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Radiofrequency Ablation in 447 Complex Unresectable Liver Tumors: Lessons Learned

From the John Wayne Cancer Institute at Saint John’s Health Center (RJB, DTN, TFW, LJF, AJB), Santa Monica, California; and the Cancer Center at Century City Hospital (DPA, LJF, AJB), Los Angeles, California.

Correspondence: Address correspondence and reprint requests to: Anton Bilchik, MD, John Wayne Cancer Institute, 2200 Santa Monica Blvd., Santa Monica, CA 90404; Fax: 310-449-5261; E-mail: bilchika{at}jwci.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
Background: Radiofrequency ablation (RFA) is a promising technique for unresectable hepatic malignancies. We reviewed our RFA experience to identify variables affecting local recurrence.

Methods: Patients undergoing RFA between 1997 and 2001 were reviewed for demographics, tumor size, pathology, diagnosis, recurrence, procedures, survival, and complications.

Results: The 447 unresectable liver tumors were ablated in 198 procedures. The 153 patients averaged 61.9 years of age and 1.25 RFA procedures per patient. Follow-up averaged 11 months. Serial ablations were performed in 28 patients, 8 of whom are without evidence of disease. Tumors were most commonly carcinomas of colorectal, hepatocellular, breast, and melanoma histologies. Colorectal carcinomas and hepatomas individually recurred more frequently than all other tumor types combined in univariate analyses (P = .009 and P = .008, respectively). Patients with multiple tumors ablated recurred significantly more frequently (P = .001). Size was also significant in univariate and multivariate analyses (P = .0032 and <.0001, respectively). Eighteen patients experienced 36 complications.

Conclusions: Size has the highest correlation with local recurrence, but multiple tumors and pathology may also predict local recurrence risk. Large, complex lesions can be safely serially ablated, but because of morbidity and recurrence, RFA should not replace resection as the primary treatment of resectable liver tumors.

Key Words: Radiofrequency ablation • Hepatic metastases • Recurrence • Serial ablations

	INTRODUCTION

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Radiofrequency ablation (RFA) is a novel technique, first used in the 1980s, for the ablation of aberrant conduction pathways in the heart.¹ Initially, there was concern that this technology would be associated with ventricular dysrhythmias, but this complication was infrequent. With only a 3% to 5% overall complication rate for cardiac ablation,² RFA was deemed safe, and its use became more widespread. Application to liver tumors was begun in the 1990s, and the prevalence of RFA has been rapidly increasing because of its versatility. Surgeons are now able to effectively perform RFA via laparotomy or through a laparoscope. More recently, percutaneous ablations have been performed by interventional radiologists under ultrasound or computed tomography (CT) guidance.³

Since its introduction, RFA has been applied to unresectable hepatic primary and metastatic malignancies.⁴ Resection remains the gold standard for liver tumors, but two thirds of these tumors are found to be unresectable at operation even after preoperative screening.⁵ Although there are no data to support RFA as a replacement for hepatic resection, it has been attempted as an alternative or adjunct to excision.⁶ However, as yet there are few data on risk factors for recurrence or on results of serial RFA procedures. One prior study of moderate size⁷ analyzed recurrence risks but did not compare recurrent and nonrecurrent follow-up or adjust for competing risk. Because the RFA experience at the John Wayne Cancer Institute is one of the largest in the world, we reviewed our data to identify prognostic factors for local recurrence (LR), determine the feasibility of serial RFA, and review the morbidities associated with the procedure.

	METHODS

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The study population comprised all patients whose primary or metastatic liver tumors were treated at the John Wayne Cancer Institute and Century City Hospital from November 1997 to January 2002. The patients who underwent RFA via open, laparoscopic, or percutaneous methods were identified by review of our computer-assisted hepatobiliary and radiographic databases. Patient age and sex; tumor histology, number, location, and size; procedural history; RFA method; disease status; follow-up date; death date; and complication data were reviewed for all patients. Disease status was classified as no evidence of disease (NED), alive with disease (AWD), dead of disease (DOD), or dead of other causes at last known follow-up. Recurrences were defined as tumors occurring at sites of prior ablation and as detected by CT imaging or via biopsy diagnosis. All intraoperative and postoperative complications and morbidities were included in the analysis.

Patient Evaluation
Patients were referred to either the primary surgeons directly (AJB and LJF) or to a multidisciplinary RFA/tumor board conference of surgeons, medical and radiation oncologists, interventional radiologists, pathologists, and allied health professionals. The modality of RFA chosen was based on the clinical judgment of the primary surgeons and interventional radiologist (DPA). RFA was not considered in lieu of resection unless patients were medically ineligible for hepatic resection or unless lesions were unresectable by virtue of their number, location, or size relative to liver volume.

RFA Methods
RFA was performed at one of two institutions (Saint John’s Health Center or Century City Hospital) by open and laparoscopic methods by the primary surgeons, and at one institution (Century City Hospital) by the primary interventional radiologist via the percutaneous CT- and ultrasound-guided method. Ablative procedures undertaken via laparotomy or laparoscopy were performed in the operating room with the patient under general anesthesia. Percutaneous RFA was performed in the radiology suite with the patient under local anesthesia with conscious sedation.

Ablations were performed as described previously.⁸ Briefly, the RITA model 30^TM (50-W) probe (RITA Medical Systems, Inc, Mountain View, CA) was used until mid 1999. This probe can ablate a 2.5- to 3-cm diameter of tissue. Since that time, the model 70^TM probe (RITA), the 5-cm Starburst XL^TM needle/150-W electrode (RITA), or a 200-W cluster probe (Cool-tip^TM; Radionics, Burlington, MA) has been used. Percutaneous ablations also initially used the 100-W LeVeen Needle Electrode^TM (Radiotherapeutics, Mountain View, CA) until March 1999. These last two probes are capable of ablating a 4- to 5-cm diameter of tissue. RFA was performed in all cases by orienting the RFA needle parallel to the plane of the ultrasound probe or under CT guidance. Tines with thermocouples were deployed through the primary channel, and 50 to 200 W of alternating current was delivered. As soon as temperatures exceeded 90°C, ablation was then timed for 8 to 25 minutes, depending on which probe was used. The formation of the coagulum during this process was monitored under real-time ultrasound. Thirty seconds after cessation of ablation, the temperature of the tines was measured. If target temperatures 60°C were not reached, as sometimes occurs with lesions near major vascular structures, which serve as a heat sink, the tines were withdrawn slightly or rotated approximately 45°. After mid 2000, percutaneous procedures were also scanned after ablation to assess the completeness of the ablation. In each case, a 1-cm margin of normal hepatic parenchyma was ablated surrounding the lesion. Margins closer than 1 cm to adjacent vascular and biliary structures were ablated up to those structures. Lesions unable to be ablated with an adequate margin on placement of the probe in the center of the lesion underwent multiple overlapping fields. After ablation, the probe tract was cauterized as the RFA needle was withdrawn.

Post-RFA Care and Follow-Up
After RFA performed via laparotomy, patients were admitted to the hospital for recovery. Laparoscopic RFA patients were usually admitted for 23 hours, and percutaneous RFA was performed either on an outpatient basis or via a 23-hour admission. Admitted patients underwent complete blood counts and liver function tests after RFA and the next morning. Those undergoing concurrent procedures were also treated in accordance with those procedures. After surgery, patients underwent repeat blood tests at their follow-up appointment approximately 1 week after operation, then every 3 months for 2 years and every 6 months thereafter. CT scanning and tumor marker evaluations were performed after surgery as deemed clinically appropriate. LRs were identified radiographically via CT scan as visible tumor found within or precisely at the margin of a prior ablation. In several cases in which imaging was not definitively characteristic of tumor recurrence, biopsy was performed for confirmation.

Data Analysis
CT scans obtained before and after RFA were reviewed to correlate the site of the recurrence and the site of the ablation. Tumor type groups consisting of fewer than four patients were grouped together as a separate category entitled "other" for statistical calculation related to pathology. All data were entered into a computerized Microsoft Excel^TM database (Microsoft, Inc., Redmond, WA). SAS^TM version 8 statistical software (SAS Institute, Inc., Cary, NC) was used for statistical analysis. Analysis for competing risk was accomplished by censoring patient data for those with follow-up <6 months, on the basis of follow-up variation between recurrent and nonrecurrent cohorts. Univariate and multivariate analyses treated lesion size as a continuous variable. The multivariate model was created to assess the effect of those factors found significant in univariate analysis. The generalized estimating equation was used for multivariate analysis to correlate lesion size, histology, number, and modality with LR. A backward procedure was used for covariate selection. An alpha level of .05 was deemed statistically significant.

	RESULTS

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Study Characteristics
There were 153 patients who underwent ablation for 447 unresectable primary and metastatic hepatic tumors. These ablations were performed in 198 RFA procedures: 66 laparotomies, 102 percutaneous procedures, and 30 laparoscopic procedures. An average of 2.92 ± 2.87 lesions (range, 1–13) were ablated per procedure (median, 2.00). Although 28 patients (18%) underwent serial ablations, only 1 patient underwent >5 ablations. Cohort demographics are listed in Table 1.

The most common histologies were colorectal cancer (38.6%), hepatocellular cancer (13.7%), breast cancer (11.1%), melanoma (8.5%), carcinoid tumor (7.2%), sarcoma (3.9%), and ovarian cancer (3.9%) origins. There were two patients each with lung, gastric, and neuroendocrine tumors; there was one patient each with tumors of cholangiocarcinoma, esophageal carcinoma, adenocarcinoma of the gastroesophageal junction, hemangiopericytoma, desmoplastic small round cell tumor, malignant inflammatory fibroblastic tumor, renal cell carcinoma, medullary thyroid, and tongue adenocarcinomas, and one patient had adenocarcinoma of unknown origin. These last 13 histological types were grouped under the classification of "other" histologies.

Analysis of variance (ANOVA) for age differences among tumor types demonstrated a significant variation (P = .0004), with hepatocellular carcinoma patients being oldest (median, 69.72 years) and melanoma patients being youngest (median, 53.17 years). The average tumor count per patient did not significantly differ among tumor types (ANOVA; P = .058), although carcinoid patients had the most tumors (mean, 5.45) and breast cancer patients had the fewest (mean, 1.94). There was no difference in tumor size between patients with differing tumor types (ANOVA; P = .13). There was also no difference in follow-up between tumor types (ANOVA; P = .39).

Local Recurrence
LRs at a prior RFA site occurred in 32 patients (20.9%) and in 52 individual tumors (11.6%). The incidence of recurrence was highest for hepatocellular carcinomas (22.0%), colorectal tumors (18.3%), and melanomas (10.9%). LRs occurred in 6.7%, 9.0%, and 15.1% of open, laparoscopically, and percutaneously ablated tumors, respectively. The age and sex of those who had recurrences were not different from those of patients who did not (P = .62 and .36, respectively). This was maintained in multivariate analysis and when adjusting statistically for competing risk (adjustment for patients who die because of other causes or progression of disease elsewhere before the opportunity for developing an LR).

The overall risk of LR increased with tumor size. This was the most significant factor in multivariate analysis (P < .0001) regardless of the model used. Tumor numbers also were significant when analyzed in univariate and multivariate fashion. Univariate and multivariate models are presented in Tables 2 and 3. Finally, univariate analysis based on histology demonstrated that colorectal carcinomas and hepatomas individually recurred significantly more frequently than all other tumor types combined, whereas carcinoid and breast lesions individually recurred significantly less frequently (P = .042 and .038, respectively). Multivariate analysis was significant for histology only before competing risk adjustment.

Morbidity
Eighteen (11.8%) of the 153 study patients experienced 1 complications directly or indirectly related to the RFA procedure (Table 4). The most common complication was discrete abscess formation; this accounted for 9 (25%) of the 36 individual complications. Biliary injury was the second most frequent morbidity encountered, with five occurrences (13.9%). There were 22.2%, 2.7%, and 75.0% of complications occurring via open, laparoscopic, and percutaneous approaches, respectively. The average tumor size was 4.23 cm for those patients with complications and 2.60 cm for those without complications (P = .0001). Neither the type of tumor nor the number of RFA procedures was correlated with morbidity. Of the 18 patients who experienced complications, 12 (67%) underwent only 1 RFA, 5 (27%) had 2 RFAs, and 1 (5.5%) had 4 RFA procedures.

	DISCUSSION

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RFA is not advocated as a replacement for resection, which remains the gold standard for treatment of liver tumors. We use RFA solely (1) for those tumors that are unresectable by virtue of their number, location, or size relative to liver volume or (2) because of a patient’s medical inability to undergo resection. Because RFA is often used as an adjunct to resection, this review included patients who underwent RFA in conjunction with resection.

Three factors affected recurrence at a previously ablated site. The first and most significant throughout the analysis was lesion size. Initial analysis used arbitrary 3-, 4-, and 5-cm thresholds, which demonstrated that recurrence risk at a prior RFA site increased with size (P = .010, .002, and .0006, respectively). Subsequent analysis was then performed instead as a continuous variable, and this remains the most important LR risk factor in univariate and multivariate analyses (Tables 2 and 3). Two prior studies^7,9 also note recurrence as a function of size; however, neither specifies competing risk, which, if not considered, may artificially decrease the apparent recurrence rate. One of these studies⁹ consisted of RFA performed via laparotomy alone and reported a 20% complication rate.

When considering tumor size, it is also important to note that four generations of probes were used during the study period. Earlier radiofrequency probe models were capable of only 3-cm ablations, whereas current models can ablate up to 7 cm. This suggests that the earlier need for more overlapping ablations may have increased the risk of incomplete or inconsistent ablation.

More frequent recurrence in larger lesions may also be due to the learning curve. The RFA technique involves both facility with the probe and the ability to properly image the procedure. RFA depends on accurate ultrasound or CT guidance to discriminate lesion boundaries. In cases of lesions requiring overlapping fields, discrimination of ablated and nonablated tissue becomes vital to ablate lesions in toto. With probe fields enlarging and experience increasing, ablation efficiency should improve. Simultaneously, however, there have been more aggressive attempts to ablate larger lesions. These factors are difficult to accurately isolate but may be reflected in the risk associated with lesion size.

Despite these caveats, however, we do not recommend abandoning RFA for such tumors at this time. The higher LR and complication risks must be considered in light of RFA’s primary palliative role. Serial ablation is consistent with increasing trends toward resection and cytoreduction of metastatic disease. Twenty-eight percent of our patients in this series remain NED after RFA, but whether serial ablation extends survival remains to be seen. We do recommend significant caution, however, to those ablating larger lesions (especially those >5 cm) without extensive RFA experience or if a small, earlier-generation probe is used when multiple overlapping ablations are required.

Histological type was also found to be significant in univariate analysis, but when combined for the multivariate model, it did not withstand competing risk adjustment. Colorectal and hepatocellular histologies demonstrated a univariate increase in recurrence, whereas breast and carcinoid tumors recurred significantly less frequently. Because size was not different among tumor types, this phenomenon might reflect differences in the parenchymal milieu, the tumor itself, or efficiency of ablation of particular tissue types. Characteristics such as tumor density, vascularity, tumor ingrowth into surrounding tissue, or peritumoral micrometastatic disease may influence recurrence. Differences in recurrence by segment have been reported after liver resection.¹⁰

We noted a higher recurrence rate for our hepatocellular and colorectal carcinomas than prior reports.^9,11–13 The precise reason is not clear, but our patients had larger tumors⁹ and were 10 to 13 years older than the specified patient populations in other series^12,13 for these histologies. Although we did not find that age contributed to LR, differences in population morbidities and, thus, immunological tumor surveillance may account for these differences. Technical factors such as differences in conduction by certain tumor types or even consistencies of certain probes may also be relevant. Further study is required to assess histological differences.

We also noted a higher incidence of recurrences in percutaneously ablated tumors, but when modality comparisons were placed in multivariate models, no difference was noted. An actual difference may be demonstrable with a larger cohort, but these were also patients at highest medical risk. Additionally, this technique was often applied specifically for multiply recurrent disease. This selection bias certainly influences this observation, and thus one must be careful about drawing conclusions based on these modality statistics.

We have performed serial ablations in 28 patients. More ablations may increase the risk of an incomplete cytoreduction, with subsequent tumor recurrence. Increased LRs in those with multiple tumor ablations and in serially ablated patients may reflect this. Some serial ablations were also performed because of LRs, contributing to the increased incidence. It is therefore not surprising that LR and morbidity were higher in the serially ablated population. More intriguing was the nearly identical distribution of disease status for patients who underwent single versus serial ablations. Continued follow-up is necessary in these cohorts for more definitive comparison, but these data suggest that serial RFA is feasible, because disease status remains similar.

These issues underscore the need to ensure complete and accurate ablations. Although there has been some suggestion that the addition of a hepatic portal Pringle maneuver may increase the size of the ablated field,¹⁴ no trial has determined whether this technique may improve the efficacy of RFA. We have used the Pringle maneuver on various occasions but have noted little difference. As long as wattage and temperature, monitored by the RFA device, are maintained at the goal for the proper period, no difference should be seen in the efficacy of the ablation.

Thirty-six complications occurred in 18 patients in this study. Except for one smaller series,⁹ most describe RFA morbidities by numbers of complications, instead of specifying the number of patients involved. Comparison with current literature therefore requires redefinition of complication rate from the number of patients with complications over the total number of patients, to the number of complications divided by the total number of patients. With this definition, RFA morbidity varies from 0% in a small homogeneous series of 10 patients with hepatocellular carcinoma¹¹ to 34.6% in a much larger heterogeneous series.⁷ Our series was within this range, with a 23.7% complication rate. If we define patient morbidity as the percentage of patients experiencing complications, this series demonstrated an 11.7% morbidity.

Our two most frequent complications were infectious complications and biliary injury, accounting for approximately 30% and 14% of our complications, respectively. Fever, infection, sepsis, and abscess account for more than one third of complications in at least 3 series of 68 patients.^8,12,15 Biliary injuries are also frequent and constitute approximately 20% of those series reporting them.^7,15 Although many injuries are unforeseeable, biliary injury is often predictable by tumor location. Peribiliary tumors constitute many lesions whose only treatment option is RFA. Additionally, we have noted that there have been four previously documented cases of postablation hepatic failure or insufficiency.^7,8,13 Finally, no specific risk factors for infectious complications have yet been identified.

RFA remains a viable technology for single or serial palliative cytoreduction in individuals with unresectable hepatic malignancies. We have demonstrated that whereas age and sex do not influence the pattern of recurrence, tumor size, number, and histology seem to affect risk. Percutaneous procedures were associated with more recurrences, but this is likely a product of selection bias. Further data accrual is needed to determine the optimal criteria for patient selection and outcome prediction.

	Acknowledgments

 
The authors thank Xing Ye and He-Jing Wang for their statistical expertise. Supported by funding from the Rogovin-Davidow Foundation, Los Angeles, CA, and the Rod Fasone Memorial Cancer Fund, Indianapolis, IN.

	Footnotes

 
Presented at the 55th Annual Cancer Symposium of the Society of Surgical Oncology, Denver, Colorado, March 14–17, 2002.

Radiofrequency ablation has become more widespread despite the paucity of data on patient selection. This study found that prognostic factors for local recurrence after ablation include tumor size, tumor number, and histology. Serial ablations are also feasible in individual patients.

Received for publication March 5, 2002. Accepted for publication August 19, 2002.

	REFERENCES

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 

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