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DOI: 10.1148/radiol.2321030210
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(Radiology 2004;232:154-159.)
© RSNA, 2004

Experimental Studies

Minimizing Central Bile Duct Injury during Radiofrequency Ablation: Use of Intraductal Chilled Saline Perfusion—Initial Observations from a Study in Pigs1

Steven S. Raman, MD, Donya Aziz, MD, Xinlian Chang, MD, Ming Ye, MD, James Sayre, MD, Charles Lassman, MD and David S. K. Lu, MD

1 From the Departments of Radiology (S.S.R., D.A., X.C., M.Y., J.S., D.S.K.L.) and Pathology (C.L.), David Geffen School of Medicine at UCLA, 10833 Le Conte Ave, Los Angeles, CA 90095-1721. Received February 13, 2003; revision requested May 1; final revision received October 15; accepted December 10. Supported in part by Radiotherapeutics, Mountain View, Calif. Address correspondence to S.S.R. (e-mail: sraman@mednet.ucla.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine whether intraductal perfusion with chilled saline reduces thermal injury to bile ducts during radiofrequency (RF) ablation.

MATERIALS AND METHODS: In swine, anesthesia was induced and the common bile duct was surgically cannulated with a pediatric feeding tube. RF thermal lesions were created adjacent to bile ducts by using an expandable-hook 2-cm RF electrode and 90-W generator. In three pigs, chilled saline was perfused through the ducts at 1.5 L/h (26 mL/min), and in another pig, room-temperature saline was perfused at the same rate. In three pigs (control group), RF lesions were created without perfusion. After 48 hours, animals were sacrificed. Periductal sections from all animals were reviewed by a liver pathologist. The degree of injury to biliary epithelium and subepithelial glands was assessed on a scale of 0%–100%. Significance of differences between degrees of injury was assessed with the Mann-Whitney test.

RESULTS: In the control group, there was a mean of 100% injury to biliary ductal epithelium and 99.3% to subepithelial ductal glands. In the room-temperature saline group, there was a mean of 100% biliary epithelial injury and 84.4% glandular injury. In the chilled saline group, there was a mean of 52.9% ductal epithelial injury and 12.1% subepithelial glandular injury. In comparison with the control group, there was significantly less (P < .05) thermal injury to biliary epithelium in the chilled saline group and to subepithelial glands in both the room-temperature and chilled saline perfusion groups.

CONCLUSION: RF-induced bile duct injury may be decreased significantly with an intraductal infusion of chilled saline.

© RSNA, 2004

Index terms: Animals • Bile ducts, therapeutic radiology, 76.1299 • Liver, effects of irradiation on • Liver neoplasms, therapeutic radiology, 761.1299 • Radiofrequency (RF) ablation, 761.1299


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Radiofrequency (RF) ablation is a promising, minimally invasive technique for the treatment of primary hepatocellular carcinoma and hepatic metastases primarily from colon adenocarcinoma. Although rates of major complication are low when ablation is performed by physicians experienced with this procedure (1–8), lesions have to be carefully chosen for ablation since unintended thermal injury may occur in adjacent structures and organs. Ablation of peripheral lesions may injure diaphragm, gallbladder, stomach, colon, or small bowel (9–11). Ablation of central lesions is generally contraindicated because of the risk of injury to the major bile ducts. Reported cases of biliary strictures and bile leaks are known (9–11). In one prior study (12), percutaneous intraductal chilled saline was used during RF ablation of central hepatic lesions. Although no clinically apparent biliary complications were reported in that clinical case series, pathologic correlation was not performed. Thus, the purpose of our study was to determine whether intraductal perfusion of chilled saline reduces thermal injury to bile ducts during RF ablation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals and Surgical Preparation
Approval for this study was obtained from the animal institutional review board. Seven Yorkshire pigs weighing an average of 34 kg (range, 30–39 kg) were used, and all procedures were performed with the animals under general anesthesia. The number of animals used was based on our experience with prior porcine studies. No power calculation was performed, since no prior data with regard to thermal ductal injury in pigs were available. Induction of anesthesia was achieved with an intramuscular injection of 150 mg of ketamine hydrochloride (Ketaset; Animal Health, Fort Dodge, Iowa) and 150 mg of xylazine sterile solution (Butler, Columbus, Ohio). A nasogastric tube was inserted to help decompress the stomach. The animals were then intubated, and 0.5%–1.5% halothane (Fluothane; Halocarbon Laboratories, River Edge, NJ) was administered via endotracheal tube at a rate of 5 L/min.

All procedures were performed in a dedicated animal surgery laboratory. The animals were placed in the supine position after adequate anesthesia was achieved; the right upper quadrant and epigastrium were shaved, and the surface was sterilized. Both thighs were shaved, and grounding pads were placed bilaterally. Two surgeons (X.C., 15 years of experience; M.Y., 30 years of experience) together performed a midline laparotomy and dissected the common bile duct within the hepatoduodenal ligament. An 8-F pediatric feeding tube (Vygon, Ecouen, France) was used to cannulate the bile duct. The feeding tube served as a guide to identify the bile duct in these pigs at ultrasonography (US), since these ducts tend to rapidly taper and then become difficult to discern even at intraoperative US. After the intraoperative ablation procedure, the choledochotomy was closed with sutures by the surgeons.

Ablation Procedure
Three pigs served as control animals. In these animals, the bile ducts were cannulated, but no saline was infused intraductally. A 15-gauge RF expandable-hook needle electrode (LeVeen; Radiotherapeutics, Mountain View, Calif) was used for lesion creation in all seven animals. This needle electrode is equipped with eight retractable curved distal hooks, or tines. When fully expanded, these hooks assume an umbrella shape, 2 cm in maximum diameter, perpendicular to the long axis of the probe. In normal pig livers, this electrode creates a discoid lesion perpendicular to the long axis of the probe (10). A 90-W monopolar RF generator (RF 2000; Radiotherapeutics, Sunnyvale, Calif) was used as the energy source. With US guidance, the needle electrode tip was positioned approximately 1 cm from the central ducts and, when expanded, the tines were within 5 mm of the targeted central bile ducts. The ducts were easily targeted, since the internal feeding tube was easily visualized. The tines were expanded and positioned 5 mm from the targeted duct, and several overlapping periductal thermal lesions were created in each animal. From prior experience, we knew that liver anatomy in Yorkshire pigs is variable even when controlled for age and size. In these seven animals, the length of the common duct was variable, as was the diameter of the branch hepatic ducts. In each animal, we used the length of the common duct and diameter of the branch ducts at US as a guide, since these factors determined how many thermal periductal lesions could be created. In animals with a short common duct and acutely tapering branch hepatic ducts, a smaller number of lesions were created. In animals with a longer common duct and larger diameter of the branch hepatic ducts, a larger number of lesions were created.

To ensure the relative consistency of intraductal temperature in both control and perfused animals, the internal ductal temperature was measured just prior to ablation within the bile ducts by using a wire-tipped thermistor inserted alongside the pediatric feeding tube toward the planned site of ablation. The thermistor was withdrawn before ablation to prevent potential thermally induced damage.

In the three control animals, no saline infusion was used during the creation of overlapping periductal RF lesions. In the three animals undergoing intraductal infusion with chilled saline, the saline temperature ranged between 6° and 8°C. The saline was perfused through the bile ducts at 1.5 L/h (26 mL/min) by using a programmable infusion pump (Colleague CX; Baxter, Deerfield, Ill). Saline perfused the targeted bile ducts and then flowed into the peritoneal cavity via the common duct incision site, where it was evacuated with continuous suction. The perfusion rate of 26 mL/min (1.5 L/h) was determined empirically. We settled on this rate because it consistently achieved an intraductal temperature of 6°–8°C while producing a controlled peritoneal spill that could be expediently evacuated with intraoperative suction to minimize spill of bile and chilled saline into the peritoneal cavity (which would risk peritonitis and volume overload, respectively).

In the one animal undergoing intraductal infusion with room-temperature (25°C) saline, the infusion pump was also set to a rate of 26 mL/min. Intraductal temperatures were recorded at the planned site of ablation after the electrode tines were fully deployed and withdrawn. For RF lesion creation, generator power output was initially set at 30 W and was titrated manually upward to 70–80 W to maintain maximal power without an increase in impedance for at least 5 minutes in the first cycle. Thereafter, impedance was allowed to increase rapidly ("roll off"), with automatic power adjustment, until power output was terminated. At US, an echogenic "cloud" enveloped the entire area at the end of the ablation session, as described previously (10). A second cycle was then performed with initial power at 60% of the maximal power in the first cycle, titrated to impedance, and roll-off was achieved generally at 3–5 minutes.

In the three pigs that served as control animals, 17 overlapping periductal RF lesions were created (pig 1, three lesions; pig 2, eight lesions; pig 3, six lesions). In the animal (pig 4) whose bile ducts were perfused with room-temperature saline, four overlapping RF lesions were created. In the three animals that underwent intraductal infusion of chilled sterile saline, 18 overlapping periductal RF lesions were created (pig 5, four lesions; pig 6, six lesions; pig 7, eight lesions).

Sacrifice and Tissue Evaluation
The animals were sacrificed 48 hours after lesion creation and, at postmortem examination, the liver and common duct were harvested and placed in formalin for 2–3 days. Along the length of the common duct and central intrahepatic ducts, a confluent periductal mass of thermally ablated tissue was present (in all groups). Individual periductal lesions could not be discretely identified at postmortem examination. The liver was subsequently sectioned in the transverse plane, perpendicular to the long axis of the common and branch ducts, in regions of periductal thermal injury. The green bile duct was easily identified (visually) in the surrounding thermally ablated tissue; the ablated tissue was of characteristic ovoid spherical shape, with a pale tan central color and a trilaminar border. The central bile ducts (0.2–0.5 cm in diameter) were identified, and cross sections were obtained of the duct and surrounding ablated tissue at 0.5–1.0-cm intervals. The number of sections did not match the number of lesions created, because of the confluent nature of the periductal thermal lesions and variability in porcine anatomy with respect to bile duct length and branching. The sections were processed for histologic examination, and representative subsections stained with hematoxylin-eosin were mounted on slides. A dedicated liver pathologist (C.L., 12 years of experience) graded the percentage of circumferential thermal ductal injury (coagulative necrosis to both the biliary epithelium and the subepithelial ductal glands) on a scale with 10% increments of thermal circumferential injury (range, 0%–100%).

Statistical Analysis
The significance of differences in degree of histologic thermal injury (as determined by the pathologist) to bile ducts in the control group, the room-temperature saline perfused group, and the chilled saline perfused group was determined by using both one- and two-tailed Mann-Whitney tests. A P value less than or equal to .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
In the three control animals, the thermal lesion typically invaginated approximately 50% of the bile duct but did not affect the portal vein and hepatic artery (Fig 1a). Seventeen representative histologic sections were reviewed from the nonperfused group (Table 1), in which bile duct diameters ranged from 0.2 to 0.5 cm. Just prior to RF ablation, the intraductal temperature in this group had been 35°C. Histologically assessed thermal injury to both the biliary ductal epithelium and underlying subepithelial ductal glands was uniformly near 100%. Thermal injury was severe in all bile ducts less than 0.5 cm in diameter (Fig 1b, 1c).



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  		Figure 1a. Images of typical central bile ducts in control (nonperfused) animal after periductal RF ablation. (a) Photograph of gross specimen demonstrates a typical RF lesion (arrows) encompassing 50% of the ductal circumference. (b) Medium-power photomicrograph shows diffuse pink staining suggestive of coagulative necrosis of a large bile duct, the associated biliary glands, and connective tissue fibroblasts. (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of a large bile duct shows coagulative necrosis of the surface epithelium and the immediately adjacent connective tissue cells. (Hematoxylin-eosin stain; original magnification, x400.)

 


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  		Figure 1b. Images of typical central bile ducts in control (nonperfused) animal after periductal RF ablation. (a) Photograph of gross specimen demonstrates a typical RF lesion (arrows) encompassing 50% of the ductal circumference. (b) Medium-power photomicrograph shows diffuse pink staining suggestive of coagulative necrosis of a large bile duct, the associated biliary glands, and connective tissue fibroblasts. (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of a large bile duct shows coagulative necrosis of the surface epithelium and the immediately adjacent connective tissue cells. (Hematoxylin-eosin stain; original magnification, x400.)

 


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  		Figure 1c. Images of typical central bile ducts in control (nonperfused) animal after periductal RF ablation. (a) Photograph of gross specimen demonstrates a typical RF lesion (arrows) encompassing 50% of the ductal circumference. (b) Medium-power photomicrograph shows diffuse pink staining suggestive of coagulative necrosis of a large bile duct, the associated biliary glands, and connective tissue fibroblasts. (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of a large bile duct shows coagulative necrosis of the surface epithelium and the immediately adjacent connective tissue cells. (Hematoxylin-eosin stain; original magnification, x400.)

 

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  		TABLE 1. Histologic Thermal Injury in Nonperfused (Control) Animals

 
In the animal that underwent RF thermal ablation with ductal perfusion with room-temperature normal saline (25°C), eight representative samples were analyzed (Table 2). At gross inspection, the ablation lesion was similar to those in the control group, and thermal lesions invaginated approximately 50% of the bile duct (Fig 2). The bile ducts were measured at gross inspection and ranged in diameter from 0.2 to 0.5 cm. At histologic examination, there was 100% circumferential injury to the biliary ductal epithelium and an average of 84% circumferential injury to underlying ductal glands. There was no significant difference (two-tailed Mann-Whitney test, P > .05) in the degree of ductal epithelial injury between the group of pigs perfused with room-temperature saline nonperfused (control) group. There was slightly less histologically graded injury (P < .05) in underlying ductal subepithial glands in the group perfused with room-temperature saline compared with the nonperfused group.


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  		TABLE 2. Histologic Thermal Injury in Animal Perfused with Room-Temperature (25°C) Saline Solution

 


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  		Figure 2. Photograph of gross specimen obtained from a pig in the group perfused with room-temperature saline shows a typical lesion (arrow), very similar to that in the nonperfused control animal, encompassing 50% of the ductal circumference.

 
Among the three animals that underwent intraoperative RF ablation with intraductal infusion of chilled normal saline, 14 representative sections were histologically graded (Table 3). Just prior to RF ablation, the intraductal temperature after chilled saline perfusion had a range of 6°–8°C in this group. On gross inspection, the thermal lesions extended to the bile ducts but did not completely invaginate around the ducts as had those in the nonperfused and room-temperature perfused groups (Fig 3a). In bile ducts between 0.2 and 0.5 cm in diameter, the mean severity of thermal injury was 52.9% to the ductal epithelium and 12.1% to ductal subepithelial glands (Fig 3b, 3c). On visual inspection, the epithelial glands were variably intact, although nuclear atypia was present in nearly all specimens. Compared with the degree of thermal injury in the nonperfused (control) group, there was significantly less (P < .005) thermal injury to both biliary epithelium and subepithelial ductal glands in the group perfused with chilled saline. Despite the use of chilled saline perfusion, all smaller ducts (<0.2 cm) that could be visualized were nearly completely ablated.


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  		TABLE 3. Histologic Thermal Injury in Animals Perfused with Chilled (6°-8°C) Saline Solution

 


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  		Figure 3a. Images of typical periductal RF lesion from ablation after chilled saline perfusion. (a) Photograph of gross specimen shows much less circumferential involvement of the bile duct (arrow), suggesting a partial heat sink effect. (b) Medium-power photomicrograph shows a viable large bile duct, associated biliary glands, and connective tissue cells (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of large bile duct shows viable surface epithelium, biliary glands, and fibroblast nuclei. Note the reactive appearance in surface epithelium, characterized by increased nuclear size, irregular cytoplasm, and occasional apoptotic-appearing nuclei. (Hematoxylin-eosin stain; original magnification, x400.)

 


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  		Figure 3b. Images of typical periductal RF lesion from ablation after chilled saline perfusion. (a) Photograph of gross specimen shows much less circumferential involvement of the bile duct (arrow), suggesting a partial heat sink effect. (b) Medium-power photomicrograph shows a viable large bile duct, associated biliary glands, and connective tissue cells (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of large bile duct shows viable surface epithelium, biliary glands, and fibroblast nuclei. Note the reactive appearance in surface epithelium, characterized by increased nuclear size, irregular cytoplasm, and occasional apoptotic-appearing nuclei. (Hematoxylin-eosin stain; original magnification, x400.)

 


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  		Figure 3c. Images of typical periductal RF lesion from ablation after chilled saline perfusion. (a) Photograph of gross specimen shows much less circumferential involvement of the bile duct (arrow), suggesting a partial heat sink effect. (b) Medium-power photomicrograph shows a viable large bile duct, associated biliary glands, and connective tissue cells (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) High-power photomicrograph of large bile duct shows viable surface epithelium, biliary glands, and fibroblast nuclei. Note the reactive appearance in surface epithelium, characterized by increased nuclear size, irregular cytoplasm, and occasional apoptotic-appearing nuclei. (Hematoxylin-eosin stain; original magnification, x400.)

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Both large- and medium-sized hepatic blood vessels, as well as a small amount of surrounding tissue, appear to be protected from thermal coagulation necrosis (13); this is achieved by vascular dispersal of the deposited thermal energy produced from ionic agitation at low-frequency RF ablation (15–17). Clinically, this has been termed the "heat sink" effect. One may postulate, on the basis of this phenomenon, that larger bile ducts may be protected from thermal injury by potential heat dispersal through biliary flow and blood flow in the adjacent hepatic artery and portal vein. In our study, we histologically demonstrated that RF thermal ablation in close proximity to central bile ducts causes substantial transmural thermal injury, that results in coagulation necrosis. However, protection through high rates of flow in the adjacent portal vein and hepatic artery was not observed in larger bile ducts. This may be related, in part, to the much slower rate of biliary flow. In several reports (1–11), concern regarding injury to bile ducts and resulting complications has limited aggressive treatment of central lesions, especially those near the porta hepatis. Biliary tract complications, including bile leaks and bile duct strictures, have been reported after thermal ablation (9–11).

Central lesions may be more aggressively ablated by using ductal perfusion with chilled saline. Saline may conceivably be used for ductal perfusion by using either a nasobiliary tube or a percutaneous transhepatic catheter. In a study of three patients, Dominique and colleagues (12) sought to minimize intraoperative RF ablation–induced thermal biliary injury by performing open intraoperative choledochotomy, catheter insertion, and continuous perfusion of the intrahepatic bile ducts with chilled Ringer solution. In all three patients, intraoperative RF ablation was performed within 0.5 cm of a central biliary ductal branch. These three patients were followed up clinically for 3 months and did not show signs or symptoms of biliary stricture. No stricture was demonstrated on follow-up magnetic resonance (MR) images obtained at 3 months. However, assessment of potential ductal injury by means of conventional or MR cholangiography or histologic evaluation was not performed. No assessment of tumor recurrence was performed in that study.

In our preliminary study, we demonstrated that chilled saline perfusion of the larger central bile ducts helped to significantly reduce the magnitude of thermal biliary ductal damage. The larger central bile ducts were likely protected, in part, by a heat sink effect, a phenomenon partially influenced by the flow rate and temperature of the perfused saline. In our study, we observed histologically less complete periductal thermal injury in the chilled saline group. Elvin et al (14) demonstrated a cuff of normal periductal liver (ie, thermal sparing) when the bile ducts were perfused with fluid at a lower temperature (4°C) and higher flow rates (2 L/h). These variables require more rigorous study and were not the focus of our study; however, we did observe that intraductal perfusion with room-temperature saline at equivalent flow rates offered little ductal epithelial thermal protection and produced no gross change in the periductal morphology of thermal lesions. In the clinical setting, the need for bile duct protection must be carefully balanced to avoid creation of a large heat sink that will limit tumor cell death. Parameters for the temperature and rate of intraductal saline infusion must to be adjusted accordingly.

Even with the use of intraductal chilled saline, the potential for substantial biliary injury remains, especially because chilled saline must be carefully directed to perfuse major ducts adjacent to thermally ablated lesions. Although there was significantly less thermal damage to the bile ducts in the chilled saline group than in the control group, a variable degree of protection was observed between animals. Perhaps alternate forms of intraductal temperature monitoring during RF ablation would help minimize variation in ductal thermal injury.

The degree of thermal injury to ductal subepithelial glands was consistently less severe than that to ductal epithelium for both the room-temperature saline infusion group and the chilled saline infusion group. Although this suggests that subepithelial glands are more resistant to thermal injury than are ductal epithelial cells, the implications for chronic ductal injury and stricture formation require further study. A chronic in vivo bile duct injury model will be necessary to determine whether decreased acute epithelial and subepithelial glandular injury decreases the incidence of biliary strictures.

This study was preliminary in nature and has limitations. First, we examined only the acute effects of chilled saline infusion during RF ablation. No conclusions about long-term clinical implications can be reached without additional study. Second, although we did demonstrate that intraductal chilled saline infusion protected biliary epithelium and subepithelial glands against thermal damage, we did not account for the variable nature of such protection. This variability may in part reflect greater degrees of histologic thermal injury in regions of overlap along the course of the bile duct. This effect was difficult to analyze because no changes were grossly evident; we saw only a confluent thermal lesion encompassing the common duct and branch ducts. However, this effect was present in all three groups, since the techniques were similar. This variability may also be related in part to our learning curve in performing the procedure, since perfusion experiments were performed in only four animals. However, further study will be necessary to refine the technique. Third, intraductal temperature monitoring was not performed during RF ablation because of the lack of a suitable thermistor that can withstand heating. This may be clinically relevant because balancing thermal protection against the heat sink effect will likely require knowledge of intraductal temperatures. Fourth, although chilled saline perfusion rate and temperature were held constant, an optimal temperature and flow rate were not demonstrated. Fifth, a rigorous evaluation of heat sink–related periductal thermal sparing was not performed, since the focus of the study was on limiting ductal injury. Finally, applicability of porcine data to humans is limited and requires further study.

In summary, we have demonstrated in a porcine model that RF ablation in close proximity to the bile ducts causes substantial biliary injury and that intraductal perfusion with chilled saline during RF ablation may significantly decrease the degree of histologic biliary ductal injury.

Practical application: Limiting thermal injury to central bile ducts via an intraductal chilled saline perfusion may allow more aggressive thermal ablation of central hepatic lesions.


   ACKNOWLEDGMENTS
 
The authors thank Julia Fendrick, BS, for her invaluable assistance in the manuscript preparation.


   FOOTNOTES
 
Abbreviation: RF = radiofrequency

Author contributions: Guarantors of integrity of entire study, S.S.R., D.S.K.L.; study concepts and design, S.S.R., D.S.K.L., C.L.; literature research, S.S.R.; experimental studies, S.S.R., D.A., X.C., M.Y.; data acquisition, S.S.R., D.A., X.C., M.Y.; data analysis/interpretation, S.S.R., D.A., D.S.K.L., C.L.; statistical analysis, J.S.; manuscript preparation and definition of intellectual content, S.S.R.; manuscript editing, revision/review, and final version approval, S.S.R., D.S.K.L.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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