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Vascular and Interventional Radiology |
1 From the Department of Radiology and Gastrointestinal Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-ku, Seoul 135-710, South Korea. Received February 12, 2001; revision requested March 28; revision received May 1; accepted May 15. Supported in part by clinical research fund GI-00-07 of Gastrointestinal Center, Samsung Medical Center. Address correspondence to H.K.L. (e-mail: hklim@smc.samsung.co.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: There were 43 nodular HCCs in 40 patients at follow-up CT performed not less than 12 months after RF ablation. All patients underwent follow-up multiphase helical CT immediately, 1 month, and then every 3 months after percutaneous RF ablation. The serial changes in attenuation, enhancement pattern, shape, other findings, and volume of the ablated lesions were analyzed at follow-up CT.
RESULTS: Thirty-eight (88%) of 43 ablated lesions were of low attenuation, with absence of contrast material enhancement at immediate and 1-month follow-up CT, which is suggestive of successful treatment. The remaining five lesions (12%) showed peripheral nodular enhancement, suggesting residual viable tumor. Compared with volume changes at immediate follow-up CT, the mean percentages of volume change at 1, 4, 10, 16, and 19 months were 79%, 50%, 27%, 11%, and 6%, respectively. Of 43 ablated lesions, 24 (56%) were mostly round at immediate CT and remained unchanged at subsequent follow-up CT. Peripheral rim enhancement was seen in 34 (79%) of 43 lesions at immediate CT but resolved in all 34 lesions at 1-month follow-up CT. Other associated findings included iatrogenic arteriovenous shunt in 10 patients, perihepatic hemorrhage in three, and pneumothorax in one.
CONCLUSION: Follow-up multiphase helical CT of HCCs treated with percutaneous RF ablation showed variable findings in the treated lesions and surrounding liver parenchyma.
Index terms: Computed tomography (CT), helical, 761.12115 • Liver neoplasms, CT, 761.12111, 761.12112, 761.12115 • Liver neoplasms, therapy, 761.1269, 761.323 • Radiofrequency (RF) ablation, 761.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Since the application of RF ablation to hepatic tumors in humans by Rossi et al (11), this technique has been increasingly used for the treatment of primary and secondary hepatic tumors (12–15). Since gray-scale ultrasonography (US) has a limited role in the differentiation of necrotic tissue from residual tumor, contrast material–enhanced US, computed tomography (CT), and magnetic resonance (MR) imaging have been used to determine the therapeutic response and plan further treatment after local treatment of hepatic tumors (16–22). Of these, contrast-enhanced CT has been most widely used for the follow-up after RF ablation (10). However, to the best of our knowledge, no study has focused on the serial changes at long-term follow-up multiphase helical CT after RF ablation. The purpose of this study was to determine the serial changes in HCCs treated with percutaneous RF ablation at long-term follow-up multiphase helical CT.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The diagnosis of HCC was confirmed by using US-guided percutaneous needle biopsy of 26 masses in 26 patients. The remaining 17 masses in 14 patients were considered to be HCCs on the basis of characteristic imaging (three-phase helical CT and angiography) findings and elevated serum tumor marker (
-fetoprotein level >200 ng/mL [>200 µg/L]). The tumors were 1.0–4.0 cm in diameter (mean, 2.6 cm). In the study, 35 patients had liver cirrhosis as a result of hepatitis B (n = 21), hepatitis C (n = 11), Budd-Chiari syndrome (n = 1), or alcoholism (n = 2). The remaining five patients had hepatitis B without cirrhosis. The patients were not considered for surgery and were referred for RF ablation because of a history of poor medical status (n = 20), prior hepatic resection (n = 3), tumors in both lobes (n = 2), and refusal of surgery (n = 15).
RF Ablation Procedure
RF ablation was performed by using a 50-W, 480-kHz monopolar RF generator (model 500 series; Radiofrequency Interstitial Thermal Ablation Medical System, Mountain View, Calif) and an active expandable RF needle electrode (model 30; Radiofrequency Interstitial Thermal Ablation Medical System). The RF generator has displays that indicate hook temperatures, tissue impedance value, and treatment time. The needle electrode (1.9 mm in external diameter) has a 15- or 25-cm-long stainless steel shaft insulated by a plastic membrane and a 1-cm-long exposed tip with four retractable lateral hooks at an angle of 90° to each other. The maximum deployment diameter of the hooks was 3 cm, and each hook had a thermistor in its tip for monitoring the temperature in the surrounding tissue. A grounding pad was applied to the patient’s back. Hook temperatures, tissue impedance value, and treatment time were displayed on the panel of the RF generator during the procedure.
One experienced radiologist (H.K.L.) performed all RF ablation procedures in inpatients after they had fasted for 12 hours. Laboratory examinations, including complete blood count and blood coagulation tests, were performed before each session. All patients were treated while under conscious sedation with pethidine hydrochloride (50 mg) (Pethidine; Samsung Pharmaceutical, Seoul, Korea) administered intravenously. A local anesthetic (Lidocaine; Kwang Myung Pharmaceutical, Seoul, Korea) was injected from the skin to the liver capsule along the predetermined insertion route. Whenever patients reported intolerable pain during ablation, we performed additional intravenous administration of pethidine hydrochloride (50 mg) while the cardiovascular and respiratory systems were continuously monitored. The skin was pricked with a small pointed lancet.
All US procedures were performed with a 2–5-MHz convex-array transducer (HDI 5000; Advanced Technology Laboratories, Bothell, Wash) by using a free-hand technique. After deployment of the hooks, the RF generator was activated. RF energy needed to maintain an average temperature of 100°C was delivered for 8–10 minutes for each ablation. The impedance values ranged from 30 to 60 
. The diameters of the deployed hooks varied between 1 and 3 cm, depending on the size and location of the tumor. The temperature of each hook was maintained above 90°C. For tumors smaller than 2 cm in diameter, the needle tip was placed in the center of the tumor and the hooks were deployed to reach the deepest margin of the tumor. One ablation was usually enough to destroy the entire tumor. For larger tumors, we performed multiple overlapping ablations (range, two to six ablations) according to the size and shape of the tumor.
After RF ablation, patients were kept under close observation for 12 hours. Liver function and complete blood count tests were performed within 24 hours after the procedure.
CT Examination
All patients underwent contrast-enhanced three-phase helical CT before RF ablation and four-phase helical CT—both nonenhanced and contrast-enhanced three- phase—immediately (within 30 minutes) and 1 month after treatment. If the tumors were completely treated and no recurrence was noted, repeated three-phase CT was performed after the administration of contrast material at 3-month intervals. All CT examinations were performed with a helical scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis) with 7-mm collimation and a 7-mm/sec table speed. A total of 120 mL of nonionic contrast material ([300 mg of iodine per milliliter] Ultravist 300; Schering, Berlin, Germany) was administrated at a rate of 3 mL/sec with a power injector (OP 100; Medrad, Pittsburgh, Pa). For immediate posttreatment CT, images were obtained before contrast material injection and at 30, 60, and 180 seconds after the initiation of intravenous contrast material injection for imaging during the hepatic arterial, portal venous, and equilibrium phases, respectively.
Image Analysis
All CT images were archived with a picture archiving and communication system, or PACS (PathSpeed Workstation; GE Medical Systems). Three experienced abdominal radiologists (S.H.K., S.J.L., H.J.J.) reviewed the CT images, controlling window level and center settings at the PACS workstation, without knowledge of the final outcomes of the patients. Each radiologist reviewed all the CT images obtained in the same patient at the same time, from the first to the last examination. A standard questionnaire was completed for each patient. A final decision was made with consensus. The CT findings that were evaluated were the shape of the ablated area; the presence of peripheral nodular enhancement, peripheral rim enhancement, intralesional air, and/or intralesional high attenuation on precontrast scans; vascular changes (arteriovenous shunt, pseudoaneurysm, and thrombosis); and complications.
We also evaluated findings in the abdomen or lower chest that could be related to the ablation procedure. The CT findings obtained after ablation were compared with those obtained before ablation to ensure that the changes were not present before RF ablation. A nonenhancing area of low attenuation was considered to be necrotic tissue. One radiologist (J.H.L.) measured the volume of the ablated lesions at follow-up helical CT (portal venous phase) at the maximal magnification on a 2,000 x 2,000 PACS monitor by using an area measure tool and summation-of-areas technique (23).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Peripheral rim enhancement representing reactive hyperemia was seen in 34 (79%) of 43 lesions at CT performed immediately after RF ablation. The CT images showed three enhancement patterns during three phases: high attenuation at the hepatic arterial phase, high attenuation at the portal venous phase, isoattenuation at the equilibrium phase (n = 19), high attenuation at the hepatic arterial phase, isoattenuation at the portal venous phase, isoattenuation at the equilibrium phase (n = 12), and high attenuation at all three phases (n = 3). None of the peripheral rim enhancement had low attenuation during the equilibrium phase. At 1-month follow-up CT, peripheral rim enhancement completely resolved in all 34 lesions (Fig 6).
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Other CT findings related to the procedure at immediate CT included three cases of minor perihepatic hemorrhage and one small pneumothorax that disappeared spontaneously with no specific treatment at 1-month follow-up CT.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Contrast-enhanced helical CT has been widely used in the evaluation of the residual or recurrent tumor or in complications such as abscess, infarction, or hemorrhage in patients who have undergone percutaneous ablation therapy for a hepatic tumor (10,21). However, the spectrum of long-term follow-up helical CT appearances of HCC treated with RF ablation has not been reported.
In our study, all successfully ablated lesions appeared as areas of low attenuation without contrast enhancement at follow-up CT. This nonenhancing low-attenuation area is believed to represent necrosis, as described by other investigators (16,19,20,28,29). For RF ablation to be successful and complete, all malignant tissue must be ablated. The ideal goal is to ablate a 0.5–1.0-cm peripheral margin of normal hepatic tissue that surrounds the tumor, as well as the entire tumor itself (10,30). In our study, the ablated lesion was larger than the tumor before ablation in all cases. We believe that the ablated lesion that is not larger than the tumor before ablation should be followed up closely.
The ablated lesion usually appeared round or oval because we used an electrode with expandable hooks that was designed to make a round shape after deployment, and electrode placements were applied repeatedly at approximate intervals. Four of 43 ablated lesions were irregular in shape. These four lesions were located between large branches of portal and hepatic veins. We believe that the irregular shape of ablated lesions is attributed to a cooling effect of the blood flow, overlapping ablation, or both.
Peripheral enhancing nodules were seen in five lesions at immediate CT, 1-month follow-up helical CT, or both. After local ablation therapy, residual tumors are usually seen as enhancing nodules on contrast-enhanced CT images, as described by previous investigators (10,19,24,26,30,31). Therefore, we thought that the five lesions in our study had untreated viable tumor due to limited ablation, although we had no pathologic proof. It is difficult to know the exact histologic characteristics of the whole RF-ablated area when percutaneous needle biopsy is used. Biopsy is not reliable for evaluating therapeutic effectiveness except when it shows malignancy (10,19,29).
All of the peripheral enhancing lesions at short-term follow-up CT performed within 1 month after treatment should not be regarded as residual viable tumor. Reactive hyperemia in tissue that surrounds the ablated lesion, representing inflammatory reaction to the thermal injury, frequently occurred during this period. In our study, it was noted in 34 (79%) of 43 ablated lesions at immediate CT. Similar findings at CT have been reported in patients who underwent percutaneous ethanol injection therapy and microwave coagulation therapy (18,28). Peripheral rim enhancement that results from reactive hyperemia is usually uniform in thickness and envelops the ablated lesion, whereas residual tumor shows focal and irregular peripheral enhancement. The other useful differentiating point between the two conditions is that peripheral rim enhancement indicating reactive hyperemia shows high- or isoattenuation during portal venous and equilibrium phases. The residual tumor usually becomes low in attenuation during the equilibrium phase. In addition to reactive hyperemia, nontumorous wedgelike enhancement can occur at the periphery of the ablated lesion owing to iatrogenic arteriovenous shunt.
It is well known that percutaneous needle biopsy and ethanol injection therapy can produce arteriovenous shunt along the needle tract (32,33). It is usually easy to differentiate residual tumor from arteriovenous shunt at multiphase helical CT, because residual tumor usually shows high attenuation during the hepatic arterial phase and low attenuation during the portal and equilibrium phases. If the finding of short-term follow-up CT is inconclusive, follow-up CT at 1–3-month intervals can be helpful before invasive diagnostic procedures such as percutaneous biopsy or retreatment are performed if the suspected lesion is small. The nontumorous enhancing lesions produced by reactive hyperemia and arteriovenous shunt have usually resolved by this time. During this period, even if one fails to detect small residual tumors, they seldom grow to a size where a successful retreatment is not feasible (10).
The absence of contrast enhancement in the ablated lesion at short-term follow-up CT within 3 months after treatment does not always indicate successful treatment, as later follow-up studies can demonstrate tumor regrowth at the periphery of the ablated lesion (10). In our study, eight of 38 ablated lesions with absence of contrast enhancement at 1-month follow-up CT showed tumor recurrence at the margin of the treated lesions at subsequent follow-up CT performed 4–13 months after treatment. Therefore, we believe that short-term follow-up CT performed within 3 months after treatment is a not reliable method to precisely determine the therapeutic effectiveness.
At immediate follow-up CT, we found intralesional air in 27 (63%) of 43 lesions, which were small in size and number and disappeared at 1-month follow-up CT. Mitsuzaki et al (18) reported that four of 14 lesions that contained air after microwave coagulation therapy seemed to be abscesses. In these patients, high fever and pain persisted for more than 2 weeks. However, none of the patients in our study had symptoms of infection such as fever, abdominal pain, or leukocytosis during the postprocedural period. Therefore, it is believed that air without an air-fluid level may have been introduced along the insertion path of the needle or may have resulted from tissue necrosis (18,20).
In our study, 14 (35%) of 40 patients had abnormal findings at immediate postprocedural CT. Arteriovenous shunt was detected in 10 patients, minimal hemoperitoneum in the perihepatic space in three, and a small amount of pneumothorax in one. All 14 patients were asymptomatic, and no specific treatment was required. At follow-up CT performed 1 month after RF ablation, the abnormal findings had resolved spontaneously.
The limitation of the study is that we had no pathologic proof of the ablated lesions. As stated by other investigators (22,34), the use of needle biopsy is limited in depicting residual viable tumors after RF ablation because of sampling errors. At our institution, at an early stage of RF ablation, we performed US-guided percutaneous biopsy for all suspicious lesions and found that biopsy findings did not always represent the accurate characterization of the treated lesion. Negative biopsy results do not guarantee the complete necrosis of the tumor. In addition, percutaneous biopsy is an invasive procedure, and patients with hepatic cirrhosis may need longer hospitalization owing to possible bleeding. Therefore, most investigators rely on long-term imaging follow-up to document the therapeutic response. The purpose of our study was not to evaluate the diagnostic accuracy of CT in assessing the therapeutic effectiveness after RF ablation but rather to describe the spectrum of long-term follow-up multiphase helical CT findings in the ablated lesions and surrounding liver parenchyma.
Early detection of a residual or locally recurrent tumor after RF ablation of HCC is critical and can facilitate successful retreatment at an early stage. Late diagnosis is associated with peripheral regrowth and makes retreatment difficult owing to unfavorable geometry. As a standard of reference, contrast-enhanced helical CT remains the primary modality for assessing the therapeutic response of HCC to RF ablation despite some limitations. We believe that short-term follow-up CT within 1 month after treatment is not a reliable method for assessing the precise therapeutic effectiveness, because reactive hyperemia and arteriovenous shunt often make accurate evaluation difficult.
Our current imaging strategy after RF ablation of HCC includes initial contrast-enhanced US within 24 hours after treatment to evaluate early outcome and complications. If definite evidence of residual tumor is found, the lesion is re-treated with contrast-enhanced US during the same admission period. For the later follow-up, contrast-enhanced multiphase helical CT is then performed at 1 month and every 3 months thereafter. We believe that adequate treatment has occurred when there is no evidence of tumor regrowth at the margin of the treated lesion by 12 months. Knowledge of the serial changes at long-term follow-up multiphase helical CT is helpful in assessing the therapeutic response of HCC to RF ablation.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, H.K.L.; study concepts and design, H.K.L.; literature research, D.C., J. H. Lee; clinical studies, W.J.L., S.H.K., S.J.L., H.J.J., J. H. Lim, I.W.C.; data acquisition, D.C., J. H. Lee; data analysis/interpretation, H.K.L., D.C.; manuscript preparation, D.C.; manuscript definition of intellectual content and editing, H.K.L.; manuscript revision/review, H.K.L., W.J.L.; manuscript final version approval, H.K.L.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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