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Utility of Tumor Burden Score to Stratify Prognosis of Patients with Hepatocellular Cancer: Results of 4759 Cases from ITA.LI.CA Study Group

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background

Dichotomous models like Milan Criteria represent the routinely used tools for predicting the outcome of patients with hepatocellular carcinoma (HCC). However, a paradigm shift from a dichotomous to continuous prognostic stratification should represent a good strategy for improving the prediction process. Recently, the tumor burden score (TBS) has been proposed for selecting patients with colorectal liver metastases. To date, TBS has not been validated in a large HCC population. The main objective of this study was to evaluate the prognostic power of TBS in an HCC population treated with different curative and palliative modalities.

Methods

Prospectively collected data from consecutive HCC patients managed in 24 institutions participating in the ITA.LI.CA group between Jan 2002 and Mar 2015 were analyzed (n = 4759). A sub-analysis focused on 3909 patients with the radiological evidence of vascular invasion or metastatic disease was also performed.

Results

TBS demonstrated the best discriminative ability when compared to MC and other tumor-specific scores. At multivariable Cox regression analysis, TBS was an independent risk factor of overall survival, with a 6% increased risk for patient death for each point increase in TBS. At survival analysis, when TBS ≥ 8 was connected with MELD ≥ 15 and alpha-fetoprotein ≥ 1000 ng/mL, patients presenting all these three risk factors presented the worst results (p value < 0.0001).

Conclusions

Survival prediction of HCC patients was very well done using TBS model, even stratifying the population in relation to the presence of metastases and/or vascular invasion. TBS model was the best in terms of discriminatory ability and goodness of fit when compared with other continuous or binary variables. Its incorporation in a model composed by tumor- and liver function-related variables further increases its survival prediction.

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Abbreviations

ABL:

ablation

AFP:

alpha fetoprotein

AIC:

Akaike information criterion

AJCC:

American Joint Committee on Cancer

BCLC:

Barcelona Clinic Liver Cancer

BSC:

best supportive care

CI:

confidence intervals

CPS:

Child-Pugh score

CT:

computerized tomography

DOR:

diagnostic odds ratio

ECOG PST:

Eastern Cooperative Oncology Group performance status

HCC:

hepatocellular carcinoma

HR:

hazard ratio

IAT:

intra-arterial therapies

IQR:

interquartile ranges

ITA.LI.CA.:

Italian Liver Cancer

LR:

liver resection

LT:

liver transplantation

MC:

Milan Criteria

MELD:

model for end-stage liver disease

MRI:

magnetic resonance imaging

ROC:

receiver-operating curve

SOR:

sorafenib

TBS:

tumor burden score

TNM:

tumor/node/metastasis

TTD:

total tumor diameter

TTV:

total tumor volume

UCSFC:

University of California San Francisco Criteria

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Acknowledgements

Other members of the ITA.LI.CA group

Dipartimento di Scienze Mediche e Chirurgiche, Alma Mater Studiorum-Università di Bologna: Maurizio Biselli, Laura Bucci, Paolo Caraceni, Alessandro Cucchetti, Marco Domenicali, Chiara Faggiano, Francesca Garuti, Annagiulia Gramenzi, Alessandro Granito, Donatella Magalotti, Giulia Negrini, Fabio Piscaglia, Matteo Ravaioli, Carla Serra, Francesco Tovoli, Federico Ravaioli, Giovanni Marasco; Dipartimento di Scienze Chirurgiche e Gastroenterologiche, Università di Padova: Giulia Peserico, Filippo Pelizzaro, Paola Todesca, Caterina Pozzan; Dipartimento di Medicina Interna, Unità di Gastroenterologia, IRCCS-Azienda Ospedaliera Universitaria San Martino-IST, Università di Genova: Matteo Brunacci, Alessandro Moscatelli, Gaia Pellegatta, Vincenzo Savarino; Unità Operativa di Chirurgia, Policlinico S. Marco, Zingonia: Paolo Del Poggio, Stefano Olmi; Unità di Medicina Interna e Gastroenterologia, Complesso Integrato Columbus, Università Cattolica di Roma, Roma: Nicoletta de Matthaeis; Unità Operativa di Medicina, Azienda Ospedaliera Bolognini, Seriate, Italia: Claudia Balsamo, Elena Vavassori; Unità Operativa di Gastroenterologia, Ospedale Belcolle, Viterbo: Paola Roselli, Valentina Lauria, Giorgio Pelecca; Unità Operativa di Medicina Protetta, Ospedale Belcolle, Viterbo: Serena Dell’Isola, Anna Maria Ialungo, Elena Rastrelli; Dipartimento Biomedico di Medicina Interna e Specialistica, Unità di Gastroenterologia, Università di Palermo: Calogero Cammà, Marcello Maida, Andrea Costantino; Dipartimento Biomedico di Medicina Interna e Specialistica, Unità di Medicina Interna 2, Azienda Ospedaliera Ospedali Riuniti Villa Sofia-Cervello, Palermo: Andrea Affronti-Emanuele Orlando-Maria Rosa Barcellona; Ospedale Regionale di Bolzano, Unità di Gastroenterologia, Bolzano: Andrea Mega; Unità di Medicina Interna e Gastroenterologia, Policlinico Gemelli, Università Cattolica di Roma, Roma: Emanuele Rinninella; Unità Operativa Gastroenterologia e Malattie del Ricambio, Azienda Ospedaliero-Universitaria Pisana, Pisa: Valeria Mismas; Dipartimento di Medicina Interna, Ospedale per gli Infermi di Faenza, Faenza: Anna Chiara Dall’Aglio, Vittoria Bevilacqua, Andrea Casadei Gardini, Giorgio Ercolani, Erica Fiorini, Arianna Lanzi, Federica Mirici Cappa; Unità di Malattie Infettive ed. Epatologia, Azienda Ospedaliero-Universitaria di Parma: Elisabetta Biasini, Andrea Olivani; Dipartimento di Medicina Clinica e Chirurgia, Unità di Gastroenterologia, Università di Napoli “Federico II”, Napoli: Maria Guarino; Clinica di Gastroenterologia, Università Politecnica delle Marche, Ancona: Alessio Ortolani, Alba Kostandini; Unità di Gastroenterologia, Ospedale Sacro Cuore Don Calabria, Negrar: Maria Chiaramonte, Fabiana Marchetti, Matteo Valerio; Dipartimento di Medicina Diagnostica e Prevenzione, Azienda ospedaliero-universitaria di Bologna, Unità Operativa di Radiologia: Alberta Cappelli, Rita Golfieri, Cristina Mosconi, Matteo Renzulli; Dipartimento di Medicina Clinica e Chirurgia, Unità di Epato-Gastroenterologia, Università di Napoli “Federico II”, Napoli: Piero Coccoli, Marco Sanduzzi Zamparelli; Medicina Interna ed. Epatologia, Dipartimento di Medicina Sperimentale e Clinica–Università di Firenze, Firenze: Andrea Lorenzo Inghilesi, Sami Aburas.

Contributors

AV, QL, FT, and TMP were responsible for the conception, design and analysis of the study, and for editing the final report; AV, QL, FT, and TMP wrote the paper; FF, LB, EGG, LN, FC, GLR, MDM, EC, MZ, FB, RS, GC, RV, FM, MF, FM, LB, AG, GSB, FGF, GM, AM, GN, AC, and MB were involved with the collection and interpretation of data; FF, LB, EGG, LN, FC, GLR, MDM, EC, MZ, FB, RS, GC, RV, FM, MF, FM, LB, AG, GSB, FGF, GM, AM, GN, AC, and MB participated in data management and manuscript review.

Author information

Author notes

  1. Alessandro Vitale and Quirino Lai contributed equally to this work.

Authors and Affiliations

  1. Department of Surgery, Oncology and Gastroenterology, University of Padua, Padua, Italy

    Alessandro Vitale & Fabio Farinati

  2. Liver Transplant and Hepatobiliary Surgery Unit, Sapienza University of Rome, UmbertoI Policlinic of Rome, Viale delPoliclinico 155, 00161, Rome, Italy

    Quirino Lai

  3. Department of Medical and Surgical Sciences, Division of Semeiotics, Alma Mater Studiorum–University of Bologna, Bologna, Italy

    Laura Bucci, Mauro Bernardi & Franco Trevisani

  4. Gastroenterology Unit, Department of Internal Medicine, University of Genoa, Policlinico San Martino, Genoa, Italy

    Edoardo G. Giannini

  5. Department of Medical and Surgical Sciences, Division of Internal Medicine, Alma Mater Studiorum–University of Bologna, Bologna, Italy

    Lucia Napoli & Marco Zoli

  6. Division of Surgery, San Marco Hospital, Zingonia, Italy

    Francesca Ciccarese

  7. Division of Internal Medicine and Gastroenterology, Complesso Integrato Columbus, Università Cattolica del Sacro Cuore, Rome, Italy

    Gian Lodovico Rapaccini

  8. Division of Medicine, Bolognini Hospital, Seriate, Italy

    Maria Di Marco

  9. Division of Gastroenterology, Belcolle Hospital, Viterbo, Italy

    Eugenio Caturelli

  10. Department of Medicine, Division of Radiology, Fatebenefratelli Hospital, Milan, Italy

    Franco Borzio

  11. Division of Gastroenterology and Metabolic Diseases, University Hospital of Pisa, Pisa, Italy

    Rodolfo Sacco

  12. Biomedical Department of Internal and Specialistic Medicine, Division of Gastroenterology, University of Palermo, Palermo, Italy

    Giuseppe Cabibbo

  13. Division of Internal Medicine 2, Ospedali Riuniti Villa Sofia-Cervello, Palermo, Italy

    Roberto Virdone

  14. Internal Medicine and Hepatology, Department of Experimental and Clinical Medicine, University of Firenze, Florence, Italy

    Fabio Marra

  15. Division of Gastroenterology, Bolzano Regional Hospital, Bolzano, Italy

    Martina Felder

  16. Department of Medicine and Surgery, Division of Gastroenterology, University of Naples, “Federico II”, Naples, Italy

    Filomena Morisco

  17. Department of Molecular Medicine, University of Padua, Padua, Italy

    Luisa Benvegnù

  18. Division of Internal Medicine and Gastroenterology, Policlinico Gemelli, Università Cattolica del Sacro Cuore, Rome, Italy

    Antonio Gasbarrini

  19. Division of Gastroenterology, Polytechnic University of Marche, Ancona, Italy

    Gianluca Svegliati-Baroni

  20. Department of Internal Medicine, Ospedale per gli Infermi di Faenza, Faenza, Italy

    Francesco Giuseppe Foschi

  21. Division of Infectious Diseases and Hepatology, Azienda Ospedaliero-Universitaria di Parma, Parma, Italy

    Gabriele Missale

  22. Gastroenterology Unit, Ospedale Sacro Cuore Don Calabria, Negrar, Italy

    Alberto Masotto

  23. Department of Clinical Medicine and Surgery, Hepato-Gastroenterology Unit, University of Naples “Federico II”, Naples, Italy

    Gerardo Nardone

  24. Department of Surgical and Medical sciences, Gastroenterology Unit, Alma Mater Studiorum–Università of Bologna, Bologna, Italy

    Antonio Colecchia

  25. Department of Surgery, Wexner Medical Center at The Ohio State University, Columbus, OH, USA

    Timothy M. Pawlik

Authors
  1. Alessandro Vitale
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  2. Quirino Lai
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  3. Fabio Farinati
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  4. Laura Bucci
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  5. Edoardo G. Giannini
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  6. Lucia Napoli
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  7. Francesca Ciccarese
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  8. Gian Lodovico Rapaccini
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  9. Maria Di Marco
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  10. Eugenio Caturelli
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  11. Marco Zoli
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  12. Franco Borzio
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  13. Rodolfo Sacco
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  14. Giuseppe Cabibbo
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  15. Roberto Virdone
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  16. Fabio Marra
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  17. Martina Felder
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  18. Filomena Morisco
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  19. Luisa Benvegnù
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  20. Antonio Gasbarrini
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  21. Gianluca Svegliati-Baroni
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  22. Francesco Giuseppe Foschi
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  23. Gabriele Missale
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  24. Alberto Masotto
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  25. Gerardo Nardone
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  26. Antonio Colecchia
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  27. Mauro Bernardi
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  28. Franco Trevisani
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  29. Timothy M. Pawlik
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Consortia

On behalf of the Italian Liver Cancer (ITA.LI.CA) group

Corresponding author

Correspondence to Quirino Lai.

Ethics declarations

The Institutional Review Board of the participating institutions approved the study. Informed consent was obtained as usual in clinical, surgical, and radiological practice. Patients gave written consent for procedures performed including use of data for medical and research purposes.

Conflict of Interest

The authors declare that they have no conflicts of interest.

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Vitale, A., Lai, Q., Farinati, F. et al. Utility of Tumor Burden Score to Stratify Prognosis of Patients with Hepatocellular Cancer: Results of 4759 Cases from ITA.LI.CA Study Group. J Gastrointest Surg 22, 859–871 (2018). https://doi.org/10.1007/s11605-018-3688-y

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