DOI:10.2214/AJR.07.2993
AJR 2008; 190:1659-1664
© American Roentgen Ray Society
Effect of Artificial Ascites on Thermal Injury to the Diaphragm and Stomach in Radiofrequency Ablation of the Liver: Experimental Study with a Porcine Model
Eun Joo Lee1,2,
Hyunchul Rhim1,
Hyo K. Lim1,
Dongil Choi1,
Won Jae Lee1 and
Kwang Sun Min3
1 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-ku,
Seoul 135-710, Korea.
2 Present address: Department of Radiology, Busan Paik Hospital, Inje University
College of Medicine, Busan, Korea.
3 Department of Pathology, Hallym Medical Center, College of Medicine,
University of Hallym, Seoul, Korea.
Received August 7, 2007;
accepted after revision December 5, 2007.
Address correspondence to H. Rhim
(forest{at}smc.samsung.co.kr).
This study was performed with the financial support of the 2005 Research
Fund from Samsung Biological Research Institute (# SBRI C-A5-122-1).
Abstract
OBJECTIVE. The purpose of this study was to evaluate the effect of
artificial ascites on thermal injury to the diaphragm and stomach in a porcine
model of radiofrequency ablation of the liver.
MATERIALS AND METHODS. We performed this study using eight pigs in
experimental and control groups of four pigs each. Artificial ascites was
produced before radiofrequency ablation to separate the liver from the
diaphragm and the stomach in the experimental group. Using a 1-cm exposed
internally cooled radiofrequency electrode for 5 minutes, we performed 74
hepatic ablations abutting the diaphragm and stomach. CT was performed on the
day of the procedure and 7 days after ablation. The pigs were sacrificed, and
necropsy was performed. We performed pathologic and CT examinations to compare
the frequency and extent of thermal injury to the two organs.
RESULTS. The mean number of radiofrequency ablations in each pig was
9.3 (range, 6-12). The mean number of ablation zones adjoining the diaphragm
was 5.5 (range, 3-8) and of zones contiguous with the stomach was 3.8 (range,
3-4). Thermal injury to the adjacent organs occurred more frequently in the
control group than in the experimental group (p < 0.05). The major
complications of diaphragmatic hernia and gastric perforation occurred only in
the control group. No major complications were identified in the experimental
group at necropsy. The sizes of the radiofrequency ablation zone of the liver
did not differ between the two groups (p > 0.05). The mean
diameters of the diaphragmatic and gastric lesions did differ (p <
0.05). Histopathologic examination revealed a significant difference in the
depths of thermal injury in the two groups (p < 0.05).
CONCLUSION. Artificial ascites may be a simple and useful technique
for reducing the frequency and severity of collateral thermal injury to the
diaphragm and stomach during radiofrequency ablation of subcapsular hepatic
tumors.
Keywords: ablation • animal study • liver • radiofrequency
Introduction
Many investigators
[1-12]
have found that radiofrequency ablation is a safe and effective technique for
the management of hepatic tumors and that it has minimal morbidity and
mortality. The reported complication rate is 5-25%
[1,
2]. Multiple-center studies
[3-16]
have shown a mortality rate of 0.3-4.5% and a rate of major complications of
2.2-8.9%. These findings confirm that radiofrequency ablation is a relatively
low-risk procedure for the management of hepatic tumors. The most common
complications include bleeding, infection, and collateral thermal injury to
the adjacent organs [17,
18]. The perihepatic organs at
risk of thermal injury include the diaphragm, gastrointestinal tract, and
major bile ducts.
Several reports
[19-21]
have shown that the use of artificial pleural effusion has improved the
feasibility of percutaneous radiofrequency ablation by increasing the
visibility of hepatocellular carcinoma under the diaphragm. Artificial pleural
effusion, however, cannot separate the diaphragm from an ablation zone on the
dome of the liver and can result in diaphragmatic thermal injury. The
artificial ascites technique we describe may be more effective than artificial
pleural effusion for improving the sonic window for hepatic dome lesions and
preventing thermal injury to the diaphragm.
The effect of artificial ascites on thermal injury to adjacent perihepatic
organs has been evaluated in a large animal model. We have performed
radiofrequency ablation on the normal livers of pigs, but the lack of a good
tumor model and cirrhotic liver parenchyma limited the study. The purpose of
this study was to evaluate the effect of artificial ascites on thermal injury
to the diaphragm and stomach during radiofrequency ablation of the liver in a
porcine model.
Materials and Methods
Animals
Eight 1-year-old male Yorkshire pigs (mean weight, 30.3 ± 0.4 kg;
range, 26.0-33.0 kg) were used. The pigs had free access to food and water
before and after the experiments. The pigs were kept under specified
pathogen-free conditions, and all experiments were performed under clean
conditions in our animal research center facility. All experiments were
performed according to a protocol approved by the local institutional
committee on animals and in accordance with the general guidelines issued by
the National Institutes of Health for care of laboratory animals. The animal
research committee of the medical research institute approved all experiments
and surgical procedures.
Radiofrequency Procedure
All pigs were initially anesthetized by intramuscular injection of 20 mg/kg
body weight ketamine hydrochloride (Ketara, Yuhan) and 2 mg/kg body weight
xylazine (Rompun, Bayer Korea). An 18-gauge by 1-inch IV catheter was inserted
into the dorsal auricular vein. The pigs were intubated, and anesthesia was
maintained with inhaled halo thane gas. We placed the pigs in the supine
position after adequate anesthesia was achieved. Blood pressure, respiration,
pulse, and ECG were monitored continuously. Both thighs of each pig were
shaved for placement of a grounding pad (13 x 21 cm), and the epigastric
area was sterilized after being shaved. By a predefined randomization
strategy, the pigs were divided into an experimental group of four pigs and a
control group of four pigs.
To produce artificial ascites in the experimental group, we inserted a
20-gauge 32-mm sheathed needle (Introcan Certo, B. Braun) into the
gastrohepatic space through the subxiphoid approach under sonographic guidance
(Acuson Sequoia Gastrointestinal 512 unit, Siemens Medical Solutions). After
removal of the needle, approximately 700-1,000 mL of sterile normal saline
solution (0.9% sodium chloride), at room temperature, was infused by gravity
drip into the gastrohepatic space through the remaining sheath until a
separation of at least 0.5 cm between the liver and stomach was achieved.
During the ablation procedures, we infused the additional solution to maintain
the distance of 0.5 cm between the ablation zone and the diaphragm or stomach
by opening a three-way stopcock. In the control group, all procedures were the
same as in the experimental group except for the production of artificial
ascites before radiofrequency ablation.
All ablation procedures were performed by a sonographically guided
percutaneous approach by one radiologist using an internally cooled
radiofrequency ablation system. This system combined a 480-kHz generator
(Series CC-3, ValleyLab) capable of maximum power of 250 W with a monopolar
internally cooled electrode. The electrode was equipped with two connectors
(Luer-Loc, ValleyLab) for inflow and outflow of distilled ice-water coolant,
which ensured a constant temperature of the coolant of approx imately
0-10°C. Circulation of the cooling fluid was maintained with a pump (PE-pm
perfusion pump, ValleyLab). We used a single straight-tip electrode with a
10-mm active tip. The device was operated in impedance control mode according
to the manufacturer's instructions.
We made multiple radiofrequency ablation zones in the liver depending on
the size of liver and the sonic window. However, we carefully evaluated the
site of electrode placement to not overlap previous ablation zones. We
inserted the radiofrequency electrode in a vertical position in relation to
the diaphragm or the gastric wall. The tip of the radiofrequency electrode was
kept close to the hepatic capsule abutting the diaphragm or stomach (< 3 mm
away from the hepatic capsule) as monitored with sonography (4-1-MHz convex
probe, Acuson Sequoia Gastrointestinal 512, Siemens Medical Solutions). In the
experimental group, we maintained the sheath in the peritoneum during all
ablation procedures. It was removed without additional procedures, such as
aspiration, immediately after ablation.
CT Examinations
Within 3 hours after ablation, all pigs were subjected to MDCT with coronal
reformation (LightSpeed 16 scanner, GE Healthcare). The pigs were sedated for
CT with only the induction anesthesia protocol described earlier. After
initial unenhanced images of the liver were obtained, 2 mL/kg of iopromide
(Ultravist 300, Bayer Health Care) was infused. The following CT parameters
were used: 250 mAs, 120 kV, 2.5-mm collimation, table speed of 18.75 mm/s,
pitch of 0.938. Images were acquired with 30-, 60- and 180-second delays. One
week after ablation im mediately before the pigs were sacrificed, follow-up CT
was performed with the same protocol as the original examination. One
radiologist assessed all CT images for complications related to radiofrequency
ablation. We evaluated whether pneumothorax or hemothorax, gastric wall or
diaphragmatic thickening, atelectasis, gastric perforation, or diaphragmatic
hernia or perforation was present with CT im mediately and 7 days after
ablation. We also checked whether ascites was present at follow-up CT.
Histopathologic Specimens
Immediately after the 7-day follow-up CT im ages were obtained, all pigs
were sacrificed, and their livers, stomachs, and diaphragms were extracted
through midline laparotomy. All specimens were photographed with a
high-resolution digital camera (Coolpix 5700, Nikon). For each liver, we used
calipers to measure the maximum short axis of the radiofrequency ablation zone
(white zone) perpendicular to the electrode axis of the specimen. We then
measured the maximum diameter of the thermally damaged lesions identified on
the basis of color changes at the diaphragm or stomach close to the
radiofrequency ablation zones.
The thermal damage lesions of the diaphragm and stomach were fixed in 10%
formalin for routine histologic examination. This procedure was followed by
processing with paraffin section ing and H and E staining. An experienced
pathologist performed the histopathologic analysis. The areas of diaphragmatic
injury were sectioned and graded according to the following 4-point scale: 1,
no diaphragmatic injury; 2, mild injury up to one third of the thickness; 3,
moderate injury up to two thirds of the thickness; 4, severe full-thickness
injury. Microscopic gastric wall injury was rated according to the following
5-point scale: 1, no gastric wall injury; 2, mild injury up to serosa; 3,
moderate injury up to muscularis propria; 4, moderate injury up to submucosa;
5, severe injury up to the mucosa.
Statistical Analysis
Both groups were compared in regard to the frequency, size, and severity of
the diaphragmatic and gastric injuries. Significant differences were
determined with a chi-square test, Mann-Whitney test, and Fisher's exact test.
A value of p < 0.05 was considered to indicate a statistically
significant difference. Data analyses were performed with SPSS for Windows
(version 11.0.1, SPSS).
Results
Radiofrequency Ablation
All pigs subjected to radiofrequency ablation tolerated the procedure
generally well. No changes in vital signs were observed. A total of 74
radiofrequency ablation zones were produced: 44 zones contiguous with the
diaphragm and 30 zones adjacent to the stomach. The mean number of
radiofrequency ablations in each pig was 9.3 (range, 6-12). A mean of 5.5
zones (range, 3-8) adjoined the diaphragm and 3.8 (range, 3-4) the stomach.
Artificial ascites was successfully achieved with a single puncture in all
pigs in the experimental group.
Imaging Analysis
CT immediately after ablation depicted two cases of atelectasis in the
experimental group. One case of pneumothorax and one of subsegmental
atelectasis occurred in the control group
(Fig. 1). On the immediate CT
scans, seven (30%) of 23 ablation zones exhibited diaphragmatic attenuation
changes in the experimental group. In the control group, 19 (90%) of 21
ablation zones adjacent to the diaphragm exhibited attenuation changes
(Fig. 2A). In the experimental
group, five (33%) of 15 lesions had gastric wall thickening and attenuation
changes. In the control group, 12 (80%) of the 15 ablation zones adjacent to
the stomach had gastric wall thickening and attenuation changes
(Fig. 3A).
CT 1 week after radiofrequency ablation showed only four diaphragmatic
changes in the experimental group. In the control group, however, 11 of 19
diaphragmatic changes were found. In the experimental group, three of five
gastric lesions were found. In the control group, 10 of 12 gastric wall
changes were found. The acute complications of atelectasis and pneumothorax
had resolved. The follow-up scans showed a case of diaphragmatic hernia (Fig.
2B and
2C) and a case of sealed-off
gastric perforation (Figs. 3B
and 3C) in the control group.
In the experimental group, there was no evidence of residual ascites on 1-week
follow-up CT (Figs. 4A,
4B,
4C and
4D).
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Fig. 4A —Experimental group pig with artificial ascites. Coronal
reformation CT image after radiofrequency ablation shows separation between
diaphragm and hepatic dome with accumulation of infused saline solution. Two
radiofrequency ablated zones exhibit low attenuation.
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Fig. 4B —Experimental group pig with artificial ascites. Coronal
reformation CT image 7 days after radiofrequency ablation shows artificial
ascites has disappeared and attenuation is low in radiofrequency ablation
zone.
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Pathologic Evaluation of Gross Features
Thermal injury to the diaphragm close to the radiofrequency ablation zones
was found in 11 (48%) of 23 ablation zones in the experimental group and all
21 ablation zones in the control group. The frequency of thermal injury was
significantly different in comparison of the two groups (chi-square,
p < 0.001). Thermal injury to the stomach close to the
radiofrequency ablation zone was found in 10 (67%) of 15 ablation zones in the
experimental group and all 15 ablation zones in the control group. The
frequency of thermal injury was significantly different in comparison of the
two groups (chi-square, p < 0.05). There was a significant
difference in the size of thermal injuries to the diaphragm and stomach in
comparison of the control and experimental groups (p < 0.05)
(Table 1). In a comparison of
the control and experimental groups, however, there was no difference in the
size of the radiofrequency ablation zone in the liver (p > 0.05)
(Table 1). There were no
complications related to the use of artificial ascites, including
hemoperitoneum and thermal damage at remote sites caused by thermal conduction
through the artificial ascites fluid.
Pathologic Evaluation of Microscopic Features
In the experimental group, 14 (61%) of 23 ablative lesions exhibited no
diaphragmatic injury. In the control group, however, 18 (86%) of 21 lesions
produced full-thickness diaphragmatic injury
(Fig. 2D). These findings
resulted in a significant difference in the distribution of microscopic grades
of thermal injury in comparison of the two groups (Fisher's exact test,
p < 0.01) (Fig.
5). With use of artificial ascites, eight (53%) of 15 ablation
zones were free of gastric lesions. Six (40%) of 15 gastric lesions in the
control group caused grade 5 injury; one (7%) of the lesions, grade 4 injury;
seven (47%) of the lesions, grade 3 injury; and one (7%) of the lesions, no
injury There was a significant difference in distribution of microscopic grade
of gastric injury in comparison of the two groups (Fisher's exact test,
p = 0.008) (Fig.
6).
Discussion
Radiofrequency ablation has become the standard nonsurgical percutaneous
approach to treatment of patients with primary and metastatic malignant
hepatic tumors [2,
9,
22]. Although radiofrequency
ablation is known to be relatively safe and effective, a variety of
complications, including bleeding, infection, tumor seeding, pneumothorax,
collateral thermal injury, and grounding-pad burns, can occur. The collateral
thermal injuries are caused by heat generated from delivery of current to
adjacent organs during the tumor ablation procedure. If a tumor is located
immediately beneath the hepatic capsule, the risk of thermal injury to
contiguous organs increases during the percutaneous ablation procedure. The
organs most vulnerable to thermal injury are the diaphragm, colon, bile ducts,
and gallbladder. Diaphragmatic injury has been described in several reports
[5-7,
11,
12,
14]. Two fatal burns have
occurred as a result of bile leak into the chest and the development of an
associated abscess. Two additional burns caused pain lasting 10 days to 3
months. Another patient sustained diaphragmatic paresis. Two colonic burns
have been reported [6,
12,
13], one resulting in
perforation and the other in a fistula. One jejunal perforation necessitated
surgery, and one gastric burn has been reported
[7,
12,
13]. In cases in which a
subcapsular tumor is adjacent to organs at risk of injury, the clinician must
decide between safe ablation and complete ablation.
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Fig. 3D —Control pig with sealed-off gastric abscess. Photomicrograph
of stomach section with grade 5 injury shows coagulative necrosis
(arrows) of muscularis propria and inflammatory cell infiltration
through all layers of stomach and focal ulceration (arrowheads). (H
and E, x12.5)
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Radiofrequency ablation by the intraoperative or laparoscopic approach
ensures separation of the liver from adjacent at-risk organs. Radiofrequency
ablation, however, is more invasive and complicated than thermal ablation,
requires more medical personnel, and is associated with a higher morbidity
rate. Although several studies
[19-21,
23,
24] have shown percutaneous
ablation with artificial ascites to be a simple and cost-effective technique
for managing subcapsular tumors contiguous with at-risk organs, most reports
have been anecdotal. In only a few experimental studies has the effect of
artificial ascites on reduction of thermal damage to the diaphragm and stomach
been assessed.
We performed an experimental study with imaging follow-up in a large-animal
experimental model. The induction of artificial ascites was technically
successful in all cases in the experimental group. The infused solution had
been completely absorbed by follow-up CT 1 week after the ablation procedure.
Visual inspection during necropsy revealed no evidence of hemoperitoneum or
peritonitis related to artificial ascites.
Contrast-enhanced helical CT has been widely used for the evaluation of
complications after radiofrequency ablation
[25-27].
In our study, CT showed a variety of complications, including thoracic and
gastric complications. CT immediately after the procedure depicted 13 lesions
with attenuation or thickening of the adjacent diaphragm and stomach among 38
ablation zones in the experimental group and 31 lesions among 36 ablation
zones in the control group. Some lesions visualized on CT immediately after
the procedure were reduced, but some progressed to diaphragmatic hernia or
sealed gastric abscess. Although CT performed immediately after ablation
showed a variable degree of thickening and attenuation change in the adjacent
organs, CT 1 week after ablation did not show serious complications such as
gastric or diaphragmatic perforation. Therefore, careful follow-up is required
in the care of patients with hepatic tumors adjacent to the diaphragm and
stomach managed with percutaneous radiofrequency ablation.
Normal saline solution is used for artificial ascites because it is
isoosmolar and well absorbed in the peritoneal cavity with maintenance of
homeostasis. Saline solution, how ever, is an ionic fluid and thus conducts
electricity. In one study of an animal model
[28], instillation of 5%
dextrose into the peritoneal cavity before hepatic radiofrequency ablation
decreased the risk and severity of diaphragmatic and lung injury compared with
use of normal saline solution.
Our study had several limitations. First, the follow-up period was too
short to prove the long-term safety of artificial ascites. We do not know
whether artificial ascites increases the probability of postprocedural
bleeding, especially in cases of cirrhosis and severe co-agulopathy. In
addition, there is concern about the possibility of peritoneal seeding after
ablation of subcapsular tumors. Second, because of the small number of pigs,
we did not study variable ablation parameters, such as safe distance, type of
electrode, and duration of ablation. Further investigation should address the
safest ablation parameters with and without artificial ascites. Third, we did
not evaluate thermal injury to the colon, which is more vulnerable to thermal
injury than is the stomach because the colonic wall is thinner than the
gastric wall. It was difficult to study this ablation site because the tip of
the liver abutting the colon in the pigs was too slender for placing the
electrode properly. Fourth, instead of 5% dextrose solution, we used 0.9%
normal saline solution, which might have affected the outcome of the
study.
We performed radiofrequency ablation on normal pig livers. Conduction of
heat in the parenchymal wall of normal liver varies from that of tumorous and
cirrhotic liver parenchyma owing to differing patterns of vascularity and
thermoconduction. Thus the study results may change in clinical cases of
underlying cirrhosis in human patients. Further evaluation with a larger
number of animals and with a longer follow-up period is necessary to evaluate
whether artificial ascites plays a role in the development of peritonitis or
delayed hemoperitoneum and peritoneal seeding after ablation.
Collateral thermal damage to the diaphragm and stomach was grossly observed
in all pigs in the control group, in which artificial ascites was not used.
These injuries were present in approximately one half of the pigs in the
experimental group, in which artificial ascites was used. In addition, the
degree of thermal injury at histologic examination was more severe in the
control group than in the experimental group. As a result, all serious
complications, such as diaphragmatic herniation and gastric perforation, were
found only in the control group. Our results suggest that percutaneous
radiofrequency ablation with artificial ascites may be a simple, safe, and
effective technique for decreasing the frequency and degree of thermal injury
to the diaphragm and stomach in patients with subcapsular hepatic tumors
adjacent to at-risk organs.
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J. Cha, H. Rhim, J. Y. Lee, Y.-s. Kim, D. Choi, M. W. Lee, W. J. Lee, and H. K. Lim
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Am. J. Roentgenol.,
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Abstract
Introduction
