DOI:10.2214/AJR.04.0968
AJR 2005; 185:1299-1306
© American Roentgen Ray Society
Radiofrequency Ablation in a Porcine Lung Model: Correlation Between CT and Histopathologic Findings
Akira Yamamoto1,
Kenji Nakamura1,
Toshiyuki Matsuoka1,
Masami Toyoshima1,
Tomohisa Okuma1,
Yoshimasa Oyama1,
Yoshihiro Ikura2,
Makiko Ueda2 and
Yuichi Inoue1
1 Department of Radiology, Osaka City University Graduate School of Medicine,
1-4-3 Asahi-machi, Abeno-ku, Osaka 545-8585, Japan.
2 Department of Pathology, Osaka City University Graduate School of Medicine,
Abeno-ku, Osaka 545-8585, Japan.
Received June 18, 2004;
accepted after revision November 10, 2004.
Address correspondence to A. Yamamoto.
Abstract
OBJECTIVE. The objective of our study was to investigate the time
course changes of the ablated lesion after radiofrequency ablation in the
porcine lung and the correlation between CT and histopathologic findings.
CONCLUSION. Ground-glass attenuation on CT led to overestimation of
the size of necrotic lesions. The layered structural findings on CT were
consistent with the histopathologic findings. Although CT findings reflect the
histopathologic findings, attention should be paid to the dissociation of
ablated lesions and high-density areas in clinical interpretation of CT
images.
Introduction
Radiofrequency ablation is a therapeutic method that uses thermal energy
generated by radiofrequency waves for thermal coagulation of the affected
tissues. Percutaneous radiofrequency ablation is widely accepted as a safe and
effective technique for treatment of primary and metastatic hepatic tumors
[1-5].
In recent years, radiofrequency ablation has also been applied to lung,
kidney, and bone tumors as a minimally invasive technique
[6-9].
Its remarkable progress has been observed, especially for treatment of
unresectable lung tumors
[10-18].
We have performed CT-guided radiofrequency ablation by applying the lung
nodule biopsy technique in many cases
[19-21].
However, to our knowledge, there are few reports
[22-24]
describing the time course changes and morphologic findings of the tissues on
diagnostic images. No previous reports have directly correlated the CT
appearance of ablated lesions with histopathologic findings during the time
period after radiofrequency ablation. Therefore, we anticipated that by
comparing the macroscopic and histopathologic findings with CT images of
normal pig lung after ablation, we could gain the basic knowledge necessary to
judge the effects of radiofrequency ablation and to follow up patients. More
specifically, the following knowledge could be obtained: the method of
confirming the necrotic lesion in normal lung at the time of radiofrequency
ablation and radiologic-pathologic correlation might help guide management and
interpretation during the period after radiofrequency ablation.
Materials and Methods
Fourteen swine (body weight: range, 17-27 kg; mean, 23 kg) were used and
divided into the following five groups: Group A consisted of four pigs that
were sacrificed within 2 hr after radiofrequency ablation; group B of two pigs
sacrificed 3 days after radiofrequency ablation; group C of four pigs
sacrificed 10 days after radiofrequency ablation; group D of two pigs
sacrificed 4 weeks after radiofrequency ablation; and group E of two pigs
sacrificed 8 weeks after radiofrequency ablation. The protocol for this study
was prepared in compliance with the guidelines for animal experiments by Osaka
City University and was approved by the Animal Experimentation Committee,
Osaka City University.
For all procedures, anesthesia was induced with midazolam (40 mg/kg),
medetomidine hydrochloride (0.2 mg/kg), ketamine hydrochloride (10-20 mg/kg),
and atropine sulfate (0.5 mg/kg). Pentobarbital sodium (50-150 mg) was used to
maintain anesthesia. We used 15-gauge needles that have four retractable hooks
with a maximum diameter of 3.0 cm (Model 30, RITA Medical Systems). After a
swine was prepared without tracheal intubation and was placed in the left or
right lateral position on a CT table, grounding pads were placed on the
thighs. Percutaneous radiofrequency ablation was performed under CT guidance
(ProSpeed, GE Healthcare) at four to eight random points per animal so that
they did not overlap with each other. A 50-W radiofrequency ablation generator
was used in the Power Control mode. The emission power was initially set at 10
W and was increased by 5 W every 2 min. Radiofrequency energy was applied
until the generator automatically stopped due to the increased resistance
caused by tissue dehydration. After a cooling period of 30 sec, the second
session was performed in a similar manner to the first. However, the second
session was started with 75% of the maximum power of the first session and was
allowed to be terminated by automatic power adjustment.
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Fig. 1A —Group A: swine sacrificed immediately after radiofrequency
ablation. CT image shows ablated lesion immediately after radiofrequency
ablation. Area with ground-glass attenuation is observed.
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Fig. 1B —Group A: swine sacrificed immediately after radiofrequency
ablation. Photograph shows ablated lesion after fixation. Ablated lesion has
two-layered structure presenting as ring shape and is surrounded by brown
strips (arrows) situated at outer layer. Boundary between ablated and
nonablated areas is not clear.
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Fig. 1C —Group A: swine sacrificed immediately after radiofrequency
ablation. Low-power photomicrograph of H and E-stained section, fixed by
Heitzman's method, of tissue presented in B shows outermost layer
(arrows).
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Fig. 1D —Group A: swine sacrificed immediately after radiofrequency
ablation. Photomicrograph shows H and E section of tissue presented in
B. Histopathologically, normal lung (N), congestion in outermost layer
(C), and effusion in pulmonary alveoli lumens in intermediate layer (E) are
observed. (H and E, x40)
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The follow-up axial CT images were obtained using a helical CT scanner
(ProSpeed, GE Healthcare). The following CT parameters were used: 100-150 mA,
120 kV, 5-mm collimation, and pitch of 1. Group A was imaged within 2 hr after
therapy; group B, immediately and 3 days after therapy; group C, immediately,
3 days, and 10 days after therapy; group D, immediately, 10 days, and 4 weeks
after therapy; and group E, immediately, 10 days, 4 weeks, and 8 weeks after
therapy. The CT images were analyzed, the reformatted CT images were viewed on
workstations, and measurements of the maximum diameter of the ablated lesions
were electronically performed. The measurements of the diameter of the ablated
lesions were based on the consensus of two observers.
The swine in each group were sacrificed immediately after the final CT
examination. After heparinization, the animals were sacrificed with an
overdose of IV-injected pentobarbital sodium (60-120 mg). The lung specimens
were fixed and inflated by Heitzman's method
[25,
26] using a fixative composed
of polyethylene glycol 400, 95% ethanol, 40% formaldehyde, and distilled water
in proportions of 10:5:2:3. As a preliminary step, we distended and fixed the
specimen with 10% formalin before proceeding to Heitzman's method. The
duration of preliminary formalin distention was 3 hr. After fixation, as much
formalin as possible was removed by manual compression. Afterward, the
fixative was injected through the trachea at 30 cm of H2O pressure
for 4 days and air was inflated for 2 or 3 days. Subsequently, each
radiofrequency lesion was axially sliced at 5-mm intervals for comparison
between CT and histopathologic findings.
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Fig. 1E —Group A: swine sacrificed immediately after radiofrequency
ablation. Photograph of H and E-stained frozen section of ablated lesion shows
outermost layer (C, arrows), intermediate layer (E),
and normal lung parenchyma (NL). (H and E, x20)
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Fig. 1F —Group A: swine sacrificed immediately after radiofrequency
ablation. Photograph of nicotinamide adenine dinucleotide (NADH)
diaphorase-stained section of tissue presented in E shows outermost
layer observed on H and E-stained frozen section is found on border of NADH
diaphorase-stained lesions. In its internal regions (E),
not-NADH-stained lesion conforms to ablated lesion, which is same as
coagulation necrosis. However, outermost layer contains admixture of stained
and not-stained cells (arrows). (NADH diaphorase, x20)
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The visible ablated lesions were photographed and measured with calipers in
each pathologic specimen. The border of the ablated lesions was determined by
macroscopic change. This border corresponded to the margin of cell change in
the histopathologic analysis. Measurements of the maximum diameter of the
ablated lesion were based on the consensus of two observers. In addition,
these slices were embedded in paraffin, cut 4 µm in thickness, and stained
with H and E. Frozen sections were obtained from two swine of group A and used
for enzyme histochemical staining for nicotinamide adenine dinucleotide
diaphorase (NADH diaphorase). Because frozen sections could not be inflated,
the maximum diameter was not measured.
The CT findings of all radiofrequency lesions were correlated with the
histopathologic results. The maximum lesion size as measured on CT was then
correlated with the histopathologically determined lesion size. The
correlation between the ablated lesion on CT and that on macroscopic
observation was investigated using Poisson's correlation coefficient, which
was used to describe the degrees of correlation between all possible
two-variable combinations. Statistical significance was established by the
Student's two-tailed t test. A p value of 0.05 was
considered to be statistically significant.
Results
Seventy-three radiofrequency lesions were created. The time course changes
of histopathologic findings were compared with those of CT images (group A, 21
lesions; group B, 10; group C, 22; group D, 11; group E, nine). Ablation was
technically successful in all pigs. In four pigs, minor asymptomatic
pneumothorax occurred. The average time for ablation ± SD was 12.75
± 6.75 min (range, 4-28.5 min), and the average maximum output ±
SD was 28 ± 11.0 W (range, 13-50 W). The average impedance (initial
value) that indicated the resistance value of tissues ± SD was 104
± 12.4 
(range, 65-120 ).
Group A: Sacrificed Within 2 Hr After Radiofrequency Ablation
In group A, the ablated lesions were typically shown as areas with a
ground-glass attenuation on CT images (Fig.
1A). Macroscopically, the ablated lesions had a two-layered
structure presenting as a ring shape (Fig.
1B). The boundaries of the two layers were not clear.
Histopathologically, the ablated lesions presented as a three-layered
structure. In the outermost layer, strong congestion was seen and was
accompanied by hemorrhage, neutrophil infiltration, and fibrin deposition
(hemorrhagic rim) (Fig. 1C). The average width of the outermost layer ± SD was 2.6 ± 0.66 mm
(range, 2.0-4.1 mm). In its intermediate layer, alveolar spaces were filled
with effusion, and hyaline membrane formation was observed in the inner
surfaces of the alveolar walls. Congestion was also observed in the
intermediate layer but was milder than that seen in the outermost layer. In
the innermost portion, the alveolar structure and cell nuclei were seemingly
retained. However, the cytoplasm showed acidophilic changes and the nuclei had
condensed chromatin. Around the needled areas, the tissue structure
disappeared and only an amorphous eosinophilic matrix remained. These changes
collectively indicated that the innermost portion was necrotic lesion. Enzyme
histochemical staining for NADH (n = 12) confirmed that nonstained
cells in the innermost portion and intermediate layer completely lost cellular
integrity (ongoing necrosis) and the outermost layer contained an admixture of
stained and nonstained cells (Figs.
1D and
1E).
Group B: Sacrificed 3 Days After Radiofrequency Ablation
The ablated lesions from group B were typically observed as a two-layered
ring-shaped structure on CT images. Macroscopically, the lesions in group B
showed a three-layered structure similar to that in group A. The boundaries
between the outermost layer and nonablated portion were clearer than those in
group A. Histopathologically, the ablated lesions presented as a three-layered
structure as with group A, and almost no difference in the structure was
observed between group A and B lesions. On the other hand, the ring-shaped
lesion in the outermost layer was clear and inflammatory cell infiltration was
enhanced in group B lesions.
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Fig. 2C —Group C: swine sacrificed 10 days after radiofrequency
ablation. Photomicrograph of H and E-stained section of tissue shows two
layers. Normal lung (L), strong infiltration of inflammatory cells, and
increased granulation tissues rich in collagen fibers (F) are recognized. In
layer (N), lesion contains completely coagulated tissue with no viable cells.
(H and E, x40)
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Group C: Sacrificed 10 Days After Radiofrequency Ablation
In group C, the ablated lesions were observed as ring-shaped structures on
CT (Fig. 2A). The ring was
clearer than those in group B lesions. Histopathologically, two layers were
observed (Fig. 2B). In the
outer layer, strong infiltration by inflammatory cells and increased
granulation tissues rich in collagen fibers were observed. The lesion was
sharply demarcated from the adjacent lung. The congestion had disappeared
(Fig. 2C). In the inner layer,
cell structure remained, whereas there were lesions in which the nuclei and
the tissue structure had disappeared. These lesions contained completely
coagulated tissue with no viable cells.
Group D: Sacrificed 4 Weeks After Radiofrequency Ablation
On CT images, the overall size of group D lesions had decreased compared
with the overall size of group C lesions and the lesions were typically
recognized as high-density masslike lesions. Histopathologically, a two-layer
structure was seen. Hyperplasia of granulation tissues in the outer layer and
necrotic tissues in the inner layer were observed. The decreased area of the
inner layer resulted in a decrease in the overall size (Figs.
3A,
3B, and
3C).
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Fig. 3A —Group D: swine sacrificed 4 weeks after radiofrequency
ablation. Photograph shows slice of tissue after fixation. Pale lesion is
considered to be obstructive pneumonitis only in periphery of ablated areas
(arrows). Decreased size of inner layer area results in decrease of
overall size as compared with group C.
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Fig. 3B —Group D: swine sacrificed 4 weeks after radiofrequency
ablation. CT image shows slice of ablated lesion tissue presented in A
with obstructive pneumonitis. Ablated lesion observed on CT is larger than
ablated lesion seen at macroscopic examination. Pale lesion only in periphery
of ablated areas plus ablated lesion on macroscopic examination is observed as
wedge-shaped high-density masslike lesion (arrows).
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Fig. 3C —Group D: swine sacrificed 4 weeks after radiofrequency
ablation. Photomicrograph of H and E-stained section of tissue presented in
A shows that polyplike formation of granulation tissues
(arrows), which originated from organization of necrotic layers, is
found in bronchus in ablated lesion. (H and E, x100)
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Group E: Sacrificed 8 Weeks After Radiofrequency Ablation
The group E lesions either were not visible on both CT and macroscopic
examinations or were observed to be small high-density mass-like lesions on CT
and small areas of granulation tissues on histopathology at macroscopic
examination.
For all the imaging techniques we used, the average maximum lesion sizes
are summarized in Figure 4.
The diameters of the high-density areas observed on CT and those of the
ablated lesions microscopically observed were significantly correlated in
groups A, B, and C. However, the correlation in group D was not
significant.
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Fig. 4 —Graph shows that diameters of high-density area observed on
CT and those of ablated lesion observed in macroscopic examination (Macro) are
correlated significantly (p < 0.05) in groups A, B, and C.
r = correlation coefficient.
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During the follow-up period, among the 52 lesions in all groups except
those in group A, 21 (40.4%) showed a wedge-shaped high-density area to the
periphery that was found in only the periphery of the ablated areas on CT
(Fig. 3B).
Histopathologically, in the ablated lesions of the bronchus, stenosis or
obstruction by granulation tissues or a polyplike formation of granulation
tissues, which originated from organization of the necrotic layers
(Fig. 3C), was found. This was
considered because of bronchial stenosis or obstruction, wedge-shaped
occlusive pneumonitis, and lowered pneumatization were observed in the
peripheral lung parenchyma (Fig.
3A).
For all the lesions excluding those in group A, a cavity that was similar
to pulmonary abscesses on CT was found
(Fig. 5A) (18 cases in 52
nodes [34.6%]). Histopathologically, the border of this cavity was covered
with granulation tissues in the outer layer, which was found in groups C and
D, and the inner layers were necrotic tissue or completely empty of tissue
(Fig. 5B). This was considered
to be due to draining of internal necrotic tissues into bronchus.
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Fig. 5B —Group C: swine sacrificed 10 days after radiofrequency
ablation. Low-power photomicrograph of H and E-stained section of tissue in
A shows border of this cavity is covered with granulation tissues in
outer layer, which are found in groups C and D
(Fig. 2B), and inner layer are
necrotic tissues or not found.
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Discussion
Radiofrequency ablation has been clinically applied against lung tumors as
a technique requiring minimal invasion
[10-21].
CT images are generally used to plan the procedure and to perform follow-up.
However, comprehensive knowledge regarding changes in the ablated lesions or
tissues as shown on CT images is not yet accessible. It is important in the
clinical sense to know which lesions are ablated, what time course the CT
images follow, and whether the findings on CT are the same as those seen on
histopathologic views after radiofrequency ablation. In light of this, we
primarily investigated the following issues: first, the method of confirming
the necrotic lesion in normal lung at the time of the therapy; and, second,
radiologic-pathologic correlation, which can guide management and
interpretation during the period after radiofrequency ablation. Using a swine
model, we described the characteristics of radiofrequency ablation lesions in
normal lungs.
The first characteristic is that unlike radiofrequency ablation used
against liver tumors in which the ablated lesions can be monitored by
sonography and the postoperative ablated areas can be determined by dual CT,
radiofrequency ablation of lung tumors has no appropriate technique for
follow-up. There is no uniform view about the image findings that indicate
effective ablation areas in cases receiving radiofrequency ablation for lung
tumors because the lung is not satisfactorily visible on sonograms or enhanced
CT. In this study, the ablated lesions showed as areas with a ground-glass
attenuation on CT immediately after ablation. The maximum diameters of the
ablated lesions were significantly correlated with the size of the areas
showing ground-glass attenuation on CT.
Histopathologically, the areas with a ground-glass attenuation consisted of
three-layered structure (innermost portion, intermediate layer, and outermost
layer). The ground-glass attenuation was observed mainly because the alveolar
spaces were filled with effusion in the intermediate layer. Effusion in the
intermediate layer was considered to reflect the increased permeability of
blood vessels due to a defect of functional endothelial cells. Are all
three-layered structures necrotic lesion? In H and E staining performed
immediately after radiofrequency ablation, nuclei are still present and
histopathologic changes are slight, so it is difficult to determine which
areas are necrotic. A method to make up the deficit of H and E staining is
NADH staining. This staining method permits evaluation of tissue ablation
based on cell viability rather than on histologic characteristics
[26-29].
The complete absence of NADH stain indicates a lack of cellular viability.
In our study, the innermost portion and intermediate layer showed a complete
absence of NADH stain, but the outermost layer contained an admixture of
viable lung parenchyma. The ground-glass attenuation on CT corresponded to the
inner necrotic lesion plus the hemorrhagic rim (Figs.
6A and
6B). The ground-glass
attenuation on CT led to overestimation of the size of the completely necrotic
lesion. The average width of the outermost layer was 2.6 mm, and the maximum
width was 4.1 mm. These results suggest that the edge of tumors should be
identified in the ablated lesion (i.e., areas surrounded by ground-glass
attenuation) and that an adequate safety margin (at least 4.1 mm from the edge
of the tumor to the edge of the ablated lesion) should be obtained on CT
immediately after radiofrequency ablation in the ablation for lung tumors.
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Fig. 6A —Schematic representations of ablated lesion immediately after
radiofrequency ablation. Ablated lesion is observed as area with ground-glass
attenuation. Maximum diameter on CT is measured.
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Fig. 6B —Schematic representations of ablated lesion immediately after
radiofrequency ablation. Histopathologically, ablated lesion presents
three-layered structure, outermost layer (hemorrhagic rim) mainly consists of
congestion (C); intermediate layer mainly consists of effusion in pulmonary
alveoli lumens (E); and innermost portion mainly consists of cytoplasm, which
shows acidophilic change and nuclei that have condensed chromatin (N). Maximum
diameter on macroscopic (macro) examination is measured. Completely necrotic
lesion is intermediate layer and innermost portion (E + N). Maximum diameter
on macroscopic examination is inner necrotic lesion plus outermost layer
(hemorrhagic rim). Maximum diameter on CT and on macroscopic examination is
significantly correlated. Therefore, area with ground-glass attenuation on CT
leads to overestimation of necrotic lesion.
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The second characteristic is that in the tissues after ablation the
inflammatory cells infiltrated from the border where congestion was observed
in the early stage (0-3 days after radiofrequency ablation). During that
period, CT showed mainly areas with a ground-glass attenuation. The layer of
granulation tissues that was gradually replaced by collagen fibers was
observed in the chronic stage (10-28 days after radiofrequency ablation). CT
reflected such histopathologic changes primarily on the outer layer as a
ring-shaped high-density area.
As the follow-up examinations progressed, the difference between the
maximum diameter measured on CT images and that measured macroscopically
became larger (group D). This was thought to be because the areas including
the obstructive pneumonitis region and the real lesion of ablation were
regarded as the ablated lesions on CT. Attention should be paid to the
dissociation of ablated lesions and high-density areas in clinical
interpretation of CT images. The high-density areas were revealed to differ
from the actual ablated areas as follow-up examinations progressed.
Clinically, tumors after ablation are often detected as larger on CT than
before ablation [13,
14,
18]. This is because normal
lung parenchyma and tumors are ablated together and the tumor and outer layer
(granulation tissue) are recognized as an ablated lesion. We have to interpret
the follow-up CT examinations to account for the influence of the ablated
change of normal lung parenchyma on follow-up CT.
During the follow-up examinations, cavitation was observed in about one
third of the samples. This cavitation has also been reported clinically
[11,
13,
14,
18]. In our study, the lesion
presented an image finding that was similar to that of a lung abscess. The
results of this study suggest that this change is caused by completely
necrotized tissues being drained into the bronchus and the remaining rigid
outermost layer. Because this finding was relatively prevalent, we believe
that this can be treated as a normal change in images after radiofrequency
ablation as long as there are no clinical issues such as fever or increased
inflammation.
The changes in layer structures were similar to those in the liver
generated by radiofrequency ablation
[30-32].
Goldberg et al. [22] and Miao
et al. [23] also found the
similar layer structures using their unique radiofrequency needles in rabbits'
lungs. Goldberg et al. investigated the feasibility and safety of performing
percutaneous radiofrequency ablation for the lung in eight rabbits and used CT
to assess the tissue 24 hr, 3 days, 10 days, 21 days, and 28 days after
radiofrequency ablation. Miao et al. performed radiofrequency ablation for VX2
tumors in 18 rabbits and confirmed the layer appearance of ablated lesion. Our
histopathologic findings support their results. However, in their study, the
number of ablated lesions was low, quantitation of lesion size was not based
on CT, histopathology studies were not performed and there was no
circumstantial histopathologic report. Because they relied only on H and E
staining, they did not discuss the completely necrotic lesion. Moreover, in
their report, such cavitations or obstructive pneumonitis was not reported.
This is because their number of ablated lesions was low or they used their
unique radiofrequency needle.
The limitations of this study are as follows: First, the number and flow of
respirations in the swine under general anesthesia differed from those in
patients under local anesthesia. Second, in the case of a tumor, the image
findings in our model could be different from those in clinical cases
containing lung cells and tumors. Third, the potential differences in lung
tissues between humans and swine might influence the extrapolation of data
from swine to humans. Fourth, a 50-W radiofrequency ablation generator is old
technology. The effects of higher wattage in the modern equipment may
influence our results. In their study, de Baere et al.
[33] reported that the
cooled-tip needle by a 200-W generator induced significantly larger lesions
than the expandable needle by a 50-W generator. However, there was no
difference in histopathologic findings between the two. We believed that the
same results could be obtained from the high-power generator.
In conclusion, in this study using a porcine lung model, NADH staining
suggested that the area with a ground-glass attenuation on CT performed
immediately after radiofrequency ablation overestimates the size of completely
necrotic lesions. In the ablation of lung tumors, the edge of tumors should be
identified in the ablated lesion (surrounded by ground-glass attenuation), and
an adequate safety margin should be obtained on CT immediately after
radiofrequency ablation. The lesions after radiofrequency ablation presented a
layer structure that exhibited pathologic changes chronologically. The layered
structural findings on CT reflected the histopathologic findings. As the
follow-up examinations progressed, the difference between the diameter
measured on CT images and on macroscopic examination became larger. Attention
should be paid to the dissociation of ablated lesions and high-density areas
in clinical interpretation of CT images. We believed the information obtained
would be useful for designing tumor ablation protocols and understanding the
changes in images at the time of follow-ups.
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Abstract
Introduction
