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Sonographically Observed Echogenic Response During Intraoperative Radiofrequency Ablation of Cirrhotic Livers

Pathologic Correlation

¹ Department of Radiology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78284-7800.
² Department of Surgery, University of Texas Health Science Center at San Antonio, San Antonio, TX 78284-7800.
³ Department of Pathology, University of Texas Health Science Center at San Antonio, San Antonio, TX 78284-7800.

Received March 30, 2001; accepted after revision October 22, 2001.

 
Address correspondence to G. D. Dodd III.

Abstract

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OBJECTIVE. We performed a study to determine the correlation between the diameter of the echogenic response observed with intraoperative sonography during radiofrequency ablation of the cirrhotic liver and the mean diameter of tissue necrosis.

SUBJECTS AND METHODS. A total of 22 intraoperative radiofrequency ablations were created in 11 cirrhotic livers. The largest diameter of the sonographically observed echogenic response surrounding and perpendicular to the radiofrequency probe was measured. The subsequent zone of necrosis observed at pathology in the hepatectomy specimens after liver transplantation was measured in three planes and compared with the measured diameter of the echogenic response.

RESULTS. During all except three ablations, a hyperechoic region was visualized surrounding the radiofrequency probe. The diameter of the echogenic response correlated significantly with the mean diameter of necrosis (correlation coefficient, 0.84). However, the echogenic response overestimated the minimal diameter of necrosis (mean difference, 0.8 ± 0.4 cm) in 18 of 22 ablations and underestimated the maximum diameter of necrosis (mean difference, 0.9 ± 0.8 cm) in 16 of 22 ablations.

CONCLUSION. The diameter of the echogenic response observed with intraoperative sonography during radiofrequency ablation of the cirrhotic liver correlates closely with the mean diameter of the subsequent area of tissue necrosis. However, the solitary diameter of the echogenic response as measured in our study was often greater than the smallest diameter and less than the largest diameter of the area of tissue necrosis. Therefore, the echogenic response associated with radiofrequency ablation of the cirrhotic liver should be viewed only as a rough approximation of the area of induced tissue necrosis; the final assessment of the adequacy of ablation should be deferred to an alternative imaging technique.

Introduction

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Hepatocellular carcinoma is a common complication of cirrhosis. Surgical resection remains the primary means of achieving a cure in patients with hepatocellular carcinoma, but many of these patients are poor surgical candidates [1,2,3]. Radiofrequency ablation is a promising, minimally invasive therapy for hepatocellular carcinoma that creates a focal thermal injury in the hepatic parenchyma through local ionic agitation and subsequent frictional heat [4]. Preliminary work has shown that radiofrequency ablation is effective in destroying malignant tissue in the liver with a low complication rate [5,6,7,8,9,10,11,12,13,14]. Failure to accomplish the complete destruction of malignant cells in a tumor will result in local recurrence at the ablation margin. Sonography is the most commonly used method of needle guidance for radiofrequency ablation of the liver, but attempts to correlate the sonographically observed postablation lesion with the area of necrosis have been disappointing. Work in porcine models has shown relatively poor correlation between findings on sonography and the area of necrosis detected at pathologic examination of the liver, with both over- and underestimation of ablations reported [15,16,17].

Although most small hepatocellular carcinomas are amenable to percutaneous radiofrequency ablation, the laparoscopic and intraoperative approaches are still practiced, either because the lesion is not safely accessible by the percutaneous route or because these approaches are used in combination with a surgical procedure. In some instances, additional clinically relevant information becomes available through these alternative routes [18]. Because intraoperative CT or MR imaging is not an option at most institutions, the operator must rely on sonography not only to guide the procedure but also to assess the immediate result of ablation. Also, because intraoperative sonography can be performed with a sonographic transducer placed directly on the liver, eliminating intervening soft tissues, one can expect improved visualization of the resulting lesion, possibly making the intraoperative assessment of the ablation size and the adequacy of ablation more accurate.

To our knowledge, uniformity in reported sonographic criteria used to estimate ablation size is lacking in the literature, so the preferred method of ablation measurement with unenhanced sonography remains to be determined. The relatively poor performance of sonography in previous studies has led some investigators to examine the role of sonographic contrast agents in assessing ablation adequacy. These contrast agents have the potential to reveal persistent vascularity in the margins of ablated lesions, suggesting residual viable tumor. However, results with this technique are preliminary, and the use of a contrast agent adds to the expense of the procedure.

The most consistent sonographic finding during ablation is an area of increased echogenicity that progressively envelops the radiofrequency probe early in the ablation to reach maximal diameter by the completion of the procedure. We refer to this as the echogenic response. This phenomenon results from microbubble formation that occurs at temperatures greater than 95°C (Kruskal et al., presented at the Radiological Society of North America meeting, December 2000). This hyperechoic region has been used clinically by some physicians to provide an initial assessment of the results of ablation during the procedure, although it has not been thoroughly evaluated as an indicator of ablation adequacy in humans [14, 19].

Many studies examining the accuracy of sonography for assessing radiofrequency ablation size used animal models of healthy livers. However, radiofrequency ablation is commonly performed for hepatocellular carcinoma in the setting of cirrhosis. Data are lacking correlating sonography with pathology in human cirrhotic livers.

Because of the observations stated previously, we sought to correlate the size of the echogenic response observed on intraoperative sonography with the size of the thermal injury created by radiofrequency ablation of the cirrhotic liver. Our goal was to determine whether the echogenic response could be used as a rapid estimate of the size and adequacy of a single ablation. Ultimately, such information would be useful to determine which patients would likely benefit from reablation or additional immediate imaging, such as with intravascular sonographic contrast material.

Subjects and Methods

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Patient Population
This study was approved by our institutional review board, and informed consent was obtained from all patients. The study population consisted of 11 patients (seven men, four women; mean age, 53 years; age range, 44-71 years) who had endstage cirrhosis and no known hepatic malignancy and who were undergoing liver transplantation.

Ablation Procedure
A total of 22 radiofrequency ablations were created using one of three devices (Model 500LA, RITA Medical Systems, Mountain View, CA; Radiofrequency2000, RadioTherapeutics, Mountain View, CA; and Model CC-1, Radionics, Burlington, MA). All ablations were performed in vivo during liver transplantation before removal of the diseased liver. Portal venous flow and hepatic arterial flow were maintained during the ablation process. Five patients underwent ablation with all three devices, each in a separate location in the liver. A sixth patient underwent ablation with two separate devices. Five additional patients underwent ablation with the Radionics device only. Each radiofrequency probe was placed so that the needle tip was at least 4 cm deep relative to the capsule and 3 cm from major portal or hepatic veins. All ablations were conducted according to the manufacturer's recommended protocol for each device.

Imaging and Pathology
Intraoperative real-time monitoring of the ablation process was performed with the same sonographic machine and probe (128 XP and V4 operated at 4 mHz; Acuson, Mountain View, CA). The sonographic probe was placed directly on the liver's surface. The maximal transverse diameter of the echogenic response was measured as close to perpendicular as possible to the radiofrequency probe using electronic calipers. True perpendicular measurements were usually impossible because of poor definition of the deep margin caused by posterior acoustic shadowing induced by the echogenic response. Thus most measurements were actually oriented obliquely to the shaft of the radiofrequency probe. Measurements were taken once the echogenic response surrounding the radiofrequency probe reached a maximal, stable diameter. A single diameter measurement was used rather than a volume measurement because the former technique is more likely to be performed clinically, and the latter measurement is typically impossible to obtain because of obfuscation of the posterior margin by posterior acoustic shadowing.

The explanted liver was sectioned in bread-loaf fashion at 5-mm intervals and examined grossly. The size of the necrotic zone exclusive of the hemorrhagic rim was measured by a pathologist (using a millimeter ruler) in three dimensions with the mean diameter of necrosis determined by averaging the three orthogonal measurements.

Data Analysis
Correlation was determined for the diameter of the echogenic response measured sonographically and for the pathologically determined mean diameter of necrosis using the Pearson's correlation coefficient. This statistical method was chosen specifically to allow direct comparison with results of previous studies [16, 17, 20].

Results

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During all except three ablations, an echogenic response was visualized surrounding the radiofrequency probe (Fig. 1A,1B). The Pearson's correlation coefficient between the mean diameter of necrosis determined by pathology and the diameter of the echogenic response was 0.84 cm (Fig. 2). The mean difference between the maximum and minimum diameters of necrosis at pathologic examination was 1.0 ± 0.6 cm for all 22 ablations. The echogenic response overestimated the minimum diameter of necrosis (range, 0-1.6 cm; mean difference, 0.8 ± 0.4 cm) in 18 of 22 ablations (Fig. 3) and underestimated the maximum diameter of necrosis (range, 0.1-3.2 cm; mean difference, 0.9 ± 0.8 cm) in 16 of 22 ablations.

View larger version (163K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Method of measuring echogenic response and tissue necrosis. Sonogram obtained during radiofrequency ablation shows typical hyperechoic region surrounding needle electrode. Diameter of echogenic response (arrowheads) is measured as close to perpendicular to needle (arrow) as possible.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Method of measuring echogenic response and tissue necrosis. Photograph of pathologic specimen shows pale tissue centrally corresponding to area of complete tissue necrosis (arrowheads). Surrounding hemorrhagic rim (arrow) was excluded from measurements.

View larger version (14K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —Scatter plot shows correlation between mean diameter of necrosis determined at pathology and diameter of echogenic response measured on sonography. Dashed line represents perfect correlation. In general, as diameter of echogenic response increases, mean diameter of necrosis increases.

View larger version (14K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Scatter plot shows correlation between minimum diameter of necrosis determined at pathology and diameter of echogenic response measured on sonography. Dashed line represents perfect correlation. Note that most data points fall below line of perfect correlation, indicating that diameter of echogenic response overestimated short axis of ablation in most cases.

Discussion

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Radiofrequency ablation has been used successfully for the treatment of hepatocellular carcinoma, which is not amenable to conventional forms of therapy such as resection or transplantation. To achieve a cure, the zone of tissue death must encompass the entire tumor. Failure to create an adequate zone of necrosis will result in local recurrence at the ablation margin because of growth of residual tumor cells. Real-time imaging of the ablation process offers the potential to ensure that an adequate zone of necrosis is achieved. The use of sonography has become routine for radiofrequency ablation because it permits real-time visualization of the entire procedure, is relatively inexpensive, and is widely available. However, reports in the literature have questioned the ability of sonography to accurately predict the zone of necrosis [15,16,17, 20].

Although our study shows that the echogenic response observed with intraoperative sonography during radiofrequency ablation of cirrhotic liver tissue correlates significantly with the mean diameter of resultant tissue necrosis, we have shown that overestimation of the minimal diameter and underestimation of the maximal diameter occurs. The former observation implies that a poor echogenic response should be considered indicative of an inadequate ablation. Of the latter two observations, overestimation of the minimal diameter of necrosis is the most clinically significant because this may lead to inadequate ablation margins and predispose patients to tumor recurrence. The three ablations in our study failed to produce any measurable echogenic response, despite causing some limited tissue death. That tissue necrosis was created in these three patients suggests that the devices used produced sufficient energy to result in cellular death despite operating at temperatures below the threshold for microbubble production. When ablations producing no echogenic response are omitted from analysis, the minimal diameter of necrosis is overestimated in almost all cases using our technique. Therefore, the sonographically observed echogenic response diameter should be considered only an estimate of ablation size and may be most useful in alerting the operator when an ablation is likely to be inadequate.

Intravascular sonographic contrast agents have been used to evaluate the presence of residual tumor after radiofrequency ablation in humans and animal models [21,22,23,24,25]. These contrast agents provide evidence for residual viable tumor by showing foci of persistent vascularity in treated tumors, although the ideal time to image with these contrast agents remains to be determined. In their study of the use of a microbubble contrast agent after radiofrequency ablation in 40 patients, Choi et al. [22] chose to wait until the next morning to evaluate patients with sonography to allow time for the echogenic response to dissipate. However, according to Solbiati et al. [21], four of their 20 patients treated with radiofrequency ablation were studied with an intravascular sonographic contrast agent within 15 min of ablation

...because the area of increased echogenicity surrounding the radiofrequency electrode at the completion of the treatment session was substantially smaller than that usually observed, which suggested that these tumors may have been inadequately treated.

Residual foci of enhancement were revealed in all four of these patients who underwent additional ablation on the basis of these results. This latter article also shows the use of the echogenic response to immediately assess ablation adequacy as we suggest, with the small size of the echogenic response alerting the investigators to the possible need for additional imaging and treatment. Ultimately, the echogenic response may prove useful in determining which patients would benefit from immediate assessment with intravascular contrast material, although the previously mentioned studies suggest that sonographic contrast agent will ultimately provide a more accurate assessment of residual tumor.

Our study differs substantially from previous reports evaluating the use of sonography to assess the size of radiofrequency ablation. First, we evaluated the peak echogenic response, whereas prior articles have focused on either early or delayed sonographic findings [15,16,17].

Second, we evaluated intraoperative sonography using a transducer placed directly on the liver's surface. Despite the fact that many centers, including our own, currently perform a large number of hepatic radiofrequency ablations via the percutaneous approach, we consider our results relevant because intraoperative and laparoscopic techniques are also currently used for radiofrequency ablation of liver tumors [8,9,10,11, 18, 19]. One argument given for intraoperative or laparoscopic ablation of primary and metastatic liver tumors is that intraoperative findings may alter the treatment course despite thorough preprocedural imaging [18, 26].

Third, in our study, a considerable number of ablations were created with the Radionics device, whereas Cha et al. [16] and Raman et al. [17] used the RITA and Radiotherapeutics devices in their studies, respectively. De Baere et al. [27] recently reported that considerable differences in ablation size may exist between radiofrequency devices. In their animal study, they compared a cooled-tip triple-cluster needle, similar to the Radionics device used in our study, with an expandable needle, similar to the RITA device we used. These investigators found that the Radionics device produced a substantially larger ablation, presumably attributed to the higher power generator and increased energy deposition of the cooled-tip device. Dodd et al. (presented at the Radiological Society of North America meeting, December 1999) reported similar findings in humans. The same factors contributing to the larger size of ablation may also result in a more sonographically visible echogenic response with the cooled-tip electrode. Finally, many previous reports were based on normal animal models, whereas our ablations were performed in cirrhotic human livers. The sonographic response may be different for porcine and cirrhotic human livers.

Our study has several limitations. First, we did not evaluate the echogenic response in tumors. The degree to which the presence of tumor cells or tumor neovascularity may change the relationship between the echogenic response and tissue necrosis is unknown. However, the influence of a small tumor on the size of the subsequent necrosis is likely to be minimal. We have not noted a difference in the size of thermal injury produced by a single ablation of tumors of various sizes less than 3 cm in the same patient. Second, we did not correlate the relationship of the size of the echogenic response produced by multiple overlapping ablations with the composite area of ischemic necrosis. It is widely believed (although, to our knowledge, not specifically reported) that the echogenic response produced by multiple overlapping ablations is too ill defined and heterogeneous to be of much clinical use for predicting the size of the area of tissue necrosis. Third, our ablations were performed in cirrhotic human livers. Thus our results may not be applicable to noncirrhotic livers. Nonetheless, our results have particular relevance for the treatment of hepatocellular carcinoma that typically occurs with cirrhosis. Lastly, the accuracy of measurement of the echogenic response might have been better if we had measured the volume of the echogenic response rather than a single diameter. However, the posterior acoustic shadowing produced by the echogenic response makes such measurements virtually impossible.

In conclusion, we have shown that a significant correlation exists between the diameter of the echogenic response observed with intraoperative sonography during radiofrequency ablation of the cirrhotic liver and the mean diameter of the subsequent area of tissue necrosis. However, a single measurement, as performed in our study, is frequently larger than the smallest diameter and smaller than the largest diameter of the area of induced tissue necrosis. Therefore, monitoring of the echogenic response may be most useful in providing a rapid and convenient approximation of ablation size and alerting the operator when an ablation is likely to be inadequate. In other words, a small echogenic response suggests a small zone of necrosis and should prompt consideration of reablation or further assessment with an alternative technique such as contrast-enhanced sonography or CT. Because the echogenic response is transient and provides only an estimate of ablation size, an alternative form of cross-sectional imaging, such as CT or MR imaging, should be performed when feasible, both as a baseline study and for future follow-up.

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