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AJR 2004; 183:1425-1429
© American Roentgen Ray Society

Combined Radiofrequency and Alcohol Injection for Percutaneous Hepatic Tumor Ablation

Sridhar Shankar1,2,3, Eric vanSonnenberg2,3, Paul R. Morrison3, Kemal Tuncali3 and Stuart G. Silverman3

1 Department of Radiology, University of Massachusetts, 55 Lake Ave. N, Worcester, MA 01655.
2 Department of Radiology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Boston, MA 02115.
3 Department of Radiology, Brigham and Women's Hospital, Boston, MA 02115.

Received January 13, 2004; accepted after revision April 20, 2004.

 
Address correspondence to S. Shankar (shankars{at}ummhc.org).


Abstract
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 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. We sought to determine if alcohol potentiates radiofrequency energy by obtaining larger ablative volumes in 30 liver tumors in human patients.

SUBJECTS AND METHODS. We compared two groups of patients: one group treated with radiofrequency ablation alone (radiofrequency-alone group), and a second group treated with radiofrequency ablation and immediate prior injection of alcohol (combined group). The radiofrequency-alone group comprised 20 ablations (mean diameter, 8.4 cm; colorectal cancer metastases [n = 15]; other metastases [n = 5]). The combined group consisted of 30 radiofrequency ablations (mean diameter, 8.8 cm; metastatic colorectal cancer [n = 17]; other metastases [n = 8]; and hepatocellular carcinoma [n = 5]) treated with alcohol injection immediately before radiofrequency ablation. The amount of alcohol injected was determined by the size and location of tumors. Preprocedural laboratory tests (complete blood cell count with differential, liver function tests, and coagulation parameters) were performed in all patients, along with pre- and postprocedural CT, MRI, and PET. Measurements of tissue necrosis were obtained on the postprocedural CT scans and MR images. Volumes of necrosis calculated in each group were corrected for the number of radiofrequency applications and were statistically compared using the Student's t test. In addition, tissue impedances obtained during the radiofrequency ablation procedure were compared between the two groups.

RESULTS. The mean ablation volumes for the radiofrequency-alone group were 32.3 cm2 (median, 28.6 cm2; range, 14.4–61.8 cm2) and for the combined group, 84.6 cm2 (median, 78.3 cm2; range, 34.6–149 cm2). The difference in the necrosis volumes was significantly larger (p < 0.0001) in the combined group. Overall, the combined treatment group underwent fewer radiofrequency applications per session. Tissue impedance during radiofrequency ablation was higher in the combined group (mean, 62.7 vs 57.3 {Omega} in the radiofrequency alone group; p = 0.0005) at comparable times during the ablations. No major complications were seen in either group.

CONCLUSION. Percutaneous radiofrequency ablation appears to be potentiated by immediate prior alcohol injection into the tumor. Consistently larger lesions are obtainable in fewer sessions, without any increase of complications, using the combined method.


Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Much current research in percutaneous radiofrequency ablation, particularly in hepatic tumors, is focused on obtaining larger and more consistent volumes of tissue necrosis with commercially available devices [1–4]. Experimental work has been attempted using synergistic measures in combination with radiofrequency ablation, such as direct infusion of hypertonic saline into the tumor [5], IV injection of chemotherapeutic agents [6], and the intraoperative Pringle maneuver [7], in an effort to obtain larger ablation volumes. Alcohol has been used extensively in the past to ablate liver tumors, primarily hepatocellular carcinoma (HCC) [8]. In an animal model experiment, alcohol was shown to potentiate radiofrequency ablation therapy and resulted in significantly larger ablations [9].

The alcohol and radiofrequency ablation combination has also been used in the treatment of HCC in two studies, and the results showed an increased volume of coagulative necrosis [10, 11]. Our study was performed prospectively in human subjects to determine whether injection of alcohol potentiated radiofrequency ablation by obtaining larger volumes of tumor ablation in hepatic tumors of various etiologies. We also assessed the safety and feasibility of the combined technique (compared with radiofrequency ablation alone).


Subjects and Methods
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 Subjects and Methods
Results
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We included patients with primary or metastatic liver tumors measuring more than 5 cm in maximal diameter. All patients were referred by their oncologists; each patient was evaluated for the procedure by a hepatic surgeon, anesthesiologist, and the interventional radiology team, all of whom agreed on the treatment plan.

The study included two groups: patients who underwent percutaneous radiofrequency ablation without injection of alcohol (radiofrequency-alone group) and a second subset of patients who underwent percutaneous injection of alcohol into the tumors initially, followed by radiofrequency ablation (combined group) in the same session. All patients were deemed unresectable and were referred for treatment by their oncologists. All radiofrequency ablations were performed under an institutional review board–approved innovative therapy protocol. All procedures were performed with the patient under general anesthesia. Written informed consent was obtained from all patients.

Radiofrequency-Alone Group
The radiofrequency-alone group included 12 men, and 8 women (age range, 49–88 years; mean, 67.3 years). Twenty ablation sessions were undertaken, and 22 tumors were treated in this group. Tumor size ranged from 5.5 to 15 cm (mean, 8.8 cm), and volume ranged from 44.8 to 295.8 cm2 (mean, 114 cm2).

Combined Group
This combined group comprised 19 men and 11 women (age range, 39–84 years; mean, 67.1 years). Thirty ablation sessions were performed, and 36 lesions were treated in this group. Tumor sizes ranged from 5 to 11. 5 cm in diameter (mean, 8.4 cm), and volume ranged from 48.6 to 330 cm2 (mean, 126 cm2). Details of the treated tumors are summarized in Table 1.


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  		TABLE 1 Histopathology of Primary Tumors

 

Radiofrequency Ablation Technique
Radiofrequency ablation was performed in all cases using a three-prong, 17.5-g-cluster, Cool-tip probe (Radionics). The probes ranged from 10 to 20 cm in length, with 2.5-cm-long active tips. Grounding was achieved by attaching four dispersive pads with a combined surface area greater than 400 cm2 to both thighs in each patient. The electrode was then attached to a generator capable of producing 200 W of power. Each radiofrequency application was 12 min long, automatically impedance-controlled by the internal algorithm of the generator, according to the protocol recommended by the manufacturer.

Injection of Alcohol
Dehydrated sterile alcohol (98%) was injected through 10- to 20-cm-long 22-g Chiba needles placed into the center of the tumor under CT guidance. The total volume of alcohol injected varied from 2 to 20 mL (mean, 9.8 mL). Depending on the size and location of the tumors before radiofrequency ablation in all cases, we injected alcohol in small aliquots of 1–2 mL, using CT imaging to ensure that the needle had not backed out of the intended injection site and to assess extravasation. The volume of alcohol used was empiric and based on the maximum volume that we could safely inject into the tumor without leakage from the sides. The injection of alcohol was accomplished usually through two or three needles placed in approximately the center of the tumor. For larger tumors not close to critical structures, injection was usually begun at the deepest portion of the tumor and continued while slowly retracting the needle by 1- to 2-cm increments during the injection, depending on size and location. Radiofrequency ablation followed the alcohol injection within 2–5 min in all cases.

Number of Radiofrequency Ablation Applications
Each tumor was treated with a range of 1–8 radiofrequency ablation applications of 12 min each in the radiofrequency-alone group (mean, 3.5; median, 3). In the combined group, a range of 1–4 radiofrequency applications (burns) were performed (mean, 2.1; median, 2).

Preprocedural and Follow-Up Imaging
All patients underwent CT, MRI, and PET before the procedure. A contrast-enhanced CT scan was obtained immediately after the procedure, and a contrast-enhanced MR image, within 24 hr. Follow-up PET, CT, and MRI were performed at 3- to 6-month intervals after the procedure.

Volume Calculation
Baseline tumor sizes were measured on the preprocedural MR images (obtained without and with IV contrast material). Measurements after ablation were obtained on the postablation MR images (1.5-T scanners, Signa, GE Healthcare). Transverse T1-weighted spin-echo images (TR/TE, 600/14; section thickness, 4 mm; field of view, 34 cm), transverse T2-weighted fast spin-echo images (5,100/100; echo-train length, 12; section thickness, 4 mm; field of view, 30 cm), and transverse fast multiplanar spoiled gradient-echo images (285/1.6; flip angle, 75°; section thickness, 5 mm; field of view, 34 cm with fat suppression) were obtained, with imaging performed before and after the IV injection of 20 mL of gadopentetate dimeglumine (Magnevist, Berlex Laboratories). Measurements were obtained on a PACS system in three dimensions by two experienced radiologists in consensus using electronic calipers. Volume calculation was performed using the formula for an ellipsoid (V = (4{pi}/3)xyz, in which x, y, z are the three radii). The obtained ablation volume was corrected for number of burns (total volume/number of radiofrequency applications).

Impedance Measurement
The mean impedance was recorded from the read-out on the radiofrequency ablation device between the first 3–6 min (chosen because of consistency of obtaining readings) of radiofrequency energy application in all cases for each location in which radiofrequency ablation was applied. The average impedance in each of the two groups was calculated.

Statistical Analysis
The mean ablation volumes achieved in the two groups were compared using the two-sample Student's t test. Similarly, the mean impedance values were also compared using the same statistical test.


Results
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 Subjects and Methods
 Results
Discussion
 References
 
The mean corrected ablation volume in the radiofrequency-alone group (n = 20) was 32.3 cm2 (median, 28.6 cm2; range, 14.4–61.8 cm2; SD, 14.9 cm2) (Fig. 1A, 1B, 1C). In the combined group (n = 30), the mean volume was 84.6 cm2 (median, 78.3 cm2; range, 34.6–149 cm2; SD, 33.6 cm2) (Fig. 2A, 2B, 2C, 2D). The p value, using the two-sample Student's t test, was < 0.0001.



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  		Fig. 1A. —88-year-old woman with solitary 5.5-cm colon cancer metastasis in liver. T1-weighted contrast-enhanced axial MR image shows rim-enhancing mass in right lobe of liver.

 


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  		Fig. 1B. —88-year-old woman with solitary 5.5-cm colon cancer metastasis in liver. Intraprocedural unenhanced CT scan shows radiofrequency probe within lesion. Three radiofrequency applications were performed.

 


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  		Fig. 1C. —88-year-old woman with solitary 5.5-cm colon cancer metastasis in liver. Contrast-enhanced MR image obtained after radiofrequency ablation shows necrosis as nonenhancing area measuring 71.5 cm2.

 


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  		Fig. 2A. —40-year-old woman with colon cancer metastatic to liver. T1-weighted contrast-enhanced axial MR image shows large mass in inferior right lobe of liver, measuring 9.5 cm in longest axis.

 


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  		Fig. 2B. —40-year-old woman with colon cancer metastatic to liver. Intraprocedural unenhanced CT scan shows alcohol injection within tumor; 10 mL of alcohol was injected.

 


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  		Fig. 2C. —40-year-old woman with colon cancer metastatic to liver. Intraprocedural CT scan shows radiofrequency ablation in progress; two radiofrequency applications were performed. Note relatively large amount of gas around probe.

 


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  		Fig. 2D. —40-year-old woman with colon cancer metastatic to liver. T1-weighted contrast-enhanced MR image obtained after procedure shows large area of necrosis; 249 cm2 of necrosis was obtained with two radiofrequency applications.

 

Impedance
In the radiofrequency-alone group (n = 59 radiofrequency applications), the mean impedance was 57.3 {Omega} (range, 48–74 {Omega}; median, 57 {Omega}). In the combined group (n = 55 radiofrequency applications), the value was 62.7 {Omega} (range, 50–108 {Omega}; median, 61 {Omega}). The difference was found to be statistically significant, with a p value of 0.0005, using the two-sample Student's t test.

Complications
In the radiofrequency-alone group, two patients had brachial plexopathy (resolved spontaneously in both), one patient had a large biloma requiring drainage, and three patients experienced prolonged recovery (> 3 days in hospital). The postablation syndrome, manifested by low-grade fevers (≤ 100°F [37.8°C]), myalgias, and malaise for up to 1 week after the procedure, was seen in two patients, and one patient was hospitalized for 7 days for various medical problems unrelated directly to the procedure.

In the combined group, one patient had a small biloma that resolved without any specific therapy, and the postablation syndrome occurred in two patients. No other complications were seen in this group, and none of the patients had any symptoms suggesting alcohol toxicity.

Subjective Observations
Larger-than-usual amounts of gas were seen around the probe tip during radiofrequency ablation in the combined group compared with the radiofrequency-alone group. Portal venous gas also was seen more frequently in the combined group.


Discussion
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Percutaneous ethanol injection treatment of liver tumors has been shown to be successful, particularly in HCC in several Japanese and Italian series [12–15], and is as effective as surgery for the treatment of small HCCs [14–18]. Ethanol is directly cytotoxic and acts on living tissue by inducing coagulation necrosis, dehydration, and denaturation of cytoplasmic proteins with consequent coagulation necrosis followed by fibrosis. Ethanol also enters the microcirculation and induces necrosis of endothelial cells and platelet aggregation with consequent thrombosis of small vessels, followed by ischemia of tumor tissue [9, 19–21].

Radiofrequency ablation induces coagulation necrosis by ionic agitation and consequent heating of tissue. Substantial evidence suggests that the degree of tissue perfusion determines the extent of coagulation necrosis produced by thermal ablation: the more well perfused the tissue, the less the size of the achieved ablation [7, 22]. This outcome is probably best exemplified by the heat sink effect seen with radiofrequency ablations adjacent to large vessels [23].

Animal experiments have shown that the composite ablation induced by the two successive treatments of ethanol followed by radiofrequency ablation is more than simply additive when alcohol was administered before radiofrequency ablation [9]. Similar results have also been reported in HCC in humans [10]. Our study shows an increased volume of necrosis when radiofrequency ablation is used after intratumoral injection of ethanol in a variety of tumors, compared with radiofrequency ablation alone.

Although the mechanisms of the observed synergy between direct alcohol injection and radiofrequency ablation are not clear, there are several theories. One possible mechanism is the decrease of blood flow to the tumor and consequent tissue cooling before application of radiofrequency energy. The increased temperature of tissue from decreased perfusion-mediated cooling in turn leads to improved heat deposition within the tumor. Injection of alcohol thromboses vessels and probably decreases perfusion and therefore increases the radiofrequency effect. Thus, percutaneous ethanol injection therapy theoretically may also be synergistic when used with other heat ablation techniques such as laser, microwave, or focused ultrasound [9].

Another possible explanation for the observed synergy is that ethanol injected immediately before radiofrequency ablation may be heated or even boiled (boiling point of ethanol, 78.3°C) by radiofrequency heating; this effect results in an increased ablation volume by hot ethanol [24, 25]. Additionally, diffusion of ethanol into the areas not treated by radiofrequency ablation (e.g., adjacent to large vessels) may aid in achieving increased ablation volumes [11].

Significantly greater tissue impedance values were observed in tumors treated with the combined technique compared with radiofrequency alone. This finding may be secondary to both the presence of ethanol within the treatment area and alcohol-induced tissue changes because tissue coagulation can reasonably be expected to increase impedance. Also, decreased perfusion in tissue as a result of alcohol injection may contribute to increased tissue impedance. Increased impedance within tissue that has undergone radiofrequency ablation is best exemplified by the "roll-off" effect that occurs when ablation is complete, using commercially available devices (LeVeen needle probe, Boston Scientific) that use impedance control as an end point [26]. Hence, the increased ablation volume observed in the combined group could be due to greater tissue heating achieved during radiofrequency application secondary to higher tissue impedance.

Subjective observations in our study included a larger-than-usual amount of gas produced around the probe tip during ablations in the combined group and gas seen more frequently in portal venous branches. This increased gas also may account for the increased impedance observed during radiofrequency ablation in the combined group.

Overall, the complications encountered in the combined group were fewer and less severe than in the radiofrequency-alone group. The average number of radiofrequency applications for a given volume of tumor was also less in the combined group than in the radiofrequency-alone group. Taken together, these factors could be extrapolated to mean shorter procedure times and increased safety, obvious goals with ablation therapy, albeit unproven. Brachial plexopathy sustained in two patients in the radiofrequency-alone group was due to what we determined to be improper positioning of the patients' arms on the CT table. The positioning was corrected in our subsequent patients, and we believe that this complication was not related to the type of ablation performed.

A limitation of our study is that outcome analysis was not performed. However, our intention was to determine whether there was a synergistic effect of radiofrequency ablation with direct percutaneous alcohol injection in various hepatic tumors compared with radiofrequency ablation alone. Another possible limitation is that we did not assess ablation volumes stratified by tumor type, even though the tumor types in the two groups we studied were similar. The results of our study should encourage future research using other percutaneously injected substances such as acetic acid and hot saline with thermal ablation. Another outgrowth of our study is the question of whether combined therapy is useful in treating larger tumors in other organs and systems as well.

In summary, our study indicates that direct intratumoral alcohol injection potentiates radiofrequency ablation by achieving significantly larger ablation volumes. The use of the combined technique is straightforward and adds little cost and time to the procedure. Additionally, the data suggest that combined therapy requires fewer radiofrequency applications and may be safer.


References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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