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Vascular and Interventional Radiology |
1 From the Department of Radiology, Duke University Medical Center, Duke North-Room 1417, Erwin Rd, Durham, NC 27710 (E.M.M.); Department of Radiology, University Hospitals of Cleveland/Case Western Reserve University, Cleveland, Ohio (S.G.N.); and Department of Radiology, Johns Hopkins University, Baltimore, Md (J.S.L.). From the 2004 RSNA Annual Meeting. Received May 13, 2004; revision requested August 2; revision received September 14; accepted October 20. Address correspondence to E.M.M. (e-mail: elmar.merkle@duke.edu).
| ABSTRACT |
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MATERIALS AND METHODS: After providing written informed consent, 18 patients (17 men, one woman; mean age, 71.2 years) with RCC underwent MR imagingguided percutaneous RF thermal ablation, which was performed by using protocols approved by a comprehensive cancer center protocol committee and the institutional review board for human investigation. The study was Health Insurance Portability and Accountability Act compliant. Follow-up unenhanced T2-weighted MR images and unenhanced and gadolinium-enhanced T1-weighted MR images were acquired immediately, 2 weeks, 3 months, and 6 months after ablation. Thermal ablation zone size was analyzed, and contrast-to-noise ratios (CNRs) were calculated from the signal amplitudes of the thermal ablation zone, perirenal fat, and normal renal cortex on the MR images. Statistical analyses were performed by using the paired Student t test. P < .05 was considered to indicate statistical significance.
RESULTS: The mean follow-up time was 16.1 months (range, 6.041.2 months). The mean sizes of the thermal ablation zones were 6.8, 7.0, 6.1, and 4.7 cm2, respectively, at immediate, 2-week, 3-month, and 6-month follow-up MR imaging examinations. Thermal ablation zones were uniformly hypointense and had a surrounding bright rim on T2-weighted images and were predominantly hyperintense on T1-weighted images. Thin rim enhancement with central hypointensity was noted on the gadolinium-enhanced images. Gadolinium-enhanced T1-weighted and unenhanced T2-weighted MR images showed significantly higher CNRs than unenhanced T1-weighted MR images. Residual tumor was detected after RF thermal ablation in two cases and was best seen on unenhanced T2-weighted and gadolinium-enhanced T1-weighted MR images.
CONCLUSION: After initially increasing in size within the first 2 weeks, renal RF thermal ablation zones involuted during the remainder of the MR imaging follow-up period.
© RSNA, 2005
| INTRODUCTION |
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Although radical nephrectomy has long been considered the standard treatment for localized RCC, nephron-sparing surgery has been used increasingly (5). Segmental resection is particularly valuable in patients who have previously undergone nephrectomy or had a contralateral nonfunctioning renal unit. Other minimally invasive treatment modalities, such as laser ablation and radiofrequency (RF) thermal ablation, also have become of interest. These procedures are being performed increasingly in patients who either are not surgical candidates because of comorbidities or refuse to undergo surgery.
During the past 5 years, limited experience with RF thermal ablation in patients with RCC has been gained by numerous research groups (615). The surveillance protocol after performing this procedure usually consists of dedicated contrast materialenhanced computed tomography (CT) of the kidney. However, a considerable number of eligible patients cannot receive contrast agents that contain iodine because of preexisting impaired renal function or severe contrast material allergies. These patients are usually referred for contrast-enhanced magnetic resonance (MR) imaging of the kidney. Thus, the purpose of our study was to prospectively evaluate the short- and midterm MR imaging findings seen after RF thermal ablation of RCC.
| MATERIALS AND METHODS |
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The 18 patients underwent 21 RF thermal ablation procedures with MR imaging guidance, which was performed by using an open 0.2-T system (Magnetom Open; Siemens Medical Solutions, Erlangen, Germany). One patient had two RCC foci, another patient had an additional contralateral RCC, and a third patient with RCC was treated a second time after incomplete ablation. All tumors were either located peripherally away from the renal sinus or exophytic. Detailed descriptions of the interventional MR imaging suite and the MR imagingguided ablation procedure that we used have been reported previously (15).
Follow-up MR Imaging
Follow-up MR imaging was performed in all patients immediately after the completion of the RF ablation, while the patient was still in the open MR imaging system. The low-field-strength (0.2-T) follow-up MR imaging protocol involved the acquisition of transverse T1-weighted spin-echo (SE) images (440/15, five signals acquired, 169 or 215 x 256 matrix, 30 x 40-cm or 36 x 36-cm field of view) before and after intravenous administration of 0.2 mL of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) per kilogram of body weight (0.1 mmol/kg) or 0.2 mL/kg (0.1 mmol/kg) gadodiamide (Omniscan; Nycomed-Amersham, Princeton, NJ) and unenhanced coronal T2-weighted fast SE images (4000/102, four signals acquired, 126 or 182 x 256 matrix, 25 x 40-cm or 36 x 36-cm field of view, echo train length of seven).
High-field-strength (1.5-T) MR imaging was performed (with Magnetom Vision, Magnetom Symphony, or Magnetom Sonata system; Siemens Medical Solutions) 2 weeks after RF ablation, quarterly within the first year, and every 6 months thereafter. The high-field-strength follow-up MR imaging protocol involved unenhanced coronal T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE) imaging (single-shot turbo SE sequence, 800/42, one signal acquired, 169 or 205 x 256 matrix, 30 x 40-cm or 36 x 36-cm field of view) and transverse two-dimensional T1-weighted gradient-echo (GRE) imaging (fast low-angle shot sequence, 222/2.6, 70° flip angle, 169 or 205 x 256 matrix, 30 x 40-cm or 36 x 36-cm field of view) performed before and 3 minutes after intravenous administration of 0.2 mL/kg (0.1 mmol/kg) gadopentetate dimeglumine or 0.2 mL/kg (0.1 mmol/kg) gadodiamide.
The mean and longest follow-up durations were 16.1 months ± 11.3 (standard deviation) and 41.2 months, respectively; all patients were followed up for at least 6 months.
Image and Data Analyses
The follow-up MR images acquired within the first 6 months after ablation were evaluated for ablation zone size, signal intensity characteristics, and evidence of recurrent or residual tumor, which was defined as either an area of hyperintense soft tissue within the ablation zone or along its margin on T2-weighted images or an area of abnormal contrast enhancement on contrast-enhanced T1-weighted images within the treated region.
The bidimensional thermal ablation zone sizes at each follow-up time point (immediately, 2 weeks, 3 months, and 6 months after ablation) were measured by using electronic calipers on the workstation monitor (Leonardo; Siemens Medical Solutions) and compared on the T2-weighted fast SE images. Only the hypointense area within the perirenal space was considered to be a thermal ablation zone (16).
The signal amplitudes of the uninvolved renal cortex (remote from the ablation site), the RF thermal ablation zone, and the perirenal fat were measured with each follow-up MR imaging sequence by defining the regions of interest (ROIs) on the free-standing MR imaging workstation. All measurements were performed by the same board-certified radiologist (S.G.N.), who had undergone fellowship training in MR imaging. The sizes of the ROIs used to measure the signal intensity amplitude in tissue ranged from 37 to 899 mm2 and were chosen in homogeneous, artifact-free areas of the tissue being measured. The standard deviation of the noise also was measured by using noise ROIs ranging in size from 535 to 676 mm2. The ROIs used for noise measurements were oval and had a long axis perpendicular to the phase-encoding direction. The noise measurement ROIs were positioned anterior to the abdominal wall (in front of the treated kidney) at transverse MR imaging and lateral to the treated kidney at coronal MR imaging (17). Each signal intensity amplitude value was calculated as the average value for three separately sampled ROIs. Contrast-to-noise ratios (CNRs) were calculated from the signal amplitudes in the thermal ablation zone, the normal renal cortex, and the perirenal fat divided by the standard deviation of the background noise.
Statistical Analyses
Statistical analyses were performed by using the paired Student t test (with Microsoft Excel and Microsoft Windows XP Professional software; Microsoft, Redmond, Wash) to test the null hypothesis that CNRs calculated by using various MR imaging sequences are the same. P values were derived from comparisons of the uninvolved renal cortextothermal ablation zone CNRs and the perirenal fattothermal ablation zone CNRs calculated with different follow-up MR imaging sequences immediately, 2 weeks, 3 months, and 6 months after ablation. P < .05 was considered to indicate statistical significance.
| RESULTS |
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Signal Intensity Characteristics
At T2-weighted fast SE MR imaging performed at 0.2 T immediately after RF ablation, the ablation zone in all cases appeared as a round or ovoid hypointense region that replaced the intermediate- or high-signal-intensity tumor seen on the preablation image. The hypointense thermal ablation zone was surrounded by a faintly bright rim with a well-defined inner border and an ill-defined outer border. The ablation zones did not have a consistent appearance on the unenhanced T1-weighted SE images: Compared with the intact renal cortex, the ablation zone appeared isointense, with a difference in signal intensity of less than 10%, in 33% of the cases; hyperintense, with a difference in signal intensity of more than 10%, in another 33% of the cases; and hypointense, with a difference in signal intensity of more than 10%, in the remaining 33% of the cases. Thin rim enhancement was noted on all contrast-enhanced MR images obtained immediately after ablation. The uninvolved perirenal fat had a higher signal intensity than the ablation zone at all postprocedural MR imaging examinations. Table 1 shows the mean CNRs between the thermal ablation zone and the surrounding tissueeither the renal cortex or the perirenal fatcalculated at immediate follow-up MR imaging.
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Perirenal fattoablation zone CNRs were not significantly different at immediate-follow-up low-field-strength MR imaging (Table 4). During the further course of the follow-up period with 1.5-T MR imaging, both the T2-weighted half-Fourier RARE sequence and the contrast-enhanced T1-weighted GRE sequence yielded significantly higher CNRs between the perirenal fat and the ablation zone than the unenhanced T1-weighted GRE sequence (Table 4).
Residual and Recurrent Tumors
The two patients in this series with the largest and most central tumors (maximal diameters, 3.6 and 4.0 cm) were treated with the primary aim of debulking the tumors. One of these patients underwent one ablation session, and the other underwent two. In both patients, residual tumor was clearly visualized on the intraprocedural intermittently acquired T2-weighted fast SE images as hyperintense tissue that was well contrasted against the hypointense ablation zone. In terms of depiction on the MR images obtained immediately and at subsequent follow-up examinations after ablation, residual RCC was seen best on the T2-weighted imagesas hyperintense tissueand it was seen as enhancing tissue on the contrast-enhanced T1-weighted images (Fig 4).
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| DISCUSSION |
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Parallel to nephron-sparing surgery, minimally invasive therapeutic modalities such as image-guided percutaneous RF thermal ablation also have been refined (3,7). The monitoring protocol after these procedures usually consists of dedicated contrast-enhanced CT of the kidneys performed within 1 month after the ablation and then at 3 and 6 months. Additional surveillance CT scans are usually obtained every 612 months (7). Thermal ablation areas are poorly visualized on contrast-enhanced CT surveillance images, however, and the diagnosis of residual or recurrent tumor is based only on contrast enhancement characteristics (19,20). Although the use of CT as the primary imaging modality is justified because of cost and availability issues, a substantial number of eligible patients cannot be exposed to iodine-containing contrast agents owing to preexisting allergies or impaired renal function, with creatinine levels higher than 2.0 mg/dL (176.8 µmol/L) (7). These patients are usually referred for contrast-enhanced MR imaging of the kidneys (7).
Thermal Ablation Zone Size and Involution over Time
Thermal ablation zonesdefined as hypointense areascould be clearly delineated on all postprocedural T2-weighted MR images obtained in our study. After an average initial increase in the RF thermal ablation zone size of approximately 10% at bidimensional measurements obtained within the first 2 weeks after ablation, the involution of these zonesby an average of approximately 30%was observed during the following 6 months of the MR imaging follow-up period. This involution most likely reflected the elimination of coagulation necrosis by macrophages and other components of the human immune system and was consistent with the involution pattern that has been seen in the liver, pancreas, and kidneys in animal studies (2123).
Signal Intensity Characteristics of Thermal Ablation Zones
RF thermal ablation involves a spectrum of tissue damage processes, including deactivation of enzymes, cell membrane rupture and alteration of tissue structure, protein denaturation and aggregation, and vasoconstriction and intravascular coagulation (24). These effects manifest during different temperature elevations and heating durations, and probably only a subset of these effects are observable as obvious MR imaging signal intensity alterations. In addition, various tissue types have varied responses after thermal treatment in terms of MR imaging signal intensity characteristics. Graham et al (24) found that various tissue types can be classified into four groups: fat, blood, neural tissue such as brain, and fibrous or glandular tissue such as muscle, liver, and kidney.
Fat predominantly consists of triglycerides that undergo reversible effects during the thermal ablation process (24). This phenomenon explains the lack of permanent MR imaging signal intensity alterations after thermal treatment in perirenal fat tissue. In short, thermal ablation zones extending into the perirenal fat appear bright on T1- and T2-weighted MR images.
In contrast, fibrous or glandular tissue such as the renal parenchyma demonstrates irreversible effects, including denaturation and shrinkage of proteins such as collagen and increased hydrophobic interactions, that result in the extrusion of water. These irreversible effects most likely represent the underlying cause of the shortened T2 relaxation time after thermal ablation, which ultimately leads to the uniform hypointense appearance of the ablation zones on T2-weighted MR images. This hypointense appearance on T2-weighted MR images obtained in humans coincides with the experimental data acquired in animal models after renal thermal ablation (16,25); it also resembles the signal intensity pattern seen in other human organs such as the liver and brain.
On the other hand, the appearances of thermal ablation zones on unenhanced T1-weighted MR images have a high degree of variability compared with the uniform hypointense appearance of these zones on T2-weighted MR images. In the current study, although the appearances of the thermal ablation zones as hypointense, isointense, or hyperintense relative to the uninvolved renal cortex were equally common at low-field-strength unenhanced T1-weighted SE MR imaging performed immediately after ablation, the thermal ablation zones appeared hyperintense compared with the uninvolved renal cortex in the majority of cases at further follow-up MR imaging performed with T1-weighted GRE sequences and high-field-strength systems.
The level of reduction in T1 relaxation time during thermal ablation correlates with the degree of tissue vascularity (24). This correlation explains why RF thermal ablation zones appear slightly hyperintense on unenhanced T1-weighted GRE MR images in the majority of cases in the liver and kidney. It also explains why renal RF thermal ablation zones should appear slightly brighter than hepatic RF thermal ablation zones: The degree of vascularity in the kidney is higher than the degree of vascularity in the liver (26). However, this correlation does not explain why renal RF thermal ablation zones have variable appearancesfrom hypointense to markedly hyperintense compared with uninvolved renal cortexon unenhanced T1-weighted MR images; these findings usually are not seen following RF thermal ablation of focal hepatic lesions. Procedure-related diffuse hemorrhage within the thermal ablation zone may be the most likely explanation for this discrepancy. Reasons for this hemorrhage are probably twofold: First, the risk of bleeding during renal biopsy is higher than that during hepatic biopsy owing to the purely arterial blood supply of the kidneys compared with the mainly portal venous blood supply of the liver. Second, RCC is generally a more hypervascular tumor than hypovascular colorectal metastases to the liver. Blood itself exhibits an abrupt decrease in T1 and T2 relaxation times at temperatures higher than 60°C, which results in a hyperintense appearance on T1-weighted MR images (24). Diffuse hemorrhage may also explain why the hyperintense appearance of renal RF thermal ablation zones is more often appreciated on high-field-strength GRE MR images than on low-field-strength SE MR images.
At contrast-enhanced T1-weighted MR imaging, no substantial enhancement was observed within the RF thermal ablation zone. However, rim enhancement that gradually resolved over time and was barely detectable after the 3-month examination was noted on all contrast-enhanced postablation images.
Residual or Recurrent Tumor
The major reason for performing surveillance imaging after renal RF thermal ablation is the early detection of residual or recurrent tumor. Although contrast-enhanced MR imaging findings are quite similar to the findings seen at CT, the RF thermal ablation zone also is very well depicted on unenhanced T2-weighted MR images. This additional information is very helpful, as seen in the two cases of residual tumor following RF thermal ablation in the current series. In these cases, residual RCC was best seen on the unenhanced T2-weighted and contrast-enhanced T1-weighted MR images.
Study Limitations
The major limitations of our study were the relatively small number of patients examined and the lack of a true reference standard, such as results of gross pathologic and/or microscopic analysis of the RF ablation zone, for comparison with the MR imaging findings. The minor limitations of our study were the two contrast agents and two magnetic field strengths used. However, the statistical analyses were performed by using data acquired at the same follow-up imaging session only and not by using data from different follow-up imaging sessions. Thus, these two minor limitations probably did not substantially affect our quantitative data analyses.
RF thermal ablation zones in the kidneys have the same pattern as RF thermal ablation zones in the liver in terms of the temporal evolution of the ablation zone size. After an initial increase in size within the first 2 weeks, involution occurs during the remainder of the MR imaging follow-up period. Although the signal intensity characteristics of the kidneys on T2-weighted MR images obtained after RF thermal treatment are the same as those of the liverboth organs appear hypointensethe appearance of the renal RF thermal ablation zone on T1-weighted MR images is brighter than that of the hepatic RF thermal ablation zone. This appearance is best appreciated on GRE MR images and most likely reflects diffuse hemorrhage within the thermal ablation zone. The high vascularity of RCCs and the purely arterial blood supply of the kidneys compared with the mainly portal venous blood supply of the liver may explain this finding.
| FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, E.M.M., J.S.L.; study concepts and design, E.M.M., S.G.N., J.S.L.; literature research, E.M.M.; clinical studies, E.M.M., S.G.N., J.S.L.; data acquisition and analysis/interpretation, E.M.M., S.G.N., J.S.L.; statistical analysis, E.M.M.; manuscript preparation, definition of intellectual content, revision/review, and final version approval, E.M.M., S.G.N., J.S.L.; manuscript editing, E.M.M., S.G.N.
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