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Vascular and Interventional Radiology |
1 From the Department of Radiology, Ospedale Civile, Vimercate, Italy (T.L., F.M.); Department of Radiology, Beth Israel Deaconess Medical Center, Boston, Mass (S.N.G.); Department of Radiology, Ospedale Generale, Busto Arsizio, Italy (L.S., T.I.); Decision Analysis and Technology Assessment Group, Department of Radiology, Massachusetts General Hospital, Zero Emerson Pl, Suite 2H, Boston, MA 02114 (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 July 5, 2000; revision requested August 16; revision received October 17; accepted November 1. Address correspondence to G.S.G.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Twenty-four consecutive patients with 64 metastases measuring 1.0–6.6 cm in diameter (mean, 1.9 cm) underwent ultrasonography-guided percutaneous RF ablation with 18-gauge, internally cooled electrodes. Treatment was performed with the patient under conscious sedation and analgesia or general anesthesia. A single lesion was treated in 16 patients, and multiple lesions were treated in eight patients. Follow-up with serial computed tomography ranged from 4 to 44 months (mean, 10 months; median, 19 months).
RESULTS: Complete necrosis was achieved in 59 (92%) of 64 lesions. Among the 59 lesions, complete necrosis required a single treatment session in 58 lesions (92%) and two treatment sessions in one lesion (2%). In 14 (58%) of 24 patients, new metastases developed during follow-up. Ten (71%) of these 14 patients developed new liver metastases. Currently, 10 (63%) of 16 patients whose lesions were initially confined to the liver are free of disease. One patient died of progressive brain metastases. No major complications occurred. Two minor complications were observed.
CONCLUSION: On the basis of preliminary study results, percutaneous RF ablation appears to be a simple, safe, and effective treatment for focal liver metastases in selected patients with breast cancer.
Index terms: Breast neoplasms, metastases, 00.324 • Liver, CT, 761.12112 • Liver neoplasms, secondary, 761.332 • Radiofrequency (RF) ablation, 761.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Metastatic breast cancer, even if it appears to be limited to a single organ, is generally considered to be a disseminated disease that requires systemic, rather than local, therapy. However, it has been reported that in 5%–12% of patients metastases can be confined to the liver (8,9). Furthermore, there have been recent reports of improved survival in patients undergoing surgical resection of limited liver metastases from breast cancer (10–14). On the basis of these reports, as well as the reported success of RF ablation in achieving local control of liver metastases from other primary tumors, we recently began to treat patients with liver metastases from breast cancer. The purpose of our study was to evaluate our initial experience with RF ablation in a consecutive series of 24 patients who were followed up with serial computed tomography (CT) for 4–44 months after treatment.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Patients
Between January 1996 and September 1999, we used percutaneous RF ablation to treat 64 individual breast cancer liver metastases, measuring 1.0–6.6 cm (mean, 1.9 cm), in 24 consecutive patients who had previously undergone resection of their primary tumors. All patients were women with a mean age of 51.5 years (range, 40–70 years). At the time of initial RF ablation therapy, a single liver metastasis was detected and treated in 16 (67%) of the 24 patients, whereas multiple lesions (two lesions in four patients, three lesions in two patients, and eight and 13 lesions in one patient each) were detected and treated in the other eight patients (33%). There were a total of 28 treatment sessions: Twenty (83%) of the 24 patients were treated with RF ablation during a single treatment session, whereas the remaining four patients (17%) were treated during two treatment sessions each. During these four additional treatment sessions, one local recurrence and a total of 13 new lesions detected during routine follow-up were treated. The single local recurrence was detected 1 month after initial RF ablation. Among patients with new lesions, one had two new lesions, one had three new lesions, and two had four new lesions. Overall (ie, taking into account 51 initial and 13 new lesions), 63 (98%) of 64 lesions were treated during a single treatment session, whereas the remaining lesion was treated during two sessions.
Patients were considered for RF ablation only if (a) their liver metastases were well seen at conventional gray-scale ultrasonography (US), and (b) either there was no evidence of extrahepatic metastases or extrahepatic metastases appeared stable in the face of progressive intrahepatic metastases. At presentation, 16 (67%) of the 24 patients had metastases confined to the liver (six of these patients had already received systemic chemotherapy), whereas the other eight patients (33%) also had metastases to other sites (bone metastases in four patients, lung and bone metastases in one patient, brain and bone metastases in one patient, and lymph node metastases in two patients). Two patients had previously undergone surgical resection of liver metastases (one metastasis in one patient, two metastases in the other). Following liver resection, both of these patients received intraarterial chemotherapy by means of a catheter placed into the hepatic artery prior to RF ablation.
Pretreatment Diagnostic Work-up
Pretreatment diagnostic work-up included hepatic gray-scale and color Doppler US examinations (Technos and AU5; Esaote, Genoa, Italy and Elegra; Siemens Medical Systems, Issaquah, Wash), as well as nonenhanced and dual-phase contrast material–enhanced abdominal helical CT (Somatom DRH, Siemens Medical Systems, Erlangen, Germany; PQ5000, Picker, Cleveland, Ohio; CT HiSpeed Advantage, GE Medical Systems, Milwaukee, Wis). CT scanning was performed during and immediately after the injection of 150 mL of iopamidol (Iopamiro; Bracco, Milan, Italy) at a rate of 3 mL/sec. The entire liver was scanned twice, once beginning 20 seconds (hepatic arterial phase) and then again 60 seconds (portal venous phase) following the initiation of contrast material injection, by using 5-mm section thickness, 7-mm collimation, and a 1:1 pitch. Additional pretreatment work-up included CT scanning of the brain and chest, as well as whole-body bone scintigraphy. The diagnosis of liver metastasis was established by means of either fine-needle biopsy (six patients) or imaging studies (CT and/or US) that demonstrated the development and progressive growth of lesions in a pattern consistent with metastatic disease (18 patients). Levels of serum alanine aminotransferase and aspartate aminotransferase, alkaline phosphatase, bilirubin, hemoglobin, and fibrinogen, as well as prothrombin activity and complete blood count, were checked before and 24 and 48 hours after RF ablation in all patients.
Technique
Treatment was performed with the patient under either conscious sedation and analgesia (three treatment sessions in three patients) or general anesthesia (21 treatment sessions in 21 patients). In cases where treatment was anticipated to require only one or two electrode insertions (ie, solitary lesions <3 cm in diameter), treatment was performed with the patient under conscious sedation and analgesia induced by administering atropine sulfate 0.5 mg intramuscularly (Atropina; SALF, Bergamo, Italy), diazepam 
drop per kilogram of body weight by mouth (Ansiolin; Doppel, Piacenza, Italy), droperidol 2.5 mg intravenously (Sintodian; Farmitalia, Milan, Italy), ketorolac tromethamine 30 mg intravenously (Lixidol; Roche, Milan, Italy) 2 hours before treatment, and tramadol hydrochloride 200 mg intravenously (Fortradol; Bayer, Milan, Italy) 
hour before treatment. In patients treated while under conscious sedation and analgesia, local anesthesia was achieved by using 5 mL of 2% lidocaine (Xylocaine; SALF). Vital signs were continuously monitored during the procedure. When a tumor measured greater than 3 cm in diameter, when multiple tumors were to be treated, or when the patient was particularly anxious, treatment was performed with the patient under general anesthesia with endotracheal intubation and mechanical ventilation. This had the additional advantage of allowing temporary suspension of respiration with controlled pulmonary inflation, as necessary, to facilitate electrode placement.
RF ablation was performed under real-time US guidance (AU5; Esaote) by using a 3.5-MHz probe (CA B411; Hitachi, Tokyo, Japan). A guide device incorporated into the US probe was used for electrode placement. After cleansing the skin with iodized alcohol (which also served as a contact medium), the most appropriate approach for electrode insertion was selected. For lesions located in the right lobe, an intercostal approach with the patient in the left lateral decubitus position was generally preferred. For lesions located in the left lobe, a subcostal approach was most often used. Two types of 20-cm-long, 18-gauge internally cooled RF electrodes (Radionics, Burlington, Mass) were used, depending on the size and location of the tumor. For all tumors measuring 2–3 cm in diameter, a single electrode with 2 or 3 cm of exposed metallic tip was used. In these cases, we attempted to place the electrode into the center of the lesion. For tumors greater than 3 cm in diameter, a triple electrode cluster (three internally cooled electrodes spaced 5 mm apart) was generally used (six lesions). However, in some cases, the cluster electrode could not be inserted owing to a narrow intercostal space or because a very oblique subcostal approach was required. These tumors were treated with two to four insertions of a single electrode.
Grounding was achieved by attaching two dispersive pads, each with a greater than 400 cm2 surface area, to the patient’s thighs. The RF electrodes were attached to a 500-kHz RF generator (series CC-1; Radionics) capable of producing 200 watts of power. During the procedure, a thermocouple embedded within the electrode tip continuously measured local tissue temperature. Tissue impedance was monitored by using circuitry incorporated within the generator. A peristaltic pump (Watson-Marrow, Medford, Mass) was used to infuse 0°C normal saline solution into the lumen of the electrodes at a rate sufficient to maintain a tip temperature of 20°–25°C. No more than 3 L of saline was required for any patient.
As RF energy was applied to the treatment probe(s), a hyperechoic focus was observed to develop around the uninsulated portion of the electrode(s). This was attributed to microbubble formation and tissue vaporization. The area of increased echogenicity was round, most often progressively increased in size over the course of ablation, and generally enveloped the entire tumor with variable extension into the surrounding liver by the end of treatment. Hyperechoic microbubbles were often seen escaping into the hepatic veins during RF application. In some cases, the hyperechoic focus did not develop progressively but appeared rather suddenly and was accompanied by an audible "popping" sound emanating from the liver. The appearance and progression of hyperechogenicity was used to guide the duration of therapy. RF energy was applied until the tumor appeared to be completely hyperechoic and/or the hyperechoic focus did not increase in size for several minutes. Furthermore, in cases where multiple electrode insertions were required, each subsequent electrode placement was directed to an area of the tumor where hyperechogenicity was not evident. In some of these cases, however, hyperechogenicity obscured the deeper portions of the tumor and made repositioning of the RF electrode difficult. Each application of RF energy lasted for 8–12 minutes, and in all but one case (the patient with 13 lesions), the entire treatment session lasted less than 1 hour.
Following RF therapy, patients were hospitalized for 2 days. Patients were hospitalized largely owing to limited experience with this type of tumor, in addition to conformity with established practice patterns at the two institutions where the procedures were performed. A second treatment was scheduled if residual areas of vital neoplastic tissue were detected during follow-up.
Assessment of Therapeutic Effectiveness
To evaluate the response to RF therapy, contrast-enhanced CT was performed, by using the same parameters as those used for pretreatment scanning, on the day following treatment (to detect any treatment-related complications and identify persistent foci of contrast enhancement that might represent untreated tumor), 1 month after the procedure, and every 3–4 months thereafter. Follow-up ranged from 4 to 44 months (mean, 10 months; median, 19 months). Each follow-up CT scan was interpreted prospectively by a total of four investigators (T.L., L.S., F.M., T.I.), two from each institution. No more than two of these investigations had been involved in the treatment of any individual patient. In all cases, a consensus of the readers was used to judge treatment effectiveness. Tumor necrosis was considered complete when no focal enhancement was seen within the tumor or at its periphery on CT scans obtained at least 4 months after treatment (Figs 1, 2) (15). Tumors were categorized on the basis of their size at the time of initial RF ablation into those that were 1.0–1.9 cm, 2.0–2.9 cm, 3.0–3.9 cm, 4.0–5.0 cm, or 5.1–6.6 cm in diameter.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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One patient died because of progression of brain metastases after 6 months; the remaining 23 patients were alive at the time of this writing. The longest survivor to date (44 months) had a single lesion 3.5 cm in diameter and was the first patient treated in this series.
Imaging Findings
On CT scans obtained 24 hours following RF therapy, treated areas were devoid of contrast enhancement, and their attenuation was lower than the attenuation of the surrounding liver parenchyma and lower than that seen at pretreatment CT. This area was often surrounded by a thin rim or peripheral contrast enhancement, believed to represent peritumoral hyperemia. In tumors greater than 3 cm in diameter, areas of necrosis were approximately the same size as the tumors prior to treatment, whereas in those lesions less than 3 cm in diameter, areas of necrosis were generally larger than the tumors. On subsequent follow-up images, areas of successfully treated tumor either remained unchanged or diminished moderately in size. Peripheral hyperemia was not seen on these studies.
Side Effects and Complications
Serum aspartate and alanine aminotransferase levels generally increased up to two to three times the baseline values, but they normalized by the time of the 1-month follow-up examination. No changes were observed in other serum element levels. The majority of patients treated under sedation and analgesia experienced mild pain during the procedure. This disappeared immediately following the cessation of RF application.
No mortality or major complications occurred as a result of the procedures. Two (8%) of the 24 patients had minor complications; neither of these complications required further treatment, and both resolved spontaneously. One patient developed an asymptomatic perirenal hematoma after RF ablation with the cluster electrode of a lesion in segment 7. One patient with multiple lesions in segment 8 developed a focus of diaphragmatic thickening (likely due to inflammatory reaction) with pain that lasted 10 days.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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However, Zinser et al (8) reported that survival in breast cancer patients with liver-only metastases (19 months) or those with liver and bone metastases (17 months) was longer than that in patients with metastases to other sites (12 months). The authors therefore concluded that the presence of isolated liver metastases may not indicate as poor a prognosis as previously believed. In addition, recent reports in the surgery literature have suggested that survival can be improved by performing resection of limited liver metastases from breast cancer. Elias et al (10) and Schneebaum et al (11) reported median survivals in patients undergoing hepatic resection that were at least three times those in comparable patients treated with standard nonsurgical therapies. Raab et al (12) reported better survival with R0 (complete) resection than with R1 or R2 (incomplete) resection. Some patients described in these series remain alive and free of disease up to 5 years after resection (10,13,14). However, these reports describe only small patient cohorts, and all investigators noted considerable heterogeneity in the presentation and progression of metastatic disease. Thus, and despite initially promising results, most patients with metastatic breast cancer continue to be treated with systemic chemotherapy alone.
On the strength of the results obtained with RF ablation for the treatment of both liver metastases from colon cancer (3,4,6,7) and hepatocellular carcinoma (1,2,5,6), we recently began to treat patients with liver metastases from breast cancer. Herein, we have summarized our initial experience and results. On the basis of results in this initial series, the effectiveness of RF ablation in achieving complete tumor necrosis ("local control") appears to be comparable to that reported for hepatocellular carcinoma and better than that reported for colorectal cancer metastases. In our series, complete tumor necrosis was achieved in 96% of tumors less than 3 cm in diameter and in 75% of tumors 3–5 cm. In contrast, Lencioni et al (16), Rossi et al (6), and Solbiati et al (3) reported complete necrosis in 87%, 86%, and 75%, respectively, of colorectal cancer metastases less than 3 cm in diameter. In the same studies, Lencioni et al and Solbiati et al reported complete necrosis in 53% and 58%, respectively, of metastases 3–5 cm in diameter. The apparent differences in treatment response between our series and those of Lencioni et al, Rossi et al, and Solbiati et al may be due to distinctive features of the surrounding hepatic tissue or to differences in tumor histologic features and behavior, or both. Larger series are needed to confirm this finding and elucidate the causes.
An important determinant of long-term outcome following surgical resection of liver metastases is the surgical margin, and it has been suggested that tumor recurrence is likely if less than 1 cm of normal tissue surrounding the tumor is not removed (17,18). In colorectal metastases, Shirabe et al (17) demonstrated the presence of occult (microscopic) intrahepatic invasion within 10 mm from the edge of the tumors in 22% of lesions less than 4 cm in diameter and in 85% of lesions greater than 4 cm. Elias et al (18) demonstrated improved survival when the resection margin was more than 10 mm, but not if only 5–9 mm of normal tissue was removed. Thus, the goal of RF ablation should be to destroy not only the tumor that is targeted for treatment but also a rim of normal tissue to approximate a "surgical margin." Unfortunately, experience to date (principally with metastases from colorectal carcinoma) suggests that RF ablation cannot always achieve necrosis of a 10-mm tissue margin, particularly with lesions greater than 3 cm in diameter. In the setting of occult invasion of surrounding, otherwise normal liver tissue, the failure to achieve necrosis of adequate tissue margins is likely to result in delayed local tumor recurrence. The higher rate of local control observed in this study, in comparison with experiences reported with colorectal cancer liver metastases, suggests that occult invasion of surrounding liver tissue may be less frequent, or absent, in breast cancer metastasis.
Compared to surgery, RF ablation offers the advantages of being less expensive and considerably less invasive. It may thus be reasonable to use RF ablation rather than surgery as a first-choice local therapy, particularly given the natural history of this disease, which suggests that local therapies (eg, surgery and in situ tumor ablation) will be curative in only a minority of patients. The use of RF ablation does not prevent the simultaneous or subsequent use of other, potentially complementary, treatments. Hormonal therapy, systemic chemotherapy, and intraarterial infusion chemotherapy each can be given before or after RF ablation, according to local preferences and practice guidelines. The possibility of placing an intraarterial catheter for hepatic infusion chemotherapy at the time of surgical resection was previously an advantage of surgery over RF ablation. These catheters can now be inserted percutaneously, obviating laparotomy and eliminating this as a potential advantage of surgery (19). However, because liver metastases from breast cancer are usually hypoechoic and easily detected with US, and because chemotherapy may damage the hepatic parenchyma and alter its echogenicity (making tumor detection more difficult), it may be better to postpone systemic or intraarterial chemotherapy until after focal liver metastases have been treated with RF ablation.
A critical issue, and one that was not directly assessed in this study, is whether the use of any local therapies can be justified in patients with metastatic breast cancer. Local therapies have proved valuable in patients with isolated liver metastases from colorectal and other primary tumors, principally because of the tendency of these tumors to metastasize exclusively or primarily to the liver and because liver metastases have a dominant influence on survival in these patients. It remains to be proved whether the treatment of liver metastases from breast cancer—even if successful—can result in the same survival benefit.
In conclusion, RF ablation appears to be a safe, relatively simple, and effective treatment for liver metastases from breast cancer. The absence of major complications and the high rate of local control achieved in this series suggest that RF ablation may be a valid alternative to surgery in a select population of patients with metastatic breast cancer. Even if the proportion of patients with liver-only metastases from breast cancer is relatively lower than that from other primary tumors, the high overall prevalence of breast cancer suggests that a large number of patients may be eligible for RF treatment.
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FOOTNOTES |
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Abbreviation: RF = radio frequency
Author contributions: Guarantors of integrity of entire study, T.L., G.S.G.; study concepts, T.L.; study design, T.L., S.N.G., G.S.G.; literature research, T.L., G.S.G.; clinical studies, F.M., T.L., T.I., L.S.; data acquisition, T.L., F.M., T.I., L.S.; data analysis/interpretation, T.L., S.N.G., G.S.G.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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