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Vascular and Interventional Radiology |
1 From the Department of Radiology, Ospedale Generale, Busto Arsizio, Italy (L.S., T.I., M.D., L.C.); Department of Radiology, Ospedale Civile, Vimercate, Italy (T.L., F.M.); Department of Radiology, Beth Israel Deaconess Medical Center, Boston, Mass (S.N.G.); Decision Analysis and Technology Assessment Group, Department of Radiology, Massachusetts General Hospital, Zero Emerson Pl, Suite 2H, Boston, MA 02114 (E.F.H., G.S.G.); and Department of Health Policy and Management, Harvard School of Public Health, Boston, Mass (G.S.G.). From the 1999 RSNA scientific assembly. Received October 5, 2000; revision requested November 22; revision received February 15, 2001; accepted April 3. S.N.G. supported by Radionics. Address correspondence to G.S.G.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: In 117 patients, 179 metachronous colorectal carcinoma hepatic metastases (0.9–9.6 cm in diameter) were treated with RF ablation by using 17-gauge internally cooled electrodes. Computed tomographic follow-up was performed every 4–6 months. Recurrent tumors were retreated when feasible. Time to new metastases and death for each patient and time to local recurrence for individual lesions were modeled with Kaplan-Meier analysis. Modeling determined the effect of number of metastases on the time to new metastases and death and effect of tumor size on local recurrence.
RESULTS: Estimated median survival was 36 months (95% CI; 28, 52 months). Estimated 1, 2, and 3-year survival rates were 93%, 69%, and 46%, respectively. Survival was not significantly related to number of metastases treated. In 77 (66%) of 117 patients, new metastases were observed at follow-up. Estimated median time until new metastases was 12 months (95% CI; 10, 18 months). Percentages of patients with no new metastases after initial treatment at 1 and 2 years were 49% and 35%, respectively. Time to new metastases was not significantly related to number of metastases. Seventy (39%) of 179 lesions developed local recurrence after treatment. Of these, 54 were observed by 6 months and 67 by 1 year. No local recurrence was observed after 18 months. Frequency and time to local recurrence were related to lesion size (P 
.001).
CONCLUSION: RF ablation is an effective method to treat hepatic metastases from colorectal carcinoma.
Index terms: Liver neoplasms, secondary, 761.33 • Liver neoplasms, therapy, 761.1269 • Radiofrequency (RF) ablation, 761.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Considerable interest has focused on the potential role of RF ablation in patients with liver malignancies (13–27). Early results have been promising; however, published series have often included patients with both primary and secondary tumors or metastases from multiple primary tumors, or authors have reported only relatively short-term results. The combination of primary and secondary tumors and/or the relatively short-term follow-up in these earlier reports makes it difficult to properly evaluate the merits of RF ablation in patients with colorectal carcinoma. The purpose of this study was to report the results of an ongoing study of RF ablation in patients with hepatic colorectal carcinoma metastases.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients
One hundred seventeen consecutive patients with 179 metachronous colorectal carcinoma liver metastases were treated with percutaneous RF ablation from July 1995 to October 1999. Seventy-five patients were treated at Busto Arsizio, while the remaining 42 were treated at Vimercate. Written informed consent was obtained from all patients prior to treatment. There were 81 men (69.2%) and 36 (30.8%) women. Ages ranged from 36 to 85 years (mean, 64.8 years; SD, 10.8; median, 67 years). At the initial RF ablation procedure, 74 (63.2%) of 117 patients had one metastasis, while 29 (24.8%), nine (7.7%) and five (4.3%) patients had two, three, and four metastases, respectively. These 179 metastases ranged from 0.6 to 9.6 cm in diameter (mean, 2.8; SD, 1.2; median, 2.6). The largest metastasis in each patient ranged from 0.7 to 9.6 cm (mean, 3.2 cm; SD, 1.3; median, 3.0 cm). All metastases were at least 1 cm from the hepatic hilum, gallbladder, or bowel wall.
All patients had undergone primary tumor resection 6–30 months prior to the initial RF ablation procedure. At the time of primary tumor resection, two (2%) of 117 patients underwent resection of synchronous liver metastases (two and five metastases in one patient each). Proof of malignancy for at least one metastasis was obtained in all 117 patients with ultrasonography (US)-guided fine-needle aspiration biopsy. Patients were not considered for surgical metastasectomy due to extrahepatic metastases (13 patients); prior hepatic metastasectomy (24 patients); age, disease extent, and/or comorbidity (58 patients); or refusal to consent for surgery (22 patients). The decision to perform RF ablation was made by the treating physicians, in consultation with the patients and referring oncologists in all cases. Twenty (17%) of 117 patients underwent systemic chemotherapy only prior to RF ablation, 84 (72%) of 117 patients underwent systemic chemotherapy prior to and following RF ablation, and 13 (11%) of 117 patients did not undergo any chemotherapy.
Pretreatment Diagnostic Work-up
Pretreatment diagnostic work-up included both hepatic US examination and abdominal helical computed tomography (CT) in all patients. US (Technos or AU5, Esaote, Genoa, Italy; Elegra, Siemens, Issaquah, Wash) was performed by using 3.5-MHz convex probes equipped with attachments for biopsy and electrode insertion. No contrast material was administered. CT (Somatom DRH, Siemens, Erlangen, Germany; PQ5000, Picker, Cleveland, Ohio; Hi-Speed Advantage, GE Medical Systems, Milwaukee, Wis) was performed during and immediately following injection of 200 mL of iopamidol (Iopamiro; Bracco, Milan, Italy) at 3–4 mL/sec. Scanning was initiated 25 seconds and again 60 seconds following the initiation of contrast material injection, to obtain images during arterial- and portal-dominant phases of enhancement, by using 5-mm section thickness, 7-mm collimation, 1:1 pitch, 120 or 140 kVp, and 280–300 mA.
RF Ablation Technique
All procedures were performed by one of two radiologists (L.S., T.L.). Both had at least 15 years of experience performing image-guided in situ tumor ablation procedures. Ablation was performed with general anesthesia, endotracheal intubation, and mechanical ventilation (219 treatments in 107 patients), assisted ventilation during short-acting anesthesia by using propofol (one treatment in one patient) or conscious sedation and analgesia (nine treatments in nine patients). When using conscious sedation, anesthetic cream containing prilocaine and Xylocaine (EMLA, Astra, Sweden) was applied to the skin 1 hour before treatment. Subsequently, a neuroleptic (droperidol [Sintodian]; Farmitalia, Milan, Italy; 1.25–2.5 mg) and an analgesic (fentanyl [Fentanest]; Farmitalia, 50–250 µg) were intravenously administered by an anesthesiologist. Blood pressure, respiration, pulse, pulse oxygenation, and electrocardiogram were monitored continuously.
Internally cooled, 18-gauge, RF electrodes (Cool-tip; Radionics, Burlington, Mass) with 2.5–4.0 cm of exposed tip were used to deliver RF energy to the tumors. These electrodes contained two central lumina through which 0°C sterile water was perfused to the electrode tip, and warmed effluent was returned to an external collection unit. A peristaltic pump maintained perfusion at 10–25 mL/min. Tip cooling reduced heating immediately adjacent to the electrode and thereby minimized tissue vaporization and its deleterious effects on circuit impedance. This permits increased energy deposition and increases the volume of coagulation necrosis (28).
RF ablation was performed with real-time US guidance by using a 3.5-MHz scanning probe. A guide incorporated into the US probe was used for electrode placement. After cleaning the skin with iodized alcohol (also used as contact medium), the RF electrode was advanced into the tumor. For lesions in the right lobe, an intercostal approach with the patient in the left lateral decubitus position was generally used. For lesions in the left lobe, a subcostal approach was most often used. Single RF electrodes were used for 133 treatments, while clusters of three electrodes spaced 5-mm apart were used for 96 treatments. The cluster-electrode technique increases coagulation necrosis compared with a single electrode technique (29). Grounding was achieved with two or more 1,000-cm2 grounding pads placed on the skin.
Electrodes were attached to a 500-kHz, monopolar RF generator (Model 3D or CC-1; Radionics) capable of producing 150–200 watts of power. A thermocouple embedded in the electrode tip continuously measured local tissue temperature. Tissue impedance was continuously monitored by using circuitry incorporated into the generator. RF energy was applied for 10–20 minutes. After measuring baseline tissue impedance, generator output was slowly increased to generator maximum or until circuit impedance increased. If impedance increased more than 10–20 
above baseline, current was stopped for 10 seconds and then reapplied at the same milliamperage. If uncontrolled impedance increases were observed (usually in the latter third of the procedure), peak current was reduced by 25–50 mA until stable impedance was obtained. Pulsed RF application has been shown (30) to increase coagulation compared with continuous RF application.
Mean total procedure time was 45 minutes per session, including tumor localization, treatment, electrode removal, and immediate postprocedure US. No technical problems were encountered. Electrode tip temperature increased to greater than 80°C immediately following the cessation of RF application and electrode cooling and remained above 60°C for at least 2 minutes in all cases. Following RF ablation, all patients were hospitalized for 2 days, largely due to local preferences.
Assessment of Treatment Effectiveness
Follow-up CT was performed by using the same technique as before treatment. Initial posttreatment scans were obtained 7–14 days following ablation. Areas of hypoattenuation that did not enhance with contrast medium were considered to represent necrotic tissue (16,17,28,31). When residual tumor was identified on initial posttreatment CT, a second session of RF ablation was performed. US was not used to determine treatment effect, since it does not accurately predict the extent of induced coagulation necrosis (16).
Subsequently, patients underwent follow-up with contrast material–enhanced CT, initially at 3–4 months following therapy and thereafter at 4–6 month intervals. Each CT image was compared with baseline studies. Follow-up CT scans were interpreted prospectively by a total of four investigators (L.S., T.L., T.I., F.M.) two from each institution. No more than two of these were involved in the treatment of any individual patient. In all cases, a consensus of the readers was used to judge treatment effectiveness. Treated tumors were classified according to (a) interval stability or reduction in size indicating local control or (b) interval enlargement and/or contrast enhancement indicating local tumor recurrence. The presence of any new metastases was also recorded. If local tumor recurrence was observed, repeat treatment with RF ablation was considered. The decision to retreat was made, in consultation with the patient and referring oncologist, based on the likelihood of achieving local control and the patient’s overall condition. All complications that occurred during follow-up were also recorded based on the results of imaging tests and interval medical history.
Statistical Analysis
Time to death and to the first occurrence of new metastases for each patient and time to first local recurrence of an individual lesion were modeled with a Kaplan-Meier analysis. If a lesion underwent local recurrence, all of that patient’s other lesions were considered censored in this measure at that time. Modeling determined the effect of the number of metastases on the time to new metastases and to death and the effect of tumor size on local recurrence. In each case, the potential explanatory factor was treated as a continuous covariate and significance determined by the Wilcoxon and log-rank tests. The explanatory factor was then treated as a grouping factor, with lesions separated into those lesions 2.5 cm or less, those 2.6–4.0 cm (inclusive), and those 4.0 cm or larger in diameter. This was used to create tables reflecting the estimated median and mean time to death, new metastases, or local recurrence for each group, and to generate the Kaplan-Meier curves in Figures 1–5.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patient Outcomes
Follow-up ranged from 6 to 52 months. Patient status was determinable at 12, 24, 36, and 48 months in 96 (82%), 64 (55%), 45 (38%), and 38 (32%) of 117 patients, respectively.
Thirty-six patients (31%) died. Estimated median survival for all patients was 36 months (95% CI; 28, 52 months). One, 2-, and 3-year survival was 93%, 69%, and 46%, respectively, estimated from the survival curves.
Time until death was not significantly related to the number of metastases (P = .84; Table 1, Fig 1) or the size of the largest lesion (P = .21; Table 2, Fig 2). The mean time to death appears to decrease as the number of metastases or the maximum diameter increases; however, this may have been a function of our initial conservative choice (ie, patients with fewer and/or smaller metastases) of the cases treated (earliest cases have the longest potential follow-up and thus the longest potential survival).
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.001). Time to local recurrence decreased with increasing lesion size, while frequency of recurrence increased (Table 4, Fig 4).
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When comparing patients (with recurrences) who underwent retreatment to those who did not, retreatment did not significantly affect survival. Table 5 and Figure 5 present the number and percentage of patients surviving among patients with no local recurrence and, among those with local recurrence, the percentage surviving with and without retreatment. Among those with local recurrence, retreatment does not appear to alter the likelihood of survival (P = .80, Fisher exact test). However, there was a trend (P = .073) toward longer survival in patients undergoing retreatment.
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One additional patient in whom a metastasis was treated at the dome of the liver reported abdominal pain 3–4 hours postprocedure. Orthostatic hypotension was noted and a CT demonstrated a small intraperitoneal hemorrhage. This patient remained in the hospital for 72 hours but did not require transfusion as the hematocrit stabilized at 36.2 mg/dL (from 40.7 mg/dL). All other patients were discharged uneventfully on the second day postprocedure.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Hepatic resection (metastasectomy) has been considered the only potentially curative treatment for patients with metastatic disease isolated to the liver. To our knowledge, the first reported (44) resection of a liver metastasis was in 1888, and, as early as 1963, Woodington and Waugh (45) reported a 20% 5-year survival rate after hepatic resection in selected patients. More recently, findings (39,46–67) have demonstrated that—in appropriately selected patients—a 5-year survival rate of 24%–50% can be achieved with an operative mortality of less than 10%. Unfortunately, in many patients, liver metastases are so numerous or widely distributed that resection is infeasible. Furthermore, patients may not be considered for metastasectomy due to age or comorbidity.
Recently developed minimally invasive techniques for in situ tumor ablation may provide reasonable alternatives for patients who are not surgical candidates. Furthermore, they may be reasonable alternatives to metastasectomy in some patients due to their decreased morbidity and cost. Ablation has the additional advantage of being easily repeatable; new or recurrent metastases can be treated or retreated as they are detected. Promising early results have been reported; however, the most appropriate role for these therapies in patients with metastatic colorectal carcinoma and their performance relative to metastasectomy remain to be determined.
To our knowledge, our experience with percutaneously applied cooled-tip RF ablation to treat 179 hepatic colorectal carcinoma metastases in 117 patients is the largest such series with the longest follow-up reported in the medical literature. Our results suggest that RF ablation can be easily performed, is associated with minimal complications, and can result in favorable patient outcomes. Estimated median survival was 36 months, with 1-, 2-, and 3-year survival rates of 93%, 69%, and 46%, respectively. Local tumor control was achieved in 61% of tumors overall and in 78% of tumors 2.5 cm or less in diameter. Treatment failure in the majority of patients was due to new (intra- and/or extrahepatic) metastases. These results compare favorably to hepatic resection, despite the fact that patients in this series were not considered to have been candidates for resection.
A number of prior authors (13–22) have described the results of RF ablation of liver tumors. Though encouraging, these studies have been limited due to either their inclusion of patients with primary and secondary liver tumors or because of relatively short patient follow-up after therapy. Our results confirm these encouraging preliminary results and provide additional data, which concern the effect of RF ablation on patient survival.
An important limitation of in situ ablation relates to tumor size, in that smaller tumors are more easily destroyed than larger tumors. Our results confirm that better outcomes are obtained with smaller tumors. We achieved local control in 69 (78%) of 88 tumors 2.5 cm or less, 34 (47%) of 72 tumors 2.6–4.0 cm, and only 6 (32%) of 19 tumors 4.0 cm or larger in diameter. Our study was not biased toward smaller lesions (fewer than half were 2.5 cm), and thus our overall results were not unduly influenced by tumor size. Furthermore, though local tumor control was strongly influenced by tumor size, and survival was not significantly (P = .21) related.
An interesting finding concerns the effect of repeat treatment on patient survival. Though based on only a limited number of patients (34 patients had retreatment of at least one tumor), retreatment did not significantly affect the chance or duration of survival (there was a nonsignificant trend toward longer survival with retreatment). This finding is counter to intuition and current clinical practice, according to which lesions that are observed to recur locally are aggressively re-treated, if possible. Larger series will be required to confirm this finding, as we may not yet have sufficient data. We believe that our inability to demonstrate a significant survival benefit from repeat treatment should not dissuade physicians from pursuing local control when possible.
Survival in our series was also not influenced by the number of metastases at the time of initial therapy. This is counter to the results of some surgical series that reported (36,68,69) tumor recurrence and/or survival following metastasectomy were negatively influenced by the number of metastases removed. However, authors of larger and/or more recent reports (48,51, 52,55,59,62,64,66,70,71) have failed to confirm this correlation and have suggested that—in the range of the analyses (generally one to eight metastases removed)—survival following hepatic metastasectomy is not correlated with the number of metastases removed. Our results are consistent with those of the latter studies and suggest that the decision to treat should be guided more by the likelihood of achieving tumor control than the number of lesions present.
In conclusion, the results of this study, in which we treated 179 colorectal carcinoma liver metastases in 117 patients by using cooled-tip RF ablation, suggest that the technique is safe and effective. We did not directly compare RF ablation to surgery. However, our results compare favorably to those reported in recent surgical series, although the patients in this series were not considered candidates for surgery. We hope that these results not only support expanded use of RF ablation in selected patients, but also encourage and assist in the planning of more comprehensive clinical trials to determine its most appropriate role.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, G.S.G., L.S., T.L.; study concepts and design, G.S.G., S.N.G., L.S., T.L.; literature research, G.S.G., S.N.G., L.S., T.L.; clinical studies, L.S., T.L., T.I., F.M., M.D., L.C.; data acquisition, L.S., T.L., T.I., F.M., M.D., L.C.; data analysis/interpretation, G.S.G., E.F.H., L.S., T.L.; statistical analysis, G.S.G., E.F.H.; manuscript preparation, G.S.G., S.N.G., T.L., L.S.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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T. J. M. Ruers, J. J. Joosten, B. Wiering, B. S. Langenhoff, H. M. Dekker, T. Wobbes, W. J. G. Oyen, P. F. M. Krabbe, and C. J. A. Punt Comparison Between Local Ablative Therapy an |
) and patients with one metastasis (
), two metastases (
), three metastases (x), and four metastases (*) are illustrated. Time to death was not significantly related to the number of metastases (P = .84).
