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(Radiology. 1999;212:665-668.)
© RSNA, 1999

Vascular and Interventional Radiology

Hepatic Intraarterial 131I Iodized Oil for Treatment of Hepatocellular Carcinoma in Patients with Impeded Portal Venous Flow1

Thierry de Baere, MD, Patrice Taourel, MD, Jean Michel Tubiana, MD, Viseth Kuoch, MD, Michel Ducreux, MD, Jean Lumbroso, MD and Alain J. Roche, MD

1 From the Departments of Interventional Radiology (T.d.B., V.K., A.J.R.), Medicine (M.D.), and Nuclear Medicine (J.L.), Institut Gustave Roussy, 94805 Villejuif, France; the Department of Medical Imaging, Saint Eloi Hospital, Montpellier, France (P.T.); and the Department of Medical Imaging, Hôpital Saint Antoine, Paris, France (J.M.T.). Received May 4, 1998; revision requested July 6; final revision received December 14; accepted March 26, 1999. Address reprint requests to T.d.B.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the efficacy and safety of intraarterial hepatic iodine 131 iodized oil for treatment of hepatocellular carcinoma in patients with impeded portal venous flow.

MATERIALS AND METHODS: Twenty-four patients (mean age, 61 years) with hepatocellular carcinoma underwent 38 courses of 131I iodized oil (one to three per patient), with a mean dose of 2,146 MBq injected into the proper hepatic artery. Hepatocellular carcinoma manifested as single nodules (n = 8; mean, 7.75 cm), multiple nodules (n = 13; mean, 5.46 cm), or a mass (n = 3) occupying more than two hepatic segments. Portal venous thrombosis was complete (n = 10), right (n = 9), left (n = 2), or multisegmental (n = 1). Two patients had hepatofugal portal flow.

RESULTS: Among the 23 patients with evaluatable results, response to treatment was partial in three, and disease was stable in 12 and progressive in eight. Estimated actuarial survival rates were 70%, 33%, 12%, and 6% at 3, 6, 9, and 12 months, respectively, with two patients alive at 9 and 11 months. The median survival time was 147 days. Adverse events were the early death of one patient owing to hepatic failure and transient symptomatic hepatic failure after 12 courses in nine patients.

CONCLUSION: In this preliminary experience, intraarterial hepatic 131I iodized oil did not demonstrate high efficacy in the treatment of hepatocellular carcinoma in patients with portal venous thrombosis, as side effects were not rare.

Index terms: Hepatic arteries, therapeutic blockade, 952.1266 • Iodine and iodine compounds, radioactive, 761.1266 • Liver neoplasms, chemotherapeutic infusion, 761.1266, 761.323 • Portal vein, stenosis or obstruction, 957.751 • Radionuclides, therapeutic, 761.1266, 761.323 • Therapeutic radiology, 761.1266, 761.323


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Lipiodol Ultra-Fluide (Guerbet, Roissy, France) is an iodinated ethylic ester of poppy-seed oil. To our knowledge, iodized oil was first injected into the hepatic arteries in the early 1980s. Because of its capacity to target and remain fixed in tumors, iodized oil was first used as a diagnostic tool (1,2) and is still used in association with delayed computed tomography (CT) for the evaluation of disseminated hepatocellular carcinoma. Injection of iodized oil mixed with various drugs into hepatic arteries is widely used for the treatment of hepatic tumors and has been described frequently in the literature (3–6) during the past decade.

More recently, iodine 131 iodized oil (Lipiocis; Cis Bio International Laboratory, Gif sur Yvette, France) was injected into hepatic arteries for interstitial radiation therapy. Some clinical success has been reported with this method without the need for additional arterial embolization, notably in the treatment of hepatocellular carcinoma (7–11). The French Drug Agency recently approved 131I iodized oil for the treatment of inoperable hepatocellular carcinoma with portal venous thrombosis.

The aim of this study was to evaluate the efficacy and safety of hepatic intraarterial injection of 131I iodized oil in the treatment of hepatocellular carcinoma in patients with impaired portal venous flow.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
From October 1994 to January 1997, 24 patients (20 men, four women; age range, 52–75 years; mean age, 61 years ± 8 [SD]) with inoperable hepatocellular carcinoma entered the study at the authors' three institutions after the approval of the institutional review boards was obtained. After a full explanation of the nature of the treatment, patients gave their oral informed consent. No patients had undergone previous therapy, and the time between diagnosis and the initiation of 131I iodized oil therapy was 3 days to 4 weeks (median, 13 days).

The diagnosis of hepatocellular carcinoma was made on the basis of either histologic examination results or an {alpha}-fetoprotein level exceeding 500 ng/mL (500 µg/L; normal value < 10 ng/mL [10 µg/L]) together with characteristic CT features. Eight patients had a single-nodule tumor 3–15 cm in diameter (mean, 7.75 cm ± 3.96), 13 patients had a multinodular tumor with the largest nodule 2–13 cm in diameter (mean, 5.46 ± 3.62), and three patients had a massive tumor occupying more than two hepatic segments.

In all patients, the tumor was inoperable because of either extensive disease or severe cirrhosis. All patients had disease confined to the liver except two who had lung or bone metastases. The cause of cirrhosis was alcohol (n = 10), virus (n = 9), or hemochromatosis (n = 1), or the cause was unknown (n = 4).

Because portal venous obstruction is a well-known risk factor for hepatic failure and infarction after hepatic arterial embolization (12), portal flow was considered insufficient to ensure safe embolization of the hepatic artery if two or more segmental branches feeding nontumorous liver were occluded in addition to the ones feeding tumorous segments. This insufficient portal flow was due to obstruction of the portal trunk (n = 10), the right branch (n = 9), the left branch (n = 2), or more than three segmental branches (n = 1), and portal flow was hepatofugal in two patients.

Before the first hepatic intraarterial injection of 131I iodized oil was administered, the underlying hepatic disease, according to the Child classification, was as follows: Child A (n = 14), Child B (n = 8), and Child C (n = 2). Tumor stages according to the Okuda classification (13) were as follows: Okuda I (n = 10) and Okuda II (n = 14). Blood test results showed an increase in {alpha}-fetoprotein of 59–273,000 ng/mL (59–273,000 µg/L; normal value < 10 ng/mL [10 µg/L]) in 12 patients and a bilirubin value of 8–67 µmol/L (mean, 27 µmol/L ± 16; normal value < 17 µmol/L), a prothrombin time of 45%–100% (mean, 75% ± 14; normal value, 70%–100% [100% = 10–14 seconds]), and a serum albumin level of 25–54 g/L (mean, 35 g/L ± 9; normal value, 32–55 g/L) in all patients.

After iodized oil was labeled with an exchange isotopic reaction, 131I iodized oil was produced. Labeling efficacy has been found to be greater than 99% with chromatography, and stability has been demonstrated without dehalogenation over a 3-month period (14). One to three hepatic intraarterial injections (mean, 1.6) were performed bimonthly, with a total of 38 courses. The dose injected for each treatment was 58 mCi ± 4.6 (2,146 MBq ± 170.2; range, 52–60 mCi [1,924–2,220 MBq]), except for one treatment that was performed with half the dose (ie, 30 mCi [1,110 MBq]). All the procedures were performed with local anesthesia.

After angiographic confirmation of insufficient portal flow for embolization, the proper hepatic artery was selectively catheterized, and 5–7 mL of 131I iodized oil was injected without reflux, as fast as was allowed by arterial flow. No superselective injection of the 131I iodized oil in tumorous segments was performed. In two patients, there was an additional replaced left hepatic artery, which prompted us to inject half of the dose of 131I iodized oil into each hepatic artery.

After the injections, the patients were isolated for 7 days for radiation protection of other patients, and only short visits were authorized. The handling of all radioactive materials and the care of patients receiving radioisotope treatment were in accordance with local rules and recommendations of the French Organization for Protection against Ionizing Radiations.

Planar scintiscans of the liver and thorax were obtained 2–3 days later to allow quantification of the activity ratio of liver to lung plus liver. Tumor response was evaluated on CT scans 1 month after each course of treatment. Tumor size was appreciated by using the product of the two largest perpendicular diameters. A partial response was a decrease of at least 50% of this product, and progression was an increase of at least 25%. Survival was measured from initiation of 131I iodized oil therapy by using the Kaplan-Meier method.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
All hepatic arteries were catheterized successfully and injected with 131I iodized oil, and no adverse event occurred during the procedure, except in one patient who had mild abdominal pain within a few seconds after the injection of 5 mL of 131I iodized oil. The ratio of liver to lung plus liver after the first injection was higher than 75% in 13 patients, lower than 50% in one, intermediate in four, and not evaluated in six.

The tumor size was evaluated in 23 patients. One patient died before follow-up assessment of tumor size. After the first course, three (13%) of 23 patients had a partial response, 12 (52%) had stable disease, and eight had progressive disease. Among the three who responded, two died 69 and 145 days after the initiation of 131I iodized oil therapy and received only one course of treatment, and one was still responding when lost to follow-up after 4 months and three courses of treatment.

Among the 12 patients with stable disease, six underwent only one course of treatment and died 85–230 days (mean, 154 days) after the initiation of 131I iodized oil therapy. Six continued treatment, and disease remained stable at CT for 42–140 days (mean, 91 days) after the initiation of 131I iodized oil therapy. Among these six patients, four underwent two courses of treatment and died after 142–329 days (mean, 189 days), and two patients who underwent three courses are still alive after 9 and 11 months. The eight patients with progressive disease died after 43–278 days (mean, 145 days) despite one course of treatment in four patients and two courses in the other four.

The median survival time was 147 days (mean, 137 days ± 83), with one patient lost to follow-up at 4 months and two patients alive after 9 and 11 months. The 3-, 6-, 9-, and 12-month estimations of actuarial survival with the Kaplan-Meier method (Fig) were 70%, 33%, 12%, and 6%, respectively.



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  		Figure 1. Graph shows the actuarial survival estimation with the Kaplan-Meier method in 23 patients with evaluatable results who were treated with intraarterial hepatic 131I iodized oil. The patient lost to follow-up after 4 months has been excluded.

 
Complications during the 1st month after treatment included one early death due to hepatic failure and transient symptomatic hepatic failure after 12 injections in nine patients. The early death occurred in a patient with Child A disease who developed jaundice, ascites, and encephalopathy 3–4 days after treatment and who died of hepatic insufficiency 28 days after the first course of treatment. Transient hepatic failure symptoms were ascites (n = 10), edema of the lower limb (n = 5), and jaundice (n = 6). These transient failures occurred in five patients with Child A disease, two with Child B, and two with Child C. Treatment was stopped in six patients owing to these adverse events, including in three patients who twice presented with symptomatic hepatic failure less than 2 weeks after injection of 131I iodized oil.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Selective fixation of iodized oil in hepatic tumors is explained by its propensity to pass preferentially through tumor arteries and to embolize them temporarily (15), its ability to pass from the artery into the portal veins via the peribiliary plexus (16), the increased permeability of tumor vessels that allows the passage of iodized oil through their layers (17,18), the incorporation of iodized oil by tumor cells as vesicles by pinocytosis (19–21), and the low clearance of iodized oil by Kupffer cells in the tumor compared with clearance in healthy hepatic cells (16). The ratio of iodized oil fixation in tumors to that in healthy liver has been reported by various authors (22–25) to be roughly between five and 10, and this advantage has long been exploited for tumor targeting by mixing anticancer drugs with iodized oil. However, additional arterial embolization is needed to enhance the efficacy of drug targeting (26), which renders this technique inapplicable in patients with portal venous thrombosis.

More recently, iodized oil was labeled with a radioisotope, more often 131I than rhenium 188 (24). This radiolabeled iodized oil allows the delivery of interstitial radiation therapy that targets tumors. Such treatment can be used in patients with portal venous thrombosis because additional embolization is not needed.

With this treatment, survival in our series is very similar to that reported for the group treated in the only randomized study published, to our knowledge, on hepatocellular carcinoma in patients with portal venous thrombosis, treated with 131I iodized oil (27). Survival rates at 3, 6, and 9 months were 71%, 48%, 7% in the study by Raoul et al (27) and 70%, 33%, 12% in our series. These comparable survival rates were obtained in patients sharing, in both series, the same nationality and similar underlying hepatic disease and tumor stages.

Despite these similar survival rates, toxicity and tolerance were different in the two series. The response rate was 44% for Raoul et al (27) and 13% in our experience. Thus, response to treatment does not seem to have influenced survival to any notable extent, and in our experience survival was even slightly shorter for those who responded than for those who did not. Our median survival time is within the limits of the 2–7-month survival time usually reported in the literature (28–32) for all confounded untreated hepatocellular carcinoma. Moreover, the survival rates of 3, 6, and 9 months are very close to those of the untreated group of patients with hepatocellular carcinoma and portal venous thrombosis reported by Lee et al (33).

We had to deal with a high rate of treatment-induced hepatic failure. With the exception of one death, most cases of hepatic failure were reversible, but treatment had to be discontinued in six patients because of these side effects. Although intraarterial hepatic injections of 131I iodized oil are reported by most authors (9, 10, 22, 27, 34) to be well tolerated, such frequent hepatic failure after treatment was reported by Bhattacharya et al (7) in a series of 26 patients with a 30-day mortality rate of 15%, despite the absence of portal venous thrombosis. Portal venous thrombosis alone is therefore not a valid explanation for these treatment-induced hepatic failures, nor is the severity of cirrhosis, because these side effects occurred both in patients with Child C disease and in patients with Child A disease.

We did not report adverse pulmonary events, such as chronic inflammatory interstitial infiltration and interstitial fibrosis, which have been reported in other studies (8,27) to occur 3–8 weeks after treatment. It occurred once in 27 patients of Raoul et al (27), and they used the same dose as was used in our study. It occurred in 57% of treated patients of Preketes et al (35), and they used a higher dose, although they subsequently reduced the dose injected for each session.

In other respects, hepatic therapy with intraarterial 131I iodized oil is a relatively cumbersome therapy. First, appropriate isolation facilities are needed in which patients can spend several days. Second, radiation protection is difficult for the physicians who inject high-energy radioisotopes through a catheter, with fluoroscopic guidance, slowly enough to avoid reflux. Third, this treatment is relatively expensive because the cost of a dose of 131I iodized oil is roughly eight- to 10-fold higher than that of the chemotherapy, iodized oil, and absorbable gelatin sponge (Gelfoam; Pharmacia and Upjohn, Portage, Mich) used for standard chemoembolization.

In spite of the disappointing results in our limited series, further studies are needed to reevaluate our findings in a larger series and also to refine the technique. This technique could be optimized in a number of ways. In an experimental model, we previously demonstrated that a fourfold lower lung passage of iodized oil could be achieved by using an appropriate emulsion of iodized oil with saline solution instead of pure iodized oil and, moreover, that the ratio between iodized oil fixation in tumor and nontumorous liver could be increased by a factor of two (25). Such emulsions, which seem appropriate in theory, potentially could maximize radiation doses to the tumor and minimize lung damage, a frequent side effect in at least one study (35). In addition, drugs emulsified with 131I iodized oil could allow radiation therapy to be combined with administration of cytotoxic agents. However, use of such emulsions in clinical practice will be hampered by the mandatory radiation protection precautions required to prepare them.

Embolization after the intraarterial administration of 131I iodized oil is an alternative that, to our knowledge, has never been tested experimentally or in clinical practice: Findings in a recently published article (11) by one of the teams most experienced in the use of 131I iodized oil suggested using embolization to enhance the efficacy of 131I iodized oil in patients without portal venous impediment.

Owing to the complexity of and the poor tolerance for the procedure, the low response rate, and the doubtful gain in survival, hepatic therapy with intraarterial 131I iodized oil cannot be considered a routine clinical treatment for hepatocellular carcinoma in patients with portal venous thrombosis. Refinement of the technique by using an emulsion combined with cytotoxic agents or embolization should be evaluated.


   Acknowledgments
 
We express our appreciation to Ms Lorna Saint Ange for her expert assistance in the linguistic revision of this manuscript.


   Footnotes
 
Author contributions: Guarantors of integrity of entire study, P.T., J.M.T., A.J.R., T.d.B.; study concepts, J.L., T.d.B., M.D.; study design, J.L., T.d.B.; definition of intellectual content, J.L., P.T., J.M.T., T.d.B., M.D.; literature research, V.K., T.d.B.; clinical studies, J.L., J.M.T., A.J.R., M.D., P.T., V.K.; data acquisition, J.M.T., P.T., T.d.B.; data analysis, T.d.B., M.D.; statistical analysis, M.D.; manuscript preparation, T.d.B., P.T.; manuscript editing, T.d.B.; manuscript review, J.L., P.T., V.K.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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