Brief Report

Multipolar radiofrequency ablation in controlling hemorrhage from blunt Liver trauma^?

Li Yekuo MD^a,?, Wang Shasha PhD^a, Huo Feng PhD^b

^aDepartment of Ultrasound, Liuhuaqiao Hospital, Guangzhou 510010, China

^bDepartment of Hepatobiliary Surgery, Liuhuaqiao Hospital, Guangzhou 510010, China

Received 27 January 2008; accepted 31 January 2008

Abstract

Objective: The aim of this study is to investigate the use of multipolar radiofrequency (RF) ablation with internally cooled electrodes to control hemorrhage percutaneously from blunt liver trauma.

Methods: Blows were used to 10 heparinized and anesthetized domestic pigs, resulting in blunt liver trauma. Eight pigs were percutaneously treated by using multipolar RF ablation with internally cooled electrodes. Two pigs were not treated (control group). The treated pigs were killed humanely 2 hours after the treatment.

Results: Blunt liver trauma was successfully produced by the application of abdominal impact in all pigs. Hemostasis was achieved in all treated pigs with 8.5 +- 4.5 minutes of RF ablation treatment. No delayed hemorrhage, bile leakage, pus, or other fluid was found in the livers in all treated pigs when they were killed 2 hours after the treatment.

Conclusions: Multipolar RF ablation with internally cooled electrodes is effective in producing hemostasis percutaneously by direct treatment of injured parenchyma in blunt liver trauma.

(C) 2009

Introduction

Radiofrequency (RF) electrode with monopolar system was effective to achieve hemostasis in liver trauma in Animal experiments [1]. However, it has some limitations. Firstly, second or more RF treatment must be performed if the volume of injured liver exceeds 4 cm because the diameter of the monopolar RF ablation zones usually does not exceed 4 cm [2]. Secondly, unpredictable electrical current paths between the ablation electrode and grounding pad may lead to heterogeneous energy deposition and to eccentric ablation zones or even collateral damage. Skin burns at the grounding

^? Our work was supported by the Natural Science Foundation of Guangdong Province of China (06019712).

* Corresponding author. Tel.: +86 20 36653450.

pad have been reported in some instances [3]. Finally, RF has not been used in Blunt hepatic trauma, which is more difficult and complicated to treat than penetrating one. One of the main causes is that it is difficult to rapidly guide the accurate insertion of RF electrodes into the bleeding sites in blunt liver traumas.

In recent years, advancement in RF ablation device has allowed it to be more effective in treating liver trauma than the traditional one. Radiofrequency ablation devices have developed from the monopolar system to the bipolar and multipolar system [4]. Multipolar RF ablation with internally cooled electrodes is the recently developed RF ablation device. No grounding pad is required, and the electrical current runs between up to 6 electrodes and up to 15 possible electrode combinations within and closely around the lesion. Because the energy is focused on the target zone, more

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homogeneous energy deposition and larger ablation zones should be possible. In addition, internally cooled tip electrodes capable of distributing the heat deeper in the tissue result in larger ablatED volumes.

Advancement in medicine imaging technology has made RF ablation possible to percutaneously treat blunt hepatic trauma. Low-mechanical index, contrast-enhanced ultraso- nography (CEUS) is based on the ability of microbubbles containing gases to produce real-time, contrast-related, gray- scale images. It has been largely used in the evaluation of focal liver lesions. In recent years, it has also been used to improve sonography accuracy in detecting parenchymal injury after blunt abdominal trauma, and the sites of hemorrhage from injured liver can be clearly detected by CEUS in real time [5-8].

The aim of this study was to report the successful application of percutaneous multipolar RF with internally cooled electrodes under the guidance of CEUS in controlling hemorrhage in blunt liver trauma in pigs.

Methods

This study was performed in 10 healthy Guangzhou domestic pigs weighing 37 to 45 kg. All procedures were conducted in accordance with the guidelines of the National Institutes Health for use of laboratory animals with the approval of the Liuhuaqiao Hospital’s Institute of Animal Care and Use Committee. The animals were initially anesthetized with ketamine hydrochloride (50 mg/kg) by Intramuscular injection. Additional injections with 2% pentobarbital (0.25 mg/kg) were conducted to maintain effective anesthesia for at least 2.5 hours. They were intubated and ventilated with oxygen and 1% to 2% isoflurance, with the concentration varied to maintain normal vital signs. Femoral vein and artery catheters were introduced for blood sampling and arterial pressure monitor- ing. The femoral artery catheter tip was advanced into the abdominal aorta. Electrocardiogram leads were attached for monitoring. Intravenous fluid was administered at a main- tenance rate of approximately 3 mL/kg per hour throughout the study. The pigs were heparinized before injury with an Intravenous bolus of 200 U/kg followed by a continuous infusion of 50 to 75 U/kg per hour. The purpose of the heparin was to create a state to facilitate ongoing bleeding, thus permitting more effective evaluation of the hemostatic technique under adverse conditions. Blood samples were taken before heparin was given, after the heparin bolus, after the injury, and then at hourly intervals. These were taken to measure partial thromboplastin time. Intravenous saline was administered during the study when systolic blood pressure fell to less than 70% below the baseline pressure.

Blunt liver trauma was produced following a technique reported by Cohn et al [9]. A nail-driving gun (SDQ307, Nanshan, Sichuan, China) was modified to impact the pigs to

produce the animal models with blunt liver trauma. The muzzle of the gun was placed and fired against an iron cylinder 2 cm in diameter and 2 cm thick (weight, 300 g). The gun was loaded with the S5 (5.6 x 16.0 mm) charge. The iron cylinder was positioned and oriented in the preferable direction on the abdomen in the upper quadrant over the region of the liver using Ultrasound imaging, and then the gun was fired.

After the impact, the pigs remained monitored in the operation room and were supported with Fluid replacement and epinephrine. Two pigs were left untreated as control group to determine the severity of the injuries. To test the efficacy of RF ablation in controlling hemorrhage after the liver injury, we inserted the electrodes into the injured site under the guidance of CEUS, and then the tissue ablation procedure was started. A laparoscope (Olympus VISERA OTV-S7) was used to monitor the dynamic changes of the livers during the RF ablation treatment.

A multipolar RF generator (Celon Power, Berlin, Germany) that provided a maximum power output of 250 W was used for the treatment. It can simultaneously operate up to 3 internally cooled (with 30 mL/min of normal saline solution) bipolar coagulation probes with an active tip length of 20, 30, or 40 mm. The bipolar probes have a diameter of

1.8 mm (15F) and a shaft length of 10 to 25 cm. When one bipolar application was connected to the RF generator, the energy applied was in a bipolar mode. When 2 or 3 bipolar applicators were connected, the RF operation was in a multipolar mode [10]. Radiofrequency ablation can be performed with 1, 2, or 3 probes, depending on the lesion size, shape, location, and accessibility. If 2 or 3 probes are used simultaneously, the probes should run parallel, and the distance between the probes should not be less than 5 mm or greater than 30 mm. The power output was set according to the total length of the active tips (1.0 W/mm). The needle electrodes were inserted in the bleeding sites. In this way, the area around the electrodes was gradually coagulated. A session was stopped when the operator’s judgment was that the bleeding from this part of the injury was controlled.

Contrast-enhanced ultrasonography was performed using sulfur hexaflouride microbubbles (SonoVue, Bracco, Italy). Contrast-specific software (Contrast Pulse Sequencing, CPS, Siemens Acuson, USA) in a continuous mode with low mechanical indexes (0.18-0.21) was used for all the examinations. Generally, a 1.2-mL intravenous bolus injec- tion of SonoVue was made, always followed by a flush of

5.0 mL of saline. Contrast-enhanced ultrasonography was performed to detect the injured livers 5 minutes after the impact. As soon as the damaged lesion was found, the RF electrodes were inserted percutaneously into the bleeding sites under the guidance of the CEUS.

Each pig was observed under general anesthesia for 2 hours after the RF ablation treatment. For the killing of the pigs, a dose of 1.0 g thiopenbtal was administrated under general anesthesia. After death of the pigs, the liver was harvested, and ex vivo cholangiography and angiographies through the portal vein and hepatic artery were performed.

The remaining blood in the peritoneal cavity was collected and estimated total blood loss.

Results

Blunt liver trauma was effectively produced by the application of the abdominal impact. A stellate Liver laceration (3.0-6.5 cm long, 2.5-4.5 cm deep) was found in one lobe in all pigs. Active bleeding from the liver fractures in each pig was observed through CEUS and laparoscopy. Other Organ injuries seen included internal bleeding in the left lung (n = 3) and bowel ecchymosis (n = 2). In all pigs, the arterial blood pressure dropped within 25 seconds of impact. In 6 of these, the blood pressure spontaneously recovered within a few minutes to near baseline. The blood pressure then later fell as blood was lost. In 2 pigs, the blood pressure dropped to

zero shortly after the impact; the electrocardiogram showed sinus rhythm. It was necessary to briefly give external cardiac massage until pressure pulsation was obtained.

One probe was used in 1 of the 8 ablations, 2 probes were used in 5 ablations, and 3 probes were used in 2 ablations. In ablation performed with more than one probe, the mean distance between the probes was 22 mm (range, 9-28 mm). The mean puncture time per liver trauma was 5.5 +- 2.3 minutes (range, 2-9 minutes). The mean total ablation time was 8.5 +-

4.5 minutes (range, 4.2-16 minutes). The mean total energy was 86 +- 51 kJ (range, 16-150 kJ) per treatment. The mean ablation zone volume was 55 +- 23 mL (range, 36-96 mL).

Under the guidance of CEUS, RF probes were accurately inserted into the bleeding sites of the livers (Fig. 1A, B). With increase of temperature, the bleeding from the liver began to coagulate, resulting in an accumulation of bubbles. Then, the speed of bleeding decreased slowly. The blood flow from the ruptured liver formed a layer of coagulated blood covering

Fig. 1 Photographs of the blunt liver trauma experiments. A, Hemorrhage was detected by CEUS (arrow 1), and the RF ablation electrodes (arrows 2 and 3) were successfully inserted into the right sites of the damaged liver under the guidance of CEUS. B, Hemorrhage (white arrow) from the liver fractures (black arrow) was observed by the laparoscopy after the impact. Two bipolar applicators were inserted into the damaged site of the liver. C, The hardened coagulated blood (white arrow) sealed off the disrupted surface of the liver 9.5 minutes after the RF ablation treatment. D, A photograph of gross pathology: the damaged tissues were coagulated (black arrow) and the coagulated blood sealed up the internal fractures (white arrow).

the damaged site of the liver (Fig. 1C). The tissues around and between the electrodes were coagulated gradually (Fig. 1D). In this way, the successful hemostasis was achieved for the damaged liver in all the cases in the treatment group. In 3 cases, hemorrhage from the ruptured hepatic veins 4 mm in diameter was also stopped by the heat of the electrodes.

Two hours after the RF ablation treatment, all cases in the treatment group stayed alive, and no delayed hemorrhage, bile leakage, pus, or other fluid was found in the abdomen at killing. Their arterial systolic blood pressure increased gradually near the baseline after the RF ablation and remained stable 2 hours after the RF ablation. The blood loss was 120 to

250 mL in the treatment group. The total infused fluid averaged 2.1 +- 0.8 L from the beginning of the operation until the end of the postoperative period of observation. The hourly administration rate averaged 16.6 +- 5.8 mL/kg per hour. Despite the fluid replacement therapy and the epinephrine administrated, the control group pigs presented sign of hemorrhagic shock and died 50 minutes after the liver injury. Blood loss was 550 and 620 mL, respectively.

The partial thromboplastin time values (averaging 180 +- 41 seconds) were obviously higher than in baseline (25 +- 6 seconds) throughout the observation period. It indicated that coagulation was significantly impaired in these pigs and may have contributed to the bleeding found at laparotomy.

Discussion

Because of its large size and location, the liver is easy to be injured. motor vehicle accidents are the most common causes of blunt hepatic injuries [10]. The treatment of blunt liver traumas has changed in the past years toward Nonoperative management [11,12]. Although severe liver injuries are more often treated nonoperatively, they may require resuscitation and several interventions to achieve hemostasis [13]. Radiofrequency ablation is a relatively new method of controlling bleeding from the injured liver. Its hemostatic effect originates from protein denaturation, vessel wall injury, coagulation of the blood proteins, and formation of an occlusive coagulum, which are produced by the increase of the tissue temperature it causes [14].

The limited coagulation zone size is a crucial issue in local thermoablative treatment of hepatic trauma and liver tumor. Several new RF ablation techniques have been developed in an attempt to increase the coagulation volume. One such approach is multipolar RF ablation with internally cooled electrodes. The theoretical benefit of the use of the multipolar technique has been demonstrated in an experi- mental setting [4]. Clasen et al [4] presented the report about multipolar RF ablation with internally cooled electrodes with 3 probes and showed that maximum ablation volume of 132 cm³ were achievable in ex vivo bovine liver.

The first important step in RF ablation treatment of blunt liver traumas is to guide the accurate insertion of the

electrodes into the right sites of injured livers. Baseline sonography is often used to guide RF ablation of liver tumors with sensitivity to the tumors in real time, but its sensitivity in direct demonstration of abdominal solid organ injury is lower [15]. Therefore, it is not wise to use baseline sonography to guide the insertion of RF ablation needles in the treatment of blunt liver traumas. Because CEUS is based on the capability of demonstrating real-time and contrast-related images through microbubbles produced, it can detect the injured parenchyma and the site of active bleeding clearly. It is a useful tool in the evaluation of blunt liver traumas, being more sensitive than baseline sonography. On these grounds, we used CEUS to guide the insertion of RF ablation needles into the exact sites of the bleeding from the injured liver. In fact, we succeeded in inserting the RF needles into the desired regions in all the cases to produce real-time and contrast- related images of the injured hepatic tissue.

Our results demonstrate that percutaneous multipolar RF ablation with internally cooled electrodes is efficacious in treating blunt liver trauma in pigs and may have a significant potential to be and effective treatment for human injury. To stop the hepatic hemorrhage effectively, the bipolar applica- tors should be inserted into the sites of the damaged liver and be placed in a right array to ensure all the injury area can be ablated. To achieve a better hemostasis, it is very important for us to adjust the space and number of the electrodes according to the size and shape of the liver injury. The number and spacing of the bipolar applicators should vary according to the specific severity of the injury as we did in the experiment. Three probes produced larger coagulation zone size than 2 probes and 1 probe. Just because effective hemostasis was achieved, the volume of blood loss in the treatment group was less than that in the control group. Further evaluation of the technique needs to be performed to determine the size of lesion and size of ruptured vessel that can be treated.

Rebleeding, delayed hemorrhage, sepsis, bile leakage, and biliary fistulas are the most common complications after liver trauma. No clinically detectable complications were observed in any of the animals in our study 2 hours after RF treatment. In summary, CEUS-guided percutaneous multipolar RF ablation with internally cooled electrodes is effective in stopping hemorrhage from injuries in blunt liver traumas. However, in our study, it is not to be learned whether this method will be more advantageous than other treatment approaches. We feel further investigation is indicated both to refine it and to learn definitively how it compares with

other managements.

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