Published online before print March 1, 2002, 10.1148/radiol.2231010862
(Radiology 2002;223:115-120.)
© RSNA, 2002
Vascular and Interventional Radiology |
CT-guided Transthoracic Percutaneous Ethanol Injection for Hepatocellular Carcinoma Not Detectable with US1
Toshiya Shibata, MD,
Yuji Iimuro, MD,
Yuzo Yamamoto, MD,
Iwao Ikai, MD,
Kyo Itoh, MD,
Yoji Maetani, MD,
Fumie Ametani, MD,
Takeshi Kubo, MD and
Junji Konishi, MD
1 From the Departments of Diagnostic Imaging and Nuclear Medicine (T.S., K.I., Y.M., F.A., T.K., J.K.) and Gastroenterological Surgery (Y.I., Y.Y., I.I.), Kyoto University Graduate School of Medicine, Shogoin, Sakyoku, Kyoto 606-8507, Japan. Received April 30, 2001; revision requested May 21; revision received August 7; accepted September 28. Address correspondence to T.S. (e-mail: ksj@kuhp.kyoto-u.ac.jp).
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ABSTRACT
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PURPOSE: To evaluate the safety and effectiveness of computed tomography (CT)-guided percutaneous ethanol injection (PEI) for the treatment of hepatocellular carcinoma (HCC) not detectable with ultrasonography (US).
MATERIALS AND METHODS: Between April 1994 and January 2001, 51 patients with 57 HCC nodules not detectable with US underwent CT-guided transthoracic PEI. Complications associated with the transthoracic approach, effectiveness of transthoracic PEI, and prognosis of the patients were evaluated.
RESULTS: Seventy-one PEI sessions were performed for 57 nodules. Complications included pneumothorax in 21 sessions (30%) for 19 nodules (33%), moderate pleural effusion in four sessions (6%) for four nodules (7%), and hemoptysis in three sessions (4%) for two nodules (4%). A chest tube was required for pneumothorax in five sessions (7%) for five nodules (9%), and pleural effusion drainage was performed in two sessions (3%) for two nodules (4%). Apparent tumor necrosis was noted at CT in 51 nodules (89%). During follow-up (range, 3 months to 5
years; mean, 29 months ± 18 [SD]), local recurrence was seen in seven nodules (12%), three of which received repeat treatment with transthoracic PEI. Twenty-six patients survived, and 25 patients died of multiple tumors, hepatic failure, or rupture of esophageal varices.
CONCLUSION: Transthoracic PEI seems to be relatively safe and effective for the treatment of HCC not detectable with US.
© RSNA, 2002
Index terms: Alcohol ablation, 761.323, 761.1299 • Liver, interventional procedures, 761.1299 • Liver neoplasms, therapy, 761.12119, 761.323, 761.33
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INTRODUCTION
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Hepatocellular carcinoma (HCC) is one of the most common malignancies in Far East Asia and Southeast Asia (1). Surgical resection is the standard curative treatment for HCC. However, patients with HCC usually have associated cirrhosis or chronic hepatitis, and thus most patients are not suitable for surgical resection. Several tumor ablation therapies (eg, percutaneous ethanol injection [PEI], radio-frequency ablation, or percutaneous microwave coagulation therapy) have been performed for local control of HCC (2–6). PEI has been used most widely as an effective, minimally invasive therapy for small HCC 3.0 cm or smaller (2,3). The prognosis of patients with small HCC who are treated with PEI is comparable to that of patients treated with surgical resection (7,8). Standard percutaneous ablation therapy is performed with real-time ultrasonographic (US) guidance. Sometimes some nodules cannot be detected with US, however, such as nodules that are located in the hepatic dome, in the deep region of the liver, and on the liver surface, or small nodules that are 1.0 cm or smaller. Computed tomographic (CT) guidance can also be used with percutaneous ablation therapy (9). Yet, most nodules that are located in the upper portion of the liver, mainly those in the hepatic dome, would require transthoracic introduction of the needle. The purpose of this study was to evaluate the safety and effectiveness of CT-guided transthoracic PEI for the treatment of HCC not detectable with US.
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MATERIALS AND METHODS
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Patients
Between April 1994 and January 2001, CT-guided transthoracic PEI was performed for 57 HCC nodules not detectable with US in 51 patients (43 men and eight women; age range, 47–83 years; mean age, 67 years). Forty-four patients received a positive test result for hepatitis C virus, and five patients received a positive test result for hepatitis B surface antigen. Serum 
-fetoprotein levels were greater than 200 µg/L in 12 patients, and plasma levels of protein induced by vitamin K absence on antagonist II (PIVKA II) were greater than 50 mAU/mL in 10 patients. Platelet counts were more than 50 x 109/L, and prothrombin activity was greater than 40% in all patients.
Our criteria for selection of patients who were suitable for tumor ablation therapy (ie, PEI, percutaneous microwave coagulation therapy, or radio-frequency ablation) were three or fewer HCC nodules 3.0 cm in diameter or smaller. A combination of transcatheter arterial embolization and tumor ablation therapy was performed for solitary nodules to enhance curative treatment (10,11). Transcatheter arterial embolization was performed by injecting an emulsion of 3–5 mL of iodized oil (Lipiodol; Laboratoire Guerbet, Aulnay-sous-Bois, France) and 30–50 mg of epirubicin hydrochloride (Farmorubicin; Kyowa Hakko, Tokyo, Japan) into the proper, right, or left hepatic artery, followed by injection of gelatin sponge particles (Spongel; Yamanouchi Pharmaceutical, Tokyo, Japan). As palliative treatment, tumor ablation therapy was applied for local recurrent nodules after transcatheter arterial embolization or for nodules 5.0 cm or smaller in which transcatheter arterial embolization was not effective.
During our study period, CT-guided ablation therapy was performed in 76 consecutive nodules not detectable with US. Among these, 57 nodules located in the upper region of the liver (mainly in the hepatic dome) that were treated with CT-guided transthoracic PEI were included in the present study. PEI was chosen for these nodules because the needle used with PEI is smaller than the electrode used with either radio-frequency ablation or percutaneous microwave coagulation therapy. The size of the 57 nodules ranged from 1.0 to 3.0 cm in diameter (mean, 2.3 cm). Twenty-seven nodules were located in the anterosuperior segment of the liver, 15 were in the posterosuperior segment, seven were in the medial segment, six were in the lateral segment, and two were in the caudate lobe.
Diagnosis of HCC was confirmed (a) in 22 nodules by means of CT-guided needle biopsy, which was performed with the coaxial method immediately before the first ablation therapy procedure (12,13); (b) in 28 nodules according to characteristic findings of both hepatic angiography and CT, which were performed after injection of iodized oil at transcatheter arterial embolization; and (c) in seven nodules according to characteristic findings of dynamic CT and high serum -fetoprotein levels or high plasma levels of PIVKA II. The Human Subjects Research Review Board at our institution approved our review study. Before treatment, informed consent was obtained from all patients. Each patient was provided with a comprehensive treatment description, which specified that complications associated with the transthoracic approach could possibly occur and that his or her records and images could be reviewed at a later date.
PEI Technique
One author (T.S.) performed transthoracic PEI. Atropine sulfate (0.5 mg) (Tanabe Seiyaku, Osaka, Japan) and pentazocine (15 mg) (Sosegon; Yamanouchi Pharmaceutical) were administered intramuscularly as premedication for sedation. The selected body position was supine, prone, or lateral decubitus, depending on the proximity of the lesion to the abdominal wall. After a plastic grid was applied to the skin, pretreatment CT with a 3- or 5-mm section thickness was performed to determine the optimal skin entry point, the most direct route to the HCC nodule, and the shortest route for bypassing the lung parenchyma. When nodules could not be detected clearly at nonenhanced CT, dynamic contrast material–enhanced CT was performed: Early- and late-phase CT scans were obtained after injection of 80–100 mL of 65% iopamidol (Iopamiron 300; Nihon Schering, Osaka, Japan), which was injected at a rate of 3 mL/sec. Iodized oil spots in the nodules were targeted in 28 of 57 nodules following transcatheter arterial embolization. The procedure was performed by using conventional CT guidance with a HiSpeed Advantage scanner (GE Medical Systems, Milwaukee, Wis) between April 1994 and December 1998 and by using CT fluoroscopy with a HiSpeed LX/I scanner (GE Medical Systems) between January 1999 and January 2001 (14).
CT-guided transthoracic liver biopsy was performed for 22 nodules. After disinfection of skin and local anesthetization with 1% lidocaine (Xylocaine; AstraZenca Japan, Osaka, Japan) a 19-gauge introducer needle (Co-Axial Introducer Needle; Boston Scientific, Natick, Mass) was inserted with CT guidance. Needle passes were transpulmonary. Then, needle biopsy was performed with a 20-gauge automatic biopsy needle (Temno gun; Bauer, Via del Fosso, Italy). After withdrawal of the biopsy needle, a 21-gauge needle with three side holes and no end hole (PEIT Needle; Hakko, Tokyo, Japan) was inserted through the introducer. If necessary, an additional one or two PEI needles were introduced with the tandem method. The standard dose of injected ethanol was calculated according to the following equation: V = 4/3 · 
· (r + 0.5)3, where V is the volume of ethanol in milliliters and r is the radius of a nodule in centimeters (2). However, injected ethanol shows markedly low attenuation at CT, so we administered ethanol until the size of the marked low attenuation became equal to or larger than the size of the nodule. The diffusion of ethanol in the nodule was monitored with conventional CT guidance by performing CT after every 5-mL ethanol injection. The diffusion of ethanol was monitored in real time by using CT fluoroscopy. In our study, 5–20 mL of absolute ethanol was injected per session. Pentazocine (15 mg) was intravenously injected in patients who complained of severe pain during ablation therapy.
Data Evaluation
The number of transthoracic PEI sessions required for each nodule, the patient position in which each PEI session was performed, and the number of pleural passes of the needle in each PEI session were evaluated. A single needle puncture produced two pleural passes on both sides of the chest wall and diaphragm. A total number of pleural passes was assessed for nodules in which PEI was performed immediately following needle biopsy.
Immediately after PEI, CT scans of the lower chest and upper abdomen were obtained and interpreted by one author (T.S.). Posteroanterior chest radiographs were routinely obtained 3 and 12 hours after completion of therapy and were interpreted by one of three authors (Y.I., Y.Y., I.I.). Any complications associated with the transthoracic approach, including pneumothorax with and without the need for a chest tube, minor and moderate pleural effusion, minor (ie, hemoptysis) and major lung bleeding, and air embolism, were evaluated. Pleural effusion was classified as minor or moderate effusion. Minor effusion was defined as effusion that was depicted on CT scans obtained immediately after PEI but was not detected on chest radiographs. Moderate effusion was defined as effusion that was detected on chest radiographs. Lung bleeding was classified either as hemoptysis (ie, minor bleeding), which improved with conservative treatment, or as major lung bleeding, which required blood transfusion or surgical intervention.
Patients were routinely admitted to the hospital for 24 hours, and those with complications were admitted for 2–6 days. A relationship between the number of pleural passes and incidence of pneumothorax was statistically analyzed by using the Mann-Whitney test. Dynamic CT was performed with the HiSpeed Advantage scanner to assess therapeutic effectiveness 1 month after PEI. The CT protocol was performance of noncontrast CT and early- and late-phase CT after injection of 100 mL of 65% iopamidol, which was injected at a rate of 3 mL/sec. If no lesion enhancement was seen in the treated nodule at CT, apparent tumor necrosis was diagnosed.
Local recurrence (ie, regrowth of the treated nodule) was assessed with dynamic CT that was performed at 3-month intervals. Tumor seeding was evaluated by means of chest radiographs that were obtained at 2- or 3-month intervals and dynamic CT scans that were obtained at 3-month intervals. These CT scans and posteroanterior radiographs were evaluated by one of four authors (Y.M., F.A., K.I., T.K.). Follow-up periods ranged from 3 months to 5 years after therapy (mean follow-up, 29 months ± 18 [SD]). Patient status (ie, living or deceased [and cause of death], presence of local recurrence, or presence of tumor seeding) was recorded at the end of the follow-up period.
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RESULTS
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A total of 71 sessions of PEI were performed for 57 nodules (Figs 1, 2). A single session of PEI was performed for 46 nodules, two sessions were performed for eight nodules, and three sessions were performed for three nodules. Fifty-four sessions were performed with the patient in the supine position, 15 sessions were performed with the patient in the prone position, and two sessions were performed with the patient in the lateral decubitus position. Two to 16 pleural passes were performed (mean, 7.3 passes ± 3.5; median, six passes) during each session.
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Figure 1a. Transverse CT scans obtained in a 71-year-old woman with HCC in the hepatic dome. (a) Early-phase scan obtained before PEI shows a 1.4-cm nodule (arrow) in the anterosuperior segment of the liver. (b) At CT fluoroscopy, two needles were inserted into the nodule with a right-sided approach, and 10 mL of absolute ethanol was injected. (c) Early-phase scan obtained 1 year after PEI shows no enhancement (arrowhead) in the tumor area.
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Figure 1b. Transverse CT scans obtained in a 71-year-old woman with HCC in the hepatic dome. (a) Early-phase scan obtained before PEI shows a 1.4-cm nodule (arrow) in the anterosuperior segment of the liver. (b) At CT fluoroscopy, two needles were inserted into the nodule with a right-sided approach, and 10 mL of absolute ethanol was injected. (c) Early-phase scan obtained 1 year after PEI shows no enhancement (arrowhead) in the tumor area.
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Figure 1c. Transverse CT scans obtained in a 71-year-old woman with HCC in the hepatic dome. (a) Early-phase scan obtained before PEI shows a 1.4-cm nodule (arrow) in the anterosuperior segment of the liver. (b) At CT fluoroscopy, two needles were inserted into the nodule with a right-sided approach, and 10 mL of absolute ethanol was injected. (c) Early-phase scan obtained 1 year after PEI shows no enhancement (arrowhead) in the tumor area.
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Figure 2a. Transverse CT scans obtained in a 65-year-old woman with a recurrent nodule after transcatheter arterial embolization. (a) Early-phase scan obtained before PEI shows a 2.3-cm recurrent nodule (arrows). (b) A PEI needle was introduced into the nodule with the coaxial method, and 10 mL of ethanol was injected with CT fluoroscopic guidance. Chest CT scan (not shown) obtained immediately after PEI showed no pneumothorax or pleural effusion.
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Figure 2b. Transverse CT scans obtained in a 65-year-old woman with a recurrent nodule after transcatheter arterial embolization. (a) Early-phase scan obtained before PEI shows a 2.3-cm recurrent nodule (arrows). (b) A PEI needle was introduced into the nodule with the coaxial method, and 10 mL of ethanol was injected with CT fluoroscopic guidance. Chest CT scan (not shown) obtained immediately after PEI showed no pneumothorax or pleural effusion.
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Complications associated with the transthoracic approach are listed in the Table. Pneumothorax was first seen on CT scans obtained immediately after PEI in 10 of 21 sessions (Fig 3), on a posteroanterior chest radiograph obtained 3 hours after PEI in six sessions, and on a posteroanterior chest radiograph obtained 12 hours after PEI in five sessions. Minor pleural effusion was first seen on CT scans obtained immediately after PEI in six sessions, and moderate pleural effusion was first seen on a posteroanterior chest radiograph obtained 12 hours after PEI in four sessions. Interventional procedures were required for complications in six sessions (8%) for six nodules (11%). Chest tube placement for pneumothorax was required in five sessions for five nodules, and in one of these sessions, drainage of moderate pleural effusion was performed (for one nodule). Needle aspiration of moderate pleural effusion was performed in one session for one nodule. In other sessions in which complications were experienced, no interventional procedures were necessary. No serious life-threatening complications (ie, major lung bleeding or air embolism) were encountered. The number of pleural passes in the group with pneumothorax (n = 21) versus the number of passes in the group without pneumothorax (n = 50) was two to 16 passes versus two to 14 passes, respectively (mean, 7.6 passes ± 3.8 vs 7.1 passes ± 3.4, respectively; median, eight passes vs six passes, respectively). There was no statistically significant relationship between the number of pleural passes and the occurrence of pneumothorax (P = .71).
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Figure 3a. Transverse CT scans obtained in a 63-year-old man with an HCC nodule in the hepatic dome. (a) Early-phase scan obtained before PEI shows a 1.2-cm nodule (arrow) in the anterosuperior segment. (b) Scan obtained during PEI shows a small pneumothorax site (arrows). Pneumothorax resolved without chest tube placement.
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Figure 3b. Transverse CT scans obtained in a 63-year-old man with an HCC nodule in the hepatic dome. (a) Early-phase scan obtained before PEI shows a 1.2-cm nodule (arrow) in the anterosuperior segment. (b) Scan obtained during PEI shows a small pneumothorax site (arrows). Pneumothorax resolved without chest tube placement.
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Apparent tumor necrosis was seen at CT in 51 nodules (89%), and residual enhancement of the treated nodule was seen in six nodules (11%). Local recurrence was seen in seven nodules (12%) 3–18 months after PEI (mean, 9.9 months ± 4.7). Of seven nodules with local recurrence, three received repeat treatment with transthoracic PEI. No tumor seeding was seen during follow-up. Twenty-six patients survived, and 25 patients died of multiple tumors, hepatic failure, or rupture of esophageal varices. Of the 26 patients who survived, four had evidence of local recurrence.
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DISCUSSION
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Several reports have described transthoracic CT-guided lung biopsy (13,15–19). Pneumothorax is the most frequent complication of the procedure; reported rates of pneumothorax range from 8% to 61%, and chest tube placement is required in 2%–18% of these cases. Major complications of transthoracic CT-guided lung biopsy include tumor seeding, air embolism, and major lung bleeding, but incidence of these complications is low (13, 15–19). The effectiveness of transthoracic lung biopsy for the diagnosis of malignant lesions has been well established, and the procedure is performed worldwide. Moreover, Dupuy et al (20) have performed percutaneous radio-frequency ablation for malignancies in the lung.
CT-guided PEI or CT-guided microwave coagulation therapy has been performed in a small number of HCC nodules that were undetected with US (21–23). In these 17 sessions, transthoracic CT-guided PEI was performed for 11 nodules, and pneumothorax occurred in three of 17 sessions (18%). Gervais et al (12) reported the use of percutaneous transpulmonary CT-guided liver biopsy in 13 patients, none of whom developed pneumothorax. In comparison to these results, the rate of pneumothorax (30%) in our study seems higher. However, two pleural passes on both sides of the chest wall and diaphragm were needed to access the hepatic nodule with the transthoracic approach. Thus, the rate of pneumothorax in our study might be reasonable and comparable to rates in other studies in which CT-guided transthoracic lung biopsy was performed. Also, when our results are compared with results of these studies, it seems that moderate pleural effusion might have occurred more frequently in our study. All four nodules associated with moderate pleural effusion were located on the liver surface near the diaphragm. Pleural effusion might represent tissue reaction to reflux of the injected ethanol into the thoracic cavity. Although tumor seeding was not seen in our study, this complication may occur in rare instances. Zerby et al (24) reported a case of pleural seeding from HCC after PEI. Neff et al (25) described the deaths of four patients following transgression of the pleural space during biliary drainage, but they also stated that needle puncture of the pleura was not risky.
Ablation therapy following intraperitoneal saline infusion (ie, the artificial ascites method) has been reported as an alternative technique (26,27). This method is suitable for nodules in the anterosuperior segment of the hepatic dome. However, in patients who have already undergone hepatectomy or abdominal surgery, saline might not spread adequately due to adhesion. This technique is not suitable for nodules in the posterosuperior lateral segment or the caudate lobe. Furthermore, some small nodules in cirrhotic liver tissue are actually undetectable with US. Thoracoscopic transdiaphragmatic ablation therapy has been described as an alternative method for treatment of HCC in the hepatic dome (28). However, thoracoscopy is usually performed with use of general anesthesia and thus is more invasive than percutaneous ablation therapy.
Several types of tumor ablation therapy may be performed, such as radio-frequency ablation, percutaneous microwave coagulation therapy, or PEI (4–6). Dupuy et al (20) reported that performance of percutaneous transthoracic radio-frequency ablation for malignancies in the lung was safe and effective. We believe, however, that the risk of complications (ie, pneumothorax, major lung bleeding, or tumor seeding) may be higher with transthoracic radio-frequency ablation or percutaneous microwave coagulation therapy because the needle is larger than that used with transthoracic PEI. Further evaluation seems necessary on the use of radio-frequency ablation or percutaneous microwave coagulation therapy during the transthoracic procedure.
Percutaneous ablation therapy has been the treatment of choice for small HCC in many institutions because of its effectiveness and its cost (which is less than the cost of hepatic resection) and because it can be performed in patients with poor hepatic function. In our study, apparent tumor necrosis was noted at CT in 51 of 57 nodules (90%), and the rate of local recurrence (12%) was comparable to the rates of 0%–17% from previous studies in which large series of HCCs were treated with PEI (2,3,29). Transthoracic CT-guided PEI was effective for the local control of HCC, and, thus, this procedure is considered clinically acceptable.
In conclusion, while pneumothorax and pleural effusion can potentially occur with transthoracic CT-guided PEI, we believe that it is a suitable alternative procedure for the treatment of HCC not detectable with US on the basis of its relative safety and effectiveness.
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FOOTNOTES
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Abbreviations: HCC = hepatocellular carcinoma,
PEI = percutaneous ethanol injection
Author contributions: Guarantors of integrity of entire study, all authors; study concepts and design, T.S., Y.I., Y.Y.; literature research, T.S., I.I., Y.M.; clinical studies, T.S., Y.M., F.A.; data acquisition, all authors; data analysis/interpretation, T.S., I.I., F.A.; statistical analysis, T.S., Y.M., T.K.; manuscript preparation, T.S., K.I., J.K.; manuscript definition of intellectual content, T.S., T.K., J.K.; manuscript editing, Y.I., I.I., F.A.; manuscript revision/review and final version approval, all authors.
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ABSTRACT
INTRODUCTION
