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 »  Abstract
 » Introduction
 »  Materials and Me...
 » Results
 » Discussion
 » Conclusion
 »  References
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  Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 52  |  Issue : 6  |  Page : 84-90
 

Comparison of the gallbladder damage caused by microwave ablation and cryoablation in vivo porcine livers


1 Center for Interventional Medicine, The Affiliated Hospital of Qingdao University, Qingdao 266000, Shandong Province, China
2 Department of Medical Imaging and Interventional Radiology, Cancer Center and State Key Laboratory of Oncology in South , Sun Yat-sen University, Guangzhou 510060, Guangdong Province, China

Date of Web Publication24-Dec-2015

Correspondence Address:
F Weijun
Department of Medical Imaging and Interventional Radiology, Cancer Center and State Key Laboratory of Oncology in South China, Sun Yat-sen University, Guangzhou 510060, Guangdong Province
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0019-509X.172520

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 » Abstract 

Purpose: To compare the imaging, anatomy, and histopathology of the porcine liver tissue adjacent to the gallbladder, as well as the temperature of the gallbladder wall and the damage degree of gallbladder wall at different times after microwave ablation (MWA) and cryoblation. Materials and Methods: Sixteen pigs were randomly divided into MWA group (Group M) and cryoblation group (Group C). The pigs were randomly divided into 8 subgroups according to their execution time, with 2 pigs in every subgroup. The pigs were executed immediately after operation, or at 1-, 2-, and 4-weeks postoperatively according to their assigned subgroup. The imaging and anatomy change of the liver ablation zone and the gallbladder wall were recorded. Histopathological observation was carried out for the damage portion of the gallbladder and the adjacent liver parenchyma. Results: (1) There were no significant statistical differences of the damage degree of the gallbladder between the two groups (P = 0.842). (2) Gallbladder wall edema occurred in Group M immediately after ablation (6/8), of which, 3 cases of gallbladder wall reached full-thickness damage; overlapping of ice ball and gallbladder wall occurred in Group C (5/8), of which, 4 cases of gallbladder wall reached full-thickness damage. However, there was neither perforation of gallbladder, biliary fistula, nor liver abscess in all cases. Conclusion: Both MWA and cryoablation for liver tissues adjacent to the gallbladder could lead to different damage degrees of the gallbladder wall, but not gallbladder perforation even under the condition of full-thickness damage.


Keywords: Cryoablation, gallbladder damage, livers in vivo, microwave ablation, perforation


How to cite this article:
Hao Z, Wan C, Han Q, Ze S, Xin L, Weijun F. Comparison of the gallbladder damage caused by microwave ablation and cryoablation in vivo porcine livers. Indian J Cancer 2015;52, Suppl S2:84-90

How to cite this URL:
Hao Z, Wan C, Han Q, Ze S, Xin L, Weijun F. Comparison of the gallbladder damage caused by microwave ablation and cryoablation in vivo porcine livers. Indian J Cancer [serial online] 2015 [cited 2019 Aug 24];52, Suppl S2:84-90. Available from: http://www.indianjcancer.com/text.asp?2015/52/6/84/172520



 » Introduction Top


Liver cancer is one of the most common malignant tumors in the world, with its incidence rate is increasing every year globally.[1] Image-guided local ablation has been increasingly widely applied due to simple operation, good repeatability, relatively less complications, etc., when compared to surgery.[2],[3],[4],[5] The most commonly used techniques are radiofrequency ablation (RFA), microwave ablation (MWA), and cryoablation. Literature reports indicated that the survival rate of RFA, MWA, and cryoablation for treating small liver tumors (diameter <3 cm) is comparable to surgical resection.[3],[6],[7] However, local ablation treatment for liver tumors that are closed to gallbladder, diaphragm, big blood vessels, digestive systems can cause damage to the nearby organs in risk. Thus it is hard to achieve complete ablation.[8] As for treating liver tumors closed to the gallbladder, it seems very difficult to achieve complete ablation using local ablation, concerning the possibility of biliary-cardiac reflex, thermal subsidence effects of bile, and damage of gallbladder. Some scholars believe that local thermal ablation for treating liver tumors closed to the gallbladder, can lead to thermal damage of the gallbladder,[9],[10],[11] whereas others consider it as a safe and an effective way for treating liver tumors closed to the gallbladder.[12],[13]

Further research is required to find out the mechanism for causing damage using local thermal ablation for liver tumors near the gallbladder, especially for MWA and cryoablation, which has been rarely studied. As MWA and cryoablation work in different ways, it remains a question to find out the difference of these two techniques in the perspective of damage to the gallbladder wall. Up to this point, no comparative study of damage of gallbladder wall caused by MWA and cryoablation has been done using animal experiments. In this study, computed tomography- (CT) guided MWA and cryoablation are carried out in vivo porcine livers, and enhanced CT scan was conducted immediately after ablation, and at 1-, 2-, and 4-week periods after ablation. The pigs were executed and dissected, and a pathological section of the gross specimen was made. The imaging of the nearby gallbladder, anatomy, tissue pathological changes, and damage of the gallbladder wall at different times was studied, so as to provide a theoretical basis for clinical application of MWA and cryoablation for treating liver tumor closed to the gallbladder.


 » Materials and Methods Top


Animal, anesthesia, and grouping

Sixteen adult Wuzhishan miniature pigs weighed 21–30 kg (average 24.5 ± 2.6 kg), and all with a health certificate. The pigs were fasted for 12 h, and given an intramuscular injection of Sumianxin II (0.1 ml/kg) and sodium pentobarbital (1 ml/kg). After the pigs were anesthetized, intravenous line were established through marginal ear veins. The normal saline drip was maintained. The pigs were divided into eight groups (M0, M1, M2, M4 and C0, C1, C2, C4) according to their execution time after ablation, with 2 pigs in each group. The output power/time of microwave was 60 W/10 min; 2 cycles were set for cryoablation (the freezing time/rewarming time for each cycle was 15 min/5 min). Only one ablation site was done for each pig to avoid the impact of superimposed ablation.

Ablation device

MWA device

An MTC-3 microwave generator (FORSEA: Qinghai Microwave Electronic Institute, Nanjing, China) was used in this study. The system has a frequency of 2450 MHz, an adjustable power output of 10–150 W, a 15-cm long MWA antenna with 15G water-cooling circulation.

Cryoablation device

A Cryo-HIT cryogenic ablation system (GALIL Company, Israel) was used. The system has a 17G cryogenic probe (outer diameter was 1.47 mm), length 20 cm. The working pressures for argon and helium were 3400 and 2000 psi, respectively. The freezing rate was set to 100%.

Experimental procedure

The left lateral decubitus position of the anesthetized pig was stabled on the CT scan station. Needle puncture path was designed after CT scan. Routine disinfection for the surgical area was done. Microwave antenna or cryogenic probe was inserted into liver parenchyma under CT guidance. The position of the ablation needle was adjusted to make it about 1 cm parallel to the gallbladder. Bolus contrast agent iopamidol (1 ml/kg) was rapidly injected through marginal ear vein right after the operation, and the enhanced-CT scan was carried out. The pigs in Group M0 and C0 were executed after ablation, whereas the others were executed after 1, 2, or 4 weeks of rearing depending on which group they were in. Another enhanced CT scan was carried out before the execution (10 ml, 10% potassium chloride solution was given intravenously through marginal ear veins). The pigs were dissected right after, and the change of gallbladder wall, liver ablation lesion, and liver parenchyma were observed. The gallbladder was dissected, and the change of the inner wall, which was closed to the ablation zone, was observed. The gallbladder and the ablation lesion were dissected along the largest diameter of the ablation lesion. The section was then fixed with 10% buffered formalin solution for at least 24 h. The damaged part of the gallbladder and its nearby liver parenchyma was cut into 5-mm thick slices, embedded in paraffin, and continuous reduction to 6-μm thick, stained using HE. The slices were used for histopathological observation.

Pathological grading of gallbladder damage

The damage degree of the gallbladder were classified under microscope according to the thickness of the damaged gallbladder wall: Grade 0, no damage (no abnormal change of the full thickness of the gallbladder wall); Grade I, mild damage, the thickness of the damaged gallbladder wall did not exceed 1/3 of full thickness; Grade II, moderate damage, the thickness of the damaged gallbladder wall was between 1/3 and 2/3 of full thickness; Grade III, severe damage, damaged thickness exceeded 2/3 of full thickness, reached full-thickness damage, and even perforation.

Statistical analysis

The imaging and anatomical major diameter of the liver ablation lesion (D1) was collected. Of which, the imaging data collected right after operation was D1 (immediate), and the data collected after 1, 2, and 4 week was D1 (delay), displayed was mean ± standard deviation. Independent sample t-test was used for statistical analysis of the comparison of ablation lesion major diameter D1. Fisher's exact test was used for comparison of pathological grading. All statistical analysis was performed by using of SPSS 16.0 statistical software (version 16.0, SPSS, Chicago, Illinois), and P < 0.05 were considered statistically significant.


 » Results Top


The results are shown in [Table 1] and [Table 2].
Table 1: Statistics of experimental MWA group

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Table 2: Statistics of cryoablation group

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Imaging

Enhanced CT scan was done immediately after the ablation for the 8 cases of pigs in Group M, and it had showed irregular edges of the liver ablation zone with the cavity. Of all the 8 cases, the edge of liver ablation zone was adjacent to the gallbladder. Six cases had edematous gallbladder wall. The enhanced CT scan after 1, 2, and 4 weeks had showed no significant change of the liver ablation zone comparing to the immediate postoperative CT scan. However, the enhanced CT scan after 1 week showed the disappearance of edema of gallbladder wall. In Group C, the edge of ice ball was adjacent to the gallbladder in all the 8 cases of experimental pigs. Of which five cases had superimposed zone between the ice ball and gallbladder, and enhanced CT scan showed no obvious edematous gallbladder wall. The enhanced CT scan after 1, 2, and 4 weeks showed significant smaller area of the liver ablation zone comparing to the immediate postoperative CT scan; the liver ablation zone was adjacent to the gallbladder. In Group C2, pseudocapsule formed at the edge of liver ablation zone in one case [Figure 1].
Figure 1: Imaging and gross anatomy (red arrow indicated the gallbladder wall edema immediately after ablation; white arrow indicated the gallbladder wall closed to the ablation lesion after dissection

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The postoperative result showed that there was no difference between the ablation range of Group M and ice ball range of Group C (4.13 ± 0.21 cm vs. 4.26 ± 0.14 cm, P = 0.149). After 1 week, the liver ablation zone of Group C was significantly smaller than that of Group M (2.98 ± 0.43 cm vs. 3.95 ± 0.12 cm, P = 0.000) [Table 3].
Table 3: Comparison of imaging and anatomical major ablation zone diameter Dl between the two groups

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Anatomy

MWA group

Two cases of pigs in Group M0 were executed and dissected immediately after the MWA. The section of the liver ablation zone and gallbladder showed significant thickened and edematous gallbladder wall (about 5 mm) with the edge of ablation zone adjacent to the gallbladder wall. One week after the ablation (Group M1), the section of gallbladder and liver ablation zone displayed that the liver ablation zone was not fully connected to the gallbladder wall. The gallbladder wall had no edema. Two weeks later (Group M2), two cases had an oval dark-brown ulcer area with size about 0.5 cm × 1.0 cm and 1.0 cm × 1.2 cm at the inner surface of gallbladder walls. The liver ablation zone was fully connected with gallbladder wall. Four weeks later (Group M4), one case had round dark-brown ulcer area with size about 0.8 cm × 0.8 cm at the bottom of the gallbladder wall. The gallbladder and liver ablation zone was dissected. There was no significant abnormal change of gallbladder wall in the other case [Figure 2].
Figure 2: Gallbladder anatomy (red arrow showed the ablation lesion on the liver surface immediately after ablation; white arrow showed the ulceration change of inner gallbladder wall)

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Cryoablation group

In Group C0, dark red ablation area was shown on the liver ablation zone surface in both 2 cases. The ablation zone was adjacent to the gallbladder wall, which had nonapparent abnormality. In addition, the gallbladder wall had no obvious edema. One week after the ablation (Group C1), the gallbladder bottom of one case had the black irregular ulcer area in one case. The liver ablation zone was fully connected with the gallbladder wall with unclear boundary, but the gallbladder wall had no perforation. Two weeks later (Group C2), the inner surface of gallbladder displayed dark-brown ulcer area with clear boundary and size of 1.0 cm × 1.8 cm and 1.1 cm × 1.4 cm in the two cases. The liver ablation zone was completely connected with gallbladder wall but no perforation of the gallbladder wall. Four weeks later (Group C4), one case's inner surface of gallbladder had a brown polypoid tissue, and the pedicle of polypoid tissue was connected to the gallbladder. The gallbladder was connected with liver ablation zone without perforation or leakage of bile.

The major diameter Dl in gross anatomy of Group M was greater than that of Group C at 1–4 weeks after the ablation (3.44 ± 0.185 cm vs. 2.73 ± 0.344 cm, P = 0.004). The edge of ablation zone in Group M was irregular and rugged. However, the ablation zone in Group C had comparatively neat and regular edge. The immediate dissection after ablation had showed that all the four cases in Group M0 and Group C0 had no color change in the inner surface of the gallbladder, but the two cases in Group M0 had edematous gallbladder. All the ulcer-like changes in the inner surface of gallbladder occurred 1 week after ablation. Of which, Group M had 3 cases (the edematous gallbladder occurred immediately after ablation), whereas Group C had 4 cases (the ice ball superimposed with the gallbladder wall immediately after ablation).

Histopathology

MWA group

Liver ablation zone immediately after ablation (Group M0) showed hyperemia, liver cell deformability, unobvious inflammatory cell infiltration, unclear boundary between the ablation zone and normal liver, disappearance of gallbladder mucosal folds, exfoliation of some mucosal epithelium, and obvious edema of submucosa and outer membranes. One week after ablation (Group M1), the liver ablation zone showed coagulation necrosis, calcium deposits, fibrous tissue and bile duct hyperplasia in its surrounding area, exfoliation of mucosal epithelium of gallbladder, disappearance of gallbladder mucosal folds, unobvious inflammatory reaction. Two weeks later (Group M2), the liver ablation zone showed obvious surrounding inflammation, hyperplasia of fibrous tissue and part of the small bile duct and connection between liver ablation zone and gallbladder. Both two cases had full-thickness damage of gallbladder wall, exfoliation, and degeneration of mucosal epithelium, disappearance of submucosa, a disorder of muscular layer. Four weeks later (Group M4), one case had significant inflammation, full-thickness damage of gallbladder wall, the disappearance of folds, and infiltration of multinucleated giant cell in the outer layer of the gallbladder wall [Figure 3].
Figure 3: Pathology of live ablation zone and gallbladder wall

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Cryoablation group

Immediate result after cryoablation (Group C0) showed intact lobular architecture near the gallbladder, mild vasodilation in the portal area, intact gallbladder mucosal folds and unobvious vasodilation. One week after ablation (Group C1), liver ablation zoned in two cases showed coagulation necrosis, disappearance of normal lobular structure, inflammation zone around the necrotic area, calcium deposits, and liver ablation zone in one case was connected to the gallbladder which had coagulation necrosis in full thickness without significant inflammation. Two weeks after ablation (Group C2), two cases' ablation zone showed coagulation necrosis, surrounded inflammation zone (infiltration of plasma cells, neutrophils, and multinucleated giant cell), the connection between all the liver ablation zone and gallbladder, full-thickness necrosis of gallbladder wall, and no significant inflammation in the gallbladder wall. Four weeks after ablation (Group C4), one case had full-thickness damage of gallbladder wall, polyp-like changes outside the gallbladder (most were coagulation necrosis), together with hyperplasia of collagen fiber in the outer membrane of gallbladder, and infiltration of multinucleated giant cell in the outer membrane.

Damage degree of gallbladder wall

The gallbladder damage was classified based on the pathological grading standard. Group M had two cases of Grade I damage, three cases of Grade II damage, and three cases of Grade III damage. Group C had two cases of Grade I damage, two cases of Grade II damage, and four cases of Grade III damage. All cases of Grade III damage had reached the full-thickness damage. According to Fisher's exact test, there was no statistically significant difference of gallbladder damage degree between the two groups (P = 0.842).

For pathological changes, eight cases in Group M had various degrees of exfoliation of gallbladder mucosal epithelium and disappearance of gallbladder mucosal folds, even the ablation necrosis zone did not involve the gallbladder wall, but Group C had three cases did not have exfoliation of gallbladder mucosal epithelium and disappearance of gallbladder mucosal fold.


 » Discussion Top


Image-guided local ablation has been increasingly widely applied for treating liver tumor. However, it can cause severe damage to adjacent organs if ablation is not controlled properly. There are still controversial opinions among the scholars globally regarding whether to perform local image-guided ablation for liver tumor closed to the important organs such as diaphragm, gallbladder, intestines, and hepatic portal. Many scholars believe that it is a contraindication to make the local ablation for liver tumor <1 cm away to organs in risk, or the local ablation should be performed after the bile suction, gallbladder separation with water or cholecystectomy.[11],[14] Livraghi et al.[15] had done a multicenter study of complications after RFA, and they recommended resection or laparoscopic-guided ablation for the liver tumor <1 cm away to organs in risk. Meanwhile, there are a lot of literature showing that it is safe and effective to perform local ablation for liver tumors closed to organs in risk.[8], 11, [16],[17],[18],[19] Clinical reports indicate that the main complication of RFA for liver tumor near the gallbladder was acute cholecystitis and gallbladder perforation.[9],[10],[15],[20] Chopra et al.[10] believe that the RFA for liver tumor near the gallbladder is safe and feasible because gallbladder-related complications are self-limited. Lee et al.[21] believe that RFA could cause heat damage or even perforation to the gallbladder wall, and the safe distance between electrode and gallbladder should be at least 1 cm. In order to have a further systematic study of the features and differences of damage to the adjacent gallbladder between MWA and cryoablation, we created an in vivo animal experiment. The imaging, anatomy, and histopathology of the ablation zone near the gallbladder, and the damage degree of gallbladder wall at different times after MWA and cryoblation were compared.

From this experimental study, the edematous gallbladder wall caused by MWA and the imaging of overlap between gallbladder wall and the ice ball caused by cryoablation, both indicated the damage, even full-thickness damage of the gallbladder wall. The immediate enhanced CT scan after MWA indicated significant edema of gallbladder wall (6/8). Combined with the pathological result, it could be explained that heat stimulation of gallbladder wall could lead to edema of lamina propria and outer membrane with rich tissue, but there was no significant edema response to low-temperature stimulation. The edema of gallbladder wall after MWA can be clearly detected by enhanced CT scan. By the anatomical and pathological study, we found that the edema of the gallbladder wall occurred during the ablation would later become different degrees of damage or even full-thickness damage of gallbladder wall. The overlap between gallbladder wall and ice ball could occur immediately after cryoablation (5/8). It was found that damage of gallbladder wall occurred in all the five cases through anatomical and pathological study (4 cases reached the full-thickness damage). Thus, superimposed ice ball and gallbladder wall often indicates damage of gallbladder wall.

The liver ablation zone had significant anatomical and pathological changes immediately after MWA, but it would take 1 week for cryoablation to show the changes. Significant edema of lamina propria and outer membrane, and pathological changes in liver ablation zone occurred immediately after MWA, but that was not significant in cryoablation. However, both Group M and Group C had the pathological changes such as coagulation necrosis of liver tissue and damage of gallbladder wall 1 week after ablation. The coagulation necrosis in Group C was more even than Group M, and inflammation in Group C was more significant than in Group M [Figure 4]. This indicated that liver tissue damage in MWA was an acute process, whereas damage process of liver tissue in cryoablation was relatively slow.
Figure 4: The pathological change of surrounding area of the necrotic zone 1 week after ablation (inflammation response band of C1 was wider than M1, with more obvious bile duct hyperplasia)

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Based on the condition that the ablation zone of liver tissue had no significant difference between MWA and cryoablation, the gallbladder damage was classified based on the pathological grading standard: The number of cases of Grade I, Grade II, and Grade III damage in Group M was two, three, and three, respectively, whereas the number of cases of Grade I, Grade II, and Grade III damage in Group C was two, two, and four, respectively. All the Grade III damage in both Group M and Group C reached full-thickness damage. (The inner layer of gallbladder wall showed ulcerative change.) There was no statistically significant difference of gallbladder damage between the two groups (P = 0.842). The results indicated that the degree of damage of gallbladder wall caused by MWA was similar to the damage caused by cryoablation under the condition of similar ablation zone. (All the damage could lead to the full-thickness damage of gallbladder wall, but without perforation, biliary fistula, liver abscess, etc.)

Under the condition that there was no abnormal pathological changes in the muscle layer and outer membrane of the gallbladder wall, MWA can lead to exfoliation of mucosal epithelium of gallbladder, which was consistent with the study done by Lee et al.[21] However, there were relatively less similar phenomena occurred in cryoablation. It might be because the mucosal epithelium of gallbladder was more sensitive to the stimulation of high temperature than low temperature.


 » Conclusion Top


Both MWA and cryoablation for liver tissues near the gallbladder could lead to different damage degrees of the gallbladder wall, but not gallbladder perforation even under the condition of full-thickness damage.

 
 » References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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