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1 Department of Radiology, Taipei Municipal Jen-Ai Hospital, No. 10, Sec. 4,
Jen-Ai Rd., Taipei 106, Taiwan.
2 Department of Radiology, Taipei Medical University School of Medicine, Taipei
110, Taiwan.
3 Department of Gastroenterology, Taipei Municipal Jen-Ai Hospital, Taipei 106,
Taiwan.
Received November 25, 2002;
accepted after revision July 2, 2003.
Address correspondence to R.-C. Chen.
Abstract
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SUBJECTS AND METHODS. Our study population was 44 patients with 53 viable portions of tumors or recurrent hepatocellular carcinomas that had developed after the initial treatment of the primary tumor. The tumors were treated with CO2-enhanced sonographically guided percutaneous ethanol injection via the catheter that had been placed in the hepatic artery for angiography. Thirty-seven (84.1%) of the 44 patients had cirrhosis. Of these 37 patients, 23 had Child-Pugh class A cirrhosis, and 14 had Child-Pugh class B.
RESULTS. Overall, thirty-four (64.2%) of the 53 tumors showed complete necrosis after treatment, eight (15.1%) of the 53 showed partial necrosis, and 11 (20.8%) of the 53 showed no response. The cumulative survival rates of patients who underwent CO2-enhanced sonographically guided percutaneous ethanol injection were 81%, 71%, and 44% for 1, 2, and 3 years, respectively. The small tumors were more responsive to the treatment. The tumor recurrence rate was 56.8%. In 9.1% of these cases, carcinoma had metastasized to other organs.
CONCLUSION. CO2-enhanced sonographically guided percutaneous ethanol injection is effective for patients with viable portions of a treated tumor or new tumors who have undergone transcatheter arterial chemoembolization, percutaneous ethanol injection, or a combination of the two treatments. This finding is especially true of patients who are not good candidates for repeated treatments.
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Detecting the viable part of a treated tumor on unenhanced sonography is difficult. Thus, using conventional sonographically guided percutaneous ethanol injection to treat these tumors is ineffective. The literature documents the usefulness of color Doppler sonography, power Doppler sonography, and contrast-enhanced sonography in assessing such tumors [7, 8]. The detection rate of viable tumors using Doppler sonography is low compared with the rate using contrast-enhanced sonography [9]. Contrast-enhanced sonographically guided percutaneous ethanol injection has been reported to be effective for treating viable tumors [8, 10]. However, the duration of enhancement provided with a sonographic contrast agent (Levovist [galactose palmitric acid], Schering, Berlin, Germany) is brief [10], making it difficult to perform sonographically guided percutaneous ethanol injection.
The carbon dioxide (CO2) enhancement in viable tumors is much longer than that of Levovist [10, 11]. Some researchers have reported using CO2-enhanced sonographically guided percutaneous ethanol injection to treat hepatocellular carcinomas that cannot be identified on unenhanced sonography [12, 13]. To our knowledge, using CO2-enhanced sonographically guided percutaneous ethanol injection to treat the difficult-to-treat viable tumor portions or recurrent hepatocellular carcinomas has not been previously described. The purpose of our study was to evaluate the efficacy of CO2-enhanced sonographically guided percutaneous ethanol injection in treating patients with these tumors.
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Dynamic CT findings indicated that 25 patients had 27 tumors suspected to
be viable portions of treated tumors or recurrent tumors, whereas MRI findings
showed nine patients with 11 such tumors. The 10 tumors in the remaining 10
patients were suspected to be viable portions of tumors because of the
patients' elevated 
-fetoprotein levels (> 200 ng/mL), although the
presence of the tumors could not be confirmed on dynamic CT because of a dense
concentration of Lipiodol (iodized oil, Andre Guerbet, Aulnay-sous-Bois,
France) retained from a previous transcatheter arterial chemoembolization.
Therefore, these patients underwent diagnostic angiography with
CO2-enhanced sonography (Fig.
1A,
1B,
1C), on which the lesions were
evident. Three of the 10 patients underwent CO2-enhanced
sonographically guided biopsy and were known to have viable portions of tumors
before the CO2-enhanced sonographically guided percutaneous ethanol
injection was performed. Five additional small tumors were found on
CO2-enhanced sonography. Of these five additional tumors, two were
also seen on angiography; the remaining three were removed during
CO2-enhanced sonographically guided biopsy, and pathologic
examination confirmed that they were hepatocellular carcinomas.
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We treated 44 patients with 53 tumors with CO2-enhanced sonographically guided percutaneous ethanol injection because the viable portions of the primary tumor or the recurrent tumors could not be detected on conventional sonography. The tumor size at the time of the procedure ranged from 1 to 13 cm (mean, 3.2 cm); 25 tumors were smaller than 2 cm, 18 were between 2 and 5 cm, and 10 were larger than 5 cm. The specific reasons that the patients were treated with CO2-enhanced sonographically guided percutaneous ethanol injection were as follows: small portions of viable tumor were seen on CO2-enhanced sonography but not on unenhanced sonography after repeated (more than three) transcatheter arterial chemoembolizations (16/44 patients or 36.4%); the feeder arteries were occluded because of repeated transcatheter arterial chemoembolizations, a viable tumor portion or recurrent tumor (with or without small collateral arteries to supply it) was detected on CO2-enhanced sonography but not on unenhanced sonography, or a repeated transcatheter arterial chemoembolization had failed (10/44 or 22.7%) (Fig. 2A, 2B, 2C, 2D, 2E); one or two small recurrent tumors or viable portions of tumors were visualized on CO2-enhanced sonography after percutaneous ethanol injection or combined chemoembolization and ethanol injection treatment (13/44 or 29.5%) (Fig. 3A, 3B, 3C, 3D, 3E); and liver or renal function had deteriorated after previous treatments and small viable tumors were not identifiable on unenhanced sonography (4/44 or 11.4%).
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The CO2-enhanced sonographically guided percutaneous ethanol injection was performed by experts in the procedure after the patient underwent angiography. Through the angiographic catheter in the hepatic propria artery, 2–6 mL of CO2 gas was injected as a bolus into the hepatic artery. We used a gray-scale sonography scanner to monitor the flow of the CO2 gas and the enhancement of the treated liver tumor. Then, an entire liver survey was performed in every patient to detect additional small hepatic tumors.
With the catheter left in the hepatic artery, the patients were prepared for the percutaneous ethanol injection procedure. Again, a bolus of 2–6 mL of CO2 gas was injected into the liver. The CO2 gas stayed in the tumor for 12–15 min, which was long enough to perform the percutaneous ethanol injection. Each procedure was performed using 2–3 mL of 99% pure ethanol solution with the patient under local anesthesia [14]. Each tumor required from two to six sessions of CO2-enhanced sonographically guided percutaneous ethanol injection. The catheter was removed immediately after the procedure in all but six patients. In these patients, the catheter was left in the hepatic artery because more than three injection sessions were required, and the remaining sessions had to be performed on subsequent days. Continuous heparinization kept the catheter open. The longest period that the catheter remained in the patient was 3 days.
After treatment with CO2-enhanced sonographically guided
percutaneous ethanol injection, -fetoprotein levels were checked, and
unenhanced sonography (for detecting tumor recurrence and monitoring the size
of the treated tumors) was performed every 3 months. Dynamic CT was performed
3–6 months later in 35 patients; contrast-enhanced MRI was performed in
the remaining nine patients. Contrast-enhanced MRI (two patients), angiography
with CO2-enhanced sonography (four patients), or needle biopsy (one
patient) was performed in patients with a discrepancy between the results of
sonography and the results of CT or MRI or of tests for -fetoprotein
levels. Thereafter, dynamic CT or contrast-enhanced MRI was performed once a
year until the patient died. The overall duration of followup ranged from 6 to
37 months (mean, 26 months) after the injection procedure.
Results of follow-up dynamic CT, contrast-enhanced MRI, or angiography were divided into three categories: complete necrosis with no contrast medium enhancement, partial necrosis with enhanced portions seen in the treated tumors, or no response, with continuing tumor growth [15]. Tumor necrosis was evaluated independently by two radiologists. The final results were obtained by consensus. Complete necrosis was confirmed 6 months later on contrast-enhanced CT or MRI.
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Eleven (20.8%) of the 53 tumors were recurrent tumors; eight showed complete necrosis, one showed partial necrosis, and the other two showed no response. The size of the recurrent tumors ranged from 1.0 to 1.6 cm. We used an analysis of variance test to correlate tumor size with the effectiveness of the treatment. The smaller the tumor, the more necrosis was achieved (p < 0.001).
Overall, 34 (64.2%) of 53 tumors showed complete necrosis, eight (15.1%) of 53 showed partial necrosis, and 11 (20.8%) of 53 showed no response. The patients with the 34 completely necrotic tumors were followed up with contrast-enhanced dynamic CT (28 tumors) or MRI (two tumors) 6 months after the first follow-up CT or MRI examination. The patients with the four remaining tumors died as a result of coexisting nonnecrotic tumors or distant metastasis.
Twenty-five (56.8%) of the 44 patients developed remote recurrent tumors within 3 years of receiving the CO2-enhanced sonographically guided percutaneous ethanol injection. Five of the 25 patients also had local recurrence after treatment. All five tumors showed either partial necrosis or no response to CO2-enhanced sonographically guided percutaneous ethanol injection. Four of the 25 showed metastases to other organs.
The cumulative survival rates of patients who underwent CO2-enhanced sonographically guided percutaneous ethanol injection were 81%, 71%, and 44% for 1, 2, and 3 years, respectively. The 1-, 2-, and 3-year survival rates of patients whose largest tumor was smaller than 2 cm were 93%, 86%, and 73%, respectively; survival rates of patients whose largest tumor was between 2 cm and 5 cm were 74%, 67%, and 52%, respectively; and survival rates of patients with a tumor larger than 5 cm were 57%, 42%, and 28%, respectively. The difference in survival rates between the patients with tumors smaller than 2 cm and the patients with tumors larger than 5 cm was statistically significant when analyzed using a log-rank test (p < 0.05), but there was no significant difference found in other groups.
The 1-, 2-, and 3-year survival rates of patients with Child-Pugh class A cirrhosis were 90%, 79%, and 65%, respectively, and same survival rates for patients with Child-Pugh class B cirrhosis were 60%, 50%, and 30%, respectively. Obviously, the survival rate of patients with Child-Pugh class A was significantly better than those with Child-Pugh class B (p < 0.05).
The cumulative survival rates of patients since the initial diagnosis of hepatocellular carcinoma were 92%, 85%, 72%, 66%, and 43% for 1, 2, 3, 4, and 5 years, respectively.
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We found that the CO2 gas could remain in a tumor for 10 to 15 min [11]. Thus, the viable portion of the tumor could be well defined [14]. The length of the enhancement, the obvious CO2 stain in viable tumor portions and new tumors, the low cost of CO2, and the lack of limitations associated with small doses of CO2 injection have made the CO2-enhanced sonographically guided procedure an attractive treatment option.
In our study, we used CO2-enhanced sonographically guided percutaneous ethanol injection in patients who were not good candidates for further treatment after repeated transcatheter arterial chemoembolization or percutaneous ethanol injection or who had small tumors seen on CO2-enhanced sonography but not on unenhanced sonography. In most patients, the difficulties associated with further transcatheter arterial chemoembolization were noted during the chemoembolization procedure; thus it was easy to perform CO2-enhanced sonography while the patient was on the table for chemoembolization or for diagnostic angiography with the angiographic catheter already inserted into the artery.
Of the 53 tumors identified, 34 (64.2%) showed complete necrosis, eight (15.1%) showed partial necrosis, and 11 (20.8%) showed no response. Therefore, 42 tumors (79.2%) that could not be treated with further transcatheter arterial chemoembolization or percutaneous ethanol injection showed a response after the CO2-enhanced sonographically guided percutaneous ethanol injection.
The indication for CO2-enhanced sonographically guided percutaneous ethanol injection is similar to that for percutaneous ethanol injection. It is effective in treating small viable tumor portions or tumors smaller than 2 cm [17]. In our study, the effectiveness of CO2-enhanced sonographically guided percutaneous ethanol injection correlated well with the size of the tumor. The smaller the tumor, the more effective the treatment was. Our study also showed that patients with tumors smaller than 2 cm had a significantly better survival rate than those with tumors larger than 5 cm. Therefore, we believe that for patients with large tumors or more than three viable tumor portions or recurrent tumors, CO2-enhanced sonographically guided percutaneous ethanol injection would not be suitable. Radiofrequency (RF) ablation therapy could be used in these patients [18]. RF ablation under CO2-enhanced sonographic guidance might be possible, but more study is needed.
The survival rates were also affected by the degree of cirrhosis. The patients with Child-Pugh class A cirrhosis lived significantly longer than those with Child-Pugh class B.
The long-term survival rate for patients with hepatocellular carcinoma after transcatheter arterial chemoembolization is low [19, 20]. The survival rate can be improved by repeated transcatheter arterial chemoembolization. Ikeda et al. [15] showed cumulative survival rates of 76.5%, 54.5%, and 41.1% for 1, 2, and 3 years after treatment, respectively. Cumulative survival rates can also be improved by combining transcatheter arterial chemoembolization and percutaneous ethanol injection therapy. Tateishi et al. [21] reported survival rates of 92%, 52% and 32% for 1, 3, and 5 years after combined therapy. Tanaka et al. [22] found 68% and 35% survival rates for 3 and 5 years after combined treatments. Ito et al. [23] reported survival rates of 66%, 33%, and 18% for 1, 3 and 5 years after multidisciplinary treatments, respectively.
In our study, the cumulative survival rates for the patients after CO2-enhanced sonographically guided percutaneous ethanol injection were 81% at 1 year and 44% at 3 years after treatment. Most of these patients cannot be treated further with any method other than CO2-enhanced sonographically guided percutaneous ethanol injection. The cumulative survival rates of the patients since the initial diagnosis of hepatocellular carcinoma were 92% at 1 year, 72% at 3 years, and 43% at 5 years, which were significantly higher than the survival rates that have been reported previously (chi-square test, p < 0.05) [15, 23].
Although the effect of treatment in the tumors was good, the recurrence of tumors is a critical problem in the treatment of hepatocellular carcinoma. In our series, approximately 56.8% patients had a recurrent tumor, thus lowering the survival rate. High recurrence rates have also been reported in other treatment methods such as surgery (44%) [24, 25] and percutaneous ethanol injection alone (51%) [26]. A treatment to prevent the recurrence of tumors is a major task for future study.
In conclusion, our results suggest that CO2-enhanced sonographically guided percutaneous ethanol injection may be an effective treatment technique for patients with viable tumor portions or recurrent tumors who have undergone previous transcatheter arterial chemoembolization, percutaneous ethanol injection, or a combination of the treatments, especially those with tumors smaller than 5 cm who are not appropriate candidates for further transcatheter arterial chemoembolization or percutaneous ethanol injection. For those with viable tumor portions or recurrent tumors larger than 5 cm, use of other treatment methods is suggested.
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