Major Complications after Radio-frequency Thermal Ablation of Hepatic Tumors: Spectrum of Imaging Findings 1

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1 EDUCATION EXHIBIT 123 Major Complications after Radio-frequency Thermal Ablation of Hepatic Tumors: Spectrum of Imaging Findings 1 ONLINE-ONLY CME See /rg_cme.html. LEARNING OBJECTIVES After reading this article and taking the test, the reader will be able to: Recognize the imaging features of major complications that occur after RF ablation of hepatic tumors. Discuss the importance of early detection and proper management of major complications after RF ablation of hepatic tumors. List the risk factors for the complications encountered after RF ablation of hepatic tumors. Hyunchul Rhim, MD Kwon-Ha Yoon, MD Jeong Min Lee, MD Yoonkoo Cho, MD June-Sik Cho, MD Seung Hoon Kim, MD Won-Jae Lee, MD Hyo Keun Lim, MD Gyoung-Jin Nam, MD Sang-Suk Han, MD Yun Hwan Kim, MD Cheol Min Park, MD Pyo Nyun Kim, MD Jae-Young Byun, MD Although radio-frequency (RF) ablation has been accepted as a promising and safe technique for treatment of unresectable hepatic tumors, investigation of its complications has been limited. According to the multicenter (1,139 patients in 11 institutions) survey data of the Korean Study Group of Radiofrequency Ablation, a spectrum of complications occurred after RF ablation of hepatic tumors. The prevalence of major complications was 2.43%. The most common complications were hepatic abscess (0.66%), peritoneal hemorrhage (0.46%), biloma (0.20%), ground pad burn (0.20%), pneumothorax (0.20%), and vasovagal reflex (0.13%). Other complications were biliary stricture, diaphragmatic injury, gastric ulcer, hemothorax, hepatic failure, hepatic infarction, renal infarction, sepsis, and transient ischemic attack. One procedure-related death (0.09%) occurred (due to peritoneal hemorrhage). Three important strategies for decreasing the rate of complications are prevention, early detection, and proper management. A physician who performs RF ablation of hepatic malignancies should be aware of the broad spectrum of major complications so that these strategies can be used. RSNA, 2003 Abbreviation: RF radio-frequency Index terms: Interventional procedures, complications, Liver, interventional procedures, Liver neoplasms, therapy, , Radiofrequency (RF) ablation, ; 23: Published online /rg From the Korean Study Group of Radiofrequency Ablation (H.R., K.H.Y., J.M.L., Y.C., J.S.C., S.H.K., W.J.L., H.K.L., G.J.N., S.S.H., Y.H.K., C.M.P., P.N.K., J.Y.B.); the Department of Diagnostic Radiology, Hanyang University Hospital, 17 Haengdang-Dong, Sungdong-Ku, Seoul , Korea (H.R.); the Department of Radiology, Wonkwang University Hospital, Iksan, Korea (K.H.Y.); the Department of Diagnostic Radiology, Chunbuk University Hospital, Jeonju, Korea (J.M.L.); the Department of Diagnostic Radiology, Korean Veterans Hospital, Seoul (Y.C.); the Department of Diagnostic Radiology, Chungnam University Hospital, Daejon, Korea (J.S.C.); the Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea (S.H.K., W.J.L., H.K.L.); the Department of Diagnostic Radiology, Dong-A University Hospital, Busan, Korea (G.J.N.); the Department of Diagnostic Radiology, Inje University Busan Paik Hospital, Busan, Korea (S.S.H.); the Department of Diagnostic Radiology, Korea University Hospital, Seoul (Y.H.K., C.M.P.); the Department of Diagnostic Radiology, Asan Medical Center, Seoul, Korea (P.N.K.); and the Department of Diagnostic Radiology, Catholic University Hospital of Korea, Seoul (J.Y.B.). Recipient of a Cum Laude award for an education exhibit at the 2001 RSNA scientific assembly. Received March 12, 2002; revision requested April 29 and received June 20; accepted June 21. Address correspondence to H.R. ( rhimhc@hanyang.ac.kr). RSNA, 2003 See the commentary by Razavi following this article.

2 124 January-February 2003 RG f Volume 23 Number 1 Introduction Despite having excellent therapeutic effect, any interventional procedure should be performed only after it has been proved safe with minimal morbidity and mortality. Although radio-frequency (RF) thermal ablation has been accepted as a promising technique for treating unresectable hepatic tumors (1 17), there have been few systematic analyses of complications in large series (18 25). Early detection and proper management of complications are possible only if the physician performing RF ablation understands the broad spectrum of complications encountered after ablation. Furthermore, knowledge about such complications enables the operator to minimize complications after ablation as well as exclude highrisk patients during preablation assessment. The purpose of this article is to present the various imaging features of complications that occur after RF ablation of hepatic tumors according to the survey data of the Korean Study Group of Radiofrequency Ablation. Representative cases of each complication as well as technical tips for avoiding the complication are presented. Materials and Methods In May 2001, the Korean Study Group of Radiofrequency Ablation surveyed 11 institutions about the major complications that occurred after RF ablation of hepatic tumors. A major complication was defined as any symptom that developed after RF ablation and persisted for more than 1 week or required any type of management. Thus, transient postablation syndrome including mild and transient pain and fever was excluded from the survey. Answers to the detailed questionnaire about the complications after RF ablation were collected. The questions were divided into two categories: basic information and information related to complications. Basic information included date of RF ablation of the first patient, total number of patients, total number of ablation sessions, total number of ablated tumors, guidance modality, inclusion and exclusion criteria, and anesthesia method. Information related to each complication included age and sex of the patient, tumor type, maximum diameter and number of tumors, date of the procedure, date the complication was identified, modality used to diagnose the complication, RF equipment used, procedure time, anesthesia method, guidance modality, method of approach (percutaneous vs open), management of the complication, final result of the complication, and lessons learned from the complication. The types of lesions treated and the numbers and characteristics of the complications attributed to the procedure were evaluated. Inclusion criteria for RF ablation in the survey were as follows: single tumor smaller than 5 cm in maximum diameter; multiple tumors (up to four) with each 3 cm in maximum diameter or smaller; absence of portal venous thrombosis or extrahepatic metastases; Child-Pugh class A or B liver cirrhosis; prothrombin time ratio greater than 50%; and platelet count greater than 70,000/ L ( /L). A total of 1,520 RF ablation procedures in 1,139 patients with 1,663 hepatic tumors (1,303 hepatocellular carcinomas and 360 metastases) were included in the survey. The equipment used for RF ablation was as follows: Five institutions used equipment from RITA Medical Systems (Mountain View, Calif), four used equipment from Radiotherapeutics (Mountain View, Calif), and two used equipment from Radionics (Burlington, Mass). All procedures were performed percutaneously under ultrasonographic (US) or computed tomographic (CT) guidance on an inpatient basis. The spectrum of major complications including prevalence and prognosis is reported with representative cases. Statistical analysis was performed with the Student t test (P.05). Results Thirty-seven major complications (2.43%) were encountered (Fig 1): 10 hepatic abscesses (0.66%), seven peritoneal hemorrhages (0.46%), three bilomas (0.20%), three ground pad burns (0.20%), three pneumothoraces (0.20%), two vasovagal reflexes (0.13%), one biliary stricture (0.07%), one diaphragmatic injury, one gastric ulcer, one hemothorax, one case of hepatic failure, one hepatic infarction, one renal infarction, one case of sepsis, and one transient ischemic attack. One procedure-related death (0.09%) occurred (due to a peritoneal hemorrhage). The prevalence of complications was 1.8% in the hepatocellular carcinoma group and 5.2% in the metastasis group (P.05).

3 RG f Volume 23 Number 1 Rhim et al 125 Figure 1. Broad spectrum of major complications after RF ablation for hepatic tumors according to the survey data of the Korean Study Group of Radiofrequency Ablation. One procedure-related death occurred (due to peritoneal hemorrhage). Abscess An abscess is one of the most common major complications encountered after RF ablation. Diagnosis of an abscess can sometimes be delayed because fever after RF ablation is a frequent symptom of not only hepatic abscess but also of postablation syndrome. Fever is the second most common symptom of postablation syndrome. The prevalence of postablation fever was reported as 19% 34%, with a duration of 1 9 days (22,23). Therefore, if a fever lasts for over 2 weeks, the possibility of abscess formation should be considered. The reported prevalence of hepatic abscesses in our survey (0.66%) was similar to that after transarterial oily chemoembolization (0% 1.4%) (26). Although the mechanism of abscess development after RF ablation is still not established, subsequent bacterial contamination of the ablated hepatic parenchyma may lead to abscess formation. Therefore, a colonized biliary tract (eg, bilioenteric anastomosis, endoscopic papillotomy, bilioenteric fistula, external biliary drainage, and pneumobilia of unknown origin) or an immunocompromising condition such as diabetes can be important risk factors for abscess or sepsis after RF ablation as well as after transarterial oily chemoembolization (26,27). Thus, an operator should keep in mind the risk factors for abscess formation as well as the importance of an aseptic technique during the whole procedure. Prophylactic use of antibiotics may be beneficial for patients with a high risk of infection. Early detection will be possible only if the operator is alert to the presence of prolonged fever after the ablation and close clinical follow-up of the patient with risk factors is performed. The imaging appearance of abscesses that develop after RF ablation is very similar to that of usual hepatic abscesses (Fig 2). New gas bubbles not previously seen could signal an infection, although minimal air bubbles within the ablated area can often be seen at CT performed immediately after ablation. These minimal amounts of air within the ablated area at immediately performed CT are aggregated microbubbles produced during the ablation and usually resolve within 1 month (28). Thus, such microbubbles seen at immediate follow-up CT should not be misdiagnosed as an abscess, especially if the patient demonstrates postablation syndrome.

4 126 January-February 2003 RG f Volume 23 Number 1 Figure 2. Hepatic abscess in a 55-year-old man with hepatocellular carcinoma. (a) Contrast material enhanced CT scan obtained before RF ablation shows a 1.5-cm-diameter hyperattenuating nodule of hepatocellular carcinoma (arrow) in segment VI. The patient was readmitted due to abrupt development of a fever 1 week after ablation. (b) One-week follow-up CT scan shows a gas-forming abscess (arrow) in the ablated area with a perihepatic fluid collection. The abscess was successfully managed with US-guided percutaneous catheter drainage. (c) One-week follow-up CT scan shows moderate improvement of the abscess (arrow). Most abscesses can be successfully managed with simple aspiration or percutaneous catheter drainage coupled with adequate antibiotics (Fig 2). The prophylactic use of antibiotics to prevent an abscess remains controversial. Bleeding Bleeding is another important complication that occurred during and immediately after ablation. Several factors are related to bleeding after RF ablation. Coagulopathy in cirrhotic patients is the most commonly encountered problem. Screening for coagulopathy should be performed before the procedure because needle electrodes of large diameter (17 14 gauge) are used. In addition, any ablative procedure should be postponed until the coagulopathy is corrected to avoid bleeding. The bleeding may develop from direct mechanical injury to the vascular structure by the RF needle electrode rather than from RF thermal injury to the vessel. Thus, real-time monitoring of the whole procedure including positioning of the needle electrode is mandatory. The potential for Figure 3. Peritoneal bleeding in a 75-year-old man with hepatocellular carcinoma. Contrast-enhanced CT scan obtained immediately after RF ablation of a hepatocellular carcinoma nodule in the caudate lobe shows peritoneal hemorrhage in the perihepatic space (arrows). The bleeding was managed with transfusion. bleeding depends on the operator s skill in placing the RF needle electrode safely without traversing major vessels and in minimizing the amount of needle repositioning. In addition, traversing sufficient normal hepatic parenchyma as well as cauterization of the needle tract after ablation are practical tips for minimizing bleeding (9).

5 RG f Volume 23 Number 1 Rhim et al 127 Figure 4. Intrahepatic bleeding in an 87-year-old man with hepatocellular carcinoma. (a) Contrast-enhanced CT scan shows a 3.0-cm hyperattenuating tumor (arrow) in segment VIII of the liver. (b) CT scan shows an expandable RF electrode (arrow), which was used to perform RF ablation. (c) Doppler US scan shows massive intrahepatic bleeding (arrow) from the margin of the ablated area. (d) Angiogram shows that the bleeding was controlled with placement of coils (arrow). (e) Threemonth follow-up CT scan shows complete ablation of the tumor. Note the metallic areas of increased attenuation (arrow) adjacent to the tumor margin. On the basis of personal experience (9), color Doppler study of the needle tract can also be helpful in early detection of arterial bleeding along the needle tract immediately after removal of the RF electrode. Furthermore, close clinical evaluation of vital signs as well as analysis of laboratory values including complete blood cell count, prothrombin time, and partial thromboplastin time immediately after the ablation is essential for early detection and proper management of this complication, which is life threatening if overlooked or improperly managed (1 4). Although most venous bleeding tends to be self-limited with conservative treatment or transfusion, transarterial embolization or surgery may be necessary in cases of arterial bleeding (Figs 3, 4). Besides bleeding, an arteriovenous fistula or pseudoaneurysm can also develop from direct traumatic injury. In addition, hepatic or portal venous thrombosis can occur as a vascular complication after RF ablation because the sequela of thermal injury to the vessels is known to be vascular thrombosis (17,29).

6 128 January-February 2003 RG f Volume 23 Number 1 Figure 5. Bile duct injury in a 55-year-old woman with hepatocellular carcinoma. (a) Contrast-enhanced CT scan shows a 3-cm-diameter hypervascular mass (arrow) in segment VIII of the liver. (b) Follow-up CT scan obtained immediately after RF ablation shows complete ablation with a 1-cm safety margin (arrow). (c) Six-month follow-up CT scan shows contraction of the ablated area without marginal recurrence. However, mild dilatation of an intrahepatic bile duct (arrow) is noted in the left lobe. There was mild jaundice at admission. (d) Endoscopic retrograde cholangiopancreatogram shows moderate dilatation of the intrahepatic bile duct (arrow) with normal size of the extrahepatic bile duct. (e) Follow-up CT scan obtained 2 weeks after biliary drainage with a percutaneous catheter (arrow) shows improvement of the biliary dilatation. Bile Duct Injury Heat from RF energy produces nonspecific thermal injury to tumor tissue as well as the adjacent normal structures (17,18,23). Bile ducts are no exception (Figs 5, 6). This is one of the dilemmas in achieving successful ablation with a 1-cm safety margin of normal liver. If a mass abuts a major bile duct, the situation becomes difficult. As the operator tries to overcome the heat sink effect of the major vessel around the central mass, the risk of injury to the major bile ducts may be increased (30 32). Thus, the risk of thermal damage to the bile ducts should be weighed in terms of potential risks versus benefits. RF ablation therapy combined with transarterial chemoembolization or percutaneous ethanol injection can be

7 RG f Volume 23 Number 1 Rhim et al 129 Figure 6. Biloma in a 46-year-old woman with hepatocellular carcinoma. (a) Doppler US scan obtained 45 days after RF ablation shows a 4-cm-diameter biloma (arrow) in the left lobe of the liver. Note the faint Doppler signal from the biloma. (b) Close-up US scan of the abdominal wall obtained with a high-frequency linear transducer shows a biconvex fluid collection (arrow) adjacent to the biloma. (c) Doppler US scan shows a fistulous communication (arrow) between the biloma and the subcutaneous collection. considered as an alternative treatment in patients with a hilar mass adjacent to major hepatic ducts. A bile duct stricture usually develops slowly compared with biloma formation. Percutaneous transhepatic biliary drainage may be necessary in severe cases associated with jaundice. Cholecystitis can also develop after RF ablation of a mass adjacent to the gallbladder (17). Although minimal wall thickening can be seen at follow-up imaging immediately after the ablation, symptomatic cholecystitis or gallbladder perforation is very rare, as in our survey, because fluid content within the gallbladder lumen plays a role in dissipation of heat around the gallbladder fossa. Figure 7. Skin burns in a 62-year-old man with hepatocellular carcinoma. Photograph shows thirddegree skin burns (arrows) that developed at the ground pad site after RF ablation of multiple hepatocellular carcinoma nodules in segment VI, which had been treated with iodized oil (Lipiodol; Guerbet, Roissy, France). The patient received skin grafts after conservative treatment for 1 month. Burns The ground pad acts as a dispersive electrode in an RF circuit. A larger surface area of the return ground pad is required for more energy (heat) to be dispersed. The risk of burns at the ground pad site has increased with use of a high-current RF technique if the surface area of the ground pad is not increased. Serious skin burns have become relatively rare, although they were reported during the early experience when insufficiently sized ground pads were used. In addition, any interface between the skin and ground pad should be eliminated to prevent skin burns (Fig 7) (33).

8 130 January-February 2003 RG f Volume 23 Number 1 Figure 8. Pneumothorax in a 47-year-old woman with hepatocellular carcinoma. Chest CT scan obtained after RF ablation of a tumor in segment VIII of the liver shows pneumothorax (arrow) in the right hemithorax. The pneumothorax was self-limited. Thoracic Complications Pneumothorax or hemothorax can occur, especially when a mass is located in the dome of the liver. A safe window of needle positioning by a skillful operator is the only way to avoid these complications. If a patient experiences dyspnea or chest pain after the ablation, chest radiography or follow-up CT is recommended to exclude these thoracic complications (Figs 8, 9). Interventional treatment for pneumothorax or hemothorax should be considered on a case-by-case basis. In addition, diaphragmatic thermal injury is possible when a mass is located in the dome of the liver. However, most diaphragmatic injury is self-limiting with conservative treatment. Figure 9. Hemothorax in a 47-year-old woman with hepatocellular carcinoma. Chest CT scan obtained after massive RF ablation of a tumor in segment VII of the liver shows a fluid collection of relatively high attenuation (arrow) in the right hemithorax, a finding indicative of hemothorax. The hemothorax was self-limited. Bowel Injury The relatively fixed colon seems to be at more risk for perforation than the stomach or small intestine because of the thick gastric wall and peristalsis of the small intestine (17). Thus, ablation of a subcapsular mass within 1 cm of the adjacent bowel loops should be carefully performed and followed up closely. A needle electrode of the straight type is recommended over one of the expandible type because the tips of the expandible internal prongs can penetrate into the bowel wall without perception by the operator when there is a poor sonic window (2). If the mass is close to the bowel loops, oral intake should be suspended until no bowel injury is identified at immediate follow-up CT (Fig 10). Tumor Seeding Tumor seeding is very rare but can be another serious complication after RF ablation. In our series, there was no case of tumor seeding during the survey period. Afterward, four cases of tumor seeding along the needle tract were reported from several institutions in our study group (Fig 11). According to Llovet et al (24), subcapsular location and poorly differentiated nature of the tumor may be associated with a higher risk of tumor seeding. To avoid tumor seeding, the number of punctures and the amount of repositioning of the RF needle electrode should be minimized and a sufficient portion of normal hepatic parenchyma along the needle tract is required, especially in the case of a subcapsular tumor. Furthermore, it is recommended that one avoid treating an exophytic tumor percutaneously. This complication can be managed with transarterial oily chemoembolization in some cases.

9 RG f Volume 23 Number 1 Rhim et al 131 Figure 10. Bowel injury in a 55-year-old woman with hepatocellular carcinoma. (a) Contrast-enhanced CT scan obtained before RF ablation shows a hyperattenuating 1.5-cm-diameter hepatocellular carcinoma nodule (arrow) in segment V. The patient experienced abdominal pain and fever after the procedure. (b) Follow-up CT scan obtained immediately after ablation shows intraperitoneal free air (arrow) around the hepatic flexure of the colon adjacent to the ablated tumor. Emergent exploratory laparotomy revealed a 0.5-cm-diameter colonic perforation at the hepatic flexure. Segmental resection of the colon was required. The pathologic diagnosis was focal transmural ischemic necrosis with perforation. Figure 11. Tumor seeding in a 55-year-old woman with hepatocellular carcinoma. (a) Follow-up CT scan obtained immediately after a second session of RF ablation for a marginal recurrent mass in the left lateral segment of the liver shows a nonenhancing ablated area (arrow), which indicates complete ablation. (b) Follow-up CT scan obtained 1 month after the second session of RF ablation shows a small enhancing nodule in the extrahepatic space (arrow), a finding suggestive of tumor seeding along the needle tract. (c) Arteriogram shows that the internal mammary artery supplies the tumor nodule (arrows).

10 132 January-February 2003 RG f Volume 23 Number 1 Discussion Any interventional procedure can remain as a therapeutic option when the benefits are greater than the risks of the procedure. Although there have been many reports claiming therapeutic effects of RF ablation for local control of unresectable hepatic malignancies, investigation of the complications has been limited (17 24). The prevalence of major complications in sporadically reported studies of smaller series ranged from 0% to 12.7% (17,18,36 38). Our multicenter study of a larger series of patients (1,139) showed a complication rate of 2.4% and mortality of 0.09%. An Italian multicenter study of 1,766 patients recently reported a mortality rate of 0.11% and a major complication rate of 1.52% (17). The causes of the two deaths in the Italian survey were septic shock due to Staphylococcus aureus peritonitis and liver failure (17). The results of both surveys supported those of previous studies, which found that the morbidity of RF ablation is a little higher than that of percutaneous ethanol injection (39) but that the morbidity and mortality of RF ablation seem to be acceptable for a safe procedure. The common complications in our survey were infection and bleeding, as in the Italian survey. Other complications included biliary complications, ground pad burns, and thoracic or bowel complications. However, the rate of complications after RF ablation may have decreased as the operator s experience accumulated because our survey data include all cases in the period of initial experience of each operator. The recent investigations including our survey indicate that the rates of complications following RF ablation are not negligible but can be minimized. Therefore, a physician performing RF ablation should understand the spectrum of complications encountered after ablation for careful selection of candidates as well as early detection and proper management of complications. There are several strategies for decreasing complications after RF ablation of hepatic tumors (1 5,17). The first key strategy is prevention. A simple shortcut to minimizing complications is not to perform ablation in patients at high risk. Therefore, meticulous preevaluation of candidates should be performed, especially in regard to coagulopathy, underlying hepatic reserve, and tumor proximity to major structures such as the bile duct or intestine. In a patient with correctable coagulopathy, ablation should be postponed until all parameters are corrected. RF ablation combined with transarterial oily chemoembolization or percutaneous ethanol injection can be considered in patients with a mass close to a major organ because this combined approach can reduce the need for the operator to completely ablate the entire tumor as well as a 1-cm safety margin (34,35,40). We believe that the complication rate may decrease as we have more experience with this procedure (9). An issue that will still need to be addressed is that many vendors of RF equipment are developing a more powerful device to produce a larger ablated lesion in a shorter time. Thus, the complication rate could contrarily increase if a physician takes a more aggressive posture for successful ablation with a wider safety margin including the perivascular area. Another tip for preventing complications is selection of the proper guiding modality. The prevalence of complications may be related to how difficult it is to place the needle electrode in the desired portion of the liver. Poor visualization of the target lesion or difficulty in the approach to the lesion can increase the risk of damage to adjacent structures. Therefore, the operator should select the best guiding modality on a case-by-case basis. A final issue in prevention of complications is the method of approach to the lesion: open versus percutaneous. The open or laparoscopic approach may be beneficial for isolating the lesion from adjacent critical structures and potentially better control of bleeding from the surface of the liver. The second strategy in minimizing major complications is early detection. Although early detection cannot reduce the frequency of complications such as infection or bleeding, it can potentially minimize their clinical magnitude. Thus, the operator and other medical personnel should be knowledgeable about the spectrum of various complications after RF ablation because complications can be detected even during the procedure in some cases. Sound knowledge about complications may be helpful for an operator in stopping the ablation, which will prevent more serious complications. Close immediate follow-up with clinical and laboratory data is also essential for early detection of complications. Monitoring of vital signs with a complete blood cell count and measurement of prothrombin time is mandatory. Immediate ( 24 hours) follow-up CT is a reliable modality for detecting any complications after RF ablation. The last key strategy is proper management. Adequate management at the appropriate time is another important issue because a complication is not a static situation. Even if the complication is detected early, inappropriate management can result in mortality. Thus, the operator should

11 RG f Volume 23 Number 1 Rhim et al 133 treat patients with complications properly on the basis of the unique clinical characteristics of each complication. In conclusion, a physician performing RF ablation of hepatic malignancies should be aware of the broad spectrum of major complications encountered after ablation for careful patient selection as well as early detection and proper management of the complications. References 1. Dodd GD III, Soulen M, Kane R, et al. Minimally invasive treatment of malignant hepatic tumors: at the threshold of a major breakthrough. Radio- Graphics 2000; 20: Rhim H, Goldberg SN, Dodd GD III, et al. Essential techniques for successful radio-frequency thermal ablation of hepatic tumors. 2001; 21:S17 S Gazelle GS, Goldberg SN, Solbiati L, Livraghi T. Tumor ablation with radio-frequency energy. Radiology 2001; 217: McGahan JP, Dodd GD III. Radiofrequency ablation of the liver: current status. AJR Am J Roentgenol 2001; 176: Goldberg SN, Dupuy DE. Image-guided radiofrequency tumor ablation: challenges and opportunities part I. J Vasc Interv Radiol 2001; 12: Dupuy DE, Goldberg SN. Image-guided radiofrequency tumor ablation: challenges and opportunities part II. J Vasc Interv Radiol 2001; 12: Rossi S, Di Stasi M, Buscarini E, et al. Percutaneous RF interstitial thermal ablation in the treatment of hepatic cancer. AJR Am J Roentgenol 1996; 167: Solbiati L, Goldberg SN, Ierace T, et al. Hepatic metastases: percutaneous radiofrequency ablation with cool-tip electrodes. Radiology 1997; 205: Rhim H, Dodd GD III. Radiofrequency thermal ablation of liver tumors. J Clin Ultrasound 1999; 27: Goldberg SN, Solbiati L, Hahn PF, et al. Largevolume tissue ablation with radio frequency by using a clustered, internally cooled electrode technique: laboratory and clinical experience in liver metastases. Radiology 1998; 209: Goldberg SN, Gazelle SG, Mueller PR. Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. AJR Am J Roentgenol 2000; 174: Livraghi T, Goldberg SN, Lazzaroni S, et al. Hepatocellular carcinoma: radio-frequency ablation of medium and large lesions. Radiology 2000; 214: Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radio-frequency ablation versus ethanol injection. Radiology 1999; 210: Solbiati L, Ierace T, Goldberg SN, et al. Percutaneous US-guided RF tissue ablation of liver metastases: results of treatment and follow-up in 16 patients. Radiology 1997; 202: LeVeen RF. Laser hyperthermia and radiofrequency ablation of hepatic lesions. Semin Interv Radiol 1997; 14: Rossi S, Buscarini E, Garbagnati F, et al. Percutaneous treatment of small hepatic tumors by an expandable RF needle electrode. AJR Am J Roentgenol 1998; 170: Livraghi TL, Solbiati L, Meloni F, Ierace T, Goldberg SN. Complications after cool-tip RF ablation of liver cancer: initial report of the Italian Multicenter Cooled-Tip RF Study Group (abstr). Radiology 2000; 217(P): Choi H, Loyer EM, DuBrow RA, et al. Radiofrequency ablation of liver tumors: assessment of therapeutic response and complications. Radio- Graphics 2001; 21:S41 S Zagoria RJ, Chen MY, Shen P, Levine EA. Complications from radiofrequency ablation of liver metastases. Am Surg 2002; 68: Curley SA, Izzo F, Delrio P, et al. Radiofrequency ablation of unresectable primary and metastatic hepatic malignancies: results in 123 patients. Ann Surg 1999; 230: Lees WR, Gilliam AR. Complications of radiofrequency and laser ablation of liver metastases: incidence and management (abstr). Radiology 1999; 213(P): Choi JB, Rhim H, Kim Y, et al. Radiofrequency thermal ablation of malignant hepatic tumors: post-ablation syndrome. J Korean Radiol Soc 2000; 43: Napier DH, Dodd GD III, Hubbard LG, Chintapalli KN, Chopra S, Medina D. Post-ablation syndrome following radiofrequency ablation of liver tumors. Presented at the 29th Annual Meeting and Postgraduate Course of the Society of Gastrointestinal Radiologists, Kauai, Hawaii, March 12 17, Llovet JM, Vilana R, Bru C, et al. Increased risk of tumor seeding after percutaneous radiofrequency ablation for single hepatocellular carcinoma. Hepatology 2001; 33: Lencioni R, Cioni D, Bartolozzi C. Percutaneous radiofrequency thermal ablation of liver malignancies: techniques, indications, imaging findings, and clinical results. Abdom Imaging 2001; 26: Song SY, Chung JW, Han JK, et al. Liver abscess after transcatheter oily chemoembolization for hepatic tumors: incidence, predisposing factors, and clinical outcome. J Vasc Interv Radiol 2001; 12: O Connor MJ, Schwartz ML, McQuarrie DG, Sumner HW. Cholangitis due to malignant obstruction of biliary outflow. Ann Surg 1981; 193: Lim HK, Choi D, Lee WJ, et al. Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: evaluation with follow-up multiphase helical CT. Radiology 2001; 221: Lu DS, Raman SS, Vodopich DJ, Wang M, Sayre J, Lassman C. Effect of vessel size on creation of hepatic radiofrequency lesions in pigs: assessment of the heat sink effect. AJR Am J Roentgenol 2002; 178:47 51.

12 134 January-February 2003 RG f Volume 23 Number Rossi S, Garbagnati F, Lencioni R, et al. Percutaneous radio-frequency thermal ablation of nonresectable hepatocellular carcinoma after occlusion of tumor blood supply. Radiology 2000; 217: Goldberg SN, Saldinger PF, Gazelle GS, et al. Percutaneous tumor ablation: increased coagulation necrosis with combined radiofrequency and percutaneous doxorubicin injection (abstr). AJR Am J Roentgenol 2000; 174: Patterson EJ, Scudamore CH, Owen DA, Nagy AG, Buczkowski AK. Radiofrequency ablation of porcine liver in vivo: effects of blood flow and treatment time on lesion size. Ann Surg 1998; 227: Goldberg SN, Solbiati L, Halpern EF, Gazelle GS. Variables affecting proper system grounding for radiofrequency ablation in an animal model. J Vasc Interv Radiol 2000; 11: Goldberg SN, Hahn PF, Halpern EF, Fogle RM, Gazelle GS. Radio-frequency tissue ablation: effect of pharmacologic modulation of blood flow on coagulation diameter. Radiology 1998; 209: Hansen PD, Rogers S, Corless CL, Swanstrom LL, Siperstien AE. Radiofrequency ablation lesions in a pig liver model. J Surg Res 1999; 87: Bilchik AJ, Wood TF, Allegra DP. Radiofrequency ablation of unresectable hepatic malignancies: lessons learned. Oncologist 2001; 6: Wood TF, Rose M, Chung M, et al. Radiofrequency ablation of 231 unresectable hepatic tumors: indications, limitations, and complications. Ann Surg Oncol 2000; 7: Curley S, Izzo F, Ellis EM, Vauthey JN, Vallone P. Radiofrequency ablation of hepatocellular carcinoma in 110 patients with cirrhosis. Ann Surg 2000; 232: Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radio-frequency ablation versus ethanol injection. Radiology 1999; 210: Rossi S, Garbagnati F, Lencioni R, et al. Percutaneous radio-frequency thermal ablation of nonresectable hepatocellular carcinoma after occlusion of tumor blood supply. Radiology 2000; 217: This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician s Recognition Award. To obtain credit, see

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