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Downstaging Hepatocellular Carcinoma: a Systematic Review and Pooled Analysis

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Downstaging Hepatocellular Carcinoma: a Systematic Review and Pooled Analysis LIVER TRANSPLANTATION 21:1142–1152, 2015 ORIGINAL ARTICLE Downstaging Hepatocellular Carcinoma: A Systematic Review and Pooled Analysis Neehar D. Parikh,1 Akbar K. Waljee,1 and Amit G. Singal2 1Division of Gastroenterology, University of Michigan Health System, University of Michigan, Ann Arbor, MI; 2VA Ann Arbor Health Services Research and Development Center of Clinical Management Research, Ann Arbor, MI; and 3Division of Digestive and Liver Diseases, University of Texas South Western Medical Center, Dallas, TX Downstaging can facilitate liver transplantation (LT) for patients outside of Milan criteria with hepatocellular carcinoma (HCC); however, the optimal protocol and downstaging outcomes are poorly defined. We aimed to characterize rates of suc- cessful downstaging to within Milan criteria and post-LT recurrence and survival among patients who underwent downstaging. We performed a systematic literature review using the MEDLINE and Embase databases from January 1996 through March 2015 and a search of national meeting abstracts from 2010 to 2014. Rates of downstaging success (defined as a decrease of tumor burden to within Milan) and post-LT recurrence with 95% confidence intervals (CIs) were calculated. Prespecified subgroup analyses were conducted by treatment modality, study design, and patient characteristics. Thirteen studies (n 5 950 patients) evaluating downstaging success had a pooled success rate of 0.48 (95% CI, 0.39-0.58%). In subgroup analyses, there was no significant difference comparing transarterial chemoembolization (TACE) versus transarte- rial radioembolization (TARE; P 5 0.51), but there were higher success rates in prospective versus retrospective studies (0.68 versus 0.44; P < 0.001). The 12 studies (n 5 320 patients) evaluating post-LT HCC recurrence had a pooled recur- rence rate of 0.16 (95% CI, 0.11-0.23). There was no significant difference in recurrence rates between TACE and TARE (P 5 0.33). Post-LT survival could not be aggregated because of heterogeneity in survival data reporting. Current data have heterogeneity in baseline tumor burden, waiting time, downstaging protocols, and treatment response assessments. There are also notable limitations including inconsistent reporting of inclusion criteria, downstaging protocols, and outcome assessment criteria. In conclusion, the success rate of downstaging HCC to within Milan criteria exceeds 40%; however, posttransplant HCC recurrence rates are high at 16%. Downstaging protocols for HCC should be systematically studied and optimized to minimize the risk of post-LT HCC recurrence. Liver Transpl 21:1142-1152, 2015. VC 2015 AASLD. Received March 3, 2015; accepted May 3, 2015. Liver transplantation (LT) is a lifesaving and curative See Editorial on Page 1117 treatment for patients with hepatocellular carcinoma (HCC). LT has been shown to provide the best long- Additional supporting information may be found in the online version of this article. Abbreviations: BCLC, Barcelona Clinic Liver Cancer; CI, confidence interval; EASL, European Association for the Study of the Liver; HCC, hepatocellular carcinoma; LT, liver transplantation; MOOSE, meta-analysis of observational studies in epidemiology; NOS, Newcastle-Ottawa scale; mRECIST, modified Response Evaluation Criteria in Solid Tumors; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-analysis; RFA, radiofrequency ablation; SBRT, stereotactic body radiation; TACE, transar- terial chemoembolization; TALC, Transarterial Chemo-lipiodolization; TARE, transarterial radioembolization; UCSF, University of California–San Francisco; WHO, World Health Organization. This work was conducted with support from the Agency for Health Research and Quality Center for Patient-Centered Outcomes Research (R24 HS022418). Akbar K. Waljee is funded by a Veterans Affairs Health Services Research and Development Career Development Program–2 Career Development Award 1IK2HX000775. The content is solely the responsibility of the authors and does not necessarily represent the official views of the University of Michigan or the Veterans Affairs Administration. Potential conflict of interest: Nothing to report. Address reprint requests to Neehar D. Parikh, M.D., M.S., Division of Gastroenterology, University of Michigan Health System, 3912 Taubman Center, 1500 East Medical Center Drive, Ann Arbor, MI 48109. Telephone: 11-734-936-8643; FAX: 11-734-936-7392; E-mail: [email protected] DOI 10.1002/lt.24169 View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases VC 2015 American Association for the Study of Liver Diseases. LIVER TRANSPLANTATION, Vol. 21, No. 9, 2015 PARIKH ET AL. 1143 term survival for these patients, as it both cures the can Association for the Study of Liver Diseases, Euro- HCC and underlying liver disease.1 The number and pean Association for the Study of the Liver (EASL), proportion of LTs for HCC has increased in recent American College of Gastroenterology, and the Inter- years, making it a leading indication for transplanta- national Liver Cancer Association from 2010 to 2014 2 tion. The Milan criteria for LT (1 tumor less than 5 were performed. cm, up to 3 tumors less than 3 cm in size) has been proposed, validated, and widely used as the eligibility Study Selection criteria for consideration of LT in the treatment of HCC.3 Data from numerous cohorts of patients have The search for studies and study selection was con- shown that outcomes for LT in patients within Milan ducted with meta-analysis of observational studies in criteria are excellent with high survival rates and low epidemiology (MOOSE) and Preferred Reporting Items recurrence rates. Overall, post-LT survival rates are for Systematic Reviews and Meta-analysis (PRISMA) 4,5 comparable to patients transplanted without HCC. guidance.7,8 Two investigators (N.D.P. and A.G.S.) Unfortunately, only a minority of HCC patients pres- reviewed all publication titles of citations identified by 6 ent within Milan criteria. If patients present outside the search strategy. Potentially relevant studies were Milan criteria, LT is often not an option at many retrieved, and selection criteria were applied. The transplant centers and patients are left with no other articles were independently checked for inclusion by 2 curative options for their HCC. For selected patients, investigators (N.D.P. and A.G.S.), disagreements were downstaging is attempted to bring tumors within resolved through discussion, and consensus was Milan criteria by using liver-directed therapy. Options reached on all articles. Our inclusion criteria were (1) for conducting downstaging include radiofrequency cohort studies (retrospective or prospective); (2) stud- ablation (RFA), transarterial chemoembolization ies evaluating downstaging in patients with cirrhosis (TACE), transarterial radioembolization (TARE), ste- and HCC; (3) studies in which downstaging was per- reotactic body radiation (SBRT), or a combination of formed using surgical resection, RFA, TACE, TARE, therapies. The benefits of downstaging include SBRT, or a combination of therapies; and (4) studies decreasing tumor burden and allowing time to identify that reported rates of success for downstaging those with less aggressive tumor biology. patients to within Milan criteria using imaging criteria There have been numerous reports of using and/or posttransplant outcomes (including recur- downstaging to bring patients within transplant crite- rence rates and/or survival) among those who were ria; however, these data are largely restricted to small downstaged to within Milan criteria. We excluded cohorts of patients and include disparate downstaging articles that (1) evaluated investigational procedures; protocols. Therefore, the success rates and posttrans- (2) evaluated systemic chemotherapeutic agents; (3) plant outcomes after downstaging are largely unknown used explant data for evaluation of downstaging suc- outside of single-center reports. We hypothesize that cess; (4) had incomplete data for primary outcomes of downstaging yields high success rates but is associ- interest; (5) included less than 5 patients; and/or (6) ated with high post-LT recurrence rates. To better used surgical resection as the only method for characterize the efficacy of downstaging, we performed downstaging patients. Studies in which a minority of a meta-analysis of observational studies with indi- patients had surgical resection as a downstaging viduals beyond Milan criteria who underwent modality were included. For studies that reported on downstaging with locoregional therapies. The aims of duplicate cohorts of patients, we used the most this meta-analysis were (1) to determine the success of updated cohort or the publication that provided the downstaging HCC to bring patients within Milan crite- most complete baseline and follow-up data. Additional ria and (2) to characterize post-LT recurrence rates exclusion criteria included non-English language and and survival of patients who were downstaged. nonhuman data. PATIENTS AND METHODS Data Extraction Literature Search Two investigators (N.D.P. and A.G.S.) independently Two study investigators (N.D.P. and A.G.S.) independ- extracted required information from eligible studies ently conducted a computer-assisted search of the using standardized forms developed by the investiga- MEDLINE and Embase databases to identify relevant tors. We collected data on study design (retrospective published
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