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ORIGINAL ARTICLES |
From the Departments of Surgery (WKW, GAH, RME, FGG), Radiology (GDD, VAM, DHN, LGH), and Pathology (REK, FES), University of Texas Health Science Center at San Antonio, San Antonio, Texas.
Correspondence: Address correspondence and reprint requests to: W. Kenneth Washburn, MD, University of Texas Health Science Center at San Antonio, Organ Transplantation MC 7858, San Antonio, TX 78229; Fax: 210-567-6608; E-mail: Washburn{at}uthscsa.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Methods: Five patients with advanced endstage liver disease scheduled to have orthotopic liver transplantation were enrolled in this study. After laparotomy and before hepatectomy, radiofrequency ablation was performed without and with hepatic blood flow occlusion. After hepatectomy, the liver was sectioned, the area of ablation was measured in three dimensions, and the volume of ablation calculated.
Results: Three of the patients had had previously placed transjugular intrahepatic portosystemic shunt. The mean volume of the ablation without blood flow occlusion was 22.5 ± 7.4 cm3 and that with blood flow occlusion was 48.4 ± 24.0 cm3 (P = .05).
Conclusions: Ablation area is increased significantly with hepatic blood flow occlusion in the human cirrhotic liver. This result may have application in the treatment of larger (>3 cm) hepatic malignancies.
Key Words: Radiofrequency ablation • Thermal injury • Cirrhosis • Hepatocellular carcinoma
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Radiofrequency (RF) ablation is an evolving treatment option for both primary and secondary hepatic neoplasms. One study of 169 ablated tumors in 123 patients reported a recurrence rate of only 1.8% at 15 months,1 yet others have reported a much higher rate of local recurrence. Tumor recurrence rates have been shown to be dependent on both the extent of tumor necrosis and the margin of ablation. A thorough understanding of the factors controlling these parameters is paramount in optimizing RF ablation as a treatment option for hepatic neoplasms.
Factors known to influence the size of ablation and the degree of tissue necrosis include the size of the electrode, the power output of the generator, the temperature along the electrode, the duration of ablation, and the inherent cooling effect of hepatic blood flow.2
Studies conducted on noncirrhotic livers have demonstrated that interrupting hepatic blood flow during an ablation by occluding the portal vein and the hepatic artery (Pringle maneuver) enlarged the volume of ablation.3 However, cirrhotic patients have altered hepatic blood flow and varices, which effectively diminish hepatic blood flow and shunt blood around the liver. To date, no studies have evaluated the impact of the interruption of hepatic blood flow on the thermal injury pattern during RF ablation in cirrhotic livers. This study was done to investigate whether interruption of hepatic blood flow during RF ablation in a cirrhotic liver will result in a significantly larger thermal injury than that observed in the unaltered blood flow state.
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MATERIALS AND METHODS |
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After admission to the hospital and while awaiting the donor liver, patients were offered the opportunity to participate in this study. The patient was informed of the associated risks, including prolongation of operating time, ground pad burn, and bleeding. Exclusion criteria included patients under 18 years of age, pregnancy or likelihood of pregnancy, evidence of primary or secondary hepatic neoplastic disease, the inability to self-consent, and fulminant hepatic failure.
The consenting patient was then taken to the operating room where, under general anesthesia, two standard grounding pads were placed on the patient’s back and two placed on the patient’s right leg. Liver transplantation then proceeded in a normal fashion. Once the liver was exposed, two RF ablations were performed. The first ablation was made with normal hepatic perfusion, whereas the second ablation was made while interrupting hepatic blood flow with a Pringle maneuver.
A Radionics (Radionics, Burlington, MA) 500-kHz, monopolar RF generator (Model CC-1) was used. A three-prong, parallel triangular cluster, internally cooled needle electrode with a 2.5 cm exposed tip (model #PE3-D[2.5]K) was selected. Sterile water cooled to 20°C was used as an electrode coolant.
Under ultrasound guidance, the electrode was inserted into the right lobe of the liver. The tip of the electrode was kept at least 3 cm from major blood vessels or the liver capsule to minimize the effect of these structures on the size and configuration of an ablation. The electrode was then cooled to steady-state and a 12-minute ablation was performed. On completion of the ablation, the electrode coolant was stopped and the electrode temperature was recorded at 1 minute after ablation. The electrode was then withdrawn.
The second ablation was performed in a similar fashion in another area of the right lobe of the liver while observing the same rules of electrode placement as for the first ablation. After insertion of the electrode, the hepatic artery and portal vein were cross-clamped (Pringle maneuver). Interrupted hepatic perfusion was confirmed both by blanching of the liver and by diminished portal venous and hepatic arterial flow by color Doppler. A 12-minute ablation was performed with identical RF parameters as the first ablation. Pringle maneuver was terminated after 3 minutes of ablation. The electrode coolant was stopped on completion of the ablation. As with the first ablation, the electrode temperature was recorded at 1 minute after ablation and then withdrawn.
The transplant then proceeded in standard fashion. The native liver was resected, placed on ice, and sent to surgical pathology for gross and histologic examination. The liver was sliced in a bread-loaf fashion at 0.5- to 1.0-cm intervals. Each ablation was measured in three dimensions and then prepared for histologic examination to evaluate for adequate tissue necrosis. Tissue blocks were fixed in formalin, embedded in paraffin, sectioned at 4 µm, and stained with hematoxylin and eosin. The examining pathologist was unaware of which ablation was performed with or without the Pringle maneuver. Student’s t-test was used to determine mean, standard deviation, and probability.
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RESULTS |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Radiofrequency thermal ablation uses an electric generator with an alternating current output in the range of 10 to 200 W. The frequency of the alternating electric current is in the RF range, approximately 500 kHz. As with any electric current, two leads are needed. An electrode serves as one lead and a grounding pad attached to the patient serves as the other. The electrode is placed in contact with the tissue to be ablated. As the electric current is applied, the adjacent ions within the tissue are electrically affected because they are electrically charged. They consequently begin to oscillate at the same frequency as the alternating electric current. These ions experience opposing frictional forces that subsequently liberate heat. This thermal energy elevates the ambient temperature around the electrode causing coagulation necrosis and cellular damage at temperatures between 50°C and 100°C.7
Pioneering work began in the early 1990s8,9 and efforts continue to elucidate the controlling variables in RF ablation of neoplastic tissue. The ultimate objective remains the same, to create an ablation large enough to establish a tumor-free margin. Factors influencing the size of an ablation include the size and shape of the electrode, power output of the generator, temperature along the axis of the electrode, and the inherent cooling effect of hepatic blood flow.10
To achieve a larger ablation, one can consider increasing the power output of the generator. With increasing power output, however, the tissue temperature immediately adjacent to the electrode rises rapidly. The tissue begins to boil and quickly desiccates. Consequently, tissue impedance is greatly increased and adversely affects the transfer of energy and subsequently the size of the ablation. By using electrodes with multiple prongs or clusters, one can create overlapping ablations fields that can be helpful in treating tumors up to 7 cm.11 Another concept that has proved effective is the use of a cooled-tip electrode. Coolant is passed through a double lumen electrode that maintains the temperature along the axis of the electrode at a relatively lower level. This helps minimize adjacent tissue desiccation and allows higher generator output, thereby creating larger ablations.
The size of a thermal ablation does not increase linearly to the time of the ablation. Thermal energy liberated by the electrode is dissipated radially by conduction. Therefore, the temperature of the surrounding tissue diminishes exponentially with increasing distance from the electrode. As the ablation continues, a steady-state temperature distribution is eventually achieved. Knowing that a temperature in excess of 50°C is needed to effect tissue necrosis, a curve can be created comparing the diameter of an RF thermal injury with the duration of ablation. Lorentzen12 demonstrated in the ex vivo calf liver that this curve asymptotically approaches a constant ablation diameter. Patterson et al.13 demonstrated a similar result in the in vivo porcine liver, finding that increasing the duration of ablation from 5 to 20 minutes had no affect on lesion diameter.
In addition to the radially dissipated conductive heat transfer described above, in vivo ablations are associated with a convective heat transfer provided by hepatic blood flow through both the portal venous and hepatic arterial systems. The inherent cooling effect of hepatic blood flow and the associated limiting effect on the size of a RF thermal ablation has been clearly established. Pharmacologic manipulation of hepatic blood flow can affect the ablation size. Porcine hepatic vasoconstriction induced with vasopressin results in a significantly larger ablation than that achieved with normal porcine hepatic blood flow.14 Patterson et al.13 demonstrated that an interruption of hepatic blood flow by cross-clamping the portal vein and hepatic artery during an ablation in the porcine liver significantly increased the size of thermal injury. Likewise, Goldberg et al.15 demonstrated a significant increase in the size of ablation performed in the in vivo porcine liver during portal venous occlusion as compared with that generated with normal hepatic blood flow (2.9 cm ± 0.1 vs. 2.4 cm ± 0.2 diameter; P < .01). They also demonstrated an increase in the size of ablation performed in the in vivo porcine liver during celiac and hepatic arterial occlusion as compared with that of normal hepatic blood flow (2.7 cm ± 0.2 and 2.5 cm ± 0.1, respectively). In addition, a similar effect was achieved clinically in the human phase of the study. Intraoperative RF ablation performed on 10 colorectal metastatic lesions in 7 patients revealed an average diameter of 4.0 cm ± 1.3 with portal venous occlusion versus 2.5 cm ± 0.8) with normal hepatic blood flow. Rossi et al.16 demonstrated similar findings regarding blood flow occlusion and ablation size in the healthy in vivo porcine liver. Substantial evidence in animal as well as human models indicate that hepatic blood flow occlusion, namely portal venous interruption, during RF ablation in normal livers results in a larger ablative area.
Although normal hepatic blood flow limits the size of an ablation, blood flow through a cirrhotic liver is diminished as a result of the architectural changes leading to portal hypertension and the subsequent collateralization of circulation. In addition, many patients with cirrhosis have had a prior TIPS. The sole purpose of this portosystemic shunt is to bypass the hepatic parenchyma. Intuitively, one might postulate that the effect of diminished blood flow through a cirrhotic liver and the effect of a Pringle maneuver in a noncirrhotic liver would be similar with respect to convective heat transfer. Therefore, would performing a Pringle maneuver during an RF ablation in a cirrhotic liver offer any significant advantage?
One of the added benefits of conducting RF ablation via laparoscopy or laparotomy is the ability to execute a Pringle maneuver and, consequently, achieve a larger ablation. However, one must consider if this benefit in the cirrhotic patient exceeds the increased risk, expense, and discomfort of a laparoscopy or laparotomy performed solely for the ablation of HCC. Small tumors (<3 cm) are likely to respond well to ablation without interruption of blood flow but can require longer and or multiple ablations. Larger tumors (>3 cm) may benefit more from inflow occlusion during RF ablation, especially if multiple ablations are required.
Our results indicate that interruption of hepatic blood flow during an RF ablation in a cirrhotic liver, despite the presence of TIPS, will significantly enlarge the size of an ablation. This assertion is supported by a 120% increase in volume of ablation when performing a Pringle maneuver versus normal hepatic blood flow. This finding suggests that, despite the collateral circulation that develops in endstage cirrhotic patients and the shunted hepatic blood flow in patients with TIPS, residual hepatic perfusion persists and is significant enough to be a limiting factor in the size of an RF ablation.
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FOOTNOTES |
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Received for publication September 16, 2003. Accepted for publication April 8, 2003.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This article has been cited by other articles:
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  R. S. Montgomery, A. Rahal, G. D. Dodd III, J. R. Leyendecker, and L. G. Hubbard Radiofrequency Ablation of Hepatic Tumors: Variability of Lesion Size Using a Single Ablation Device Am. J. Roentgenol., March 1, 2004; 182(3): 657 - 661. [Abstract] [Full Text] [PDF]
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