HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2212010446v1 221/2/447    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lim, H. K. Articles by Choo, I. W. Search for Related Content PubMed PubMed Citation Articles by Lim, H. K. Articles by Choo, I. W.

Hepatocellular Carcinoma Treated with Percutaneous Radio-frequency Ablation: Evaluation with Follow-up Multiphase Helical CT¹

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).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine serial changes in hepatocellular carcinomas (HCCs) treated with percutaneous radio-frequency (RF) ablation at long-term follow-up multiphase helical computed tomography (CT).

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

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
In the past decade, a variety of minimally invasive techniques have been used for the treatment of small hepatocellular carcinomas (HCCs) as alternatives to hepatic resection surgery. These include transcatheter arterial chemoembolization, local ablation techniques with a direct intratumoral injection of compounds such as absolute ethanol and hot saline, and thermal ablation techniques such as microwave ablation, interstitial laser photocoagulation, and radio-frequency (RF) ablation (1–6). These therapeutic options are selected on the basis of the size of the lesion, its position and number, the patient’s general condition, and the clinical phase of the disease (7–9). The potential benefits of these techniques include the ability to preserve more liver tissue than that preserved with surgical resection and to reduce morbidity, as compared with that associated with surgery (10). The latter benefit is an important feature, particularly for patients with HCCs, who usually have multifocal disease and limited hepatic functional reserve caused by associated cirrhosis.

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.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
Between April 1999 and November 1999, 91 patients with nodular HCC were referred for US-guided percutaneous RF ablation. Of these, 38 patients with a previous history of transcatheter arterial chemoembolization or percutaneous ethanol injection therapy were excluded from the study. We also excluded seven patients in whom follow-up CT examinations were not performed immediately after RF ablation and six patients who were lost to follow-up less than 1 year after RF ablation. The remaining 40 patients (33 men, seven women; age range, 29–82 years; mean age, 57 years) with 43 nodular HCCs who underwent multiphase helical CT immediately and more than 1 year after RF ablation formed the study population. Three patients had two HCCs. The patients had to meet the following criteria for the treatment with RF ablation: single nodular HCC not greater than 4 cm in maximum diameter; multinodular HCCs (up to three in number), with each tumor measuring 3 cm in maximum diameter or smaller; absence of portal venous thrombosis or extrahepatic metastases; Child-Pugh class A or B liver cirrhosis; and prothrombin time ratio greater than 50% and platelet count greater than 70,000/mm³ (70 cells x 10⁹/L). The study was approved by the institutional review board, and written informed consent was obtained from all patients.

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).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
After RF ablation, all patients were followed up for more than 12 months. The interval between the last follow-up CT examination and RF ablation ranged from 13 to 19 months (mean, 16 months). At immediate and 1-month follow-up CT, 38 (88%) of 43 treated lesions appeared as well-demarcated areas of low attenuation, with the absence of contrast enhancement (Fig 1). At immediate contrast-enhanced CT, the remaining five lesions showed nodular enhancement at the margin of the treated lesion, suggesting a residual viable tumor. Three of the five lesions were treated with additional ablation after immediate CT. The remaining two lesions were followed up, and lesions that showed enhancement at 1-month follow-up CT (Fig 2) were re-treated with RF ablation. Eight (21%) of 38 lesions with no evidence of contrast-enhanced foci at immediate and 1-month follow-up CT showed areas of focal enhancement within the treated lesions at subsequent follow-up CT obtained 4 months (n = 3), 7 months (n = 3), 10 months (n = 1), and 13 months (n = 1) after RF ablation (Fig 3). These enhancing lesions were considered a marginal recurrence and were treated with additional RF ablation (n = 6) or transcatheter arterial chemoembolization (n = 2).

View larger version (124K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Successful ablation of HCC. (a) Transverse helical CT scan obtained during the contrast-enhanced arterial phase before RF ablation shows a 2.5-cm-diameter HCC (arrow) in liver segment 8. (b, c) Contrast-enhanced transverse helical CT scans obtained (b) 20 minutes and (c) 1 month after RF ablation show oval ablated areas (arrow) of low attenuation with the absence of contrast enhancement that suggest complete necrosis of the tumor. (d) At 4-month follow-up transverse CT, the ablated lesion (arrow) remains nonenhanced, with decrease in size.

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Successful ablation of HCC. (a) Transverse helical CT scan obtained during the contrast-enhanced arterial phase before RF ablation shows a 2.5-cm-diameter HCC (arrow) in liver segment 8. (b, c) Contrast-enhanced transverse helical CT scans obtained (b) 20 minutes and (c) 1 month after RF ablation show oval ablated areas (arrow) of low attenuation with the absence of contrast enhancement that suggest complete necrosis of the tumor. (d) At 4-month follow-up transverse CT, the ablated lesion (arrow) remains nonenhanced, with decrease in size.

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Successful ablation of HCC. (a) Transverse helical CT scan obtained during the contrast-enhanced arterial phase before RF ablation shows a 2.5-cm-diameter HCC (arrow) in liver segment 8. (b, c) Contrast-enhanced transverse helical CT scans obtained (b) 20 minutes and (c) 1 month after RF ablation show oval ablated areas (arrow) of low attenuation with the absence of contrast enhancement that suggest complete necrosis of the tumor. (d) At 4-month follow-up transverse CT, the ablated lesion (arrow) remains nonenhanced, with decrease in size.

View larger version (120K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Successful ablation of HCC. (a) Transverse helical CT scan obtained during the contrast-enhanced arterial phase before RF ablation shows a 2.5-cm-diameter HCC (arrow) in liver segment 8. (b, c) Contrast-enhanced transverse helical CT scans obtained (b) 20 minutes and (c) 1 month after RF ablation show oval ablated areas (arrow) of low attenuation with the absence of contrast enhancement that suggest complete necrosis of the tumor. (d) At 4-month follow-up transverse CT, the ablated lesion (arrow) remains nonenhanced, with decrease in size.

View larger version (136K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Residual tumor after partial ablation. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 30 minutes after RF ablation of a 2-cm-diameter HCC in liver segment 5 shows a small nodular enhancement (arrowhead) at the lateral margin of the ablated lesion (arrow). (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after RF ablation demonstrates that the enhancing nodule (arrowhead) continues to be seen, with an interval increase in size compared with the size at immediate CT (a). The enhancing nodule was thought to be a residual viable tumor and was treated with additional ablation.

View larger version (136K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Residual tumor after partial ablation. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 30 minutes after RF ablation of a 2-cm-diameter HCC in liver segment 5 shows a small nodular enhancement (arrowhead) at the lateral margin of the ablated lesion (arrow). (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after RF ablation demonstrates that the enhancing nodule (arrowhead) continues to be seen, with an interval increase in size compared with the size at immediate CT (a). The enhancing nodule was thought to be a residual viable tumor and was treated with additional ablation.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Marginal recurrence of HCC after RF ablation. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation shows an oval ablated lesion (arrow) of low attenuation. Note the absence of contrast enhancement in the treated lesion. (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 4 months after ablation shows an enhancing nodule (arrow) in the anterolateral aspect of the ablated lesion that represented marginal recurrence. The overall size of the treated lesion has decreased. The recurrent tumor was treated with additional RF ablation, and at the time this article was written, the patient had been alive for 19 months without tumor recurrence.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Marginal recurrence of HCC after RF ablation. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation shows an oval ablated lesion (arrow) of low attenuation. Note the absence of contrast enhancement in the treated lesion. (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase 4 months after ablation shows an enhancing nodule (arrow) in the anterolateral aspect of the ablated lesion that represented marginal recurrence. The overall size of the treated lesion has decreased. The recurrent tumor was treated with additional RF ablation, and at the time this article was written, the patient had been alive for 19 months without tumor recurrence.

View larger version (166K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Nonenhanced CT appearance after RF ablation. (a) Nonenhanced transverse helical CT scan obtained immediately after ablation shows a round ablated lesion (arrow) of high attenuation probably caused by coagulation necrosis or hemorrhage. (b) On the nonenhanced transverse helical CT scan obtained 1 month after ablation, the ablated lesion (arrow) has low attenuation.

View larger version (137K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Nonenhanced CT appearance after RF ablation. (a) Nonenhanced transverse helical CT scan obtained immediately after ablation shows a round ablated lesion (arrow) of high attenuation probably caused by coagulation necrosis or hemorrhage. (b) On the nonenhanced transverse helical CT scan obtained 1 month after ablation, the ablated lesion (arrow) has low attenuation.

View larger version (25K): [in this window] [in a new window] [Download PPT slide]   Figure 5. The graph shows serial decrease in the mean volume of the ablated lesion over time. The volume of the ablated lesion at 4-month follow-up CT decreased to 50%, as compared with that at immediate CT. The volume decreased to more than 90% at 19-month follow-up CT. Note the gradual pattern of volume decrease.

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).

View larger version (149K): [in this window] [in a new window] [Download PPT slide]   Figure 6a. Peripheral rim enhancement caused by reactive hyperemia on CT scans obtained 20 minutes after RF ablation of HCC. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase before ablation shows a 1.7-cm-diameter enhancing HCC (arrow) in liver segment 4. Contrast-enhanced transverse helical CT scans obtained during the (b) arterial and (c) portal venous phases demonstrate uniform rim enhancement (arrows) surrounding the ablated lesion. (d) On the transverse helical CT scan obtained during the equilibrium phase, the rim enhancement shows isoattenuation. (e) On the contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation, the rim enhancement is no longer seen; this finding confirms the reactive hyperemia.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 6b. Peripheral rim enhancement caused by reactive hyperemia on CT scans obtained 20 minutes after RF ablation of HCC. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase before ablation shows a 1.7-cm-diameter enhancing HCC (arrow) in liver segment 4. Contrast-enhanced transverse helical CT scans obtained during the (b) arterial and (c) portal venous phases demonstrate uniform rim enhancement (arrows) surrounding the ablated lesion. (d) On the transverse helical CT scan obtained during the equilibrium phase, the rim enhancement shows isoattenuation. (e) On the contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation, the rim enhancement is no longer seen; this finding confirms the reactive hyperemia.

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 6c. Peripheral rim enhancement caused by reactive hyperemia on CT scans obtained 20 minutes after RF ablation of HCC. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase before ablation shows a 1.7-cm-diameter enhancing HCC (arrow) in liver segment 4. Contrast-enhanced transverse helical CT scans obtained during the (b) arterial and (c) portal venous phases demonstrate uniform rim enhancement (arrows) surrounding the ablated lesion. (d) On the transverse helical CT scan obtained during the equilibrium phase, the rim enhancement shows isoattenuation. (e) On the contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation, the rim enhancement is no longer seen; this finding confirms the reactive hyperemia.

View larger version (155K): [in this window] [in a new window] [Download PPT slide]   Figure 6d. Peripheral rim enhancement caused by reactive hyperemia on CT scans obtained 20 minutes after RF ablation of HCC. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase before ablation shows a 1.7-cm-diameter enhancing HCC (arrow) in liver segment 4. Contrast-enhanced transverse helical CT scans obtained during the (b) arterial and (c) portal venous phases demonstrate uniform rim enhancement (arrows) surrounding the ablated lesion. (d) On the transverse helical CT scan obtained during the equilibrium phase, the rim enhancement shows isoattenuation. (e) On the contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation, the rim enhancement is no longer seen; this finding confirms the reactive hyperemia.

View larger version (150K): [in this window] [in a new window] [Download PPT slide]   Figure 6e. Peripheral rim enhancement caused by reactive hyperemia on CT scans obtained 20 minutes after RF ablation of HCC. (a) Contrast-enhanced transverse helical CT scan obtained during the arterial phase before ablation shows a 1.7-cm-diameter enhancing HCC (arrow) in liver segment 4. Contrast-enhanced transverse helical CT scans obtained during the (b) arterial and (c) portal venous phases demonstrate uniform rim enhancement (arrows) surrounding the ablated lesion. (d) On the transverse helical CT scan obtained during the equilibrium phase, the rim enhancement shows isoattenuation. (e) On the contrast-enhanced transverse helical CT scan obtained during the arterial phase 1 month after ablation, the rim enhancement is no longer seen; this finding confirms the reactive hyperemia.

View larger version (121K): [in this window] [in a new window] [Download PPT slide]   Figure 7a. Air and arteriovenous shunt formation on CT scans obtained 15 minutes after RF ablation of HCC. (a) Nonenhanced transverse helical CT scan obtained after ablation shows small air pockets (arrowheads) within the ablated lesion. (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase immediately after ablation shows a wedgelike area of enhancement (large arrow) in the anterolateral aspect of the ablated lesion; this enhancing area represents iatrogenic arteriovenous shunt. Note the early visualization of the portal vein (small arrow). (c) Transverse helical CT scan obtained at 1-month follow-up shows that all of the air pockets and the arteriovenous shunt have resolved.

View larger version (123K): [in this window] [in a new window] [Download PPT slide]   Figure 7b. Air and arteriovenous shunt formation on CT scans obtained 15 minutes after RF ablation of HCC. (a) Nonenhanced transverse helical CT scan obtained after ablation shows small air pockets (arrowheads) within the ablated lesion. (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase immediately after ablation shows a wedgelike area of enhancement (large arrow) in the anterolateral aspect of the ablated lesion; this enhancing area represents iatrogenic arteriovenous shunt. Note the early visualization of the portal vein (small arrow). (c) Transverse helical CT scan obtained at 1-month follow-up shows that all of the air pockets and the arteriovenous shunt have resolved.

View larger version (132K): [in this window] [in a new window] [Download PPT slide]   Figure 7c. Air and arteriovenous shunt formation on CT scans obtained 15 minutes after RF ablation of HCC. (a) Nonenhanced transverse helical CT scan obtained after ablation shows small air pockets (arrowheads) within the ablated lesion. (b) Contrast-enhanced transverse helical CT scan obtained during the arterial phase immediately after ablation shows a wedgelike area of enhancement (large arrow) in the anterolateral aspect of the ablated lesion; this enhancing area represents iatrogenic arteriovenous shunt. Note the early visualization of the portal vein (small arrow). (c) Transverse helical CT scan obtained at 1-month follow-up shows that all of the air pockets and the arteriovenous shunt have resolved.

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.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
In recent years, with the further development of ablation devices, RF ablation has been increasingly used in the local treatment of malignant hepatic tumors (24–27): A tumor can be treated with minimal loss of surrounding liver parenchyma by inserting the electrode directly into the tumor.

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.

	FOOTNOTES

 
Abbreviations: HCC = hepatocellular carcinoma, RF = radio frequency

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.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Nakamura H, Hashimoto T, Oi H, et al. Transcatheter oily chemoembolization of hepatocellular carcinoma. Radiology 1989; 170:783-786.
2. Livraghi T, Giorgio A, Marin G, et al. Hepatocellular carcinoma and cirrhosis in 746 patients: long-term results of percutaneous ethanol injection. Radiology 1995; 197:101-108.
3. Honda N, Guo Q, Uchida H, Ohishi H, Hiasa Y. Percutaneous hot saline injection therapy for hepatic tumors: an alternative to percutaneous ethanol injection therapy. Radiology 1994; 190:53-57.
4. Murakami R, Yoshimatsu S, Yamashita Y, Matsukawa T, Takahashi M, Sagara K. Treatment of hepatocellular carcinoma: value of percutaneous microwave coagulation. AJR Am J Roentgenol 1995; 164:1159-1164.
5. Vogl TJ, Muller PK, Hammerstingl R, et al. Malignant liver tumors treated with MR imaging-guided laser-induced thermo-therapy: technique and prospective results. Radiology 1995; 196:257-265.
6. McGahan JP, Browning PD, Brock JM, Tesluk H. Hepatic ablation using radiofrequency electrocautery. Invest Radiol 1990; 25:264-270.
7. Yamasaki S, Hasegawa S, Makuuchi M, et al. Choice of treatment for small hepatocellular carcinoma: hepatectomy, embolization or ethanol injection. J Gastroenterol Hepatol 1991; 6:408-413.
8. Ryu M, Shimamura Y, Kawano N, et al. The present condition of the treatment for HCC. Gastroenterol Surg 1995; 18:415-419.
9. Yamanaka N, Okamoto E, Oriyama T, et al. Treatment selection for small sized hepatocellular carcinoma. Gastroenterol Surg 1995; 18:429-435.
10. Gazelle GS, Goldberg SN, Solbiati L, Livraghi T. Tumor ablation with radio-frequency energy. Radiology 2000; 217:633-646.
11. Rossi S, Fornari F, Buscarini L. Percutaneous ultrasound-guided radiofrequency electrocautery for the treatment of small hepatocellular carcinoma. J Interv Radiol 1993; 8:97-103.
12. Rossi S, Buscarini E, Garbagnati F, et al. Percutaneous treatment of small hepatic tumors by an expandable RF needle electrode. AJR Am J Roentgenol 1998; 170:1015-1022.
13. Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radio-frequency ablation versus ethanol injection. Radiology 1999; 210:655-661.
14. Goldberg SN, Solbiati L, Hahn PF, et al. Large-volume tissue ablation with radio frequency by using a clustered, internally cooled electrode technique: laboratory and clinical experience in liver metastases. Radiology 1998; 209:371-379.
15. Goldberg SN, Hahn PF, Halpern EF, Fogle RM, Gazelle GS. Radio-frequency tissue ablation: effect of pharmacologic modulation of blood flow on coagulation diameter. Radiology 1998; 209:761-767.
16. Solbiati L, Goldberg SN, Ierace T, Dellanoce M, Livraghi T, Gazelle GS. Radio-frequency ablation of hepatic metastases: postprocedural assessment with a US microbubble contrast agent—early experience. Radiology 1999; 211:643-649.
17. Choi D, Lim HK, Kim SH, et al. Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: usefulness of power Doppler US with a microbubble contrast agent in evaluating therapeutic response-preliminary results. Radiology 2000; 217:558-563.
18. Mitsuzaki K, Yamashita Y, Nishiharu T, et al. CT appearance of hepatic tumors after microwave coagulation therapy. AJR Am J Roentgenol 1998; 171:1397-1403.
19. Solbiati L, Ierace T, Goldberg SN, et al. Percutaneous US-guided radio-frequency tissue ablation of liver metastases: treatment and follow-up in 16 patients. Radiology 1997; 202:195-203.
20. Joseph FB, Baumgarten DA, Bernardino ME. Hepatocellular carcinoma: CT appearance after percutaneous ethanol ablation therapy. Radiology 1993; 186:553-556.
21. Catalano O, Esposito M, Nunziata A, Siani A. Multiphase helical CT findings after percutaneous ablation procedures for hepatocellular carcinoma. Abdom Imaging 2000; 25:607-614.
22. Sironi S, Livraghi T, Meloni F, et al. Small hepatocellular carcinoma treated with percutaneous RF ablation: MR imaging follow-up. AJR Am J Roentgenol 1999; 173:1225-1229.
23. Breiman RS, Beck JW, Korobkin M, et al. Volume determinations using computed tomography. AJR Am J Roentgenol 1982; 138:329-333.
24. Livraghi T, Goldberg SN, Monti F, et al. Saline-enhanced radio-frequency tissue ablation in the treatment of liver metastases. Radiology 1997; 202:205-210.
25. Rossi S, Di Stasi M, Buscarini E, et al. Percutaneous RF interstitial thermal ablation in the treatment of hepatic cancer. AJR Am J Roentgenol 1996; 167:759-768.
26. Solbiati L, Goldberg SN, Ierace T, et al. Hepatic metastases: percutaneous radio-frequency ablation with cooled-tip electrodes. Radiology 1997; 205:367-373.
27. Goldberg SN, Gazelle GS, Solbiati L, et al. Percutaneous radio-frequency liver tumor ablation. AJR Am J Roentgenol 1998; 170:1023-1028.
28. Ebara M, Kita K, Sugiura N, et al. Therapeutic effect of percutaneous ethanol injection on small hepatocellular carcinoma: evaluation with CT. Radiology 1995; 195:371-377.
29. Livraghi T, Salmi A, Bolondi L, et al. Small hepatocellular carcinoma: percutaneous alcohol injection-results in 23 patients. Radiology 1988; 168:313-317.
30. Lim HK. Radio-frequency thermal ablation of hepatocellular carcinomas. Korean J Radiol 2000; 1:175-184.
31. Bartolozzi C, Lencioni R, Caramella D, Falaschi F, Cioni R, DiCoscio G. Hepatocellular carcinoma: CT and MR features after transcatheter arterial embolization and percutaneous ethanol injection. Radiology 1994; 191:123-128.
32. Lee SJ, Lim JH, Lim HK, et al. Transient subsegmental hepatic parenchymal enhancement on dynamic CT: a new sign of postbiopsy arteriovenous shunt. J Comput Assist Tomogr 1997; 21:355-360.
33. Yoshikawa J, Matsui O, Kadoya M, et al. Hepatocellular carcinoma: CT appearance of parenchymal changes after percutaneous ethanol injection therapy. Radiology 1995; 194:107-111.
34. Goldberg SN, Gazelle GS, Mueller PR. Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. AJR Am J Roentgenol 2000; 174:323-331.

This article has been cited by other articles:

				Y. Park, D. Choi, H. K. Lim, H. Rhim, Y.-s. Kim, S. H. Kim, and W. J. Lee Growth Rate of New Hepatocellular Carcinoma After Percutaneous Radiofrequency Ablation: Evaluation with Multiphase CT Am. J. Roentgenol., July 1, 2008; 191(1): 215 - 220. [Abstract] [Full Text] [PDF]

				E. J. Lee, H. Rhim, H. K. Lim, D. Choi, W. J. Lee, and K. S. Min Effect of Artificial Ascites on Thermal Injury to the Diaphragm and Stomach in Radiofrequency Ablation of the Liver: Experimental Study with a Porcine Model Am. J. Roentgenol., June 1, 2008; 190(6): 1659 - 1664. [Abstract] [Full Text] [PDF]

				Y. Minami, H. Chung, M. Kudo, S. Kitai, S. Takahashi, T. Inoue, K. Ueshima, and H. Shiozaki Radiofrequency Ablation of Hepatocellular Carcinoma: Value of Virtual CT Sonography with Magnetic Navigation Am. J. Roentgenol., June 1, 2008; 190(6): W335 - W341. [Abstract] [Full Text] [PDF]

				M.-h. Park, H. Rhim, Y.-s. Kim, D. Choi, H. K. Lim, and W. J. Lee Spectrum of CT Findings after Radiofrequency Ablation of Hepatic Tumors RadioGraphics, March 1, 2008; 28(2): 379 - 390. [Abstract] [Full Text] [PDF]

				R. S. Arellano Invited Commentary RadioGraphics, March 1, 2008; 28(2): 390 - 392. [Full Text] [PDF]

				D. Choi, H. K. Lim, J.-W. Joh, S.-J. Kim, M. J. Kim, H. Rhim, Y.-s. Kim, B. C. Yoo, S. W. Paik, and C. K. Park Combined Hepatectomy and Radiofrequency Ablation for Multifocal Hepatocellular Carcinomas: Long-term Follow-up Results and Prognostic Factors Ann. Surg. Oncol., December 1, 2007; 14(12): 3510 - 3518. [Abstract] [Full Text] [PDF]

				D. Choi, H. K. Lim, H. Rhim, Y.-s. Kim, B. C. Yoo, S. W. Paik, J.-W. Joh, and C. K. Park Percutaneous Radiofrequency Ablation for Recurrent Hepatocellular Carcinoma After Hepatectomy: Long-term Results and Prognostic Factors Ann. Surg. Oncol., August 1, 2007; 14(8): 2319 - 2329. [Abstract] [Full Text] [PDF]

				M.-H. Chen, W. Wu, W. Yang, Y. Dai, W. Gao, S.-S. Yin, and K. Yan The Use of Contrast-Enhanced Ultrasonography in the Selection of Patients With Hepatocellular Carcinoma for Radio Frequency Ablation Therapy J. Ultrasound Med., August 1, 2007; 26(8): 1055 - 1063. [Abstract] [Full Text] [PDF]

				Y.-s. Kim, H. K. Lim, H. Rhim, W. J. Lee, J. W. Joh, and C. K. Park Recurrence of Hepatocellular Carcinoma After Liver Transplantation: Patterns and Prognostic Factors Based on Clinical and Radiologic Features Am. J. Roentgenol., August 1, 2007; 189(2): 352 - 358. [Abstract] [Full Text] [PDF]

				H. S. Lim, Y. Y. Jeong, H. K. Kang, J. K. Kim, and J. G. Park Imaging Features of Hepatocellular Carcinoma After Transcatheter Arterial Chemoembolization and Radiofrequency Ablation Am. J. Roentgenol., October 1, 2006; 187(4): W341 - W349. [Abstract] [Full Text] [PDF]

				W. Yang, M. H. Chen, S. S. Yin, K. Yan, W. Gao, Y. B. Wang, L. Huo, X. P. Zhang, and B. C. Xing Radiofrequency ablation of recurrent hepatocellular carcinoma after hepatectomy: therapeutic efficacy on early- and late-phase recurrence. Am. J. Roentgenol., May 1, 2006; 186(5 Suppl): S275 - S283. [Abstract] [Full Text] [PDF]

				S. H. Kim, H. K. Lim, D. Choi, W. J. Lee, S. H. Kim, M. J. Kim, C. K. Kim, Y. H. Jeon, J. M. Lee, and H. Rhim Percutaneous radiofrequency ablation of hepatocellular carcinoma: effect of histologic grade on therapeutic results. Am. J. Roentgenol., May 1, 2006; 186(5 Suppl): S327 - S333. [Abstract] [Full Text] [PDF]

				M. Akahane, H. Koga, N. Kato, H. Yamada, K. Uozumi, R. Tateishi, T. Teratani, S. Shiina, and K. Ohtomo Complications of Percutaneous Radiofrequency Ablation for Hepato-cellular Carcinoma: Imaging Spectrum and Management RadioGraphics, October 1, 2005; 25(suppl_1): S57 - S68. [Abstract] [Full Text] [PDF]

D. Choi, H. K. Lim, M. J. Kim, S. J. Kim, S. H. Kim, W. J. Lee, J. H. Lim, S. W. Paik, B. C. Yoo, M. S. Choi, et al. Liver Abscess After Percutaneous Radiofrequency Ablation for Hepatocellular Carcinomas: Frequency and Risk Factors Am. J. Roentgenol., June 1, 2005; 184(6): 1860 - 1867. [Abstract] [Full Text]