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Radiofrequency Thermal Ablation in Canine Femur: Evaluation of Coagulation Necrosis Reproducibility and MRI-Histopathologic Correlation

Department of Radiology and Institute of Radiation Medicine, Seoul National University College of Medicine, 28 Yongon-dong, Chono-gu, Seoul 110-744, South Korea.

Received July 26, 2004; accepted after revision November 3, 2004.

 
Address correspondence to J. K. Han.

Abstract

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OBJECTIVE. Our purposes were to determine whether a single application of radiofrequency energy to normal bone can create coagulation necrosis reproducibly and to assess the accuracy of MRI at revealing the extent of radiofrequency-induced thermal bone injury.

MATERIALS AND METHODS. Using a 200-W generator and a 17-gauge cooled-tip electrode, a total of 11 radiofrequency ablations were performed under fluoroscopic guidance in the distal femurs of seven dogs. Radiofrequency was applied in standard monopolar mode at 100 W for 10 min. During radiofrequency ablation, the changes in impedance and currents were recorded. MRI, including unenhanced T1- and T2-weighted images and contrast-enhanced fat-suppressed T1-weighted images, was performed to evaluate ablation regions. Six dogs were killed on day 4 after MRI and one dog on day 7.

RESULTS. In all animals, radiofrequency ablation created a well-defined coagulation necrosis and no significant complications were noted. The mean long-axis diameter and the mean short-axis diameter of the coagulation zones produced were 45.9 ± 5.5 mm and 17.7 ± 2.7 mm, respectively. At gross examination, thermal ablation regions appeared as a central, light-brown area with a dark-brown peripheral hemorrhagic zone, which was surrounded by a pale-yellow rim. On MRI, the ablated areas showed multilayered zones with signal intensities that differed from normal marrow on unenhanced images and a perfusion defect on contrast-enhanced T1-weighted images. The maximum difference between lesion sizes on MR images, established by measuring macroscopic coagulation necrosis, was 3 mm. The correlation between the diameter of coagulation necrosis and lesion size at MRI was strong, with correlation coefficients ranging from 0.89 for unenhanced T1-weighted images and 0.97 for unenhanced T2-weighted images to 0.98 for contrast-enhanced T1-weighted images (p < 0.05).

CONCLUSION. Radiofrequency ablation created well-defined coagulation necrosis in a reproducible manner, and MRI accurately determined the extent of the radiofrequency-induced thermal bone injury.

Introduction

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Radiofrequency ablation has been shown to be a reliable method for creating thermally induced coagulation necrosis, and several studies have shown the effectiveness of radiofrequency ablation as a promising image-guided, minimally invasive therapy for primary and secondary liver tumors [1-4]. Along with its reported success for liver tumors, radiofrequency ablation has been used for the treatment of neoplasms in other organs including the kidney, lung, bone, and breast [5-8]. Since the first report of the technical and clinical success of radiofrequency ablation for the treatment of osteoid osteoma by Rosenthal et al. [9], radiofrequency ablation has been increasingly used for the treatment of bone tumors including osteoid osteoma because it can be used on an outpatient basis and has a high success rate, a low complication rate, and a short recovery time [8-15].

Bone metastases are a common problem in cancer patients and frequently give rise to complications that can affect the quality of life. These complications include fractures and decreased mobility that ultimately reduce performance status [16, 17]. External beam radiation therapy is the care standard for patients with localized bone pain. Radiation therapy results in palliation in the majority of these patients, but 20-30% of patients treated with radiation therapy do not effectively respond to therapy and do not experience pain relief [18-20]. In previous studies [13-15], radiofrequency ablation of metastases involving bone provided pain relief in a relatively high percentage of treated patients.

Radiofrequency delivery has been optimized in the hepatic tumor setting. Therefore, its technical parameters may not be optimal for tumors located in bone because bone has a different electrical conductivity than liver tissue [21-23]. Thus, an improved understanding of the differences between liver and bone in this context is required. Furthermore, although required dimensions of coagulation necrosis in the liver were achieved by a single radiofrequency application in vivo and ex vivo, this was not fully elucidated in bone [24-26]. In addition, although MRI is a useful imaging technique for the guidance and evaluation of the therapeutic response of tumors to radiofrequency therapy, only a few reports have been issued regarding MRI findings of radiofrequency-induced ablation areas in bone [27, 28].

View larger version (66K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1 —Graphic depiction of changes in tissue impedance (bottom), radiofrequency current (center), and power (top) during radiofrequency ablation in bone. Note that tissue impedance increased markedly and current decreased during radiofrequency energy application.

Materials and Methods

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Animals, Anesthetics, and Preparation
The protocol of this study was approved by our institutional animal care and use committee. Eleven femurs of seven female dogs (weight range, 20-25 kg) were treated under general anesthesia. All seven dogs were anesthetized using an intramuscular injection of 50 mg/kg ketamine hydrochloride and 5 mg/kg of xylazine (Rompun, Bayer Korea). Booster injections of up to one half the initial dose were administered as needed. Endotracheal intubation was performed and anesthesia was maintained with inhaled enflurane (Gerolan, Choongwae Pharma) 1.5% until effective. Mechanical ventilation was used throughout the procedure.

One femur was treated in each of the first set of three dogs and both femurs in the second set of four after confirming that the first set had not experienced substantial dysfunction and discomfort after the procedure. The hindquarters and hip regions of each animal were shaved bilaterally. Two 15 x 20 cm wire mesh grounding pads that were coated with conductive gel were placed on the hip regions. Each dog was placed in the supine position on the fluoroscopic table (TRF 500, Shimadzu) to allow access to both femurs. After shaving and scrubbing the skin entry site, a small incision (1-2 cm) was made in the distal portion of the thigh, and the distal part of the femur was exposed. Under fluoroscopic guidance, a 2-mm diameter hole was made in the bone cortex of the distal femur using a biopsy needle system drill (Bonopty Extended Drill-REF 10-1074; Radi Medical Systems). The drill was removed and exchanged for a 17-gauge cooled-tip electrode (Cool-tip, Valleylab) with an unprotected tip length of 10 mm. The electrode was inserted into the distal portion of the femur to a depth of 2 cm perpendicular to the axis of the femur, and the tip of the electrode was centered in bone. The location of the electrode in the bone marrow was assessed by fluoroscopy in each case.

Radiofrequency Ablation
Thermal ablated regions were created using a 500-kHz 200-W radiofrequency generator (Series CC-3, Valleylab) with a 17-gauge cooled-tip electrode. Radiofrequency power was then manually increased to 100 W and held for a total of 10 min; if the impedance increased by more than 10% of initial tissue impedance, the current output was automatically reduced to a level determined by the previously designed pulsing algorithm [27]. During the procedure, a thermocouple embedded within the electrode tip continuously measured local tissue temperature. Tissue impedance was monitored using circuitry incorporated into the generator. A peristaltic pump was used to infuse normal saline solution at 0°C into the lumen of the electrodes at a rate sufficient to maintain a tip temperature of 20-25°C. The incision was closed using nonabsorbable sutures after electrode withdrawal.

View larger version (101K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone day 4 after radiofrequency ablation in distal femur of dog. Sagittal spin-echo T1-weighted image shows multilayered lesion composed of central hyperintense area (arrowheads) surrounded by dark hypointense band (small arrow), slightly hyperintense zone, and subtle hypointense rim (large arrow).

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone day 4 after radiofrequency ablation in distal femur of dog. Sagittal T2-weighted image shows four zones: slightly hyperintense thermally ablated lesion (arrowheads) followed by hypointense band (small arrow), poorly demarcated slightly hypointense peripheral zone, and peripheral hyperintense rim (large arrow).

View larger version (92K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone day 4 after radiofrequency ablation in distal femur of dog. Sagittal contrast-enhanced T1-weighed image with fat suppression shows a well-demarcated hypointense lesion surrounded by a thin enhancing rim (arrow).

View larger version (91K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone day 4 after radiofrequency ablation in distal femur of dog. Cut gross specimen shows corresponding ablation area consisting of central brown area (arrowheads), surrounding dark-red area (small arrow), and peripheral red rim (large arrow).

View larger version (142K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2E —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone day 4 after radiofrequency ablation in distal femur of dog. Photomicrograph of border zone of middle dark-red area and peripheral red rim shows severe congestion and hemorrhage of bone marrow in middle dark-red area (H) and edematous change in peripheral red rim (E). Normal bone marrow (N) surrounds the lesion periphery. (H and E; original magnification, x 20)

Measurements of Coagulation Necrosis
After MRI, six dogs were killed by barbiturate overdose on day 4 after radiofrequency ablation and one dog on day 7, and femurs were harvested. For gross pathologic examination, a central cross-sectional incision along the long axis of the femur was made through the affected area using a wet high-speed band saw. In gross specimens, we considered all marrow changes inside the thin, pale-yellow outer margin of the ablation zone to be part of the thermal lesion. For macroscopic pathologic analysis, discolored marrow regions were measured with a caliper in each case. Measurements of the maximum long-axis and short-axis diameters of coagulation perpendicular to the electrode axis were made by consensus between two observers.

Representative sections were then photographed and fixed in 10% phosphate-buffered formalin. Subsequently, they were decalcified (Decalcifier II, Surgipath Medical) and stained with H and E for histologic examination. Specimens from all treatment areas were analyzed for histologic appearance and differentiation from surrounding viable tissue.

Analysis of MRI-Histopathologic Correlation
Each MR image was displayed on a PACS (Maroview, Marotech). The signal intensities of bone on T1-weighted and T2-weighted images were classified as hypointense, isointense, or hyperintense relative to the signal intensity of normal bone marrow. According to previous studies in which the radiofrequency-ablated region in the liver showed multizonal altered signal intensities [28, 29], the radiofrequency-induced ablation regions were divided into zones based on their altered signal intensities moving from center to periphery.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone 7 days after radiofrequency ablation in the distal femur of dog. Sagittal contrast-enhanced T1-weighted image with fat suppression shows well-demarcated hypointense lesion surrounded by thin enhancing rim (arrows). Nonenhancing ablated area involves well beyond cortex, extending into soft tissue both anteriorly and posteriorly.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone 7 days after radiofrequency ablation in the distal femur of dog. Cut gross specimen shows the corresponding ablation area (arrows).

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C —MR images, gross specimen, and photomicrograph of radiofrequency-induced ablation zone 7 days after radiofrequency ablation in the distal femur of dog. Photomicrograph shows clear evidence of coagulation necrosis, hemorrhagic congestion (H), and granulation tissue (G) with immature bone formation in periphery. (H and E; original magnification, x 40)

The diameters of areas showing signal changes on T1-weighted and T2-weighted images and of the nonenhancing lesion on contrast-enhanced T1-weighted images were correlated with lesion size determined by pathologic examination and then analyzed using Pearson's correlation coefficient. The mean absolute differences between the diameters of coagulation necrosis as measured in gross pathologic specimens and in follow-up images were calculated. Statistical significance was evaluated by using the paired Student's t-test.

Results

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Technical Parameters
Tissue impedance frequently increased to more than 200 after the start of the radiofrequency application, which resulted in the automatic activation of pulsed radiofrequency application (Fig. 1). The mean radiofrequency current applied to the femur during the 10-min ablation procedure was 561 ± 577 mA, and the mean tissue impedance was 168 ± 106 .

Gross Findings
Radiofrequency ablation regions created in all treated femurs exhibited three characteristic zones: a central light-brown zone, a surrounding dark-red hemorrhagic zone, and a pale-yellow peripheral rim (Figs. 2A, 2B, 2C, 2D, and 2E). Ablated regions were cylindrically shaped with the largest diameter along the long axis of the femur. The mean long-axis diameter and the mean short-axis diameter (perpendicular to the electrode) were 45.9 ± 5.5 mm and 17.6 ± 2.7 mm, respectively.

Microscopic Findings
At histologic examination of the specimens obtained on day 4 after radiofrequency ablation, the central light-brown zone showed subtle early changes of coagulation necrosis, involving the elongation of nuclei, with small scattered hemorrhagic foci. The surrounding hemorrhagic zone showed foci of coagulation necrosis with severe hemorrhagic congestion (Figs. 2A, 2B, 2C, 2D, and 2E). At the border between the ablation region and normal marrow, granulation tissue was evident with an accumulation of edematous collagen and proliferating and dilated blood vessels. Histologic examination of the specimens obtained on day 7 after radiofrequency ablation showed more conspicuous coagulation necrosis in the ablation region than at day 4, and hematopoietic progenitors had been replaced by myxoid edematous stroma (Figs. 3A, 3B, and 3C). In addition, numerous broadened spicules with new bone formation and many empty lacunae were evident within trabecular bone in the central area. Although the cortical bone of the specimens obtained on day 4 after radiofrequency ablation did not show definite changes compared with bone marrow, the cortex of the lesions obtained on day 7 showed necrosis even though the outer cortical layers were occasionally viable.

MRI Findings
Radiofrequency-induced ablation results were analyzed in four zones (Figs. 2A, 2B, 2C, 2D, and 2E): zone 1, a broad central zone showing slight hyperintensity with some hypointense spots on T2-weighted images and hyperintense spots in T1-weighted images; zone 2, a hypointense band on both T2-weighted images and T1-weighted images; zone 3, isointense on T2-weighted images and hyperintense on T1-weighted images; and zone 4, hyperintense on T2-weighted images and hypointense on T1-weighted images and peripheral to zone 3. These four zones were numbered 1-4 based on moving from center to periphery (Table 1). On contrast-enhanced T1-weighted images, the inner three zones showed no enhancement, and zone 4 showed a peripheral rim-like enhancement.

On contrast-enhanced T1-weighted images, radiofrequency-ablated regions showed nonenhancing areas that extended beyond the cortex of bone and involved the adjacent soft tissue. These areas formed round- or oval-shaped perfusion defects surrounded by an enhancing rim (Figs. 2A, 2B, 2C, 2D, 2E, 3A, 3B, and 3C).

MRI-Histopathologic Correlation
An MRI-histopathologic correlation showed that the central zone corresponded to zone 1 on MRI and that the surrounding zone corresponded to zones 2 and 3. The peripheral zone corresponded to zone 4 on MRI. Gross examination showed that the long- and short-axis diameters of the radiofrequency-induced discolored region within the peripheral pale-yellow rim were 45.9 ± 5.5 mm and 17.6 ± 2.7 mm, respectively. In T2-weighted images, the long- and short-axis diameters of the thermal lesions were 45.7 ± 4.9 mm and 17.2 ± 3.0 mm, respectively. And in T1-weighted images, these values were 45.3 ± 4.7 mm and 17.1 ± 3.1 mm, respectively, while in contrast-enhanced T1-weighted images, they were 46.6 ± 5.6 mm and 18.8 ± 3.4 mm, respectively. The maximum difference between the dimensions of radiofrequency-induced ablation areas measured on MR images and macroscopically was 3 mm. The correlation between the long-axis diameter of coagulation necrosis and the diameter measured by MRI was strong, with correlation coefficients ranging from 0.89 for T1-weighted images and 0.97 for T2-weighted images to 0.98 for contrast-enhanced T1-weighted images (p < 0.05) (Table 2).

Discussion

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Radiofrequency ablation has been accepted as a minimally invasive treatment for primary and secondary liver tumors [1-4]. An increasing number of investigators have reported preliminary success for radiofrequency ablation in the treatment of malignancies of the kidney [5], lung [6], and bone [11-15]. Concerning its extrahepatic applications, bone radiofrequency ablation is probably offered more widely because it is relatively successful at relieving pain in patients with painful bone metastases and osteoid osteomas and because of the noninvasive character of the procedure [9-15]. Furthermore, with some bone biopsy or interventional radiology experience, radiologists can easily adapt to the bone radiofrequency ablation procedure [30, 31]. The clinical results of radiofrequency ablation for the management of bone pain due to metastases are valuable because satisfactory outcomes are achieved in a cohort of patients traditionally refractory to conventional treatments [13, 32]. Indeed, in many large centers, radiofrequency ablation has replaced surgery for the treatment of osteoid osteoma, and it is expected to have an increasing role in the treatment of bone metastases [7, 10-14, 16, 30]. However, before adopting radiofrequency ablation for pain amelioration in bone metastases or osteoid osteomas, we believe that the reproducibility of radiofrequency ablation for creating coagulation necrosis and the dimensions of coagulation necrosis achieved by a single application of radiofrequency energy using a clinically available radiofrequency generator and electrode should be evaluated.

In this study, standard monopolar radiofrequency ablation was performed for 10 min using a 200-W generator and a 17-gauge cooled-tip electrode and created a well-defined region of coagulation necrosis of long-axis diameter 45.9 ± 5.5 mm and short-axis diameter 17.7 ± 2.7 mm. The shape of the coagulation necrosis in femurs was cylindrical, which well matched the findings of previous studies that found cylindrically shaped heat distribution in bone [33, 34].

In our study, patterns of changes in current, impedance, and initial tissue impedance differed from the usual pattern observed in hepatic radiofrequency ablation. Several studies have shown a strong correlation between increased coagulation diameter and increased global system impedance [21, 26, 27]. During radiofrequency ablation, tissue impedance frequently increased to more than 200 after the start of the radiofrequency application (mean impedance 168 ± 106 ), which resulted in a decrease in current (561 ± 577 mA). Given that usual impedances and currents induced by a single application of radiofrequency energy at 100 W in the liver are in the range of 50-100 and 1000-1500 mA, impedance changes during radiofrequency ablation were larger in bone than in liver. This result is related to the poor electrical conductivity of bone marrow fat compared with liver tissue. However, the dimensions of coagulation necrosis were similar in bone and liver, though current accumulation in bone was smaller. The reason could be that the insulating properties of cortical bone retard radiofrequency energy flow, resulting in increased local heat generation, which tends to heat the marrow [35]. This process is similar to the "oven effect," in which the fibrotic cirrhotic liver functions as a thermal insulator, which concentrates heating in the tumor tissue. Therefore, radiofrequency-induced necrosis tends to conform to the size and shape of a tumor [36].

In the present study, MRI clearly showed radiofrequency-induced coagulation zones in canine bone, and the dimensions of these images closely matched gross pathologically determined sizes. The ablated lesions showed significantly increased signal intensity on T1-weighted images. The hyperintensity observed after radiofrequency ablation may be attributed to a number of factors including mild desiccation, the effect of protein denaturation, or cellular lysis [28, 29]. In specimens obtained at day 4, histopathologic examination showed subtle changes in coagulation necrosis throughout a majority of the treated zone, but in specimens obtained at day 7, coagulation necrosis was more conspicuous. In a clinical setting, MRI may be helpful for making therapeutic decisions as to whether additional radiofrequency ablation is necessary or for determining how much tumor volume remains. Signal intensity changes in ablated tissue differ from that usually found in metastatic bone tumors.

In a previous study, Dupuy et al. [35] observed decreased heat transmission in cancellous bone and an insulative effect of cortical bone in their ex vivo studies. In addition, temperature recordings within the epidural space led them to conclude that a margin of safety is provided when preserved cortical bone is present. However, on the basis of our observation from the contrast-enhanced MRI, we tend to be more conservative regarding the insulating effect of cortical bone and its protective effect from heat injury to adjacent tissue. In our studies, radiofrequency-induced thermal lesions in femurs consistently evolved into their full oval or round configurations including bone cortex. Although the cortex of the ablated region showed minimal changes compared with bone marrow at day 4 after radiofrequency ablation, the bone cortex of specimens showed necrosis with some viable outer cortical layer at day 7 after radiofrequency ablation. The reason cortical bone showed milder histopathologic changes compared with bone marrow is related to its higher tissue resistivity relative to bone marrow [34]. As a result of our experience, we believe that radiofrequency ablation in bone tumor should be performed with great caution when the lesion is located beside vital structures.

Our study has certain limitations. First, the results obtained in healthy canine bone might not reflect the situation in cases of bone metastasis in humans. Second, potential differences between normal canine bone and human metastatic bone tumors might affect the MR appearances of the radiofrequency-ablated lesions. Finally, although every attempt was made to ensure the validity of the size correlations between MRI and pathologic findings, precision was limited because of difficulty obtaining pathologic sections corresponding to the MR scanning planes.

In conclusion, radiofrequency ablation using a cooled-tip electrode produced well-defined coagulation necrosis in bone in a reproducible manner, and MRI revealed the extent of radiofrequency-induced thermal bone injury.

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