AJR 2005; 185:661-667
© American Roentgen Ray Society
Radiofrequency Thermal Ablation in Canine Femur: Evaluation of Coagulation Necrosis Reproducibility and MRI-Histopathologic Correlation
Jeong Min Lee,
Seong Hong Choi,
Hee Seon Park,
Min Woo Lee,
Chang Jin Han,
Joon-il Choi,
Ja-Young Choi,
Sung Hwan Hong,
Joon Koo Han and
Byung Ihn Choi
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
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
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].
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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.
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The purposes of this investigation were to evaluate the dimension of
coagulation necrosis induced by a single application of radiofrequency energy
to normal bone and to assess the accuracy of MRI at revealing the extent of
tissue necrosis.
Materials and Methods
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.
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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).
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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).
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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).
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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).
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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)
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MRI
MRI was performed with a 3-T scanner (Signa Excite, GE Healthcare) using a
knee coil on day 4 or 7 after the procedure. Sagittal conventional spin-echo
T1-weighted and fast spin-echo T2-weighted images were obtained using a 2-mm
section thickness, 1-mm intersection spacing, and an 18 x 18 cm field of
view. Two signals were acquired. For T1-weighted spin-echo images, a TR/TE of
467/9 and a matrix of 256 x 256 were used. For T2-weighted fast
spin-echo images, a TR/TE of 4000/122, an echo-train length of 16, and a
matrix of 384 x 256 were used. Dynamic contrast-enhanced T1-weighted
spin-echo images (467/9) with fat suppression were obtained after the bolus IV
administration of 0.1 mmol/kg gadopentetate dimeglumine (Magnevist, Schering).
Except for the addition of a fat-saturation pulse, other parameters of the
contrast-enhanced T1-weighted spin-echo sequence were the same as those used
for the unenhanced T1-weighted images. These sequences were chosen on the
basis of the findings of prior studies that showed the usefulness of
T1-weighted and T2-weighted MR images for visualizing thermally induced
lesions [28,
29].
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.
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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.
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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).
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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)
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Long-axis and short-axis diameters were measured for each sequence of the
MR images using an electronic caliper on a PACS monitor. When the
radiofrequency-induced ablated area included a soft-tissue component, we
restricted MR image measurement to the intrafemoral portion. On
contrast-enhanced T1-weighed images, enhancement of the ablated zone was
evaluated versus adjacent normal bone marrow. On MR images, we measured from
inside the enhancing rim on contrast-enhanced T1-weighted images, from inside
the hyperintense rims on T2-weighted images, and from inside the hypointense
rim on T1-weighted images.
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
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).
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TABLE 2 : Correlation Coefficients and Mean Diameter of Radiofrequency Thermal
Lesions as Observed at MRI and Compared with Gross Pathology
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Discussion
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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Abstract
Introduction
