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Published online before print February 21, 2002, 10.1148/radiol.2231010780
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(Radiology 2002;223:255-262.)
© RSNA, 2002


Gastrointestinal Imaging

Hepatic Tumors Treated with Percutaneous Radio-frequency Ablation: CT and MR Imaging Follow-up1

Clarisse Dromain, MD, Thierry de Baere, MD, Dominique Elias, MD, Viseth Kuoch, MD, Michel Ducreux, MD, Valerie Boige, MD, Peter Petrow, MD, Alain Roche, MD and Robert Sigal, MD, PhD

1 From the Departments of Radiology (C.D., T.d.B., V.K., P.P., A.R., R.B.), Surgery (D.E.), and Medicine (M.D., V.B.), Institut Gustave-Roussy, 39 rue Camille Desmoulins, 94805 Villejuif, France. From the 1999 RSNA scientific assembly. Received April 16, 2001; revision requested June 4; revision received July 30; accepted September 17. Address correspondence to C.D. (e-mail: dromain@igr.fr).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To describe the appearance of hepatic tumors treated with radio-frequency (RF) ablation on computed tomographic (CT) and magnetic resonance (MR) images and the pattern of residual tumor at the site of RF ablation and to assess prospectively the sensitivity, specificity, and positive and negative predictive CT and MR imaging values in the evaluation of RF treatment.

MATERIALS AND METHODS: Thirty-one patients with 50 tumors (nine hepatocellular carcinomas and 41 metastases) treated with RF ablation underwent CT and MR imaging on the same day at 2, 4, and 6 months; CT was performed every 3 months thereafter. CT and MR findings were interpreted separately and prospectively by two reviewers with consensus. For both imaging techniques, appearance of the treated area, treatment efficacy, and complications were assessed at each time. Sensitivity and specificity were determined by using the McNemar test.

RESULTS: After a mean follow-up of 19 months, nine tumors showed local regrowth. At 2 months, MR imaging depicted more local regrowths (eight of nine; sensitivity, 89%) than did CT (four of nine; sensitivity, 44%) but without significant differences (P = .12). In two cases, only T2-weighted imaging depicted local regrowth. All nine lesions became conspicuous at 4-month follow-up with both techniques. At 2 months, thin peripheral rim enhancement and arterioportal shunting were found in 24% and 12%, respectively, of the treated tumors. These findings disappeared thereafter and are not linked to tumor regrowth.

CONCLUSION: Despite the small number of patients, CT and MR imaging may depicted all local regrowth at 4 months or sooner. MR imaging may have an edge over CT in the early detection of local regrowth.

© RSNA, 2002

Index terms: Liver neoplasms, CT, 76.12111, 76.12112, 76.113, 76.12115 • Liver neoplasms, MR, 76.121411, 76.121412, 76.121415, 76.12143 • Liver neoplasms, therapy, 76.1269, 76.323 • Radiofrequency (RF) ablation, 76.1269


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although surgery remains the treatment of choice for hepatic tumors, minimally invasive techniques have been developed for the treatment of unresectable primary and secondary hepatic malignancies. Radio-frequency (RF) ablation is a local treatment designed to destroy tumors by heating tissue to temperatures that exceed 60°C. An RF current is emitted from an electrode that is inserted either during an open surgical procedure or percutaneously. Recent results indicate that RF ablation is well tolerated and provides a high rate of local tumor control, even if longer follow-up is necessary to evaluate the benefit of treatment (16).

Imaging plays a crucial role in the follow-up of hepatic tumors treated with RF ablation, as it is the means by which local treatment efficacy, recurrent disease, and some of therapy-induced complications are evaluated. Today, there is no clear consensus about which imaging techniques are most suited for follow-up after RF treatment, and a number of various imaging techniques were performed in different institutions. The goals of our study were to describe the appearance of hepatic tumors treated with RF ablation on computed tomographic (CT) and magnetic resonance (MR) images and the pattern of residual tumor at the site of RF ablation and to assess prospectively the respective sensitivity, specificity, and positive and negative predictive CT and MR imaging values in the evaluation of RF treatment.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Between July 1998 and September 2000, 86 consecutive patients with 122 hepatic tumors underwent percutaneous RF ablation. Of these, 31 patients (24 men, seven women; age range, 23–79 years; mean age, 61 years) with 50 hepatic tumors were prospectively examined with CT and MR imaging during a mean follow-up of 19 months; they represent our study group. The study was approved by our institutional review board, and all patients gave informed consent. Fifty-five patients were not included in the study because either they had a contraindication to one of the imaging techniques, did not choose to participate in the study, or were referred for RF therapy from another hospital and did not plan to be followed up in our institution.

In all patients, histologically proven hepatocellular carcinoma (n = 9) or metastases (n = 41) were considered unresectable. Primary tumors that gave rise to metastatic lesions were colorectal (n = 25), carcinoid (n = 5), desmoplastic small round cell (n = 4), breast carcinoma (n = 4), renal leiomyosarcoma (n = 1), renal adenocarcinoma (n = 1), and medullary thyroid carcinoma (n = 1). In 19 patients, solitary tumors required treatment; in the remaining 12 patients, two to four tumors required treatment. The greatest tumor diameter immediately before treatment was 7–45 mm (mean, 20 mm).

RF Ablation Procedure
All tumors were treated with RF ablation by using a 480-kHz RF generator (CC1; Radionics, Burlington, Mass) that delivered a maximum power of 200 W through 17-gauge monopolar cooled needle electrodes. A single needle with a 2- or 3-cm-long active tip was used for tumors smaller than 2.5 cm (18 patients with 35 tumors). As soon as it was available, a triple-cluster needle (Radionics) composed of three 2.5-cm-long single needles that formed a triangle was used for tumors larger than 2.5 cm (13 patients with 15 tumors). All percutaneous RF procedures were performed by one experienced interventional radiologist (T.d.B.) with ultrasonographic (US) guidance and were monitored by using a 3.5–5.0-MHz probe (AU-Idea; Esaote Biomedica, Le Perreux, France). For all tumors, treatment was considered complete when an RF-induced hyperechoic region totally covered the initial location of the tumor.

Imaging Methods
On the basis of findings at CT and MR imaging performed on the same day, treatment efficacy was prospectively assessed at 2, 4, and 6 months after RF ablation. Subsequently, only CT was performed at 9 and 12 months after the procedure and every 6 months thereafter.

CT images were obtained with a spiral scanner (HiSpeed; GE Medical Systems, Milwaukee, Wis) before and after a bolus injection of 100 mL of nonionic contrast material (iobitridol [Xenetix 300]; Guerbet, Roissy, France) at a rate of 3 mL/sec. A CT injector (Medrad, Pittsburgh, Pa) was used to deliver the contrast medium via a catheter that was inserted into an antecubital vein. After the injection, three spiral CT scans were obtained during the hepatic arterial phase, the portal venous phase, and the equilibrium phase at 30, 70, and 300 seconds, respectively, after initiation of the injection. Scanning was performed at 120 kV and 270 mA. Contiguously reconstructed sections (pitch of 1:1) were obtained through the liver with 7-mm section thickness. Each spiral acquisition through the liver was accomplished during a breath hold.

MR imaging was performed with a 1.5-T whole-body MR imager (Signa LX; GE Medical Systems). All MR images were obtained in the transverse plane with a phased-array multicoil for the body. Section thickness was 7 mm, with a 2-mm intersection gap for all pulse sequences. The imaging protocol comprised fat-suppressed T2-weighted respiratory-triggered fast spin-echo sequences (repetition time msec/echo time msec of 6,000– 11,000 [effective]/100 [effective], echo train length of 16, four signals acquired, interecho spacing of 10 msec, matrix of 256 x 256, bandwidth of 31.25 kHz, field of view of 40 cm, 20% respiratory trigger point, 40% trigger window, gradient moment nulling in the frequency-encoding direction). Saturation bands superior and inferior to the imaging volume were used in the attenuation of flow-related artifacts throughout MR imaging. Dynamic contrast material–enhanced MR imaging was performed at four consecutive 30-second intervals and at 5 minutes after the start of a bolus injection of 0.1 mmol per kilogram of body weight of gadoterate meglumine (Dotarem; Guerbet) into the antecubital vein by using a power injector (Spectris; Medrad). T1-weighted fast multiplanar spoiled gradient-recalled-echo (GRE) sequences (125–150/1.6–4.2, flip angle of 60°, one signal acquired, matrix of 512 x 256, bandwidth of 62.5 kHz, field of view of 40 cm, 25-second breath-hold acquisition) were performed.

Image Analysis
CT and MR images were interpreted independently and prospectively by two radiologists (C.D., T.d.B.) experienced in abdominal CT and MR imaging, who were aware of the RF treatment but were blinded to the initial histopathologic diagnosis, the posttreatment clinical and biologic findings, and the elapsed time from the RF treatment. CT and MR images were read separately for each interval of 2, 4, and 6 months. In cases of interobserver disagreement, the final decisions were reached with consensus. The size and shape of the treated area were evaluated at each imaging follow-up on both CT and MR images. On unenhanced and dynamic contrast-enhanced CT scans, the treated area was classified as hypoattenuating, hyperattenuating, or isoattenuating compared with the surrounding liver parenchyma. In addition, the appearance was classified as homogeneous or heterogeneous. On MR images, the signal intensity pattern of the treated area was compared with that of the surrounding parenchyma and was classified as hyperintense, hypointense, or isointense on T1-, T2-, and contrast-enhanced T1-weighted images, respectively. Homogeneity and heterogeneity were also classified.

According to previous reports (68), all contrast-enhanced foci on CT or MR images and/or hyperintense foci on T2-weighted images with nodular shape or irregular thickening of the boundaries of the treated area were considered as suspicious for local tumor regrowths. In such cases, biopsies were performed when suspicious areas could be visualized with US or CT guidance and when biopsy was considered possible with regard to the size (>1 cm) and depth of the area. When the suspected recurrences were not proven at biopsy, they were confirmed on the basis of an increase in size during the imaging follow-up. All areas of RF-induced necrosis that did not demonstrate contrast enhancement within the boundaries of the treated area on CT or MR images and/or hyperintense foci on T2-weighted images were considered as successfully treated tumors. These successful treatments were confirmed with imaging follow-up performed at least 12 months after RF treatment (mean follow-up, 19 months), except in two patients who died of diffuse hepatic metastases during the study period at 7 and 8 months, respectively, after the RF procedure.

With each imaging technique, the features that were of particular interest in this study were the pattern, the size, the location compared with that of blood vessels, and the date of the appearance of local recurrence at the site of the treatment. The appearance of new intrahepatic lesions and the complications generated with RF treatment were also assessed on both CT and MR images.

Statistical Analysis
The Student t test for paired data was used to compare differences between the greatest necrosis RF-induced area diameter measured at both CT and MR imaging, with a threshold P value of .05. Sensitivity, specificity, and positive and negative predictive CT and MR imaging values in the detection of local regrowth were determined with a 95% CI calculated by using the binomial distribution. Differences in sensitivity at 2 months on CT and MR images and on T2-weighted and dynamic contrast-enhanced T1-weighted images were assessed by using paired samples with the McNemar two-sided test (categoric data).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
CT and MR Imaging Follow-up at 2 Months
On unenhanced CT images, the RF-treated areas were homogeneously hypoattenuating (n = 24) or were heterogeneous and contained hyperattenuating foci in a hypoattenuating area (n = 26). Contrast-enhanced CT images showed no enhancement in 37 RF-treated areas (Fig 1). In the remaining 13 areas, CT images showed nine thin (<1 mm) rims of enhancement around the RF-treated area, three round enhancements abutting the RF-treated area, and one irregular enhanced thickening at the margin of the RF-treated area.



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Figure 1. Transverse contrast-enhanced CT image of a successfully treated colorectal metastasis obtained 2 months after RF therapy shows a well-demarcated area (arrow) without contrast enhancement.

 
On unenhanced T1-weighted MR images, 14 RF-treated areas were hypointense and homogeneous and 36 were heterogeneous with a peripheral hyperintense ring. On T2-weighted MR images, 27 RF-treated areas were hypointense and homogeneous, seven were isointense and homogeneous, eight were heterogeneous with foci of markedly high signal intensity (close to the signal intensity of liquid), and eight were heterogeneous with foci of moderately high signal intensity located at the treated area margin. Contrast-enhanced T1-weighted MR images showed a well-demarcated hypointense area without contrast enhancement in 33 RF-treated areas. In the remaining 17 areas, contrast-enhanced T1-weighted MR images depicted 12 thin (<1 mm) rims of enhancement (Fig 2), six round enhancements abutting the RF-treated area (Fig 3), and two irregular enhanced thickenings of the RF-treated area margin (Fig 4). Thin rims of enhancement were associated with areas of round enhancement in three cases.



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Figure 2a. Transverse MR images of a hepatocellular carcinoma completely destroyed after RF therapy. (a) Pretreatment fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (6,000/100) shows the tumor (arrow) with moderate hyperintensity. (b) Arterial phase breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) shows the tumor (arrow) with enhancement. (c) Fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (10,909/100) of the RF-treated area obtained 2 months after RF therapy shows a hypointense homogeneous area with a hyperintense rim. (d) On contrast-enhanced dynamic breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, no contrast enhancement was found within or in contact with the RF-treated area (arrowheads). (e) On equilibrium phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, the RF-treated area is surrounded by a thin enhancing rim (arrowheads) that matches the hyperintense rim depicted on T2-weighted image and corresponds to a vascularized inflammatory reaction surrounding the zone of coagulation necrosis.

 


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Figure 2b. Transverse MR images of a hepatocellular carcinoma completely destroyed after RF therapy. (a) Pretreatment fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (6,000/100) shows the tumor (arrow) with moderate hyperintensity. (b) Arterial phase breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) shows the tumor (arrow) with enhancement. (c) Fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (10,909/100) of the RF-treated area obtained 2 months after RF therapy shows a hypointense homogeneous area with a hyperintense rim. (d) On contrast-enhanced dynamic breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, no contrast enhancement was found within or in contact with the RF-treated area (arrowheads). (e) On equilibrium phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, the RF-treated area is surrounded by a thin enhancing rim (arrowheads) that matches the hyperintense rim depicted on T2-weighted image and corresponds to a vascularized inflammatory reaction surrounding the zone of coagulation necrosis.

 


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Figure 2c. Transverse MR images of a hepatocellular carcinoma completely destroyed after RF therapy. (a) Pretreatment fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (6,000/100) shows the tumor (arrow) with moderate hyperintensity. (b) Arterial phase breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) shows the tumor (arrow) with enhancement. (c) Fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (10,909/100) of the RF-treated area obtained 2 months after RF therapy shows a hypointense homogeneous area with a hyperintense rim. (d) On contrast-enhanced dynamic breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, no contrast enhancement was found within or in contact with the RF-treated area (arrowheads). (e) On equilibrium phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, the RF-treated area is surrounded by a thin enhancing rim (arrowheads) that matches the hyperintense rim depicted on T2-weighted image and corresponds to a vascularized inflammatory reaction surrounding the zone of coagulation necrosis.

 


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Figure 2d. Transverse MR images of a hepatocellular carcinoma completely destroyed after RF therapy. (a) Pretreatment fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (6,000/100) shows the tumor (arrow) with moderate hyperintensity. (b) Arterial phase breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) shows the tumor (arrow) with enhancement. (c) Fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (10,909/100) of the RF-treated area obtained 2 months after RF therapy shows a hypointense homogeneous area with a hyperintense rim. (d) On contrast-enhanced dynamic breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, no contrast enhancement was found within or in contact with the RF-treated area (arrowheads). (e) On equilibrium phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, the RF-treated area is surrounded by a thin enhancing rim (arrowheads) that matches the hyperintense rim depicted on T2-weighted image and corresponds to a vascularized inflammatory reaction surrounding the zone of coagulation necrosis.

 


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Figure 2e. Transverse MR images of a hepatocellular carcinoma completely destroyed after RF therapy. (a) Pretreatment fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (6,000/100) shows the tumor (arrow) with moderate hyperintensity. (b) Arterial phase breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) shows the tumor (arrow) with enhancement. (c) Fat-suppressed T2-weighted respiratory-triggered fast spin-echo image (10,909/100) of the RF-treated area obtained 2 months after RF therapy shows a hypointense homogeneous area with a hyperintense rim. (d) On contrast-enhanced dynamic breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, no contrast enhancement was found within or in contact with the RF-treated area (arrowheads). (e) On equilibrium phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (150/4.2) obtained 2 months after RF therapy, the RF-treated area is surrounded by a thin enhancing rim (arrowheads) that matches the hyperintense rim depicted on T2-weighted image and corresponds to a vascularized inflammatory reaction surrounding the zone of coagulation necrosis.

 


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Figure 3a. Biopsy-proved local regrowth depicted on transverse CT and MR images 2 months after RF ablation of a metastasis from breast carcinoma. (a) Contrast-enhanced CT scan shows a nodule (arrow) abutting the RF-treated area, whose attenuation is higher than that of the RF-induced necrosis. (b) Fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,000/100) shows that the tumor nodule (arrow) is hyperintense, contrasting with the adjacent hypointense signal of the RF-induced necrosis. (c) Unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows the hypointense tumor nodule (arrow) and the hyperintense signal of the RF-induced necrosis (arrowheads). (d) Arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows enhancement of this nodule (arrow). Peripheral rim (arrowheads) of contrast enhancement is also present and corresponds to an early inflammatory response to treatment.

 


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Figure 3b. Biopsy-proved local regrowth depicted on transverse CT and MR images 2 months after RF ablation of a metastasis from breast carcinoma. (a) Contrast-enhanced CT scan shows a nodule (arrow) abutting the RF-treated area, whose attenuation is higher than that of the RF-induced necrosis. (b) Fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,000/100) shows that the tumor nodule (arrow) is hyperintense, contrasting with the adjacent hypointense signal of the RF-induced necrosis. (c) Unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows the hypointense tumor nodule (arrow) and the hyperintense signal of the RF-induced necrosis (arrowheads). (d) Arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows enhancement of this nodule (arrow). Peripheral rim (arrowheads) of contrast enhancement is also present and corresponds to an early inflammatory response to treatment.

 


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Figure 3c. Biopsy-proved local regrowth depicted on transverse CT and MR images 2 months after RF ablation of a metastasis from breast carcinoma. (a) Contrast-enhanced CT scan shows a nodule (arrow) abutting the RF-treated area, whose attenuation is higher than that of the RF-induced necrosis. (b) Fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,000/100) shows that the tumor nodule (arrow) is hyperintense, contrasting with the adjacent hypointense signal of the RF-induced necrosis. (c) Unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows the hypointense tumor nodule (arrow) and the hyperintense signal of the RF-induced necrosis (arrowheads). (d) Arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows enhancement of this nodule (arrow). Peripheral rim (arrowheads) of contrast enhancement is also present and corresponds to an early inflammatory response to treatment.

 


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Figure 3d. Biopsy-proved local regrowth depicted on transverse CT and MR images 2 months after RF ablation of a metastasis from breast carcinoma. (a) Contrast-enhanced CT scan shows a nodule (arrow) abutting the RF-treated area, whose attenuation is higher than that of the RF-induced necrosis. (b) Fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,000/100) shows that the tumor nodule (arrow) is hyperintense, contrasting with the adjacent hypointense signal of the RF-induced necrosis. (c) Unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows the hypointense tumor nodule (arrow) and the hyperintense signal of the RF-induced necrosis (arrowheads). (d) Arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/1.6) shows enhancement of this nodule (arrow). Peripheral rim (arrowheads) of contrast enhancement is also present and corresponds to an early inflammatory response to treatment.

 


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Figure 4a. Local regrowth depicted only at MR imaging 2 months after treatment of a metastasis from colorectal cancer. (a) Transverse contrast-enhanced CT scan shows a well-demarcated hypoattenuating area (arrow) with no evidence of enhancement. The CT examination was interpreted as normal and is one of the four false-negative results among the CT scans obtained at 2 months. (b) Transverse fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,571/100) shows a hyperintense area (arrow) inside the treated area, which corresponds to local tumor regrowth. (c) Transverse unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows a hypointense area corresponding to a local tumor regrowth (arrow) adjacent to the spontaneously hyperintense RF-induced necrosis. (d) Transverse arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows enhancement of the local tumor regrowth (arrow) compared with the unenhanced RF-induced necrosis.

 


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Figure 4b. Local regrowth depicted only at MR imaging 2 months after treatment of a metastasis from colorectal cancer. (a) Transverse contrast-enhanced CT scan shows a well-demarcated hypoattenuating area (arrow) with no evidence of enhancement. The CT examination was interpreted as normal and is one of the four false-negative results among the CT scans obtained at 2 months. (b) Transverse fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,571/100) shows a hyperintense area (arrow) inside the treated area, which corresponds to local tumor regrowth. (c) Transverse unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows a hypointense area corresponding to a local tumor regrowth (arrow) adjacent to the spontaneously hyperintense RF-induced necrosis. (d) Transverse arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows enhancement of the local tumor regrowth (arrow) compared with the unenhanced RF-induced necrosis.

 


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Figure 4c. Local regrowth depicted only at MR imaging 2 months after treatment of a metastasis from colorectal cancer. (a) Transverse contrast-enhanced CT scan shows a well-demarcated hypoattenuating area (arrow) with no evidence of enhancement. The CT examination was interpreted as normal and is one of the four false-negative results among the CT scans obtained at 2 months. (b) Transverse fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,571/100) shows a hyperintense area (arrow) inside the treated area, which corresponds to local tumor regrowth. (c) Transverse unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows a hypointense area corresponding to a local tumor regrowth (arrow) adjacent to the spontaneously hyperintense RF-induced necrosis. (d) Transverse arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows enhancement of the local tumor regrowth (arrow) compared with the unenhanced RF-induced necrosis.

 


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Figure 4d. Local regrowth depicted only at MR imaging 2 months after treatment of a metastasis from colorectal cancer. (a) Transverse contrast-enhanced CT scan shows a well-demarcated hypoattenuating area (arrow) with no evidence of enhancement. The CT examination was interpreted as normal and is one of the four false-negative results among the CT scans obtained at 2 months. (b) Transverse fat-suppressed T2-weighted respitarory-trigered fast spin-echo MR image (8,571/100) shows a hyperintense area (arrow) inside the treated area, which corresponds to local tumor regrowth. (c) Transverse unenhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows a hypointense area corresponding to a local tumor regrowth (arrow) adjacent to the spontaneously hyperintense RF-induced necrosis. (d) Transverse arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) shows enhancement of the local tumor regrowth (arrow) compared with the unenhanced RF-induced necrosis.

 
The greatest diameter of the RF-induced coagulation varied from 18 to 65 mm (mean, 31 mm) for a single electrode (one to three needle insertions) and from 40 to 65 mm (mean, 52 mm) for a triple-cluster needle (one to four needle insertions), without significant (P < .005) differences between measurements on CT or MR images.

Treatment-related complications depicted on CT and MR images were two clinically unsuspected intrahepatic abscesses at the site of RF application, which were confirmed with percutaneous biopsy and drainage. Incidental imaging findings were one false aneurysm of the puncture tract (diagnosed on the basis of CT and MR imaging findings but not confirmed at arteriography), necrosis along the path of the RF electrode, and segmental dilatation of intrahepatic bile ducts that were in contact with the RF-treated area in three patients. Hepatic hyperperfusion abnormalities, depicted as a typical wedge-shaped homogeneous area of contrast material uptake, were observed at the periphery of the RF-treated area on contrast-enhanced arterial phase CT and MR images in six (12%) patients, without early enhancement of a peripheral portal branch (Fig 5).



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Figure 5. Transverse MR image of a successfully treated hepatocellular carcinoma 2 months after RF therapy. Arterial phase contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE image (125/1.6) shows a wedge-shaped enhancement (arrowheads) in the surrounding parenchyma adjacent to the RF-treated area, which corresponds to arterioportal shunts.

 
Imaging Follow-up
CT images obtained at 4 months showed four additional round areas of enhancement in contact with the RF-treated area and one additional irregular enhanced thickening of the RF-treated margin. These new areas of enhancement corresponded to abnormal findings obtained at 2-month MR imaging: four abnormal moderately hyperintense areas on T2-weighted MR images and two abnormal areas of enhancement on T1-weighted MR images. T2-weighted MR images obtained at 4 months showed one new round area of high signal intensity, which was enhanced on T1-weighted images.

At 6 months and after, no modification of the pattern of the RF-treated areas was noted. During the imaging follow-up, 27 (66%) of 41 successfully treated tumors decreased in size. This decrease attained a mean of 15% (range, 10%–30%) at 6 months and a mean of 35% (range, 15%–90%) at 12 months. At 2 months, the peripheral rim of enhancement depicted on MR images of 12 treated areas and on CT scans of nine treated areas disappeared in 10 of 12 and seven of nine treated areas, respectively, at 4 months, in 11 of 12 and eight of nine treated areas, respectively, at 6 months, and on all CT scans obtained at 12 months. The wedge-shaped areas of enhancement depicted on contrast-enhanced arterial phase CT and MR images disappeared in four of six RF-treated areas at 4 months and in all cases at 6 months.

New hepatic tumors distant from the RF-treated areas were found in 19 (61%) of 31 patients during follow-up: at 2 months in eight patients, at 4 months in seven patients, at 6 months in three patients, and at 9 months in one patient.

Assessment of the Treatment Response
After a mean follow-up of 19 months, 41 (82%) of 50 hepatic tumors treated with percutaneous RF ablation were considered completely destroyed on imaging studies and nine (18%) showed local regrowth, which was probably due to inadequate RF treatment during the follow-up. Regrowth occurred in RF-ablated hepatocellular carcinoma (n = 2), colorectal metastases (n = 5), breast metastasis (n = 1), and renal adenocarcinoma metastasis (n = 1). Eight of nine local regrowths were depicted 2 months after thermal ablation, and one became conspicuous at 4 months. These local regrowths were confirmed with US or CT-guided biopsies in four cases and with imaging follow-up in five cases.

Among the eight local regrowths detected at 2 months, all were seen on MR images and four were seen on CT scans. At 2 months, the sensitivity, specificity, and positive and negative predictive CT values were 44% (95% CI: 14%, 79%), 100%, 100%, and 89%, respectively, whereas the MR imaging values were 89% (95% CI: 52%, 100%), 100%, 100%, and 97.5%, respectively. At 2 months, the sensitivity of local regrowth detection with MR imaging was not significantly higher compared with that at CT (P = .12). The four local regrowths depicted exclusively on MR images were confirmed 2 months later (4 months after RF treatment), because the size of the suspicious area had increased on MR images and because of the appearance of contrast enhancement on CT scans in areas that were suspect on earlier MR images.

At 2 months, six of the eight local regrowths exhibited moderate high signal intensity on T2-weighted images and contrast material uptake on T1-weighted images. The two remaining local regrowths were detected only on T2-weighted images as a hyperintense nodules abutting the hypointense necrotic area, without suspicious areas being detectable on T1-weighted images before or after contrast medium injection (Fig 6). Nevertheless, the sensitivity of local regrowth on T2-weighted and dynamic contrast-enhanced T1-weighted images did not differ significantly (P > .50). However, in these two cases, enhancement appeared on postcontrast T1-weighted images at 4 months. On CT scans, local regrowths were seen as round or irregular areas of enhancement at the margin of the treatment zone, which corresponded to the area of enhancement on MR images. The appearance of the RF-treated area on CT and MR images is summarized in the Table.



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Figure 6a. Local regrowth depicted only at T2-weighted MR imaging 2 months after treatment of hepatocellular carcinoma. (a) Transverse contrast-enhanced CT scan obtained 2 months after RF therapy shows a well-demarcated area containing hyperattenuating foci (straight arrows), which correspond to hemorrage material but without evidence of suspicious enhancement at the periphery of the RF-induced necrosis. Subcapsular hyperattenuating area (curved arrow) is a residual uptake of iodized oil in a hepatocellular carcinoma treated 6 months earlier by using hepatic arterial chemoembolization. (b) Transverse fat-suppressed T2-weighted respiratory-triggered fast spin-echo MR image (8,571/100) obtained the same day as a shows a hyperintense nodule (arrow) abutting the treated area. (c) Transverse contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) obtained the same day as a and b shows no suspicious enhancement at the area where the hyperintense nodule was depicted on the T2-weighted image.

 


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Figure 6b. Local regrowth depicted only at T2-weighted MR imaging 2 months after treatment of hepatocellular carcinoma. (a) Transverse contrast-enhanced CT scan obtained 2 months after RF therapy shows a well-demarcated area containing hyperattenuating foci (straight arrows), which correspond to hemorrage material but without evidence of suspicious enhancement at the periphery of the RF-induced necrosis. Subcapsular hyperattenuating area (curved arrow) is a residual uptake of iodized oil in a hepatocellular carcinoma treated 6 months earlier by using hepatic arterial chemoembolization. (b) Transverse fat-suppressed T2-weighted respiratory-triggered fast spin-echo MR image (8,571/100) obtained the same day as a shows a hyperintense nodule (arrow) abutting the treated area. (c) Transverse contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) obtained the same day as a and b shows no suspicious enhancement at the area where the hyperintense nodule was depicted on the T2-weighted image.

 


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Figure 6c. Local regrowth depicted only at T2-weighted MR imaging 2 months after treatment of hepatocellular carcinoma. (a) Transverse contrast-enhanced CT scan obtained 2 months after RF therapy shows a well-demarcated area containing hyperattenuating foci (straight arrows), which correspond to hemorrage material but without evidence of suspicious enhancement at the periphery of the RF-induced necrosis. Subcapsular hyperattenuating area (curved arrow) is a residual uptake of iodized oil in a hepatocellular carcinoma treated 6 months earlier by using hepatic arterial chemoembolization. (b) Transverse fat-suppressed T2-weighted respiratory-triggered fast spin-echo MR image (8,571/100) obtained the same day as a shows a hyperintense nodule (arrow) abutting the treated area. (c) Transverse contrast-enhanced breath-hold T1-weighted fast multiplanar spoiled GRE MR image (125/2) obtained the same day as a and b shows no suspicious enhancement at the area where the hyperintense nodule was depicted on the T2-weighted image.

 

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Appearance of Hepatic Tumors on CT and MR Images Obtained 2 Months after RF Ablation

 
Local regrowths were 5–15 mm (mean, 10.8 mm) in diameter, nodular, and in contact with the margin of the treatment zone in seven cases. In two cases, irregular thickening that measured 4 and 5 mm in width was identified at the margin of the treatment zone. Two recurrences were in contact with a large blood vessel.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The aim of RF treatment is to generate an area of thermocoagulation whose diameter is larger or at least equivalent to that of the tumor. The area of RF-induced coagulated tissue forms a necrotic "scar" that usually shrinks with time, but most often very slowly. Thus, World Health Organization criteria, according to which improvement due to anticancer treatment is evaluated by the decrease in size, cannot be applied to assess response to thermal ablation therapy (9). Therefore, other methods are needed for early assessment of the efficacy of RF treatment.

Although US is an efficient tool for monitoring RF treatment, findings from previous reports (6,1012) have shown the limited value of this technique for the evaluation of treatment efficacy. The echogenicity of necrotic and viable tumor tissue may have a similar appearance on posttreatment US images. As reported by others, US contrast medium, which is currently under investigation in our institution, may help in the future to differentiate tumor from necrosis (13). Contrast-enhanced CT and MR imaging are at present considered the most useful modalities for the assessment of treatment efficacy. Findings from some preliminary reports (7,14) suggest that the size of the nonenhancing region depicted on CT and MR images corresponds to within 2 mm of the size of the coagulated necrosis measured at histologic examination. The criterion commonly used at CT and MR imaging to assess this efficacy is the absence of enhancement in RF-induced necrosis, which corresponds to tissue devoid of viable tumor. In most studies, CT or MR imaging is used variably and indifferently to assess the efficacy of RF treatment but, to our knowledge, the respective values of these two imaging techniques have not yet been reported.

Two months after RF therapy, uniform hypointensity on T2-weighted images, associated with lack of enhancement of the RF-treated area on contrast-enhanced T1-weighted images, always corresponded to complete efficient treatment. Most of the RF-treated areas were hyperintense on unenhanced T1-weighted images, which was probably due to hemorrhage or a proteinaceous material within the RF-treated area. Most of the RF-treated areas were hypointense on T2-weighted images, and this hypointensity could be explained by the dehydrating effect of RF-induced thermal damage that results in coagulative necrosis. However, marked hyperintensity on T2-weighted images, found in 14% of the successfully treated areas, could signify biloma or liquefactive necrosis, as active tumor always displays a less heavily intense T2 signal intensity.

Our study findings show that in four of eight cases, MR imaging allows earlier detection of residual tumor than does CT. Nevertheless, due to the small number of local regrowths in our study, no significant differences between MR images and CT scans at two months could be found. All local regrowths were detected at MR imaging follow-up at 2 months, except for one regrowth that was detected at 4 months. In this case, liquefactive necrotic material, which exhibited markedly high signal intensity on T2-weighted MR images obtained at 2 months, probably masked the less intense signal intensity induced by a minute focus of residual tumor. At 4 months, the area of markedly high signal intensity related to liquefactive necrosis disappeared and residual viable tumor that exhibited moderately high signal intensity was easily detected on T2-weighted images. This moderately high signal intensity corresponded to an area of enhancement on contrast-enhanced T1-weighted images.

The higher sensitivity of MR imaging over CT is mostly due to the T2-weighted images, which were the only imaging studies capable of depicting tumor in two cases at two months. The superior sensitivity of T2-weighted imaging could be explained by an increase in contrast between the coagulated area, which has a low signal intensity, and the viable residual tumor, which has a high signal intensity. Moderate (different from a fluid signal) hyperintensity on T2-weighted images corresponded to the presence of residual viable tumor in all cases. Therefore, T2-weighted imaging is demonstrated to be highly specific. Moreover, the moderately hyperintense area on T2-weighted images associated with corresponding enhancement on contrast-enhanced T1-weighted images offers optimal specificity (100%) for residual viable tumor in all cases.

In our experience, local regrowths were always depicted at the periphery of the treated area either as irregular thickening of one margin of the treated area or a new tumor nodule. These peripheral locations of treatment failures could be explained by lower energy deposition and reduced heating that was remote from the needle electrode. Furthermore, tissue perfusion lowers heat accumulation due to cooling, and this phenomenon is even more marked in tissue in contact with large vessels. Indeed, regrowth close to large vessels arose in two of nine cases in our study and has already been described by others (1,7).

Peripheral regrowth should not be diagnosed when one sees a thin and regular (<1 mm) rim of progressive contrast enhancement, which was present at 2 months in 32% of the entire RF-treated area in our study and better seen at the later phase after contrast material administration. It has been shown by means of comparison with histologic findings that the thin ring is a vascularized inflammatory reaction with granulation tissue surrounding the zone of coagulation necrosis (11,1416). Similar findings have been described less frequently in hepatocellular carcinoma treated with alcohol injection (1719) and in hepatic metastases treated with laser-induced thermotherapy (10,20). In our study, the peripheral rim disappeared with time and was present in only 8% of the RF-treated area at 4 months. It can easily be differentiated from an active tumor whose area of contrast enhancement is thicker and irregular. Another RF-induced modification is the presence on arterial phase images of wedge-shaped enhancement in the liver parenchyma adjacent to the RF-treated area, which was present in our study in 12% of patients. This enhancement probably corresponds to peripheral arterioportal shunts caused by either the needle puncture and/or thermal damage. These wedge-shaped areas should not be misinterpreted as tumor contrast material uptake.

Although there are many similarities between the radiologic aspect of RF-induced destruction and the necrosis induced by ethanol (17,18,21), some differences need to be pointed out. First, in our study, T2-weighted MR imaging was demonstrated to be the best indicator of the efficacy of RF treatment. In contrast, Sironi et al (17) and Nagel and Bernardino (21) described a limited value of the T2-weighted signal intensity pattern of tumors injected with alcohol in ascertaining the viability of the tumor. This might be due either to differences in technical parameters (fast spin echo with respiratory monitoring in our study versus standard spin echo with a higher rate of motion artifacts in their studies) or to histopathologic nature of the initial tumors, which is very different in our study from that of these previous reports. Second, the area of RF-induced coagulation necrosis shrank more slowly than that of ethanol-induced necrosis. Indeed, in our study, 66% of the treated area shrank, attaining a mean reduction of 15% at 6 months and 35% at 12 months. Ebara et al (22) reported shrinkage of all treated areas, which attained a mean of 45% at 6 months and 63% at 12 months in 67 hepatocellular carcinomas treated with ethanol. The value of a decrease in size of the RF-treated area appears to be even more limited than it was with alcohol, which was already not very effective given the time to total shrinkage.

Limitations of our study include the small number of patients and lesions, which limited the value of statistical analysis, the heterogeneity of tumor origin, the absence of MR imaging 6-month follow-up, and the lack of biopsy in five cases of suspected local regrowths.

In conclusion, CT and MR imaging are able to help in the accurate assessment of RF treatment efficacy. As reported by others at 6 months, MR imaging and CT depicted all local regrowths at 4 months or earlier. Knowledge of the RF-treatment zone patterns is essential for the correct evaluation of MR imaging and CT follow-up. MR imaging may have an edge over CT in the early detection of local regrowths due to the high sensitivity of T2-weighted imaging, but further studies are needed to confirm the apparent superiority of MR imaging over CT in the detection of local regrowth after RF ablation of hepatic tumors.


    ACKNOWLEDGMENTS
 
We thank Lorna Saint Ange for editing and Agnès Laplanche for statistical analysis.


    FOOTNOTES
 
Abbreviations: GRE = gradient-recalled echo, RF = radio frequency

Author contributions: Guarantor of integrity of entire study, C.D.; study concepts, C.D., A.R., T.d.B.; study design, V.B., M.D., C.D., T.d.B.; literature research, C.D., T.d.B.; clinical studies, D.E., M.D., V.B., T.d.B., V.K.; data acquisition, C.D., P.P.; data analysis/interpretation, P.P., C.D., T.d.B.; manuscript preparation, C.D., T.d.B.; manuscript definition of intellectual content, V.K., C.D., T.d.B.; manuscript editing, C.D.; manuscript revision/review and final version approval, C.D., T.d.B., R.S.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE