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Original Research |
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).
Abstract
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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
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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.
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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).
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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).
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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).
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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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