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1 Departement d'Imagerie Medicale et de Chirurgie, Institut Gustave Roussy, 39
Rue Camille Desmoulins, Villejuif 94805, France.
2 Service de Radiologie et de Chirurgie Générale et Digestive, CHU
Michallon, Grenoble, France.
Received December 30, 2002;
accepted after revision April 1, 2003.
Address correspondence to T. de Baère.
Abstract
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SUBJECTS AND METHODS. Over a 5-year period, 312 patients underwent 350 sessions of radiofrequency ablation (124 intraoperative and 226 percutaneous) for treatment of 582 liver tumors including 115 hepatocellular carcinomas and 467 metastatic tumors. The chi-square test was used for a group-to-group comparison of the occurrence of adverse events.
RESULTS. Thirty-seven (10.6%) adverse events and five (1.4%) deaths were related to radiofrequency treatment. The deaths were caused by liver insufficiency (n = 1), colon perforation (n = 1), and portal vein thrombosis (n = 3). Portal vein thrombosis was significantly (p < 0.00001) more frequent in cirrhotic livers (2/5) than in noncirrhotic livers (0/54) after intraoperative radiofrequency ablation performed during a Pringle maneuver. Liver abscess (n = 7) was the most common complication. Abscess occurred significantly (p < 0.00001) more frequently in patients bearing a bilioenteric anastomosis (3/3) than in other patients (4/223). We encountered five pleural effusions, five skin burns, four hypoxemias, three pneumothoraces, two small subcapsular hematomas, one acute renal insufficiency, one hemoperitoneum, and one needle-tract seeding. The 6.3% of minor complications did not require specific treatment or a prolonged hospital stay. Among the 5.7% major complications, 3.7% required less than 5 days of hospitalization for treatment or surveillance and 2% required more than 5 days for treatment.
CONCLUSION. Radiofrequency ablation of liver tumors is a well-tolerated technique, but caution should be exercised when treating patients with a bilioenteric anastomosis, and radiofrequency ablation during vascular occlusion in cirrhotic livers should be avoided.
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Our study population included 131 women and 181 men who were 62 ± 14 (mean ± SD) years old bearing 582 tumors including 115 hepatocellular carcinomas and 467 metastatic tumors, mostly from colorectal cancer. The tumors were treated during 350 procedures. Two hundred twenty-six procedures were percutaneous, and 124 were intraoperative. Twenty-seven patients underwent multiple radiofrequency procedures: two in 18 patients, three in seven patients, and four in two patients. Intraoperative radiofrequency ablation was always performed during open surgery, and no treatment was performed laparoscopically. Intraoperative radiofrequency ablation was combined with liver resection in 118 patients; radiofrequency ablation was the only treatment performed during laparotomy in the remaining six patients. A mean of 2.1 ± 1.92 tumors were treated during intraoperative radiofrequency ablation, and a mean of 1.32 ± 0.76 tumors were treated percutaneously. The largest tumor dimensions ranged from 5 to 55 mm with a mean value of 26 mm. An international normalized ratio below 1.5 and a platelet count above 75 x 103/µL were required before percutaneous radiofrequency treatment. Most radiofrequency treatments were performed using single or cluster cooled-tip needles (Cool-Tip Cluster, Radionics, Burlington, MA) or 3- or 4-cm diameter expandable array needles (LeVeen, Radiotherapeutics, Sunnyvale, CA). Radiofrequency systems were used according to the manufacturer's recommendations. The Radionics radiofrequency generator was activated for 15 min in the automatic mode allowing pulsed radiofrequency delivery while the needle was being cooled with chilled saline, as described elsewhere [1, 16]. The Radiotherapeutics system started radiofrequency delivery at low power with incremental power increases every minute, until a major increase in impedance, called roll-off, was obtained. One to four grounding pads were used and positioned according to the manufacturer's recommendations, which varied with time because needle designs have changed. All the intraoperative and 208 of the 226 percutaneous treatments were performed under sonographic guidance, and the remaining 18 treatments were performed under CT guidance because tumor visualization was poor with sonography or because a transpulmonary approach was required to target highly located tumors. General anesthetic was used for all intraoperative radiofrequency procedures and for 199 of the 226 percutaneous procedures. Needle-tract cauterization was not systematically performed.
The Pringle maneuver (clamping of the porta hepatis, thus interrupting hepatic arterial and portal venous flow to the liver) was applied in 59 (47%) of 126 intraoperative radiofrequency treatments, including those in five patients with hepatocellular carcinoma in the cirrhotic liver and in 54 patients with metastases. The Pringle maneuver was used either because the tumor exceeded 25 mm or because it was in contact with vessels larger than 4 mm. Intraductal cooling of the main bile duct with chilled saline was used in eight intraoperative radiofrequency treatments modeled after a technique described elsewhere [17]. Temporary vascular balloon occlusion was used in 25 of the 226 percutaneous treatments according to a technique reported elsewhere [18]. These balloon occlusions were used percutaneously when treating metastases in contact with vessels larger than 4 mm or metastases with diameters that exceeded 35 mm. The occluded vessels were one hepatic vein in 18 patients, two hepatic veins in two patients, and one segmental portal branch in five patients. Selective arterial embolization was used in addition to percutaneous radiofrequency treatment of hepatocellular carcinoma in six patients whose tumors exceeded 35 mm.
Two hundred ninety-nine of the 312 patients in this study were followed up for at least 4 months. The examinations included CT and a blood test every 2 or 3 months for 6 months in all patients whom we were able to follow up, except for four patients with an increased serum creatinine level. These four patients were followed up with MRI. Fifty additional patients underwent both CT and MRI follow-up because they were enrolled in a prospective study for follow-up evaluation. All CT and MRI included dynamic enhanced imaging. Follow-up imaging was interpreted by senior radiologists who were not in charge of the radiofrequency ablation, and clinical follow-up was performed by the physician who performed the radiofrequency ablation. Any image changes except the usual area of devascularization seen after radiofrequency ablation or tumor progression were considered as complications. Any rehospitalization or consultation in addition to the scheduled ones was considered complications. Seven patients died within the 4 months after treatment, and six were lost to follow-up imaging. In these six patients, medical files from other centers were available 2 months after radiofrequency ablation. Prophylactic antibiotic therapy with a single 1-g dose of ceftriaxone was administered to all patients who were treated during surgery. Prophylactic antibiotic therapy with an IV injection of amoxicillin and clavulanate (2 g) immediately before the radiofrequency ablation procedure and oral administration of the same antibiotic (2 g/day) over 2 days was given for percutaneous radiofrequency treatments. The three patients with a bilioenteric anastomosis received a 5-day course of amoxicillin and clavulanate, and the patient with a metallic biliary stent received ceftriaxone (2 g/day) and metronidazole (0.5 g/day) over 5 days.
Percutaneous radiofrequency ablation was performed on the basis of a one- or two-night hospital stay, with a blood test obtained the day after radiofrequency ablation for all patients. No systematic imaging was performed during the hospital stay after radiofrequency ablation unless unusual findings such as pain, jaundice, or dyspnea revealed at the postoperative clinical examination or a blood test revealing unusual major modifications.
The chi-square test was used for a group-to-group comparison of occurrence of adverse events with a significant p value below 0.05.
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Eleven vascular thromboses occurred, which included five hepatic veins and three segmental portal branches imaged at direct venography at the end of radiofrequency treatment performed during percutaneous balloon occlusion. These eight thrombotic events involved only the balloon occluded vessel without upstream extension and did not induce clinical symptoms or unusual modifications on blood tests performed on day 1. None of the thromboses previously mentioned were revealed on follow-up CT scans and MRIs obtained 2 or 3 months after treatment. The three patients with complete and extensive portal vein thromboses who presented with abdominal pain, ascites, and a major increase in bilirubin level were diagnosed on CT performed at day 1 or 2. Two of these portal vein thromboses occurred in a patient with cirrhosis who was undergoing liver resection and intraoperative radiofrequency ablation associated with the Pringle maneuver for unresectable hepatocellular carcinoma. One of these two patients underwent one radiofrequency delivery during a 10-min Pringle maneuver, and the other underwent two radiofrequency deliveries during a 5- and 7-min Pringle maneuver. The third portal vein thrombosis occurred after percutaneous treatment of a single metastasis in a patient who had already undergone two liver operations and one percutaneous radiofrequency treatment. Two of the three patients who developed portal vein thromboses after radiofrequency ablation died within 7 days after the discovery. The third patient returned home with an increase in the Child-Pugh score from B7 preoperatively to C10 postoperatively and died 4 months later.
The seven liver abscesses were discovered 13 days to 2 months after percutaneous radiofrequency treatment (Figs. 1A, and 1B). Three abscesses that were asymptomatic caused low-grade fever, and therefore the patients were not referred to the hospital before the scheduled 2-month follow-up imaging when gas collections were found on CT or MRI. Two other abscesses were discovered 3 and 4 weeks after radiofrequency on CT that was performed for unusual abdominal pain and fever. These five abscesses were punctured under sonographic guidance and drained over 3 days before removal of the drain. Cultures were positive for Escherichia coli and Streptococcus faecalis. A combination of amoxicillin and clavulanate (2 g/day) was initiated before draining the abscess and continued for 15 days; the patients recovered uneventfully. The last two of the seven abscesses caused septicemia and septic shock. The first of these last two patients underwent radiofrequency ablation for a single metastasis from colon cancer that was high-seated in a remnant liver after a previous right hepatectomy. This patient had undergone biliary drainage for 3 months because of a postoperative fistula and was finally treated with a metallic stent 2 months before radiofrequency ablation for persistent stenosis of the common bile duct. Six weeks after radiofrequency ablation, a CT scan revealed a hepatic abscess extending to the mediastinum through a perforation in the diaphragm. The second severe abscess occurred in a patient operated on for duodenopancreatic resection 4 months before radiofrequency ablation for a single metastasis from pancreatic adenocarcinoma. Two weeks after radiofrequency treatment, chemotherapy combining gemcitabine and docetaxel was begun. Three weeks after the first course of chemotherapy, three large hepatic abscesses were found on CT. Both patients with septicemia and abscesses were managed with percutaneous drainage. Drain cultures revealed Clostridium organisms and E. coli, which were treated with antibiotics. Hospitalization for these two patients lasted 41 and 42 days. Both patients died of widespread metastatic disease, 5 and 7 months, respectively, after radiofrequency ablation. Among the 350 radiofrequency procedures, an abscess occurred in all three patients with bilioenteric anastomoses.
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Lung and pleural-related complications included five pleural effusions, three pneumothoraces, and four cases of dyspnea with hypoxemia. The pleural effusions were discovered on chest radiography performed for unusual pain 1 day after percutaneous radiofrequency ablation. Four were mild and resolved spontaneously before day 7. The last one was mild on day 1 but increased in volume by day 7 and then required a thoracocentesis. The plural effusion three times during the next 2 months and required three additional thoracocenteses but finally resolved. Two of the three cases of pneumothoraces were expected because a CT-guided transpulmonary approach had been chosen to gain access to a highly located tumor. One occurred unexpectedly during sonographically guided treatment of a highly located tumor. This last one was discovered on a chest radiograph obtained to investigate right shoulder pain, which had started in the recovery room. None of the pneumothorax cases required treatment. They all resolved spontaneously, and the patients were discharged from the hospital on day 1. Dyspnea and hypoxemia were observed at day 1 in four patients after percutaneous (n = 2) and intraoperative (n = 2) radiofrequency ablation. Because these conditions mimic pulmonary embolism, single-detector helical CT was performed to rule out pulmonary embolism. No cause was found to explain the symptoms, and the hypoxemia resolved spontaneously after 2-4 days, therefore slightly prolonging the hospital stay of the two patients who were treated percutaneously.
The five skin burns were first- and third-degree burns in four patients and in one patient, respectively. The burns occurred at the edge of one of the grounding pads facing the active electrode when the maximal power of the generator was used. Treatment lasted for at least 30 min using multiple overlapping deliveries with the larger needles—that is, the Radionics Cluster or the LeVeen 4.0-cm needle.
The patient with a colon perforation was discharged from the hospital 2 days after radiofrequency treatment with no abnormal clinical findings and no pain. He returned to another hospital on the day 4 with abdominal pain and was treated with antibiotics and steroids at home for 3 days. When the patient was referred again to our hospital 8 days after radiofrequency ablation, he had obvious peritonitis with a gas-containing peritoneal effusion. At laparotomy, right colon perforation adjacent to the subcapsular liver radiofrequency destruction was found to be the cause of peritonitis. The patient died of multiorgan failure after 7 weeks in the intensive care unit.
Another patient had a peritoneal effusion that was discovered on sonography, which was performed in the recovery room because the patient had severe abdominal pain 1 hr after the percutaneous radiofrequency treatment with a 17-gauge single needle of five neuroendocrine tumors measuring less than 1 cm. The patient underwent an emergency laparotomy. Bile and blood leakage was discovered at one of the five puncture sites. The patient recovered uneventfully, without the need for a blood transfusion, after 2 days of peritoneal drainage. He was discharged from the hospital 5 days after radiofrequency ablation. He is still alive and tumor-free 3 years later.
Postoperative hepatic failure occurred in a patient treated for 13 hepatic metastases from colon cancer, including 12 metastases in the right liver lobe. He underwent a right hepatectomy, partially extended to segment IV, associated with a single radiofrequency delivery for treatment of a segment III metastasis, without the Pringle maneuver. On day 3, a small, hard remnant liver with a large area of radiofrequency destruction was found at laparotomy that was performed to investigate liver failure shown on a blood test and clinical examination. However, CT findings were normal. Hepatic failure without portal thrombosis led to the patient's death on day 6.
Transient renal failure occurred in one patient after radiofrequency treatment of a 55-mm hepatocellular carcinoma lesion requiring 10 radiofrequency deliveries with a LeVeen 4.0-cm needle after superselective hepatic artery embolization was performed. The renal failure resolved after one course of dialysis, and the patient was discharged from the hospital 4 days after radiofrequency ablation. This patient was still tumor-free at the last follow-up CT performed 8 months after radiofrequency treatment.
Tumor seeding of the abdominal wall was discovered in another patient on follow-up MRI, 4 months after treatment of a subcapsular hepatocellular carcinoma measuring 5 cm in diameter that required three punctures to achieve radiofrequency needle placements for five radiofrequency deliveries.
Concerning the two subcapsular hematomas, one was seen on a sonogram obtained immediately after radiofrequency ablation and confirmed on a CT scan obtained 24 hr later, and the other was found on a CT scan obtained 24 hr later for pain. Both hematomas were less than 5 mm thick and did not induce any drop in hemoglobin level. They both resolved spontaneously and were no longer seen on the CT at 2-month follow-up.
Incidental findings on follow-up imaging, such as segmental or subsegmental biliary tract dilatation upstream of the radiofrequency area of destruction or arterioportal shunts, were not considered as adverse events because they have been reported as usual consequences of radiofrequency liver ablation [19, 20]. Pneumothoraces occurring after a transpleurodiaphragmatic surgical approach were not taken into account because they are expected after a thoracotomy [21]. In the same manner, mild pleural effusion occurring after intraoperative radiofrequency was not taken into account because it is a common occurrence after laparotomy for hepatectomy.
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Thrombosis and coagulation of vessels smaller than 3 mm in diameter is a common occurrence after radiofrequency ablation [27]. Indeed, whenever radiofrequency ablation is performed, numerous small vessels are coagulated, but the image-monitoring technique we use cannot detect this in most patients. In contrast, thrombosis of vessels larger than 4 mm after radiofrequency ablation is uncommon, provided that normal flow is maintained through these vessels. In our experience, thromboses of large vessels were always linked to vascular occlusion when it was used as an adjunct to radiofrequency ablation, except in one patient. One third of the percutaneous radiofrequency procedures performed during temporary vessel balloon occlusion led to complete thrombosis limited to the ballooned vessel, either segmental portal branches or hepatic veins. Although these thromboses always remained asymptomatic and vessels were recanalized thereafter on 2-month follow-up imaging, one should keep in mind that before targeting a vessel for balloon occlusion, one should be sure that the patient can sustain temporary thrombosis of the targeted vessel. This means, for example, that it could be dangerous to treat a remnant liver with a single hepatic vein during balloon occlusion of this vessel. The rate of portal vein thromboses after radiofrequency ablation performed during Pringle maneuvers in cirrhotic patients (2/5) was significantly higher (p < 0.00001) than the rate in noncirrhotic livers (0/54). Moreover, these thromboses occurred despite the Pringle maneuver applied for less than 10 min for treatment of tumors at a distance from the portal trunk. In conclusion, vascular occlusion combined with radiofrequency ablation appears to be safe, except in patients with cirrhosis, even if of short duration.
In our experience, tumor seeding was rare, but a follow-up of 4 months is too short to detect all seeding. However, the rate of 0.5% during percutaneous treatment is akin to that reported by most teams with considerable radiofrequency ablation experience [28, 29], although a rate up to 12% has been reported by one center with limited experience [30]. The only seeding that we experienced occurred in a patient who had known risk factors (primary tumor; poorly differentiated, subcapsular location; and multiple needle insertions). In such patients, we would recommend first trying a route traversing nontumorous parenchyma—limiting the number of needle insertions as much as possible—and then delivering radiofrequency treatment through a guiding needle and cauterizing the tract with the radiofrequency device at the end of the radiofrequency procedure. In addition, even if cauterization remains unproven, we believe that this procedure must also be applied before any repositioning of the needle or opening of the array if one had been in contact with the tumor. Besides the increased risks of seeding, subcapsular location of the radiofrequency-targeted tumor inside the liver might be of paramount importance in terms of potential complications to adjacent organs. Because radiofrequency is supposed to destroy the tumor with a safety margin of 0.5-1 cm of healthy parenchyma, this means that organs or the liver structure located less than 0.5-1 cm from the tumor margin will be heated. To what extent adjacent organs or vital liver structures tolerate heat is not well documented. Of the adjacent organs, the colon is probably the most sensitive to heat because of its thin wall, and colon perforation is the most frequently reported complication involving adjacent organs [13, 14]. Furthermore, a history of previous colon resection was revealed by Livraghi et al. [13] in five of six patients who developed colon perforation after radiofrequency ablation, supporting the role of postoperative adhesions and the lack of peristalsis. Therefore, it is probably not advisable to percutaneously treat liver tumors that are less than 1 cm from the colon. On the contrary, thermal damage to the right kidney does not appear to give rise to complications, and this is easy to understand because radiofrequency treatment of peripheral renal tumors has been shown to be safe [31, 32]. The abdominal wall and the diaphragm also seem to be relatively resistant to thermal damage, even if few diaphragmatic perforations have been reported [22]. Radiofrequency ablation of tumors adjacent to the gallbladder has been recently reported to be safe, with a self-limited morbidity related to mild iatrogenic cholecystitis [33].
Surprisingly, we encountered four patients with self-resolved hypoxemias
after radiofrequency that were never reported previously. No abnormal imaging
findings were found. Although the explanation for this condition remains
obscure, acute lung injury as a result of systemic inflammatory response
syndrome giving rise to overexpression of cytokines is plausible. Indeed, a
major increase in the blood levels of cytokines, such as TNF-
(tumor
necrosis factor-alpha) and MIP-2 (macrophage inflammatory protein-2), and
severe lung inflammation have been described experimentally after cryotherapy
to the liver [34], which
partially explains the cryoshock sometimes encountered after cryotherapy in
clinical practice. In the same experimental study, a smaller increase in the
same cytokines and occasional mild patchy congestive lung edema were reported
after radiofrequency ablation to the liver. We hypothesize that the release of
cytokines and degradation products during radiofrequency ablation may have
been potentially toxic to the lung in four of our patients, in a manner
similar to that found after cryotherapy. Also, myoglobinuria, known to occur
after cryotherapy, was only recently reported after radiofrequency ablation
[35]. As reported in another
article [12], myoglobinuria
might be responsible for the renal insufficiency in the patient in our study
who received the highest number of radiofrequency deliveries for a single
tumor in this series. However, contrast material that is administered during
associated arterial embolization could account for renal toxicity.
Most of the pad burns occurred in our early experience with radiofrequency treatment because we used only one pad for small electrodes and two pads for larger electrodes. Increasing the number of pads according to the manufacturer's recommendations lowered the occurrence of burns. In addition, adequate skin preparation, pads positioned equidistant from the active electrode, and advice proffered in an excellent experimental study [36] can be of great help in limiting these burns. Finally, careful and regular checking of the local temperature at the edges of the pad closest to the electrode, using chilled saline to cool the edges locally if needed, or changing position for subsequent radiofrequency deliveries can be helpful to avoid burns.
Our study has several limitations. One is the heterogeneity of the tumors treated, both hepatocellular carcinomas and metastatic tumors. The second is the heterogeneity of the treatment procedures including percutaneous and intraoperative radiofrequency ablation, cooled needles, and expandable arrays. This heterogeneity allows a group-to-group comparison in a series of patients treated by the same teams with the same techniques. In this regard, we could show differences in terms of the rate of portal thrombosis after the Pringle maneuver and the rate of abscess after ablation according to technique or population. However, the series remains too small to find differences in many variables.
Another limitation of this study is that except for the blood tests and clinical examinations, no systematic examinations were performed in the early days after radiofrequency ablation. This probably lowered the number of asymptomatic adverse events such as small pleural effusions or small subcapsular hematomas, which had resolved on the systematic follow-up CT performed at 2 months. We believe that prospective registration of adverse events in our two centers, in which radiologists were trained in radiofrequency ablation since the early days of the technique, allowed us to acquire more precise data than would a questionnaire or a review of the literature, which contains most of the published articles or abstracts focused on this topic.
Radiofrequency treatment of liver tumors is most often well tolerated. Adverse events that required treatment occurred in 5.7% of procedures including death in 1.4% of procedures. These events were experienced at our two medical centers early in our learning curves. Abscesses rank first among complications for which prophylactic antibiotics may play a role that remains to be defined. Avoiding the Pringle maneuver during radiofrequency ablation in cirrhotic patients, exercising extreme caution when treating patients with bilioenteric anastomosis, or having a tumor less than 1 cm from adjacent organs, especially the colon, should help to lower the rate of complications after radiofrequency treatment of liver tumors.
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D. Choi, H. K. Lim, M. J. Kim, S. J. Kim, S. H. Kim, W. J. Lee, J. H. Lim, S. W. Paik, B. C. Yoo, M. S. Choi, et al. Liver Abscess After Percutaneous Radiofrequency Ablation for Hepatocellular Carcinomas: Frequency and Risk Factors Am. J. Roentgenol., June 1, 2005; 184(6): 1860 - 1867. [Abstract] [Full Text] [PDF]
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C. Horkan, K. Dalal, J. A. Coderre, J. L. Kiger, D. E. Dupuy, S. Signoretti, E. F. Halpern, and S. N. Goldberg Reduced Tumor Growth with Combined Radiofrequency Ablation and Radiation Therapy in a Rat Breast Tumor Model Radiology, April 1, 2005; 235(1): 81 - 88. [Abstract] [Full Text] [PDF]
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T. D. Atwell, D. J. Brandhagen, J. W. Charboneau, D. M. Nagorney, M. R. Callstrom, and M. A. Farrell Successful Treatment of Hepatocellular Adenoma with Percutaneous Radiofrequency Ablation Am. J. Roentgenol., March 1, 2005; 184(3): 828 - 831. [Abstract] [Full Text] [PDF]
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L. Frich, B. Edwin, K. Brabrand, A. R. Rosseland, T. Mala, O. Mathisen, and I. Gladhaug Gastric Perforation After Percutaneous Radiofrequency Ablation of a Colorectal Liver Metastasis in a Patient with Adhesions in the Peritoneal Cavity Am. J. Roentgenol., March 1, 2005; 184(3_supp): S120 - S122. [Full Text] [PDF]
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A. Giorgio, L. Tarantino, G. de Stefano, C. Coppola, and G. Ferraioli Complications After Percutaneous Saline-Enhanced Radiofrequency Ablation of Liver Tumors: 3-Year Experience with 336 Patients at a Single Center Am. J. Roentgenol., January 1, 2005; 184(1): 207 - 211. [Abstract] [Full Text] [PDF]
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S. H. Kim, H. K. Lim, D. Choi, W. J. Lee, S. H. Kim, M. J. Kim, S. J. Lee, and J. H. Lim Changes in Bile Ducts after Radiofrequency Ablation of Hepatocellular Carcinoma: Frequency and Clinical Significance Am. J. Roentgenol., December 1, 2004; 183(6): 1611 - 1617. [Abstract] [Full Text] [PDF]
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 A R Gillams Liver ablation therapy Br. J. Radiol., September 1, 2004; 77(921): 713 - 723. [Full Text] [PDF]
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R. P. Liddell and S. B. Solomon Thermal Protection During Radiofrequency Ablation Am. J. Roentgenol., June 1, 2004; 182(6): 1459 - 1461. [Full Text] [PDF]
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