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Radiofrequency Ablation of Unresectable Hepatic Malignancies: Lessons Learned

^a Department of Surgical Oncology, John Wayne Cancer Institute, Santa Monica, California, USA; ^b the Cancer Center at Century City Hospital, Los Angeles, California, USA

Correspondence: Anton J. Bilchik, M.D., Ph.D., F.A.C.S., John Wayne Cancer Institute, 2200 Santa Monica Boulevard, Santa Monica, California 90404, USA. Telephone: 310-449-5206; Fax: 310-449-5261; e-mail: bilchika{at}jwci.org

	ABSTRACT

Top Abstract Introduction The JWCI Algorithm for... Evolving Technology RFA Technique JWCI Experience Complications Unusual Complications Recurrence Discussion Summary References

 
Radiofrequency ablation (RFA) is increasingly used for the local destruction of unresectable hepatic malignancies. Relative contraindications include tumors in proximity to vital structures that may be injured by RFA and lesions whose size exceeds the ablation capabilities of the probe system employed. Given current technology, we believe that RFA should be cautiously utilized for lesions greater than 5 cm in diameter. Open (celiotomy) and laparoscopic approaches to RFA allow intraoperative ultrasonography, which may demonstrate occult hepatic disease. In addition, RFA performed via celiotomy can be accompanied by resection or cryosurgical ablation, and isolation of the liver from adjacent organs. Percutaneous RFA should be reserved for patients who cannot undergo general anesthesia, those with recurrent or progressive lesions, and those with smaller lesions sufficiently isolated from adjacent organs. Complications may be minimized when these approaches are selectively applied.

Key Words. Radiofrequency ablation • Hepatic malignancies

	INTRODUCTION

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The liver, a frequent site of primary and metastatic tumors, is second only to lymph nodes as the most common site of metastatic disease. Surgical resection of primary and metastatic hepatic tumors remains the gold standard of therapy. Unfortunately, because most hepatic malignancies are in unresectable locations or in patients with poor hepatic reserve, resection is possible in only 20% of these patients at the time of their presentation [1]. The remaining patients may be candidates for local ablative techniques (percutaneous ethanol injection, microwave tumor coagulation, interstitial laser photocoagulation, cryosurgical ablation, or radiofrequency ablation), hepatic-directed techniques (hepatic artery ligation, transcatheter arterial chemoembolization, hepatic artery infusional chemotherapy), or systemic chemotherapy. Cryosurgical ablation (CSA) of hepatic tumors is widely used for patients with unresectable disease [2-5]. CSA can improve overall survival [6], but it requires a celiotomy and is associated with a relatively high rate of serious complications, including coagulopathy, hemorrhage, pleural effusion, parenchymal cracking, bile duct injury, and acute renal failure [5, 7, 8]. Moreover, its instrumentation is cumbersome and expensive.

Radiofrequency ablation (RFA) destroys tumor by generating heat within a lesion (Fig. 1). During RFA, high-frequency alternating current causes thermal coagulation and protein denaturation; as the temperature is increased above 45°C, cellular proteins denature and cell structure is lost. RFA technology is commonly used in the ablation of aberrant conduction pathways in the heart and has become a primary procedure in the treatment of cardiac dysrhythmias. RFA has increasingly been utilized for unresectable hepatic malignancies.

View larger version (31K): [in this window] [in a new window]   Figure 1. Schematic diagram shows that RFA causes ionic vibration, which leads to protein denaturation, thermal coagulation, and ultimately cell death.

	THE JWCI ALGORITHM FOR MANAGEMENT OF UNRESECTABLE HEPATIC MALIGNANCIES

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At JWCI, patients with a diagnosis of primary or metastatic hepatic tumors are treated with a multimodality approach that includes surgical resection, CSA, RFA, and/or insertion of an hepatic artery infusion pump (HAIP) for delivery of hepatic-directed chemotherapy [5]. Because our group [12] and other investigators [13] have reported a disease-free and overall survival benefit associated with regional chemotherapy for metastatic colorectal cancer, we recommend placement of an HAIP in all patients who undergo resection and/or ablation. The treatment plan is determined after a history and physical, laboratory analysis including blood counts, chemistries, liver function tests, serum tumor markers, and radiologic evaluation. In addition, all patients undergo spiral-computed tomography (CT) with intravenous contrast, and select patients also undergo magnetic resonance imaging (MRI) or positron emission tomography (PET) using ¹⁸FDG.

RFA is approached either operatively, via laparoscopy or celiotomy, or percutaneously by ultrasound or CT scan guidance. Laparoscopic examination of the abdomen is undertaken in all operative cases to identify extrahepatic disease. Laparoscopy is extremely sensitive for the detection of peritoneal lesions; laparoscopic ultrasonography can detect hepatic lesions <2 cm in diameter, and it can identify disease not detected by preoperative imaging—including PET [14]. Overall, use of laparoscopy will avoid laparotomy or change the planned operation in 30% of the cases. Celiotomy is performed if laparoscopy is not possible. A formal assessment of the liver, parietal peritoneum, visceral surfaces of the stomach, small bowel, colon, lesser sac, and omentum is performed. The gastrohepatic ligament is divided and the caudate lobe is directly examined. The porta hepatis, celiac axis, and vena cava are examined and suspicious lymph nodes are biopsied. If enlarged periportal lymph nodes are not amenable to laparoscopic examination, a laparotomy is performed and the nodes are examined. Patients who have extrahepatic disease (except those with neuroendocrine tumors) are not eligible for RFA. Patients who have no evidence of extrahepatic disease undergo intraoperative ultrasonography (IOUS) of all liver segments; the size and location of each lesion are recorded and compared with preoperative imaging results.

Curative resection is always the first choice of treatment and is undertaken whenever possible. Patients who are not candidates for curative resection based on the location or bilobar distribution of hepatic tumors are considered for RFA. Patients eligible for RFA have no evidence of extrahepatic disease, a tumor volume less than 40% of total hepatic volume as determined by IOUS, and sufficient hepatic reserve to undergo ablation (Child-Pugh class A or B). Figure 2 shows our algorithm for RFA in patients with unresectable hepatic malignancies [9, 10]. A single 25-min ablation is used for lesions <3 cm in diameter. If the patient has severe hepatic dysfunction (Child B, C cirrhosis) or if laparotomy is contraindicated because of cardiac or respiratory dysfunction, larger lesions may be managed by multiple overlapping ablations performed laparoscopically. However, we generally prefer to use CSA for lesions >3 cm because in our experience, the recurrence rate for RFA of larger lesions is 35% [6]. Recurrence rates associated with newer-generation probes may be lower.

View larger version (27K): [in this window] [in a new window]   Figure 2. Algorithm for operative or percutaneous RFA at JWCI. Resectable lesions should be resected and an operative approach taken whenever possible.

	EVOLVING TECHNOLOGY

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View larger version (153K): [in this window] [in a new window]   Figure 3. Technology of RFA probes and generators is improving with the development of first-generation (top), second-generation (middle), and latest-generation (bottom) probes (RITA Medical Systems), each capable of larger areas of ablation. Reprinted with permission from Wood et al. [18].

	RFA TECHNIQUE

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Larger lesions are ablated with multiple overlapping fields. The probe is placed at the deep margin at one side of the tumor. Multiple overlapping ablations are then sequentially performed, progressing superficially and then laterally until the tumor and a 1-cm margin have been successfully ablated.

Following ablation, the probe tract is cauterized as the RFA needle is withdrawn. If target temperatures are not reached, as may be the case for lesions near major vascular structures (heat-sink), the tynes are withdrawn slightly or rotated approximately 45°C to increase the temperature in the region of ablation. Each tumor is ablated under imaging guidance with the goal of complete destruction of the tumor and a 1-cm margin of parenchyma around the lesion in all directions.

RFA via celiotomy or laparoscopy is performed with IOUS guidance in the operating room while the patient is under general anesthesia; percutaneous RFA is performed by an experienced interventional radiologist with ultrasonography or CT guidance in the radiology suite, after local anesthesia and conscious sedation.

Following laparoscopic RFA, patients are usually admitted for 23 h; percutaneous RFA is performed either on an outpatient or a 23-h-stay basis. Patients undergoing RFA via celiotomy require hospital admission. Complete blood counts and liver function tests are obtained following RFA and the next morning for patients staying in the hospital. Those patients undergoing additional procedures are treated according to the extent necessary. Patients are followed postoperatively with repeat spiral CT scanning or other anatomic imaging and tumor markers as appropriate. Scans are obtained at one week as a baseline and then every three months.

	JWCI EXPERIENCE

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We recently reported the results of RFA for the treatment of 231 unresectable hepatic tumors in 84 patients who had no evidence of extrahepatic disease [18]. The patient group was heterogeneous in terms of tumor type and previous therapy. The 84 patients underwent a total of 91 RFA procedures, most of which used an operative approach. In 51 cases, RFA was performed as the sole hepatic procedure. In the remaining 40 procedures, RFA was combined with resection, CSA, or HAIP. CSA was combined with RFA in a total of 16 patients with multiple hepatic metastases. CSA was selectively used for larger diameter lesions (>3 cm) approached via celiotomy. We previously demonstrated that RFA and CSA may be combined safely and that CSA allows more rapid ablation of larger lesions [5]. In this small group of patients, there were no significant intraoperative or postoperative complications. The median diameter of lesions treated by RFA was 3.0 cm (range, 0.3-9.0 cm). The median length of hospital stay was five days after RFA via celiotomy, one day after laparoscopic RFA, and 0 days after percutaneous RFA.

IOUS identified additional intrahepatic lesions not noted on preoperative spiral CT scans in 25 of 66 patients (38%) undergoing RFA via celiotomy or laparoscopy (Fig. 4). In all of these cases, the newly identified lesions were ablated under ultrasound guidance.

View larger version (122K): [in this window] [in a new window]   Figure 4. Intraoperative ultrasonogram shows a 0.8-cm colorectal carcinoma metastasis that was not visible on a preoperative spiral-CT scan. The RFA probe is placed into the center of the lesion and ablation performed. Reprinted with permission from Wood et al. [18].

	COMPLICATIONS

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In the study described above [18], seven patients (8%) suffered complications from RFA (Table 1). One patient sustained a third-degree skin and abdominal wall burn during the tract-ablation portion of a percutaneous procedure. This required debridement and wound care. Two other patients developed hepatic abscesses. In one of these cases, the abscess was likely secondary to a bile duct injury as a result of percutaneous RFA and was successfully treated with percutaneous drainage of the abscess and an endoscopically placed internal biliary stent (Fig. 5). Interestingly, the second case of abscess occurred five months after multiple overlapping RFAs of a 9-cm hepatoma in a patient with advanced cirrhosis. This patient did well for 20 months but recently demonstrated evidence of recurrence at the RFA site, as well as progression at other hepatic sites. These complications resulted in no permanent sequelae.

View larger version (125K): [in this window] [in a new window]   Figure 5. This patient had undergone previous right hepatic lobectomy for colorectal metastasis. Top left: Unresectable central hepatic metastasis. Middle left: The RFA probe is placed percutaneously into the lesion. Bottom left: After percutaneous RFA, the hepatic and portal veins remained patent. Top right: Post-procedure, the patient developed a bile duct stricture and subsequent hepatic abscess. Bottom right: These complications were successfully managed by percutaneous drainage of the abscess and endoscopic placement of a biliary stent. Reprinted with permission from Wood et al. [18].

	UNUSUAL COMPLICATIONS

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Since that study, we have noted two unusual complications as a result of percutaneous RFA. The first case was a 78-year-old man with a significant cardiac history, who developed a solitary colorectal metastasis in the left lobe of the liver. Percutaneous RFA resulted in a left hepatic artery pseudoaneurysm, which was subsequently successfully embolized (Fig. 6). The second case was an 80-year-old man who sustained an injury to the right hepatic artery during RFA of a hepatoma in segment 5, very close to the portal vein. Again, embolization was successful, but the patient later developed an hepatic abscess that required percutaneous drainage.

View larger version (388K): [in this window] [in a new window]   Figure 6. Left hepatic artery pseudoaneurysm following percutaneous RFA of a solitary colorectal metastasis in a 78-year-old man demonstrated on CT scan (A) and angiogram (B). Successful embolization of the pseudoaneurysm (C).

	RECURRENCE

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View larger version (128K): [in this window] [in a new window]   Figure 7. RFA recurrences appear as a rim of increased contrast uptake around an ablation scar. The left panel demonstrates a non-contrast image of an RFA recurrence as the RFA electrode is being placed percutaneously. A contrast image in the right panel demonstrates no rim enhancement after successful percutaneous ablation. Note the ablated electrode tract seen in this image. Reprinted with permission from Wood et al. [18].

	DISCUSSION

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The first RFA probes were monopolar needles that delivered current through a noninsulated tip. In an attempt to enlarge the size of the resulting lesion, bipolar needles were placed at variable distances. Although no prospective studies have compared the different probes, Rossi et al. [19] recently reported that an expandable needle electrode allowed a larger volume of ablation than did monopolar and bipolar needles.

Since the mid 1990s, various international and American studies have reported results of RFA for hepatic malignancy (Table 2) [9-11, 17-26]. To date, the largest clinical RFA report has been that of Curley et al. [11]. In this study of 169 hepatic tumors in 123 patients, approximately 75% of the population underwent RFA at laparotomy and 25% underwent RFA via a percutaneous approach. At a median follow-up of 15 months, the local recurrence rate was only 1.8% (3 of 169 lesions). Complications in this study were minimal (two abscesses and one post-RFA hemorrhage) and there was no procedure-related mortality. Smaller series [9, 10, 19, 20, 27] also have reported minimal complication rates, with local recurrence rates of approximately 10% (on a per patient basis) after short-term follow-up. Although these favorable reports have encouraged the use of RFA by both surgeons and radiologists, there is limited information on its potential risks and the optimal approaches under different clinical circumstances.

View larger version (115K): [in this window] [in a new window]   Figure 8. Resection of a liver metastasis is preferable whenever possible. In this patient with bilobar colorectal metastases, a partial left hepatic lobectomy (A) was combined with RFA of a second unresectable paracaval metastasis in segment 8 (B).

At a median follow-up of 13 months, 19% of our patients had developed recurrence; the local recurrence rate was 7% per lesion. Most of these patients had undergone RFA of large lesions, and in all cases RFA had been performed using a first-generation probe and generator. Because this probe has a small diameter of ablation (2-3 cm), all 16 patients who recurred had required overlapping ablations to encompass the tumor and 1-cm margins. We did not routinely use the Pringle maneuver (occlusion of hepatic inflow) to minimize heat loss from hepatic blood flow during RFA via celiotomy. When hepatic inflow is occluded using the Pringle maneuver, target temperatures within the lesion are reached much more quickly and the zone of ablation is enlarged [11, 30]. We have recently begun to evaluate the use of the Pringle maneuver but our study population is not yet large enough to permit meaningful analysis.

We previously reported that the rate of recurrence following ablation of lesions greater than 3 cm in diameter was significantly higher after RFA than CSA (38% versus 17%; p = 0.064) [5]. Similarly, two of the three recurrences reported by Curley et al. [11] occurred in tumors >6 cm in diameter. We believe that the maximum diameter of tumors treated with RFA depends in part on the specific probe. It also depends on the accurate delineation of the margins of ablation using ultrasonography or CT; this is especially important when multiple overlapping ablations are attempted. During CSA, the characteristic iceball is easily followed via real-time ultrasonography; by contrast, the increased echogenicity during RFA is more difficult to follow. Perhaps as RFA and intraoperative imaging technologies improve and procedures are performed under temporary occlusion of hepatic inflow (Pringle maneuver), larger lesions will be more successfully approached by RFA. However, in our limited experience with the larger probes, more time is required to ablate larger lesions. The current generators have increased output but they can power only one probe.

Our experience indicates that the rates of recurrence and complications following RFA are not negligible but can be minimized. Patients with hepatic malignancies, except those with neuroendocrine tumors, should be approached with curative intent and the goal of extending survival. IOUS during celiotomy or laparoscopy can upstage cancers by demonstrating intrahepatic disease not evident on spiral CT scans [31, 32]. Approximately 12% of patients undergoing laparoscopy prior to RFA will have extrahepatic disease and therefore will not be candidates for potentially curative procedures [5]. We prefer operative ablative procedures because either an open or laparoscopic approach allows detection of extrahepatic disease missed by preprocedure imaging. The laparoscopic approach is minimally invasive and useful for ablating a small number of small lesions. The celiotomy approach is more invasive but also more versatile; large and multiple tumors may be safely treated and RFA can be combined with other hepatic therapies (resection, CSA, or HAIP). We recommend RFA via celiotomy or laparoscopy in patients who are operative candidates; we reserve percutaneous RFA for patients who would not tolerate surgery or have recurrent or progressive disease. To avoid injury to adjacent structures, lesions approached percutaneously must not be located peripherally in the liver. Furthermore, lesion size and location must be within the capacity of the percutaneous approach.

In our experience, the risk of recurrence increases after ablation of lesions adjacent to major blood vessels. Because of the heat-sink effect of large vessels, the zone of ablation extends to near the vessel wall, but the tissue closest to the vessel is not ablated and therefore at high risk of persistent or recurrent disease. Also, a portal vein thrombosis has been reported after ablation of a periportal tumor during a Pringle maneuver [33], so due care should be exercised during ablations close to major vessels. Because major bile ducts are at increased danger for heat injury during ablation of central lesions, we place prophylactic biliary stents in patients undergoing ablation of tumor adjacent to major bile ducts. Thus far, we have been able to ablate these lesions with stents in place, without untoward biliary complications.

	SUMMARY

Top Abstract Introduction The JWCI Algorithm for... Evolving Technology RFA Technique JWCI Experience Complications Unusual Complications Recurrence Discussion Summary References

 
In summary, RFA can be safely applied via operative approaches (laparoscopy or celiotomy) or percutaneously for unresectable hepatic malignancies. Operative approaches allow more accurate assessment for the presence of extrahepatic disease, better evaluation of intrahepatic disease (IOUS), and isolation of the liver from adjacent organs that may be injured during ablation of superficial lesions. Operative approaches also are preferable in patients with multiple and large lesions, since optimal management usually requires a combination of treatment modalities. Percutaneous RFA should be reserved for patients who are not operative candidates and patients with recurrent or progressive disease. Extra care should be taken when using RFA in lesions larger than 3 cm in diameter, to reduce the rate of recurrence. Because of the relatively high rate of disease progression at intrahepatic and extrahepatic sites, consideration of hepatic-directed and systemic chemotherapy is reasonable in these patients [11, 13]. Severe complications and even death after RFA are rare but warrant careful selection of patients and RFA approaches.

Related articles in The Oncologist: Emerging New Opportunities for Patients with Hepatic Metastases from Colorectal Cancer or Primary Hepatocellular Cancer. Pinedo HM, van Groeningen CJ. The Oncologist 2001;6:12-13. Radiofrequency Ablation of Malignant Liver Tumors. Curley S. The Oncologist 2001;6:14-23.

 

	ACKNOWLEDGMENTS

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Supported in part by funding from the Rogovin-Davidow Foundation, Los Angeles, CA.

	REFERENCES

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Related articles in The Oncologist:

Emerging New Opportunities for Patients with Hepatic Metastases from Colorectal Cancer or Primary Hepatocellular Cancer

H.M. Pinedo and C.J. van Groeningen
The Oncologist 2001 6: 12-13. [Full Text]  

Radiofrequency Ablation of Malignant Liver Tumors

Steven A. Curley
The Oncologist 2001 6: 14-23. [Abstract] [Full Text]  

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