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Cited by 281Hepatocellular Carcinoma Treatment and PrognosisInflammatory Biomarkers in Disease PrognosisOrgan Transplantation Techniques and Outcomes

Recurrence After Liver Transplantation for Hepatocellular Carcinoma: A New MORAL to the Story

Halazun, Karim J., Najjar, Marc, Abdelmessih, Rita M., Samstein, Benjamin, Griesemer, Adam D., Guarrera, James V., Kato, Tomoaki, Verna, Elizabeth C., Emond, Jean C., Brown, Robert S.·2017·Annals of Surgery
DOI 10.1097/sla.0000000000001966
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Abstract

OBJECTIVE: We sought to develop a "Model Of Recurrence After Liver transplant" (MORAL) for hepatocellular carcinoma (HCC). BACKGROUND: The Milan criteria are used to allocate livers to patients with HCC requiring liver transplantation (LT) but do not include objective measures of tumor biology. Biological markers including the neutrophil-lymphocyte ratio (NLR) and alpha-fetoprotein (AFP) have been associated with recurrence risk. METHODS: Prospective cohort study of adults undergoing LT for HCC between January 2001 and December 2012. RESULTS: A total of 339 patients were included. On multivariable Cox regression analysis, 3 preoperatively available factors were independent predictors of worse recurrence-free survival (RFS), namely, an NLR ≥ 5 (P < 0.0001, hazard ratio, HR: 6.2), AFP > 200 (P < 0.0001, HR: 3.8), and Size >3 cm (P < 0.001, HR: 3.2). The Pre-MORAL score was constructed from the hazard ratios and assigning patients points in an additive fashion, with a minimum of 0 points (no factors) and a maximum of 13 points (all 3 factors). The highest risk patients in the Pre-MORAL had a 5-year RFS of 17.9% compared with 98.6% for the low risk group (P < 0.0001). The post-MORAL was constructed similarly using the 4 postoperatively available independent predictors of worse RFS, grade 4 HCC's (P < 0.0001, HR: 5.6), vascular invasion (P = 0.019, HR: 2.0), size >3 cm (P < 0.0001, HR: 3.2) and number >3 (P = 0.048, HR: 1.8). The pre- and post-MORAL were superior to Milan at predicting recurrence with c-statistics of 0.82 and 0.87, compared with 0.63, respectively. We then combined the scores to produce a combo-MORAL, with a c-statistic of 0.91 for predicting recurrence. CONCLUSIONS: The MORAL score provides a simple, highly accurate tool for predicting recurrence and risk-stratification pre- and postoperatively.

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Crossref · 10.1097/sla.0000000000001966

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  • HCC grade 4, tumor size >3 cm, >3 tumor lesions, and vascular invasion are post-transplantation negative predictive factors.

    “Likewise, HCC grade 4, tumor size >3 cm, > 3 tumor lesions, and vascular invasion have been identified as post-transplantation negative predictive factors.”

    From Artificial Intelligence: Present and Future Potential for Solid Organ Transplantation (2022) · cites this paper as [21]

  • Halazun et al. developed the MORAL model which identified predicting factors of tumor recurrence pre- and post-liver transplantation.

    “Halazun KJ et al. developed a model (MORAL - Model of Recurrence after Liver Transplant) which identified predicting factors of tumor recurrence pre- and post- liver transplantation (21).”

    From Artificial Intelligence: Present and Future Potential for Solid Organ Transplantation (2022) · cites this paper as [21]

  • Neutrophil-lymphocyte ratio ≤5, AFP > 200 ng/ml and tumor size >3 cm are pre-transplantation predictive factors of decreased recurrence-free survival.

    “Specifically, neutrophil-lymphocyte ratio ≤5, alpha-fetoprotein (AFP) > 200 ng/ml and tumor size >3 cm have been classified as pre-transplantation predictive factors of decreased recurrence-free survival.”

    From Artificial Intelligence: Present and Future Potential for Solid Organ Transplantation (2022) · cites this paper as [21]

  • Both MORAL scores demonstrated predictive superiority (C-statistic of 0.82 and 0.86, respectively) compared to Milan criteria (C-statistic of 0.63) for forecasting tumor recurrence.

    “Both scored (pre- and post-transplant) demonstrated predictive superiority (C-statistic of 0.82 and 0.86, respectively) when compared to Milan criteria for forecasting tumor recurrence (C-statistic of 0.63).”

    From Artificial Intelligence: Present and Future Potential for Solid Organ Transplantation (2022) · cites this paper as [21]

  • When combined, the two MORAL scores achieved a C-statistic of 0.91.

    “When combined, the two scores achieved a C-statistic of 0.91.”

    From Artificial Intelligence: Present and Future Potential for Solid Organ Transplantation (2022) · cites this paper as [21]

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Authors
Halazun, K. J., Najjar, M., Abdelmessih, R. M., Samstein, B., Griesemer, A. D., Guarrera, J. V., Kato, T., Verna, E. C., Emond, J. C., & Brown, R. S.
Affiliations
NewYork–Presbyterian Hospital (US)
ORCID
Venue
Annals of Surgery
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2017-03
Volume
265
Issue
3
Pages
557-564
ISSN
0003-4932 (ISSN-L)
DOI
10.1097/sla.0000000000001966
OpenAlex
W2516740959
Cited by
281
References
42
Citations by year
2026: 15 · 2025: 28 · 2024: 32 · 2023: 25 · 2022: 33 · 2021: 35 · 2020: 43 · 2019: 33 · 2018: 23 · 2017: 13 · 2016: 1
FWCI
16.86
Type
journal article
Language
en
Open access
closed
Locations
  • Annals of Surgery (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
  • Health Sciences › Medicine › Oncology › Inflammatory Biomarkers in Disease Prognosis
  • Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
Keywords
hepatocellular carcinoma, liver transplantation, tumor recurrence, recurrence risk prediction, neutrophil-to-lymphocyte ratio, alpha-fetoprotein, Milan criteria, risk stratification, tumor size, vascular invasion, tumor grade, recurrence-free survival, prognostic model, liver allocation, post-transplant monitoring
MeSH terms
Academic Medical Centers, Adult, Aged, Female, Graft Rejection, Graft Survival, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Male, Middle Aged, Neoplasm Invasiveness, Neoplasm Recurrence, Local, Neoplasm Staging, Predictive Value of Tests, Prognosis, Prospective Studies, ROC Curve, Cohort Studies, Multivariate Analysis, Proportional Hazards Models, Survival Analysis, Liver Transplantation, Databases, Factual, Risk Assessment, Disease-Free Survival, Kaplan-Meier Estimate

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