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1
Département d'Imagerie
Médicale, Service de Radiologie
Interventionnelle, Institut Gustave Roussy, 94805 Villejuif Cedex,
France.
2
Département de
Médecine, Institut Gustave Roussy, 94805
Villejuif Cedex, France.
3
Département de Chirurgie, Institut Gustave
Roussy, 94805 Villejuif Cedex, France.
Received March 21, 2001;
accepted after revision July 31, 2001.
Address correspondence to T. de Baere.
Abstract
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SUBJECTS AND METHODS. Ten tumors were treated by percutaneous radiofrequency ablation during balloon occlusion of a hepatic vein (n = 8) or a segmental portal branch (n = 2). Venous occlusion was undertaken because the tumor was in contact with a hepatic vein (n = 3) or a portal branch (n = 1); because the tumor exceeded 35 mm in width (mean, 44 mm), which was considered the maximum size amenable to ablation in a single session (n = 2); or because of both large size and contact with a hepatic vein (n = 3) or a portal branch (n = 1).
RESULTS. Vascular occlusion was always technically possible. Radiofrequency was delivered to one to three locations (mean, 1.9 locations) with a cluster electrode. The largest axis of radiofrequency-induced lesions after ablation with the cluster needle—between 42 and 51 mm (mean, 49 mm)—was always larger than the targeted tumor. These sizes were statistically larger than in a matched control group of patients who underwent radiofrequency ablation without vascular occlusion (p < 0.0003). After a mean follow-up of 12.6 months, CT and MR imaging revealed complete destruction of nine tumors after a single radiofrequency ablation treatment; one tumor required three treatments to achieve ablation. Five patients are tumorfree 12-18 months (mean, 14.4 months) after the first radiofrequency ablation treatment, and five developed new liver metastases.
CONCLUSION. Temporary hepatic vein or portal branch occlusion during radiofrequency ablation can safely facilitate the treatment of large tumors or tumors in contact with the walls of large vessels.
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A major limiting factor is the maximal size of the radiofrequency lesion that can be induced with a single probe placement. Because the ideal tool would have to create, in a single delivery of radiofrequency, an area of destruction measuring 0.5-1 cm larger than the targeted tumor (in a manner akin to surgical margins) and because the largest area of destruction that can be obtained in clinical practice with commercially available systems with single probe placement and radiofrequency delivery is roughly 4-5 cm in diameter, only tumors measuring less than 3-4 cm can be treated with a single radiofrequency delivery. This size-limiting factor remains despite recourse to a variety of ablation optimization strategies such as multiprobe devices to increase the size of areas of radiofrequency destruction obtained in one radiofrequency delivery [14], expandable probes [15], internally cooled electrodes [16], and the injection of a saline solution around the electrode to lower tissue impedance [17].
Destroying tumor foci located close to large vessels is another limiting factor of radiofrequency ablation that is difficult to negotiate. The heat sink induced by vascular flow in these large vessels may prevent sufficient heat from accumulating in the portion of the tumor in contact with the vessel walls. Many previous reports have mentioned incomplete treatment of tumors in contact with large vessel walls [13, 18].
Lowering hepatic blood flow appears to be an interesting adjunct to radiofrequency ablation, either to increase the size of the radiofrequency-induced lesion or to destroy tumors in contact with vessel walls. Indeed, previous experiments have shown that mechanical [19,20,21], and pharmacologic [19] strategies aimed at lowering hepatic perfusion can increase the size of thermally induced lesions. Furthermore, a decrease in vascular flow is expected to lower heat sink and thereby facilitate the destruction of tumors in contact with vessel walls.
We therefore decided to undertake a study to evaluate the feasibility, tolerance, and benefit of controlling hepatic flow in a segmental portal branch or a hepatic vein with balloon occlusion during radiofrequency ablation of 10 primary or secondary hepatic tumors the size of which exceeded the usual inclusion criteria for radiofrequency ablation, or which were in close contact with large hepatic veins or portal branches.
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Radiofrequency ablation with vascular occlusion was proposed in 10 consecutive patients referred for radiofrequency ablation who presented with a tumor either in contact with a large vessel wall (n = 4) or having a diameter exceeding 35 mm (n = 2) or both (n = 4). These three groups of patients presented a mean tumor diameter of 23 ± 9, 44 ± 5, and 40 ± 3 mm, respectively. Contact with a large vessel wall was defined as the absence of normal liver parenchyma between the tumor and the wall of a portal branch or a hepatic vein larger than 5 mm in diameter at sonography and confirmed at CT or MR imaging. In the eight patients with a tumor in contact with a vein, the vessels involved were the middle hepatic vein (n = 3), the right hepatic vein (n = 3), or a segmental portal branch (n = 2); these vessels were occluded. In the two patients with only large tumors, the right hepatic vein (n = 1) and the middle hepatic vein (n = 1) were occluded.
Technique
All patients were treated under general anesthesia and received a single IV
antibiotic injection at the beginning of the radiofrequency ablation
procedure, using 2 g of amoxicillin clavulanate (Augmentin; Beecham, Nanterre,
France). No patients received any anticoagulant treatment.
The right femoral vein (n = 6) or the right internal jugular vein (n = 2) was the route via which the distal tip of a 5-French Cobra catheter (JB1; Cook Europe, Bjaeverskov, Denmark) was inserted into the targeted hepatic vein under fluoroscopic guidance (Fig. 1A,1B,1C,1D,1E,1F,1G). Sonography was then used to confirm that the hepatic vein in contact with the tumor was indeed catheterized. The 5-French catheter was exchanged for an 8-French Berenstein 20-mm occlusion balloon catheter (Boston Scientific/Medi-Tech, Watertown, MA) over a 2.60-m guidewire (Amplatz super stiff exchange guidewire; Boston Scientific/Medi-Tech). In the two cases of portal occlusion, access to the portal system was achieved by percutaneous transhepatic puncture of a peripheral left portal branch with an 18-gauge transhepatic cholangiography needle (Cook, Bjaeverskov, Denmark) via a subxiphoid route under sonographic guidance. Then a 4-French introducer sheath was inserted over a 0.035-inch guidewire to advance a 3-French catheter with a 9-mm inflatable balloon (Fogarty thru-lumen embolectomy catheter; Baxter Healthcare, Irvine, CA) inside the targeted segmental portal branches (Fig. 2A,2B,2C,2D,2E). The balloon was not inflated until the radiofrequency electrode had been placed in the hepatic tumor and the radiofrequency current was ready to be delivered. The radiofrequency electrode (AU4-Idea; Esaote-Biomedica, Le Perreux, France) was placed under sonographic guidance by percutaneous puncture of the liver with a 17-gauge internally cooled triple-cluster needle with a 2.5-cm active distal tip in the nine lesions exceeding 25 mm. The only tumor measuring less than 25 mm in diameter (i.e., 13 mm) was treated with a single needle with a 2-cm active tip.
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All procedures were performed by a single senior staff radiologist trained in radiofrequency ablation, who activated the needle electrode for 15 min in one to three locations (mean, 1.9 locations) in each tumor. Hepatic vein or portal branch blood flow was interrupted by inflating the previously positioned balloon during the 15-min radiofrequency application. In all cases, the position of the balloon and its ability to occlude the target vessel were verified by phlebography and color Doppler sonography.
A 480-kHz radiofrequency generator (CC1; Radionics, Burlington, MA)
delivering a maximum power of 200 W was used for thermal ablation. Circuitry
in the generator allows continuous monitoring of impedance between the active
part of the cooled needle and the grounding pads placed on the patient's
thigh. A thermocouple embedded in the electrode ensures constant monitoring of
the temperature at the tip of the needle. During treatment application, the
maximum radiofrequency power prevented impedance from rising 10 
above
the baseline value. The current intensity was 0.8 A for the single-needle and
up to 1.8 A for the cluster-needle electrode. A peristaltic pump (312FS/D
variable speed pump; Watson-Marlow, Paris, France) ensured cooling of the
electrode with a 0°C saline solution at a flow rate sufficient to maintain
the temperature of the electrode below 25°C. At the end of the
radiofrequency application, the current and cooling circuit were switched off,
and the electrode remained in place until the thermocouple registered thermal
equilibrium, after heated tissue was allowed to reheat the electrode.
Treatment was performed under sonographic monitoring and was considered complete when a hyperechoic radiofrequency-induced area of coagulation necrosis was seen to cover the tumor site with a 0.5-cm rim of normal liver around the tumor site. Occlusion balloons were deflated immediately after the radiofrequency application; then color Doppler sonography and phlebography were used to study the previously occluded vessels.
All patients were clinically examined, and samples of their blood were analyzed for liver transaminase; bilirubin; and RBC, WBC, and platelet counts the day after treatment. Pain more severe than usual was found in three patients, so chest radiography and abdominal sonography were performed.
Follow-Up
Patients were followed up with CT and MR imaging, both performed on the
same day, every 2 months after the radiofrequency ablation procedure unless
they developed new liver metastases distant from the treated area that
required systemic chemotherapy. Indeed, when patients underwent systemic
therapy, the course of follow-up was decided by the clinical oncologist and
most often was not suitable for accurate evaluation of the
radiofrequency-treated tumor.
CT examinations were performed with a Hi-Speed helical scanner (General Electric Medical Systems, Milwaukee, WI). All patients received 100 mL of IV iobitridol (Xenetix 300; Guerbet, Aulnaysous-bois, France) at a rate of 3 mL/sec with a power injector. Triple-phase helical CT of the liver was performed during the hepatic arterial phase, the portal venous phase, and the equilibrium phase for 30 sec, 70 sec, and 5 min, respectively, after beginning the injection of the contrast medium. Scanning was performed at 120 kV and 270 mA. Contiguously reconstructed sections (pitch of 1:1) were obtained through the liver with 7-mm collimation. Each helical acquisition through the liver was accomplished in a single breath-hold.
MR imaging was performed with a 1.5-T wholebody imager (Signa LX; General Electric Medical Systems). All MR images were obtained in the axial plane with a phased array multicoil for the body. Sections were 7 mm thick with a 2-mm intersection gap for all pulse sequences. The imaging protocol comprised fat-suppressed T2-weighted images with respiratory-triggered fast spin-echo sequences (TR range/TE, 4000-8000/102; mean TR, 5454), an echo-train length of 16, 4 signals acquired, 10-msec interecho spacing, 256 x 256 matrix, 31.25-kHz received bandwidth, 40-cm field of view; and dynamic contrast-enhanced MR imaging performed at three consecutive 30-sec intervals and 5 min after a bolus injection of 0.1 mmol/kg of gadoterate meglumine (Dotarem; Guerbet, Aulnay-sous-Bois, France) at a rate of 3 mL/sec. T1-weighted imaging was acquired with fast multiplanar spoiled gradient-recalled echo sequences (TR/TE, 125/1.6), a 60° flip angle, 1 signal acquired, 512 x 256 matrix, 62.5-kHz received bandwidth, 40-cm field of view, 25 sec of acquisition time, and 17 images during a single breath-hold. Saturation bands were used with all MR sequences that were larger and smaller than the imaging volume to prevent flow-related artifacts.
Radiologic studies was interpreted in consensus by two senior radiologists for the evaluation of the efficacy of radiofrequency ablation. Radiofrequency ablation was considered incomplete and active tumor still present when the treated area had enlarged after the first 2 months of follow-up imaging, when mild hyperintense foci were seen on T2-weighted MR images, and when foci of contrast material uptake were depicted in the treated area at enhanced CT or MR imaging. Foci of enhancement that were considered active disease were nodules or thickening exceeding 2 mm. On the contrary, a regular 2-mm or thinner peripheral rim of enhancement around the treated area, previously described by others [22, 23] and known to be an inflammatory reaction that can persist for several months, was not considered active tumor. Radiofrequency treatment was defined as successful when a hypoattenuating area was seen at CT and a hypointense area on T2-weighted MR images, and when this area did not enhance after the administration of contrast material on T1-weighted imaging and CT. The size of the area of radiofrequency-induced necrosis was measured by two radiologists on the portal venous phase of the enhanced CT scans obtained 2 months after radiofrequency ablation. The largest and shortest axes of the area destroyed by radiofrequency ablation were measured in the axial plane. Size of the destroyed area was defined in a manner similar to the World Health Organization recommendations for tumor size measurement [24]. Indeed, the largest axis was defined as the largest dimension of the destroyed area measured on the CT scan on which they were the largest, and the shortest axis was defined as the largest dimension perpendicular to the previously described largest axis on the same CT scan.
All CT scans obtained 2 months after radiofrequency ablation in the nine patients treated with the cluster needle were matched, for tumor type and patient age, with the CT scans obtained 2 months after radiofrequency ablation in a control group of 18 patients treated during the same period by the same operator. The 18 patients in the control group were not in our study but were treated with the same number of cluster needle radiofrequency deliveries, but without vascular flow control. These 18 CT scans were retrospectively reviewed by two radiologists for the size of the area of radiofrequency destruction. The sizes of the areas of destruction of the nine patients who underwent radiofrequency ablation with vascular occlusion were compared with those the 18 patients who underwent radiofrequency ablation without vascular occlusion using the Student's t test.
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The smallest tumor (13 mm) that was in close contact with a hepatic vein wall was treated with a single application of a single-needle electrode. The other nine tumors were treated with cluster-needle electrodes, with one probe location of radiofrequency delivery in two cases, two locations in five cases, and three locations in two cases. A mean of 1.9 probe locations of radiofrequency delivery were used. Temperatures measured after interruption of the radiofrequency generator and cooling circuit were 77-97°C (mean, 84°C ± 7°C).
Follow-Up
On follow-up MR imaging performed 2 months after one visit for
radiofrequency ablation in the nine patients treated with the cluster-needle
electrodes, including one to three locations of radiofrequency delivery, the
sizes of the areas of radiofrequency-induced coagulation necrosis, measured in
the axial plane, were 42-65 mm (mean, 51 ± 10 mm) in the longest axis
and 40-55 mm (mean, 48 ± 6.8 mm) in the shortest axis. These areas of
coagulation were statistically larger (p < 0.0003) than the areas
in the group of 18 matched patients treated during the same period by the same
operator with the same number of cluster-needle applications per tumor without
vascular occlusion. The sizes of the areas of radiofrequency-induced
coagulation necrosis without vascular occlusion, measured in the axial plane,
were 20-38 mm (mean, 27 ± 7 mm) in the shortest axis and 25-45 mm
(mean, 33 ± 6 mm) in the largest axis,
Overall, the follow-up period of this study was at least 8 months or until death (mean, 12.6 months). Unfortunately, five patients developed new multiple liver metastases distant from the radiofrequency ablation—treated area that were depicted at imaging follow-up 2-8 months (mean, 3.2 months) after treatment. On these imaging follow-up examinations, the five tumors previously treated with radiofrequebcy ablation were considered completely necrotic. Because of the spread of their disease, these patients were not deemed eligible for further radiofrequency ablation and instead received systemic chemotherapy.
Five patients remained tumor-free at the last available follow-up imaging examination 12-18 months (mean, 14.4 ± 2.1 months) after radiofrequency ablation. Among these five successfully treated patients, four patients underwent only the single radiofrequency ablation procedure with vascular occlusion reported here. The fifth patient required three radiofrequency ablation sessions because of the appearance of small foci of enhancement at the periphery of the treated tumor but remote from the area near the occluded vessel on follow-up MR imaging. Additionally, one patient who developed a new 13-mm liver metastasis 8 months after the first radiofrequency ablation was successfully treated with another session of radiofrequency ablation.
Complications
Phlebography and color Doppler sonography, performed at the end of the
procedure, depicted three cases of complete thrombosis of the temporarily
occluded vessels, one in a middle hepatic vein and two in the segmental portal
branches (Fig.
3A,3B,3C,3D,3E).
Slow vascular flow was found in two middle hepatic veins and in two right
hepatic veins. Patients with altered flow or occluded vessels did not present
any vascular abnormalities on the follow-up imaging studies; their vessels
were therefore considered patent.
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The portal branch of liver segment II used to gain access to the portal system was dissected during placement of the 4-French introducer. Complications after the procedure included transient fever (n = 3), pleural effusion (n = 1), and minor perihepatic hematoma (n = 1). Transient fever, which occurred during the early postprocedure period, resolved spontaneously in less than 8 days with no proof of infection in these patients and was not different from that usually encountered after radiofrequency ablation without vascular occlusion. Abundant and recurrent right pleural effusion occurred in a patient treated for a central lesion (segments V—VIII) remote from the diaphragm and the pleura recess. Four thoracocentesis procedures were required to evacuate fluid. In one patient, a collection of thin perihepatic fluid was depicted on sonography at the end of the radiofrequency ablation. A conventional CT examination performed 1 day later depicted a 5-mm-thick perihepatic fluid collection that had disappeared 3 days later on the follow-up sonographic examination without need of any specific medication.
Blood screening tests revealed no modification in hemoglobin level, blood cell count, or bilirubin level. All patients showed an increase in glutamic-oxaloacetic transaminase (GOT) and glutamic-pyruvic transaminase (GPT) levels. GOT and GPT levels were below 78 and 67 U/L, respectively, in all patients before treatment (normal values, GOT < 42U/L and GPT < 40U/L). GOT rose to 142-843 U/L (mean, 562 U/L) the day after treatment, and GPT rose to 123-690 U/L (mean, 439 U/L).
Hospital Stay
Eight patients were released from the hospital the day after treatment, one
patient remained 2 days, and the patient with the perihepatic collection
remained 4 days.
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To our knowledge, no clinical study has ever evaluated the role of percutaneous portal or hepatic vein occlusion during radiofrequency ablation of large tumors or of tumors in contact with the walls of large vessels. When vascular control is wanted for a tumor in contact with a large vessel wall, it is obvious which vessel should be occluded: the one alongside the tumor. No consensus has yet been reached as to how many and which vessels to occlude when vascular occlusion is required to increase the size of interstitial thermal lesions. In a surgical series, vascular flow was most commonly controlled using the Pringle maneuver (i.e., hepatic pedicle clamping) [31]. Reproducing the Pringle maneuver with the percutaneous approach is technically possible but relatively difficult in routine clinical practice. Isolated hepatic artery occlusion has never been shown to increase the size of interstitial hyperthermia-induced lesions, and several studies have reported statistically significant differences in the increase in radiofrequency-induced coagulation necrosis obtained with portal occlusion alone or in combination with arterial occlusion [20, 29, 32]. Most studies focused on healthy nontumorous liver; thus, arterial occlusion remains, at least in theory, an interesting adjuvant option for the treatment of malignancies with predominantly arterial feeding vessels.
In this setting, two reports have recently described radiofrequency ablation during hepatic artery occlusion for large hepatocellular carcinoma [33]. However, because we were concerned with metastases that are most often hypovascularized, arterial occlusion appeared less attractive for the treatment of these lesions than for the treatment of hypervascularized hepatocellular carcinoma. Finally, most studies emphasize the usefulness of portal clamping to increase the size of thermal lesion [20, 29, 32]. In the meantime, because the transhepatic approach transforms this technique into a relatively invasive procedure, our aim is to find an alternative way of increasing the size of radiofrequency-induced coagulation necrosis in tumors that are not in contact with the portal system.
During occlusion of a hepatic vein, the occluded area is supplied only by arterial flow; portal vessels become drainage veins with outflow toward nonoccluded segments [34, 35]. Furthermore, liver perfusion is lowered, as seen by an increase in the duration of enhancement after the injection of contrast material into the hepatic artery [35]. This lowered liver perfusion should permit an increase in the size of the radiofrequency-induced lesion. Moreover, some authors suggest that acute occlusion of a hepatic vein may lead to low tissue impedance as a result of tissue stasis and hyperhydration, resulting in better heat diffusion [29]. A report of a recent experiment showed the value of hepatic vein occlusion to increase the size of the thermally induced lesion using microwaves [21]. These researchers saw no statistically significant difference in the size of thermal destruction obtained with occlusion of the portal vein, the hepatic vein, the portal vein plus the hepatic artery, or the hepatic vein plus the hepatic artery. These experimental data highlight the role of the hepatic vein occlusion that we used in clinical practice when treating large tumors. Furthermore, the same team reported a clinical experience with an increase in the size of microwave-induced areas of destruction by combining arterial and venous hepatic occlusion, but the need for combined arterial and venous occlusion has not been clearly shown in that article [30].
In our study, the size of radiofrequency-induced coagulation obtained with a combination of radiofrequency ablation and vascular occlusion was statistically superior to the size obtained in a group of matched patients treated without vascular occlusion. Moreover, the efficiency of the technique made it possible to complete tumor destruction in one radiofrequency ablation procedure for nine of the ten patients. Only one patient required further radiofrequency ablation (without vascular occlusion) for residues of the same tumor not in contact with the vessel.
Among the treated patients, the only complications we report are minor: regressive localized thrombosis of balloon-occluded vessels, minor subcapsular hematoma, transient fever, and pleural effusion. These complications never required surgery or transfusion. They prolonged hospitalization by 2 days in only one patient. Although damage to large vessels or persistent thrombosis did not occur, such complications should be feared. To our knowledge, a recent case report of portal vein thrombosis after radiofrequency ablation is the first description of a major vascular complication caused by radiofrequency ablation [36]. In that case, as in our experience (one unpublished portal trunk thrombosis), thrombosis surprisingly followed radiofrequency ablation of metastases that were remote from the hepatic hilum and the major portal branches. Because portal vein occlusion during radiofrequency ablation may increase the risk of such complications, occlusion of the hepatic vein may be an interesting alternative.
Despite a small number of patients and a relatively short follow-up period, this unique preliminary clinical experience of radiofrequency ablation during percutaneous occlusion of either the hepatic vein or the segmental portal branches proved efficient in treating hepatic malignancies larger than 3.5 cm and those in close contact with the walls of large hepatic vessels. Furthermore, because this technique appears to be feasible and to have no major complications, we suggest that larger series and clinical evaluation should be undertaken.
Acknowledgments
We thank Lorna Saint Ange for linguistic revision of the manuscript.
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