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      Salvage Liver Transplantation for Recurrent Hepatocellular Carcinoma after Liver Resection: Retrospective Study of the Milan and Hangzhou Criteria

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          Abstract

          Background

          Salvage liver transplantation (SLT) has recently been proposed for recurrent hepatocellular carcinoma after liver resection; however, criteria for candidate assessment in SLT have not been thoroughly evaluated.

          Methods and Findings

          We retrospectively analyzed outcomes and factors affecting survival of 53 recipients who received SLT in the Liver Transplantation Center, The First Affiliated Hospital of Zhejiang University between 2004 and 2012. Thirty recipients fulfilled the Hangzhou criteria, of which 16 also fulfilled the Milan criteria, while the remaining 23 exceeded both criteria. The 1-year, 3-year and 5-year overall survival rates and tumor-free survival rates were both superior in patients fulfilling Milan or Hangzhou criteria compared with those exceeding the criteria. For recipients outside Milan criteria but within Hangzhou criteria, the 1-year, 3-year overall survival rates were 70.1%, 70.1%, similar to recipients within Milan criteria, with the 1-year, 3-year and 5-year overall survival of 93.8%%, 62.1% and 62.1% (P = 0.586). The tumor-free survival rates were also similar between these two subgroups, with 51.9% and 51.9% vs. 85.6%, 85.6% and 64.2% during the same time interval, respectively (P = 0.054). Cox regression analysis identified Hangzhou criteria (within vs. outside, hazard ratio (HR) 0.376) and diameter of the largest tumor (HR 3.523) to be independent predictors for overall survival. The only predictor for tumor-free survival was diameter of the largest tumor (HR 22.289).

          Conclusions

          Hangzhou criteria safely expanded the candidate pool and are feasible in assessment of candidates for SLT. This is helpful in donor liver allocation in transplant practice.

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          Most cited references19

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          Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival.

          F Y Yao, L Ferrell, N M Bass … (2001)
          The precise staging of hepatocellular carcinoma (HCC) based on the size and number of lesions that predict recurrence after orthotopic liver transplantation (OLT) has not been clearly established. We therefore analyzed the outcome of 70 consecutive patients with cirrhosis and HCC who underwent OLT over a 12-year period at our institution. Pathologic tumor staging of the explanted liver was based on the American Tumor Study Group modified Tumor-Node-Metastases (TNM) Staging Classification. Tumor recurrence occurred in 11.4% of patients after OLT. The Kaplan-Meier survival rates at 1 and 5 years were 91.3% and 72.4%, respectively, for patients with pT1 or pT2 HCC; and 82.4% and 74.1%, respectively, for pT3 tumors (P =.87). Patients with pT4 tumors, however, had a significantly worse 1-year survival of 33.3% (P =.0001). An alpha-fetoprotein (AFP) level > 1,000 ng/mL, total tumor diameter > 8 cm, age > or = 55 years and poorly differentiated histologic grade were also significant predictors for reduced survival in univariate analysis. Only pT4 stage and total tumor diameter remained statistically significant in multivariate analysis. Patients with HCC meeting the following criteria: solitary tumor < or = 6.5 cm, or < or = 3 nodules with the largest lesion < or = 4.5 cm and total tumor diameter < or = 8 cm, had survival rates of 90% and 75.2%, at 1 and 5 years, respectively, after OLT versus a 50% 1-year survival for patients with tumors exceeding these limits (P =.0005). We conclude that the current criteria for OLT based on tumor size may be modestly expanded while still preserving excellent survival after OLT.
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            Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation.

            Sheung Fan, Ronnie Tung-Ping Poon, Jeffrey C. Liu … (2002)
            To evaluate the survival results and pattern of recurrence after resection of potentially transplantable small hepatocellular carcinomas (HCC) in patients with preserved liver function, with special reference to the implications for a strategy of salvage transplantation. Primary resection followed by transplantation for recurrence or deterioration of liver function has been recently suggested as a rational strategy for patients with HCC 5 cm or smaller and preserved liver function. However, there are no published data on transplantability after HCC recurrence or long-term deterioration of liver function after resection of small HCC in Child-Pugh class A patients. Such data are critical in determining the feasibility of salvage transplantation. From a prospective database of 473 patients with resection of HCC between 1989 and 1999, 135 patients age 65 years or younger had Child-Pugh class A chronic liver disease (chronic hepatitis or cirrhosis) and transplantable small HCC (solitary < or =5 cm or two or three tumors < or = 3 cm). Survival results were analyzed and the pattern of recurrence was examined for eligibility for salvage transplantation based on the same criteria as those of primary transplantation for HCC. Overall survival rates at 1, 3, 5, and 10 years were 90%, 76%, 70%, and 35%, respectively, and the corresponding disease-free survival rates were 74%, 50%, 36%, and 22%. Cirrhosis and oligonodular tumors were predictive of worse disease-free survival. Patients with concomitant oligonodular tumors and cirrhosis had a 5-year overall survival rate of 48% and a disease-free survival rate of 0%, which were significantly worse compared with other subgroups. At a median follow-up of 48 months, 67 patients had recurrence and 53 (79%) of them were considered eligible for salvage transplantation. Decompensation from Child-Pugh class A to B or C without recurrence occurred in only six patients. For Child-Pugh class A patients with small HCC, hepatic resection is a reasonable first-line treatment associated with a favorable 5-year overall survival rate. A considerable proportion of patients may survive without recurrence for 5 or even 10 years; among those with recurrence, the majority may be eligible for salvage transplantation. These data suggest that primary resection and salvage transplantation may be a feasible and rational strategy for patients with small HCC and preserved liver function. Primary transplantation may be a preferable option for the subset of patients with oligonodular tumors in cirrhotic liver in view of the poor survival results after resection.
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              Liver transplantation for hepatocellular carcinoma: Hangzhou experiences.

              Shu-Sen Zheng, Jian Wu, Min Zhang … (2008)
              Liver transplantation (LT) has been the treatment of choice for patients with hepatocellular carcinoma (HCC). This study was designed to summarize our experience in LT for HCC patients and establish a new set of criteria for patient selection and prognosis prediction. Data of 195 patients with HCC were retrospectively analyzed and various clinical and pathological factors for survival and tumor-free survival were examined by univariate and multivariate analyses. Macrovascular invasion, preoperative serum alpha fetoprotein (AFP) level, tumor size, multifocality, histopathologic grading, distribution, and cirrhosis background were significant factors for survival and tumor-free survival by univariate analysis. Multivariate analysis identified macrovascular invasion, tumor size, preoperative AFP level, and histopathologic grading were prognostic factors independently associated with patient survival or tumor-free survival (RR=1.688-2.779, P=0.000-0.034). Based on the prognostic stratification of different risk groups of patients without macrovascular invasion, Hangzhou criteria was established, containing one of the two following items: (a) Total tumor diameter less than or equal to 8 cm; (b) total tumor diameter more than 8 cm, with histopathologic grade I or II and preoperative AFP level less than or equal to 400 ng/mL, simultaneously. The difference between survival curves of patients fulfilling Milan criteria (n=72) and patients fulfilling Hangzhou criteria (n=99) did not achieve statistical significance (5-year survival rates: 78.3% vs. 72.3%, P>0.05). Of the patients exceeding Milan criteria (n=123), those who fulfilled Hangzhou criteria (n=26) also had better prognosis than the others (n=97) (P=0.000). The results of this study show a reliable and feasible candidates selection and prognostic criteria of LT in HCC patients.
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                Author and article information

                Contributors
                Ferruccio Bonino: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2014
                Publication date (Electronic): 27 January 2014
                Volume: 9
                Issue: 1
                Electronic Location Identifier: e87222
                Affiliations
                [1 ]Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China
                [2 ]Key Laboratory of Combined Multi-Organ Transplantation, Ministry of Public Health, Zhejiang Province, Hangzhou, China
                [3 ]Key Laboratory of Organ Transplantation, Zhejiang Province, Hangzhou, China
                University of Pisa, Italy
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SZ ZH. Performed the experiments: JZ. Analyzed the data: ZL. Contributed reagents/materials/analysis tools: JX ZQ MZ. Wrote the paper: ZH JZ JW.

                Article
                Publisher ID: PONE-D-13-41529
                DOI: 10.1371/journal.pone.0087222
                PMC ID: 3903638
                SO-VID: 43f736fe-a81b-407c-a62d-8427cfa3eae9
                Copyright statement: Copyright @ 2014
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 10 October 2013
                Date accepted : 18 December 2013
                Page count
                Pages: 7
                Funding
                This study was sponsored by grants from National S&T Major Project (No. 2012ZX10002017), the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (Grant No.81121002) and the National Natural Science Foundation of China (Grant No.81200331). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Mathematics
                Subject: Statistics
                Subject: Statistical Methods
                Subject: Medicine
                Subject: Clinical Research Design
                Subject: Retrospective Studies
                Subject: Gastroenterology and Hepatology
                Subject: Liver Diseases
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Gastrointestinal Tumors
                Subject: Hepatocellular Carcinoma
                Subject: Surgery
                Subject: Transplant Surgery

                ScienceOpen disciplines: Uncategorized
                Data availability:
                ScienceOpen disciplines: Uncategorized

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