Liver Resection vs Nonsurgical Treatments for Patients With Early Multinodular Hepatocellular Carcinoma

Author:

Vitale Alessandro1,Romano Pierluigi1,Cillo Umberto1, , , ,Busti Marco2,Nezi Giulia2,De Carlis Riccardo2,Ratti Francesca2,Milana Flavio2,Donadon Matteo2,Marinelli Laura2,Razionale Francesco2,Carissimi Francesca2,Scotti Mauro Alessandro2,Ciuli Cristina2,De Peppo Valerio2,Russolillo Nadia2,Giuffrida Mauro2,De Stefano Francesca2,Peverada Jacopo2,Larghi Laureiro Zoe2,Franceschi Angelo2,Pelizzo Patrizia2,Marchitelli Ivan2,Casella Annachiara2,Manzoni Alberto2,Malagnino Alessia2,Calcagno Pietro2,Cammarata Francesco2,Pennacchi Luca2,Cosola Davide2,Corleone Pio2,Cucchetti Alessandro2,Mantovani Guido2,Notte Francesca2,Montuori Mauro2,Allegrini Gloria2,Cammà Calogero2,Celsa Ciro2,Giuffrida Paolo2,Giacchetto Carmelo Marco2,Rancatore Gabriele2,Grassin Maria Vittoria2,Ciccia Roberta2,Grova Alessandro2,Salvato Mauro2,Biasini Elisabetta2,Olivani Andrea2,Chen Rusi2,Granito Alessandro2,Piscaglia Fabio2,Stefanini Bernardo2,Tovoli Francesco2,Biselli Maurizio2,Bucci Laura2,Lani Lorenzo2,Stefanini Benedetta2,Bevilacqua Vittoria2,Berardinelli Dante2,Borghi Alberto2,Casadei Gardini Andrea2,Conti Fabio2,Dall'Aglio Anna Chiara2,Ercolan Giorgio2,Campani Claudia2,Di Bonaventura Chiara2,Gitto Stefano2,Franzè Maria Stella2,Sauchella Assunta2,Coccoli Pietro2,Malerba Antonio2,Capasso Mario2,Guarino Maria2,Lauria Valentina2,Ghittoni Giorgia2,Pelecca Giorgio2,Sartori Anna2,Imondi Angela2,Penzo Barbara2,Inno Alessandro2,Marchetti Fabiana2,Di Bucchianico Alessandro2,Dajti Elton2,Ravaioli Federico2,Plaz Torres Maria Corina2,Pieri Giulia2,Olivieri Filippo2,Romagnoli Veronica2,de Matthaeis Nicoletta2,Cela Ester Marina2,Facciorusso Antonio2,Ponziani Francesca Romana2,Lauterio Andrea3,Sangiovanni Angelo4,Cabibbo Giuseppe5,Missale Gabriele6,Marseglia Mariarosaria7,Trevisani Franco8,Foschi Francesco Giuseppe9,Cipriani Federica10,Famularo Simone11,Marra Fabio12,Saitta Carlo13,Serenari Matteo14,Vidili Gianpaolo15,Morisco Filomena16,Caturelli Eugenio17,Mega Andrea18,Pelizzaro Filippo19,Nicolini Daniele20,Ardito Francesco21,Garancini Mattia22,Masotto Alberto23,Baroni Gianluca Svegliati24,Azzaroli Francesco25,Giannini Edoardo2627,Perri Pasquale28,Scarinci Andrea28,Fontana Andrea Pierluigi29,Brunetto Maurizia Rossana30,Iaria Maurizio31,Di Marco Maria32,Nardone Gerardo33,Dominioni Tommaso34,Lai Quirino35,Ferrari Cecilia36,Rapaccini Gian Ludovico37,Rodolfo Sacco38,Romano Maurizio39,Conci Simone40,Zoli Marco41,Conticchio Maria42,Zanello Matteo43,Zimmitti Giuseppe44,Fumagalli Luca45,Troci Albert46,Germani Paola47,Gasbarrini Antonio48,La Barba Giuliano49,De Angelis Michela50,Patauner Stefan51,Molfino Sarah52,Zago Mauro53,Pinotti Enrico53,Frigo Anna Chiara54,Baiocchi Gian Luca52,Frena Antonio51,Boccia Luigi50,Ercolani Giorgio49,Tarchi Paola47,Crespi Michele46,Chiarelli Marco45,Abu Hilal Moh’d44,Cescon Matteo43,Memeo Riccardo42,Ruzzenente Andrea40,Zanus Giacomo39,Griseri Guido36,Rossi Massimo35,Maestri Marcello34,Della Valle Raffaele31,Ferrero Alessandro29,Grazi Gian Luca2855,Romano Fabrizio22,Giuliante Felice21,Vivarelli Marco20,Jovine Elio14,Torzilli Guido11,Aldrighetti Luca10,De Carlis Luciano3

Affiliation:

1. Department of Surgical, Oncological and Gastroenterological Sciences (DiSCOG), University of Padova, Second General Surgical Unit, Padova Teaching Hospital, Padua, Italy

2. for the HE.RC.O.LE.S and ITA.LI.CA Collaborative Groups

3. Department of General and Transplant Surgery, Grande Ospedale Metropolitano Niguarda, School of Medicine and Surgery, University of Milan-Bicocca, Milan, Italy

4. Department of Gastroenterologiy and Hepatology, Foundation IRCCS Ca’ Granda Ospedale Maggiore Policlinico Milan, Milan, Italy

5. Department of Health Promotion, Mother & Child Care, Internal Medicine & Medical Specialties, PROMISE, Section of Gastroenterology & Hepatology, University of Palermo, Palermo, Italy

6. Department of Medicine and Surgery, Infectious Diseases and Hepatology Unit, University of Parma and Azienda Ospedaliero-Universitaria of Parma, Parma, Italy

7. Division of Internal Medicine, Hepatobiliary and Immunoallergic Disease, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy

8. Unit of Semeiotics, Liver and Alcohol-Related Diseases, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy

9. Medicina Interna Faenza, Dipartimento Emergenza, Medicina Interna e Cardiologia IRCCS-Istituto Scientifico Romagnolo per lo Studio dei Tumori “Dino Amadori” Meldola, AUSL Romagna, Meldola, Italy

10. Hepatobiliary Surgery Division, “Vita e Salute” University, Ospedale San Raffaele IRCCS, Milan, Italy

11. Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy; Department of Hepatobiliary and General Surgery, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

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

13. Department of Clinical and Experimental Medicine, Division of Medicine and Hepatology, University of Messina, Messina, Italy

14. Hepatobiliary Surgery and Transplant Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy

15. Department of Medicine, Surgery and Pharmacy, AOU Sassari, Italy

16. Department of Clinical Medicine and Surgery, Departmental Program “Diseases of the Liver and Biliary System”, University of Napoli “Federico II”, Naples, Italy

17. Gastroenterology Unit, Belcolle Hospital, Viterbo, Italy

18. Gastroenterology Unit, Bolzano Regional Hospital, Bolzano, Italy

19. Department of Surgery, Oncology, and Gastroenterology, Gastroenterology Unit, University of Padova, Padua, Italy

20. HPB Surgery and Transplantation Unit, Department of Clinical and Experimental Medicine, Polytechnic University of Marche, Ancona, Italy

21. Hepatobiliary Surgery Unit, Fondazione Policlinico Universitario A Gemelli, IRCCS, Catholic University of the Sacred Heart, Rome, Italy

22. School of medicine and surgery, University of Milano Bicocca, IRCCS Fondazione San Gerardo, Monza, Italy

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

24. Liver Injury and Transplant Unit and Obesity Center, Polytechnic University of Marche, Ancona, Italy

25. Gastroenterology Unit, Department of Surgical and Medical Sciences, IRCCS Azienda Ospedaliero, Universitaria di Bologna, Bologna, Italy

26. Gastroenterology Unit, Department of Internal Medicine, University of Genoa, Genoa, Italy

27. Gastroenterology Unit, IRCCS Ospedale San Martino, Genoa, Italy

28. Division of Hepatobiliary pancreatic Unit, IRCCS-Regina Elena National Cancer Institute, Rome, Italy

29. Department of General and Oncological Surgery, Mauriziano Hospital “Umberto I”, Turin, Italy

30. UO Epatologia, Azienda Ospedaliero Universitaria Pisana, Pisa, Italy

31. Department of Medicine and Surgery, University of Parma, Parma, Italy

32. Medicine Unit, Bolognini Hospital, Seriate, Italy

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

34. Unit of General Surgery 1, University of Pavia and Foundation IRCCS Policlinico San Matteo, Pavia, Italy

35. General Surgery and Organ Transplantation Unit, Sapienza University of Rome, Umberto I Polyclinic of Rome, Rome, Italy

36. HPB Surgical Unit, San Paolo Hospital, Savona, Italy

37. Gastroenterology Unit, Fondazione Policlinico Universitario A Gemelli, IRCCS, Roma, Italy

38. Gastroenterology and Digestive Endoscopy Unit, Foggia University Hospital, Foggia, Italy

39. Department of Surgical, Oncological and Gastroenterological Science (DISCOG), University of Padua, Hepatobiliary and Pancreatic Surgery Unit, Treviso Hospital, Treviso, Italy

40. Division of General and Hepatobiliary Surgery, Department of Surgical Sciences, Dentistry, Gynecology and Pediatrics, University of Verona, Verona, Italy

41. Department of Medical and Surgical Sciences, Internal Medicine–Zoli Unit, Alma Mater Studiorum,Università di Bologna, Padova, Italy

42. Department of Hepato-Pancreatic-Biliary Surgery, Miulli Hospital, Bari, Italy

43. Alma Mater Studiorum, University of Bologna, AOU Sant’Orsola Malpighi, IRCCS at Maggiore Hospital, Bologna, Italy

44. Department of General Surgery, Poliambulanza Foundation Hospital, Brescia, Italy

45. Department of Emergency and Robotic Surgery, ASST Lecco, Lecco, Italy

46. Department of Surgery, L Sacco Hospital, Milan, Italy

47. Division of General Surgery, Department of Medical and Surgical Sciences, ASUGI, Trieste, Italy

48. Internal Medicine and Gastroenterology, Fondazione Policlinico Universitario Agostino Gemelli, IRCCS and Università Cattolica del Sacro Cuore, Rome, Italy

49. General and Oncologic Surgery, Morgagni-Pierantoni Hospital, Department of Medical and Surgical Sciences, University of Bologna Forlì, Forlì, Italy

50. Department of General Surgery, Ospedale Carlo Poma, Mantua, Italy

51. Department of General and Pediatric Surgery, Bolzano Central Hospital, Bolzano, Italy

52. Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy

53. Department of Surgery, Ponte San Pietro Hospital, Bergamo, Italy; Department of Emergency and Robotic Surgery, ASST Lecco, Lecco, Italy

54. Biostatistics, Epidemiology and Public Health Unit, Department of Cardiac, Thoracic, Vascular Sciences and Public Health, University of Padua, Padua, Italy

55. Now with HepatoBiliaryPancreatic Surgery, AOU Careggi, Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy

Abstract

ImportanceThe 2022 Barcelona Clinic Liver Cancer algorithm currently discourages liver resection (LR) for patients with multinodular hepatocellular carcinoma (HCC) presenting with 2 or 3 nodules that are each 3 cm or smaller.ObjectiveTo compare the efficacy of liver resection (LR), percutaneous radiofrequency ablation (PRFA), and transarterial chemoembolization (TACE) in patients with multinodular HCC.Design, Setting, and ParticipantsThis cohort study is a retrospective analysis conducted using data from the HE.RC.O.LE.S register (n = 5331) for LR patients and the ITA.LI.CA database (n = 7056) for PRFA and TACE patients. A matching-adjusted indirect comparison (MAIC) method was applied to balance data and potential confounding factors between the 3 groups. Included were patients from multiple centers from 2008 to 2020; data were analyzed from January to December 2023.InterventionsLR, PRFA, or TACE.Main Outcomes and MeasuresSurvival rates at 1, 3, and 5 years were calculated. Cox MAIC-weighted multivariable analysis and competing risk analysis were used to assess outcomes.ResultsA total of 720 patients with early multinodular HCC were included, 543 males (75.4%), 177 females (24.6%), and 350 individuals older than 70 years (48.6%). There were 296 patients in the LR group, 240 who underwent PRFA, and 184 who underwent TACE. After MAIC, LR exhibited 1-, 3-, and 5-year survival rates of 89.11%, 70.98%, and 56.44%, respectively. PRFA showed rates of 94.01%, 65.20%, and 39.93%, while TACE displayed rates of 90.88%, 48.95%, and 29.24%. Multivariable Cox survival analysis in the weighted population showed a survival benefit over alternative treatments (PRFA vs LR: hazard ratio [HR], 1.41; 95% CI, 1.07-1.86; P = .01; TACE vs LR: HR, 1.86; 95% CI, 1.29-2.68; P = .001). Competing risk analysis confirmed a lower risk of cancer-related death in LR compared with PRFA and TACE.Conclusions and RelevanceFor patients with early multinodular HCC who are ineligible for transplant, LR should be prioritized as the primary therapeutic option, followed by PRFA and TACE when LR is not feasible. These findings provide valuable insights for clinical decision-making in this patient population.

Publisher

American Medical Association (AMA)

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