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Evidence-based Practice |
1 From the National Council of Research, Istituto Metodologie Diagnostiche Avanzate, Palermo, Italy (C.C); Department of Gastroenterology, Section of Clinical Medicine (C.C., A.C.) and Department of General Medicine and Pneumology (A.O., M.A., M.C.), University of Palermo, Piazza delle Cliniche 2, 90127 Palermo, Italy; Department of Experimental Medicine, Clinica G. Salvatore, University of Catanzaro, Italy (F.S.); Department of Internal Medicine, Cardiology, and Hepatology, University of Bologna, Italy (F.T., P.A.); and Fox Chase Cancer Center, Philadelphia, Pa (L.S.). Received July 23, 2001; revision requested September 28; revision received November 8; accepted January 8, 2002. Address correspondence to C.C. (e-mail: camma@ismeda.pa.cnr.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Computerized bibliographic searches with MEDLINE and CANCERLIT databases from 1980 through 2000 were supplemented with manual searches, with the keywords "hepatocellular carcinoma," "liver cell carcinoma," "randomized controlled trial [RCT]," and "chemoembolization." Studies were included if patients with unresectable HCC were enrolled and if they were RCTs in which chemoembolization was compared with nonactive treatment (five RCTs) or if different transarterial modalities of therapy (13 RCTs) were compared. Data were extracted from each RCT according to the intention-to-treat method. Five of the RCTs with a nonactive treatment arm were combined by using the random-effects model, whereas all 18 RCTs were pooled from meta–regression analysis.
RESULTS: Chemoembolization significantly reduced the overall 2-year mortality rate (odds ratio, 0.54; 95% CI: 0.33, 0.89; P = .015) compared with nonactive treatment. Analysis of comparative RCTs helped to predict that overall mortality was significantly lower in patients treated with transarterial embolization (TAE) than in those treated with transarterial chemotherapy (odds ratio, 0.72; 95% CI: 0.53, 0.98; P = .039) and that there is no evidence that transarterial chemoembolization is more effective than TAE (odds ratio, 1.007; 95% CI: 0.79, 1.27; P = .95), which suggests that the addition of an anticancer drug did not improve the therapeutic benefit.
CONCLUSION: In patients with unresectable HCC, chemoembolization significantly improved the overall 2-year survival compared with nonactive treatment, but the magnitude of the benefit is relatively small.
© RSNA, 2002
Index terms: Efficacy study • Liver neoplasms, 761.323 • Liver neoplasms, chemotherapeutic embolization, 761.1264, 761.1266 • Radiology and radiologists, outcomes studies
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In 1998, findings from a meta-analysis of six randomized controlled trials (RCTs), which included 370 patients, failed to show a benefit of TACE on 1-year survival (4). Since that report, findings from new RCTs have been published (5–43); however, the results remain inconsistent, and the overall assessment of the treatment effect is difficult to evaluate. In 2000, the European Association for the Study of the Liver (44) concluded that TACE was not recommended because it did not alter the overall survival; they suggested that study of additional large RCTs is needed to clarify whether differences in treatment schedules, including new agent combinations or the selection of patients, may result in a therapeutic benefit for at least a subgroup of patients with HCC who are not surgical candidates. Therefore, important questions still remain unanswered. Can chemoembolization prolong survival compared with conservative treatment? Are there differences in the effectiveness of TACE among the various embolizing agents, the diverse combinations and types of chemotherapeutic agents emulsified with or without iodized oil, and the varying number of planned courses?
The aim of these quantitative and qualitative meta-analyses was to review the available evidence to estimate the effectiveness and safety of TACE.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Studies were included in the meta-analysis if they were RCTs in which different transarterial therapies with or without a control group receiving active treatment were compared, included patients with unresectable HCC, findings had been published in English, and if a 2-year mortality was assessed as an outcome measure of the effect of treatment.
Among the 39 RCTs identified (5–43), 21 were excluded for the following reasons: only data for 1-year survival were reported (8,9,18), intraarterial injection of iodine 131–labeled iodized oil was used (10,26,29), hepatic dearterialization or hepatic artery ligation and portal vein cannulation were used (6), chemoembolization as adjuvant therapy was assessed (32–35), immunotherapy with transcatheter embolization was combined (36), TACE with percutaneous ethanol injection was combined (5,27), the same treatment administered by using a different route was evaluated (37), or studies were nonrandomized (16). If results were published as an abstract or as a preliminary report (38–42) before the final article was published, the abstract and the preliminary report were excluded.
Review of the Trials
The trials were first reviewed by using a list of predefined pertinent issues that concerned both the patients and the treatments. To assess the methodologic quality of the RCTs, two key variables—concealment of treatment allocation and handling of withdrawals—that were based on the definitions given by Nicolucci et al (46), were used as suggested by Jüni et al (47). The RCTs were classified into high quality and low quality according to these two key variables. RCTs were classified as high quality if both adequate concealment of treatment allocation and handling of withdrawals were used. Each RCT was evaluated and classified by three independent investigators (A.O., M.A., F.S.), who compared their results with consensus. If discrepancies among the reviewers were observed, the results were discussed, and a final consensus was reached among the authors.
Statistical Methods
The overall 2-year mortality was assessed as the primary measure of treatment effect. When the crude rates of an overall mortality were not available, the actuarial probabilities, reported in the text or obtained from figures, were used. The evaluation of therapeutic effectiveness was performed with an intention-to-treat method. When the overall mortality rate was not reported in the trial, it was calculated according to this method (ie, all patients were evaluated according to their allocated treatment group; cases whose endpoint was unknown were considered failures). The number of patients who discontinued their original embolization regimen because of side effects was also recorded. In addition to the analysis of overall mortality, we also assessed the effect of TACE on tumor size. Complete response was defined as no evidence of neoplastic disease at computed tomography at the end of the treatment. Partial response was defined as the reduction in the total tumor size by more than 50%.
Meta-Analysis
We used an overall 2-year mortality rate in the treated and control groups to combine the results from individual trials. With these proportions of events, the odds ratio (ie, the ratio of the odds of surviving in the treated group to the odds of surviving in the control group) was computed for each trial. We calculated the overall odds ratio among the frequencies of events in both chemoembolization and control groups according to the random-effects model (48). In addition to variance within studies, the random-effects model also considers heterogeneity among the studies. The 95% CI of the odds ratio was also calculated. The overall odds ratio was tested for significance with the Mantel-Haenszel 
2 test (49). We chose to present the random-effects model because we believe that the relevant variation in treatment effects is a consequence of several intertrial differences (50). Moreover, we excluded each study at a time to ensure that no single study would be solely responsible for the significance of any result. The number of patients needed to treat to prevent one death was derived from the inverse of the risk difference and was also used as a measure of treatment effect. All our analyses were calculated with a computer program (courtesy of Professor Joseph Lau, New England Medical Center Hospitals, Boston, Mass), by using a personal computer.
Meta–Regression Analysis
We used meta–regression analysis to explore and explain diversity (heterogeneity) among the results of different studies. To examine the extent to which differences in the overall 2-year mortality could be explained by differences in the therapeutic regimens of the patients examined or the study design features, several independent explanatory variables were included in a meta–regression model (51). For this purpose, a logistic regression model was conducted by using the overall 2-year mortality rate as the dependent variable. The mean age and the proportion of men were the two features examined. The therapeutic options assessed were the use of an embolizing agent, a chemotherapeutic agent, or an iodized oil, and the mean number of courses of treatment. Study publication year and study size were also included as independent variables. In addition, study design features that indicated the quality of the RCTs were also examined. These design features included the two key variables: concealment of treatment allocation and handling of withdrawals. For each of these variables, the RCTs were separated into high quality and low quality and used with a dummy variable. Both univariate and multivariate regression analyses were performed (SAS, version 6.07; SAS Institute, Cary, NC).
Source of Support
This meta-analysis was not supported by any company, private grants, or other grants. The entire cost of meta-analysis was supported by the respective institutions of the authors.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Differences were found in the proportion of patients with Child-Pugh class A cirrhosis. The mean proportion of patients with Child-Pugh class A cirrhosis was 59% and ranged from 13.5% to 76.0% (11,13). However, there are no data about the Child-Pugh classes in patients enrolled in six RCTs (7,11,15,19,24,30). The mean percentage of patients with uninodular tumor mass was 47.7% and ranged from 12.5% to 77.0% (15,30). In four small RCTs (11,22,24,30), only advanced liver cancers were included.
A large variability in the chemoembolization protocol among the trials was found in (a) the embolizing agent administered (gel foam particles, gelatin sponge powder or particles); (b) the number and type of chemotherapeutic agents emulsified with or without iodized oil; (c) the liver volume embolized instead of the conventional (lobar) procedures used in the first trials (7,15,17,19), selective (segmental and subsegmental) treatments were used in later trials (11,12,14,21,22,28); and (d) the mean number of courses that ranged between 1.0 and 8.3 (20). TACE was repeated at fixed intervals until the planned number of courses was reached or until the patient died.
An adequate concealment of treatment allocation was used in five trials (7,11,12,14,15) and in all but three studies (12,17,25), criteria for handling withdrawals were not clearly defined.
Overall Mortality
Meta-analysis.—A meta-analysis of the five RCTs (7,12–14,43) in which chemoembolization was compared with nonactive treatment for the overall 2-year mortality as an endpoint was performed. The effect of TACE or transarterial embolization (TAE) on mortality is shown in Figure 1 (five RCTs with seven comparisons: 424 patients, 178 controls). There was no evidence of statistical heterogeneity (P = .21). The 95% CIs for the results of individual trials are widely ranged, and results of only one of the studies (43) favored treatment significantly. The effect of TACE on mortality was favored in three RCTs (five comparisons) (7,12,43), while no benefit was observed in the remaining two RCTs (13,14).
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Meta–regression analysis.—When the 13 RCTs (11,15,17,19–25,28,30,31) in which different procedures were compared were included in the meta–regression analysis, relevant differences in the magnitude of the treatment effect were observed. To identify the optimal treatment procedure, we compared the effect of transarterial chemotherapy, TAE, and TACE versus nonactive treatment with a univariate meta–regression analysis. The risks of the overall 2-year mortality on the basis of different chemoembolization procedures compared with untreated control group are shown in Figure 2. For the overall mortality, the odds ratio was significantly lower in patients who were treated with transarterial chemotherapy (odds ratio, 0.62; 95% CI: 0.42, 0.91; P = .043), TAE (odds ratio, 0.45; 95% CI: 0.30, 0.66; P = .0001), or TACE (odds ratio, 0.45; 95% CI: 0.32, 0.63; P = .0001) than in those who received nonactive treatment.
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Table 2 provides estimates of the risk of the overall 2-year mortality with the multivariate meta–regression model, which simultaneously takes into account the effects of treatment, as well as patient and study characteristics. The model used in the 13 RCTs in which 1,605 patients were enrolled (7,11–14,17,21–25,28,31) helped to confirm that overall mortality was significantly lower in patients who underwent TACE than in those who received nonactive treatment (P = .018). All of the variables failed toindependently influence the reported treatment effects. In particular, neither patient characteristics (mean age and proportion of men) nor study characteristics (concealment of treatment allocation and study size) had an independent effect on the response to treatment. Finally, only the "handling of withdrawals" variable had a significant influence on the reported overall mortality (P = .023).
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Treatment Safety
The three most frequent complications were liver failure, sepsis (cholecystitis, liver abscess), and gastrointestinal bleeding. In the RCTs in which a chemotherapeutic agent was administered, pancytopenia was also observed. The mean rate of severe adverse events after treatment was 5.6% and ranged between 0% (15,17,20–22,28,30) and 50% (13). The percentage of treatment-related death (within 30 days) ranged between 0% (14,15,17,19–21,23,24,28,30) and 10% (15). Univariate meta–regression analysis helped to predict that the risk of posttreatment mortality was significantly higher with the administration of a chemotherapeutic agent (odds ratio, 2.69; 95% CI: 1.22, 5.92; P = .013), the mean number of courses administered (odds ratio, 1.50; 95% CI: 1.27, 1.77; P < .0001), and the treatment of patients with portal vein thrombosis (odds ratio, 3.24; 95% CI: 1.28, 8.22; P = .013). In contrast, the use of an embolizing agent had no effect on the posttreatment mortality (odds ratio, 1.36; 95% CI: 0.67, 2.77; P = .39). Finally, mortality was significantly lower in studies that used selective (segmental or subsegmental) procedures than in those that used nonselective procedures (odds ratio, 0.014; 95% CI: 0.002, 0.10; P = .0001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The key clinical question is whether all patients with unresectable HCC should receive TACE or whether chemoembolization should be administered only to a subgroup of patients who clearly stand to benefit. To date, consensus about the type of patients who are amenable to undergo TACE has not been reached. The selection criteria used to identify the candidates for TACE vary nationally and internationally. Most of these criteria characterize a disease stage that can be described as not too early or not too advanced. It has been suggested that the benefit of chemoembolization is higher in patients with Child-Pugh class A and B cirrhosis than in those with Child-Pugh class C cirrhosis. We could not evaluate the benefits of TACE in relation to the Child-Pugh class, since data about mortality that are based on the Child-Pugh class are missing from several trials.
The results of RCTs in terms of life gain, when pooled together, do not support the routine use of TACE in all patients with unresectable HCC, presumably because its indisputable antitumor effects are offset in practice by the deterioration induced in the liver function. Further large RCTs in which patients are assigned according to Child-Pugh class would be needed to solve this issue. Although severe adverse effects and death may occur even in well-compensated patients (12), there is no doubt that patients with poor liver function or portal vein thrombosis are less able to tolerate the iatrogenic insult. Thus, it is prudent to exclude patients with signs of liver decompensation, such as ascites, hepatic encephalopathy, or jaundice. Therefore, patients with advanced liver disease or portal vein thrombosis who appear to be more susceptible to the risk than to the benefit of treatment do not represent suitable candidates for TACE.
Many RCTs have been conducted to identify the optimal chemoembolization procedure that would increase the cost-effectiveness of treatment. Exploratory analysis with use of different procedures suggested that the overall 2-year mortality was significantly lower in patients who underwent TAE than in those who received transarterial chemotherapy. In contrast, there was no evidence that TACE was more effective than TAE, which suggests that addition of chemotherapeutic agents does not improve the benefit of therapy.
While the anticancer drugs currently administered are poorly tolerated in most cases, the fact that the majority of patients will not benefit from therapy highlights the urgent and ongoing need for more effective drugs for the treatment of HCC. However, firm conclusions about the results of comparisons among different chemoembolization procedures are hampered by the fact that complications and treatment-related deaths are not formally reported in many trials. Therefore, data about the efficiency of different procedures, the safety profile (particularly regarding the degree of liver dysfunction), and the worldwide and standardized therapeutic protocols (particularly the embolizing procedure) are needed to better analyze these relevant factors.
According to our model, we cannot conclude that a single treatment is just as efficient as repeated courses. In several studies, treatment was repeated at fixed intervals until the planned number of courses was reached or until the patient died. Since repeated procedures may cause progressive liver atrophy (52), repetitions planned on the basis of tumor response and patient tolerance currently seem to be the most rational and effective strategies (53,54). There is growing evidence that superselective catheterization, in which the embolizing agent can be better focused on the cancer mass, may reduce the number of treatments needed to achieve extensive tumor necrosis. In this way, injury to cirrhotic liver is minimized.
The antitumor effect of TACE has been substantiated in RCTs with a mean partial response rate of 26.9%, while the mean complete response rate was only 6%. Results of TACE performed in patients with HCC must be scrutinized on the basis of survival rather than on the tumor response, since the prognosis depends not only on cancer progression but also on the severity of the underlying liver disease, whose course can be accelerated with treatment. Prognosis is also influenced by the nature and the activity of the underlying liver disease. There is no certainty that the results of RCTs performed in the Western world, which mainly include alcoholic patients or patients infected with hepatitis C virus, remain consistent in geographic areas where HCC is commonly associated with viral hepatitis B infection or exposure to aflatoxins.
The results of this retrospective meta-analysis are subject to several limitations. Differences in the baseline severity of illness in the population and in the chemoembolization procedures may limit accuracy in RCTs. Pooled results describe variations only among the studies and not among the patients, because they reflect group averages rather than individual data. Lack of data about important confounding factors, such as severity of the underlying liver disease, number and size of the tumor lesions, and presence of portal vein thrombosis, could also affect the accuracy of results. More detailed treatment comparisons could be achieved only with meta-analysis of individual patient data. Another potential limitation of the meta–regression analysis is the indirect comparison of different chemoembolization procedures. Because of the need to maintain each study as a distinct analytic unit, it was not possible for the meta–regression analysis to directly compare the benefit of different chemoembolization procedures and to simultaneously maintain comparability of treatment groups.
We are confident that none of the relevant published trials were overlooked owing to the extensive screening (manual and computer) of the literature for pertinent studies. Publication bias was probably not substantial and considered unlikely to change the direction of our pooled estimates of treatment effect. Although quality assessment may be important in this review, the quality of individual trials seems not to bias the results of the meta-analysis.
The available evidence is sufficient to conclude that (a) chemoembolization significantly reduces overall 2-year mortality in patients with unresectable HCC and (b) TACE was not more effective than TAE, which suggests that the addition of the chemotherapeutic agents currently used does not improve the benefit of therapy and emphasizes the need for more effective anticancer drugs. Future RCTs in which TACE is compared with no treatment by using quality-assurance measures to document adherence to preestablished embolizing protocols and assignment of patients according to Child-Pugh class, as well as the number and size of the tumor lesions and the presence of portal vein thrombosis, are still needed.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, C.C., F.S.; study concepts, F.T., P.A., M.C.; study design, C.C., M.C., F.T.; literature research, M.A., A.O., L.S.; data acquisition, C.C., F.S., A.O., M.A.; data analysis/interpretation, C.C., A.O., M.A., F.S.; statistical analysis, L.S., C.C., F.S.; manuscript preparation, C.C., F.S., A.O., M.A.; manuscript definition of intellectual content, C.C., F.S., A.C.; manuscript editing, C.C., F.S.; manuscript revision/review and final version approval, A.C., M.C.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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J. M. Llovet, J. Bruix, C. Camma, M. Cottone, A. Craxi, and R. P. Myers Unresectable Hepatocellular Carcinoma: Meta-Analysis of Arterial Embolization [letter] * Dr Camma and colleagues respond: * Dr Myers responds: Radiology, January 1, 2004; 230(1): 300 - 302. [Full Text] [PDF]
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K. Stuart Chemoembolization in the Management of Liver Tumors Oncologist, October 1, 2003; 8(5): 425 - 437. [Abstract] [Full Text] [PDF]
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S. N. Goldberg, J. W. Charboneau, G. D. Dodd III, D. E. Dupuy, D. A. Gervais, A. R. Gillams, R. A. Kane, F. T. Lee Jr, T. Livraghi, J. P. McGahan, et al. Image-guided Tumor Ablation: Proposal for Standardization of Terms and Reporting Criteria Radiology, August 1, 2003; 228(2): 335 - 345. [Abstract] [Full Text] [PDF]
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 W. Qiu, D. David, B. Zhou, P. G. Chu, B. Zhang, M. Wu, J. Xiao, T. Han, Z. Zhu, T. Wang, et al. Down-Regulation of Growth Arrest DNA Damage-Inducible Gene 45{beta} Expression Is Associated with Human Hepatocellular Carcinoma Am. J. Pathol., June 1, 2003; 162(6): 1961 - 1974. [Abstract] [Full Text] [PDF]
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R. P. Myers, C. Camma, F. Schepis, M. Cottone, and A. Craxi Meta-analysis of Transarterial Embolization in Patients with Unresectable Hepatocellular Carcinoma [letter] * Dr Camma and colleagues respond: Radiology, May 1, 2003; 227(2): 611 - 613. [Full Text] [PDF]
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= the odds ratio for each trial and the overall estimate. The error bars represent the 95% CIs of each estimate. Lin refers to Lin et al (