our hospitals or at an outside institution within at least 1 month before the ablation procedure. We then perform targeted US to confirm that tumors identified at cross-sectional imaging are feasible for US-guided ablation; tumors not identifiable at US may be deferred for intraoperative or CT-guided ablation. Immediately after ablation, we performed a three-phase CT scan. Repeat CT scans are then performed every 3 months to monitor for tumor progression. CT scans were obtained on helical scanners with intravenous contrast material enhancement (at our hospitals, LightSpeed or HiSpeed Advantage, GE Healthcare, Milwaukee, Wis; and previously, Picker PQ or PQ5000, Picker International, Highland Heights, Ohio). All scans obtained at outside facilities were judged adequate for planning patient care and for evaluation of follow-up in this study.
Our standardized three-phase CT scan protocol was used in this study. Unenhanced and dual-phase contrast material–enhanced CT images of the entire liver were obtained in a craniocaudal direction. Unenhanced images were obtained as contiguous transverse scans. Arterial and portal venous phase contrast-enhanced CT scans were obtained in helical mode at 25 and 65 seconds, respectively, after starting power injection of 130 mL nonionic intravenous contrast material (ioversol 68%, Optiray 320, Mallinckrodt, St. Louis, Mo) at 3–5 mL/sec. All scans were obtained by using 7- or 8-mm collimation, 220 mA, and 120 kVp. The pitch (1.0–1.5) was adjusted to allow a single helical acquisition through the entire liver in each scan phase. Hard copies of scans were available for all patients.
Image Interpretation
Four board-certified abdominal radiologists (M.W.F., N.C.D., S.R.P., and F.M.E., with 11, 8, 7, and 4 years of experience, respectively, in interpreting abdominal CT and MR images) reviewed all images of the 29 study patients (Fig 1). At least two of the four readers were present at each interpretation session. If two readers disagreed, the images were reviewed by another reader, and the final opinion was achieved by majority rule. Readers were unaware of the patients' degree of shoulder pain and their clinical course after the procedure.
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Figure 1a: Transverse CT scans in 58-year-old man treated with RF ablation for nodular HCC in Couinaud segment VII abutting dome of the diaphragm. (a) Before ablation, arterial enhancing tumor (arrowhead) is seen. (b) After ablation, tumor with hyperemic rim and no adjacent diaphragmatic thickening is seen.
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Figure 1b: Transverse CT scans in 58-year-old man treated with RF ablation for nodular HCC in Couinaud segment VII abutting dome of the diaphragm. (a) Before ablation, arterial enhancing tumor (arrowhead) is seen. (b) After ablation, tumor with hyperemic rim and no adjacent diaphragmatic thickening is seen.
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The preablation CT or MR images were reviewed in all cases. The purpose of this was twofold: to confirm that the index tumor was in contact with the liver capsule and to establish a baseline for follow-up examinations. The review of postablation studies included all follow-up CT scans until the index tumor showed local progression or, in the case of stable findings, until the patient's most recent imaging.
Each postablation study was evaluated for six findings adjacent to the ablation zone that might indicate diaphragmatic injury, including disruption of the diaphragm, diaphragmatic thickening, soft tissue stranding, adjacent fluid collection, new pleural effusion, or pathologic changes in the lung bases. Presence or absence of diaphragmatic thickening was determined with visual judgment by the four readers, with comparison to previous and subsequent studies. The morphology of the thickening was characterized as to whether it was diffuse or focal, smooth or nodular, or otherwise. Presence of ascites and any other notable finding was recorded. Finally, any evidence of local tumor progression (ie, local failure of therapy) was also recorded. Signs of local tumor progression included foci of contrast enhancement in or at the periphery of the ablated area, any increase in tumor size after ablation, or development of indistinct margins of the ablation zone (22). Complete ablation after a session was defined as no residual unablated enhancing tumor on CT, excluding benign periablational enhancement.
Statistical Analysis
Descriptive statistics of each imaging finding were compiled and compared with patients' postablation symptoms, if any. The range, mean, and standard deviation of the maximum diameter of the tumors were calculated. A generalized estimating equation (GEE) model was applied to identify multiple risk factors for local tumor progression, and to control for possible correlation and/or data clustering effects in patients who had more than one tumor ablated. Maximum diameter and number of ablation sessions were used to predict outcome. If a factor was significant for the GEE model, a threshold value was selected in order to analyze the risk of tumor progression by the Fisher exact test. For all statistical tests, P < .05 was considered to indicate a significant difference. Statistical analysis was performed with SAS (version 9.1.3; SAS Institute, Cary, NC).
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RESULTS
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The 29 patients had a total of 33 tumors abutting the diaphragm. Sixteen patients had 18 nodules of hepatocellular carcinoma, and 13 patients had a total of 15 hepatic metastases: 10 from colorectal carcinoma, two from breast carcinoma, one from pancreatic carcinoma, one from ovarian carcinoma, and one from adenocarcinoma of unknown primary tumor. Tumor size ranged from 1.3 to 5.5 cm in maximum diameter (mean, 3.2 cm ± 1.1). Sixteen tumors were 3 cm or smaller in maximum diameter; 17 were larger than 3 cm. Nineteen tumors were located in Couinaud segment VII, eight in segment VIII, four in segment IVa, and two spanned segments VII and VIII. Repeat ablation was performed when possible in tumors that showed residual unablated tumor initially or local tumor progression later (12 reablated tumors). In total, RF ablations were performed during 53 sessions in the 29 patients. The number of ablations performed at each session ranged from one to eight (median, two ablations), with larger tumors requiring more ablations.
Symptoms after Ablation
Five (17%) patients reported right shoulder pain in the postablation period. On a scale of mild, moderate, or severe, four described the pain as mild or moderate. Only one had severe pain. In the four with mild or moderate pain, the duration ranged between 2 and 14 days (median, 5.5 days). In the patient with severe pain, the duration was 2 weeks, followed by milder chronic pain for 2 months. The patient with severe pain was treated with a multitined device. The four patients with mild to moderate pain were treated with straight-needle devices.
Imaging Findings
Preablation.—One patient had mild thickening of the diaphragm on the side of his hepatic tumor, which may have been secondary to a previous partial right lobectomy for hepatocellular carcinoma 2 years earlier. No other patients had abnormalities of the diaphragm on preablation CT scans.
Postablation.—Overall, new diaphragmatic thickening was seen adjacent to 18 of 33 ablation sites in 16 patients on postablation CT scans. This thickening was smooth in 17 instances, and nodular in one. In 11 instances, diaphragmatic thickening resolved during the reviewed follow-up (range, 4–43 months; median, 13 months). In seven patients, there was persistent diaphragmatic thickening at the end of the review period (range, 3–34 months; median, 5 months); in two of these patients, there had been recent repeat ablation of the same area. In the four patients with mild to moderate shoulder pain after ablation, postablation CT scans showed smooth diaphragmatic thickening adjacent to the ablation site in three (Fig 2). In the patient with severe right shoulder pain after ablation, postablation CT scans showed diaphragmatic thickening that was more focal and nodular than in the other patients (Fig 3), consistent with a diaphragmatic burn adjacent to the ablation site. This nodular thickening resolved as the patient's symptoms subsided.
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Figure 2a: RF ablation of tumor against diaphragm with subsequent smooth diaphragmatic thickening. (a) Transverse CT scan obtained before reablation for locally progressive metastatic tumor. (b) Transverse CT scan obtained immediately after ablation shows smooth diaphragmatic thickening adjacent to the ablation zone (arrowhead).
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Figure 2b: RF ablation of tumor against diaphragm with subsequent smooth diaphragmatic thickening. (a) Transverse CT scan obtained before reablation for locally progressive metastatic tumor. (b) Transverse CT scan obtained immediately after ablation shows smooth diaphragmatic thickening adjacent to the ablation zone (arrowhead).
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Figure 3a: Transverse CT scans in 52-year-old man after RF ablation for metastasis to liver abutting the diaphragm. (a) At 1 day after ablation, adjacent diaphragmatic thickening is seen. (b) At 1 month after ablation, focal nodular diaphragmatic thickening (arrowhead) is seen. (c) At 11 months after ablation, minimal remaining diaphragmatic thickening can be seen.
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Figure 3b: Transverse CT scans in 52-year-old man after RF ablation for metastasis to liver abutting the diaphragm. (a) At 1 day after ablation, adjacent diaphragmatic thickening is seen. (b) At 1 month after ablation, focal nodular diaphragmatic thickening (arrowhead) is seen. (c) At 11 months after ablation, minimal remaining diaphragmatic thickening can be seen.
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Figure 3c: Transverse CT scans in 52-year-old man after RF ablation for metastasis to liver abutting the diaphragm. (a) At 1 day after ablation, adjacent diaphragmatic thickening is seen. (b) At 1 month after ablation, focal nodular diaphragmatic thickening (arrowhead) is seen. (c) At 11 months after ablation, minimal remaining diaphragmatic thickening can be seen.
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Diaphragmatic thickening was the most common imaging finding that may be related to involvement of the diaphragm by RF ablation (Table). A localized fluid collection adjacent to the ablation site was the second most common, seen in 12 patients. In addition, five patients had new or increased generalized ascites after ablation, but the relevance of this finding vis-à-vis recent ablation is uncertain.
In addition to one diaphragmatic burn, two other major complications were encountered in this series. An arteriovenous fistula developed along the needle tract in one patient, and portal vein thrombosis, which resolved without treatment, occurred in another. Also, two minor complications were seen: a small hemorrhage seen with Doppler US that showed no active bleeding on subsequent angiography, and a small perihepatic hematoma that resolved spontaneously. In addition, one case of intrahepatic tumor seeding was suspected.
Completeness of ablation and follow-up.—Ablation was considered complete after one session in 27 of 33 (81.8%) tumors. No unablated disease remained after two ablation sessions in four tumors (12.1%) and after three sessions in one tumor. One tumor never showed complete ablation despite eight sessions. The follow-up times per tumor ranged from 3 to 44 months (median, 9 months). Eight patients were followed up for fewer than 6 months, but five of these patients showed local tumor progression. In total, local tumor progression was seen in 13 tumors. Thus, the local treatment failure rate (14 of 33 tumors) was 42.4%. Maximum diameter (P = .0059) was a significant predictor of progression, while number of sessions (P = .1002) was not (GEE model). On the basis of this analysis, we selected a threshold value for maximum diameter of 3.0 cm. This value has also been used in previous studies that showed a difference between local progression rates for tumors 3.0 cm or smaller versus those 3.0 cm or larger (23,24). Of 16 tumors 3.0 cm or smaller, two (12.5%) showed local progression, whereas 12 of 17 (70.6%) tumors 3.0 cm or larger showed local progression or could not be ablated completely (P = .0013, Fisher exact test). With regard to correlation and/or data clustering effects, local tumor progression occurred in three of four (75%) patients with two tumors compared to 10 of 25 (40%) patients with one tumor, but this result was not significant (P = .299, Fisher exact test) owing to the small sample size.
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DISCUSSION
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A previous review of the literature on RF ablation of the liver found that of 3670 reported ablations, there were six instances of diaphragmatic injury (7). Notably, there have been three reported fatalities involving diaphragmatic complications of RF ablation. Two of these were included in the review, and one has been reported since. One of these was a thermal injury to the diaphragm from percutaneous RF ablation leading to hepatic abscess, sepsis, and multiorgan failure (8). The second was a fatal bile leak into the chest (bronchobiliary fistula) after diaphragmatic perforation (9). The third was a case of hemorrhagic cardiac tamponade after ablation adjacent to the diaphragm and heart (10). The review also included four of the following complications (the rest of which have been reported since): three perforations of the diaphragm, associated with delayed intrathoracic hernia, abscess extending into the thorax, and nonfatal but nonresolving bronchobiliary fistula, respectively; three diaphragmatic burns with prolonged postprocedural pain and diaphragmatic thickening at CT; two instances of paralysis of the diaphragm; and one pulmonary hemorrhage not associated with perforation (11–20). Additionally, authors of an animal study suggested that RF ablation frequently leads to diaphragmatic injury: Raman et al (21) ablated porcine liver in vivo and found histopathologic evidence of diaphragmatic damage near ablation sites.
Based on this evidence, specific interventional procedures have been developed to separate the diaphragm from the liver surface by means of subphrenic peritoneal saline injection, and by means of carbon dioxide insufflation (4–6). Additionally, one manufacturer has introduced a specially designed electrode for RF ablation of tumors adjacent to the diaphragm or other critical structures (25). Another prevalent idea is that hepatic tumors near the diaphragmatic dome are too difficult to visualize with US to approach percutaneously. Several strategies have been devised to address this scenario, including artificial pleural effusion to increase nodule conspicuity, as well as thorascopic, percutaneous, and intraoperative approaches for transdiaphragmatic puncture and ablation (26–35).
Our results provide evidence that RF ablation adjacent to the diaphragm can be performed safely. Of 29 patients with 33 tumors abutting the diaphragm, only five patients developed postprocedural pain, which was mild or moderate and rapidly self-resolving in four, and severe and protracted in one. The patient who developed severe and long-lasting pain was the only one treated with a multitined expandable electrode; the others were treated with straight-needle electrodes. We have previously reported this complication (11,12). We believe this complication represented a direct ablation of the diaphragm—a diaphragmatic burn, evidenced by focal, nodular diaphragmatic thickening on follow-up CT scan. It is likely that one of the needle tines was embedded in the diaphragm at deployment and thus caused direct heating. This is the same mechanism postulated by Koda et al (16) in their case report of diaphragmatic perforation and hernia after hepatic RF ablation. A probable contributing factor in these cases is the inability to confirm the position of the retractable curved tines of a multitined electrode by using US.
An advantage of the straight-needle electrode is greater visibility of the active tip compared with the tines of an expandable electrode. Perhaps equally as important, during the ablation procedure the straight-needle electrode is readily drawn back if the patient experiences pain referred from the diaphragm. Such a maneuver with an expandable array is cumbersome and imprecise, requiring retraction of the tines and leading to an undesirably smaller ablation. However, it must be noted that straight-needle, internally cooled electrodes have been associated with a number of reported complications involving the diaphragm as well (13–15,17–20), including at least one fatality (9). Therefore, intraprocedural monitoring of the patient under conscious sedation for shoulder pain is a safety measure for ablation adjacent to the diaphragm. General anesthesia, by contrast, eliminates the feedback mechanism provided by the patient's symptoms and can mask a developing diaphragmatic burn. Using this method, we have performed large-volume ablations against the diaphragm, after which the patient did not experience symptoms referable to diaphragmatic injury.
In addition to demonstrating its safety, we have provided evidence that the effectiveness of RF ablation in treating hepatic tumors adjacent to the diaphragm can approach the effectiveness achieved with ablation of hepatic tumors in general. We found a strong association between tumor size and local progression, which is in keeping with the trends seen in larger series. The success of our study for complete ablation of tumors 3 cm or smaller in maximum diameter is near that of Livraghi et al (23,24), but our success rate for complete ablation of tumors larger than 3 cm was markedly lower (87.5% vs 90%, and 29.4% vs 47.6%, respectively). Confounding factors contributing to this discrepancy include our use of a different, now-discontinued RF ablation device prior to 1999 and our relatively small sample size. The findings of Poon et al (36), however, support the effectiveness of RF ablation adjacent to the liver capsule, with a local tumor progression rate of 4.3% in subcapsular hepatocellular carcinoma versus 12.5% in nonsubcapsular hepatocellular carcinoma, irrespective of tumor size.
Our study was limited by its retrospective nature. Also, our findings were not based on pathologic proof. Thermal injury to the diaphragm is inferred from symptomatology and imaging appearances. Finally, some of the follow-up times were short. Eight patients were followed-up for fewer than 6 months. However, an acceptable endpoint was reached in five of these cases, as these showed local tumor progression.
In conclusion, in 29 patients who underwent ablation of hepatic tumors adjacent to the diaphragm, common imaging findings included postprocedural diaphragmatic thickening in 16 (55%) patients and localized fluid collection adjacent to the ablation site in 12 (41%); clinically, however, only five (17%) patients had diaphragmatic injury, apparent because of right shoulder pain.
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ADVANCES IN KNOWLEDGE
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- After ablation of hepatic tumors adjacent to the diaphragm, imaging findings frequently include postprocedural diaphragmatic thickening and localized fluid collection adjacent to the ablation site, in 16 (55.2%) and 12 (41.4%) patients, respectively.
- Clinically, however, only five (17%) patients had diaphragmatic injury, apparent because of right shoulder pain.
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ACKNOWLEDGMENTS
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The authors thank John Schoolfield, MS, for statistical analysis, and Alison Ott Head, BJ, for graphics preparation.
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FOOTNOTES
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Abbreviations: GEE = generalized estimating equation • RF = radiofrequency
Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, H.W.H., G.D.D.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, H.W.H.; clinical studies, all authors; statistical analysis, H.W.H.; and manuscript editing, H.W.H., G.D.D.
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INTRODUCTION
