51
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

Macroscopic Characterization of Hepatocellular Carcinoma: An Underexploited Source of Prognostic Factors

, , , , , , , , , , , , ORCID Icon & ORCID Icon show all
Pages 707-719 | Received 02 Nov 2023, Accepted 29 Feb 2024, Published online: 09 Apr 2024

References

  • Cancer Tomorrow. 2024. Available from: https://gco.iarc.fr/tomorrow/en/dataviz/isotype?cancers=11&single_unit=50000&years=2030&types=1.Accessed May 6, 2022.
  • Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primer. 2021;7(1):6.
  • Rahib L, Wehner MR, Matrisian LM, Nead KT. Estimated projection of us cancer incidence and death to 2040. JAMA Network Open. 2021;4(4):e214708. doi:10.1001/jamanetworkopen.2021.4708
  • Labgaa I, Villanueva A, Dormond O, Demartines N, Melloul E. The role of liquid biopsy in hepatocellular carcinoma prognostication. Cancers. 2021;13(4):659. doi:10.3390/cancers13040659
  • Villanueva A, Hoshida Y, Battiston C, et al. Combining clinical, pathology, and gene expression data to predict recurrence of hepatocellular carcinoma. Gastroenterology. 2011;140(5):1501–1512.e2. doi:10.1053/j.gastro.2011.02.006
  • Labgaa I, Torrecilla S, Martinez-Quetglas I, Sia D. Genetics of hepatocellular carcinoma: risk stratification, clinical outcome, and implications for therapy. Dig Dis Interv. 2017;01(2):55–65. doi:10.1055/s-0037-1603577
  • Eggel H. Uber das primare Carcinoma der Leber. Beitr Pathol Anat Allg Pathol. 1901;30:506–604.
  • Martins-Filho SN, Alves VAF. The strengths and weaknesses of gross and histopathological evaluation in hepatocellular carcinoma: a brief review. Surg Exp Pathol. 2019;2(1):23. doi:10.1186/s42047-019-0047-6
  • Liver Cancer Stages. 2023. Available from: https://www.cancer.org/cancer/liver-cancer/detection-diagnosis-staging/staging.html.Accessed April 24, 2023.
  • Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334(11):693–699. doi:10.1056/NEJM199603143341104
  • Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis. 1999;19(3):329–338. doi:10.1055/s-2007-1007122
  • Kluger MD, Salceda JA, Laurent A, et al. Liver resection for hepatocellular carcinoma in 313 Western patients: tumor biology and underlying liver rather than tumor size drive prognosis. J Hepatol. 2015;62(5):1131–1140. doi:10.1016/j.jhep.2014.12.018
  • Zhang Y, Lei X, Xu L, Lv X, Xu M, Tang H. Preoperative and postoperative nomograms for predicting early recurrence of hepatocellular carcinoma without macrovascular invasion after curative resection. BMC Surg. 2022;22(1):233. doi:10.1186/s12893-022-01682-0
  • Xu XF, Xing H, Han J, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study From China. JAMA Surg. 2019;154(3):209–217. doi:10.1001/jamasurg.2018.4334
  • Welling TH, Eddinger K, Carrier K, et al. Multicenter Study of Staging and Therapeutic Predictors of Hepatocellular Carcinoma Recurrence Following Transplantation. Liver Transplant. 2018;24(9):1233–1242. doi:10.1002/lt.25194
  • Minagawa M, Ikai I, Matsuyama Y, Yamaoka Y, Makuuchi M. Staging of hepatocellular carcinoma: assessment of the Japanese TNM and AJCC/UICC TNM systems in a cohort of 13,772 patients in Japan. Ann Surg. 2007;245(6):909–922. doi:10.1097/01.sla.0000254368.65878.da
  • Meng KW, Dong M, Zhang WG, Huang QX. Clinical characteristics and surgical prognosis of hepatocellular carcinoma with bile duct invasion. Gastroenterol Res Pract. 2014;2014:604971. doi:10.1155/2014/604971
  • Vauthey JN, Lauwers GY, Esnaola NF, et al. Simplified staging for hepatocellular carcinoma. J Clin Oncol. 2002;20(6):1527–1536. doi:10.1200/JCO.2002.20.6.1527
  • Poon RTP, Fan ST. Evaluation of the new AJCC/UICC staging system for hepatocellular carcinoma after hepatic resection in Chinese patients. Surg Oncol Clin N Am. 2003;12(1):35–50. doi:10.1016/S1055-3207(02)00086-8
  • Liu W, Wang K, Bao Q, Sun Y, Xing BC. Hepatic resection provided long-term survival for patients with intermediate and advanced-stage resectable hepatocellular carcinoma. World J Surg Oncol. 2016;14:62. doi:10.1186/s12957-016-0811-y
  • Roayaie S, Jibara G, Taouli B, Schwartz M. Resection of hepatocellular carcinoma with macroscopic vascular invasion. Ann Surg Oncol. 2013;20(12):3754–3760. doi:10.1245/s10434-013-3074-7
  • Tsai TJ, Chau GY, Lui WY, et al. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery. 2000;127(6):603–608. doi:10.1067/msy.2000.105498
  • Lee YJ, Lee YR, Seo CG, et al. How should we assign large infiltrative hepatocellular carcinomas for staging? Cancers. 2020;12(9):2589. doi:10.3390/cancers12092589
  • D’Amico F, Schwartz M, Vitale A, et al. Predicting recurrence after liver transplantation in patients with hepatocellular carcinoma exceeding the up-to-seven criteria. Liver Transplant. 2009;15(10):1278–1287. doi:10.1002/lt.21842
  • Pawlik TM, Poon RT, Abdalla EK, et al. Critical appraisal of the clinical and pathologic predictors of survival after resection of large hepatocellular carcinoma. Arch Surg Chic Ill. 2005;140(5):450–457.
  • DuPont-Bierre E, Compagnon P, Raoul JL, Fayet G, de Lajarte-Thirouard AS, Boudjema K. Resection of hepatocellular carcinoma in noncirrhotic liver: analysis of risk factors for survival. J Am Coll Surg. 2005;201(5):663–670. doi:10.1016/j.jamcollsurg.2005.06.265
  • Choi GH, Park JY, Hwang HK, et al. Predictive factors for long-term survival in patients with clinically significant portal hypertension following resection of hepatocellular carcinoma. Liver Int. 2011;31(4):485–493. doi:10.1111/j.1478-3231.2010.02436.x
  • Shetty K, Timmins K, Brensinger C, et al. Liver transplantation for hepatocellular carcinoma validation of present selection criteria in predicting outcome. Liver Transplant. 2004;10(7):911–918. doi:10.1002/lt.20140
  • Iwatsuki S, Dvorchik I, Marsh JW, et al. Liver transplantation for hepatocellular carcinoma: a proposal of a prognostic scoring system. J Am Coll Surg. 2000;191(4):389–394. doi:10.1016/S1072-7515(00)00688-8
  • Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl. 2005;11(9):1086–1092. doi:10.1002/lt.20472
  • Esaki M, Shimada K, Sano T, Sakamoto Y, Kosuge T, Ojima H. Surgical results for hepatocellular carcinoma with bile duct invasion: a clinicopathologic comparison between macroscopic and microscopic tumor thrombus. J Surg Oncol. 2005;90(4):226–232. doi:10.1002/jso.20260
  • Okuda K, Peters RL, Simson IW. Gross anatomic features of hepatocellular carcinoma from three disparate geographic areas. Proposal of new classification. Cancer. 1984;54(10):2165–2173. doi:10.1002/1097-0142(19841115)54:10<2165:AID-CNCR2820541017>3.0.CO;2-7
  • Sakon M, Monden M, Umeshita K, et al. The prognostic significance of macroscopic growth pattern of hepatocellular carcinoma. Int Surg. 1994;79(1):38–42.
  • The general rules for the clinical and pathological study of primary liver cancer. Liver cancer study group of Japan. Jpn J Surg. 1989;19(1):98–129. doi:10.1007/BF02471576
  • Kudo M, Kitano M, Sakurai T, Nishida N. General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the liver cancer study Group of Japan. Dig Dis. 2015;33(6):765–770. doi:10.1159/000439101
  • Jang JY, Lee JS, Kim HJ, et al. The General rules for the study of primary liver cancer. J Liver Cancer. 2017;17(1):19–44. doi:10.17998/jlc.17.1.19
  • Hui AM, Takayama T, Sano K, et al. Predictive value of gross classification of hepatocellular carcinoma on recurrence and survival after hepatectomy. J Hepatol. 2000;33(6):975–979. doi:10.1016/S0168-8278(00)80131-2
  • Rhee H, Chung T, Yoo JE, et al. Gross type of hepatocellular carcinoma reflects the tumor hypoxia, fibrosis, and stemness-related marker expression. Hepatol Int. 2020;14(2):239–248. doi:10.1007/s12072-020-10012-6
  • He J, Shi J, Fu X, et al. The clinicopathologic and prognostic significance of gross classification on solitary hepatocellular carcinoma after hepatectomy. Medicine. 2015;94(32):e1331. doi:10.1097/MD.0000000000001331
  • Lee Y, Park H, Lee H, et al. The clinicopathological and prognostic significance of the gross classification of hepatocellular carcinoma. J Pathol Transl Med. 2018;52(2):85–92. doi:10.4132/jptm.2017.11.13
  • Choi GH, Han DH, Kim DH, et al. Outcome after curative resection for a huge (≥10 cm) hepatocellular carcinoma and prognostic significance of gross tumor classification. Am J Surg. 2009;198(5):693–701. doi:10.1016/j.amjsurg.2008.09.019
  • Hatanaka K, Minami Y, Kudo M, Inoue T, Chung H, Haji S. The gross classification of hepatocellular carcinoma: usefulness of contrast-enhanced US. J Clin Ultrasound. 2014;42(1):1–8. doi:10.1002/jcu.22080
  • Chau GY, Lui WY, Tsay SH, et al. Prognostic significance of surgical margin in hepatocellular carcinoma resection: an analysis of 165 Childs’ A patients. J Surg Oncol. 1997;66(2):122–126. doi:10.1002/(SICI)1096-9098(199710)66:2<122:AID-JSO9>3.0.CO;2-F
  • Park YK, Kim BW, Wang HJ, Kim MW. Hepatic resection for hepatocellular carcinoma meeting Milan criteria in child-Turcotte-Pugh class a patients with cirrhosis. Transplant Proc. 2009;41(5):1691–1697. doi:10.1016/j.transproceed.2008.07.146
  • Kondo K, Chijiiwa K, Makino I, et al. Risk factors for early death after liver resection in patients with solitary hepatocellular carcinoma. J Hepatobiliary Pancreat Surg. 2005;12(5):399–404. doi:10.1007/s00534-005-1009-9
  • Li L, Xu L, Zhou S, Wang P, Zhang M, Li B. Tumour site is a risk factor for hepatocellular carcinoma after hepatectomy: a 1:2 propensity score matching analysis. BMC Surg. 2022;22(1):104. doi:10.1186/s12893-022-01564-5
  • College of American Pathologists. Protocol for the examination of specimens from patients with hepatocellular carcinoma; 2023. Available from: https://documents.cap.org/protocols/Liver.HCC_4.2.0.0.REL_CAPCP.pdf.Accessed April 24, 2023.
  • Fan Z, Jin M, Zhang L, et al. From clinical variables to multiomics analysis: a margin morphology-based gross classification system for hepatocellular carcinoma stratification. Gut. 2023;2023:1.
  • Su K, Huang W, Li X, et al. Evaluation of lactate dehydrogenase and alkaline phosphatase as predictive biomarkers in the prognosis of hepatocellular carcinoma and development of a new nomogram. J Hepatocell Carcinoma. 2023;10:69–79. doi:10.2147/JHC.S398632
  • Su K, Shen Q, Tong J, et al. Construction and validation of a nomogram for HBV-related hepatocellular carcinoma: a large, multicenter study. Ann Hepatol. 2023;28(4):101109. doi:10.1016/j.aohep.2023.101109
  • Li H, Guo L, Su K, et al. Construction and validation of TACE therapeutic efficacy by ALR score and nomogram: a large, multicenter Study. J Hepatocell Carcinoma. 2023;10:1009–1017. doi:10.2147/JHC.S414926
  • Burt AD, Alves V, Bedossa P, et al. Data set for the reporting of intrahepatic cholangiocarcinoma, perihilar cholangiocarcinoma and hepatocellular carcinoma: recommendations from the International Collaboration on Cancer reporting (ICCR). Histopathology. 2018;73(3):369–385. doi:10.1111/his.13520
  • Gao Q, Zhu H, Dong L, et al. Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell. 2019;179(2):561–577.e22. doi:10.1016/j.cell.2019.08.052
  • Amaddeo G, Cao Q, Ladeiro Y, et al. Integration of tumour and viral genomic characterizations in HBV-related hepatocellular carcinomas. Gut. 2015;64(5):820–829. doi:10.1136/gutjnl-2013-306228
  • Pelizzaro F, Trevisani F, Simeon V, et al. Predictors of non-transplantable recurrence in hepatocellular carcinoma patients treated with frontline liver resection. Liver Int. 2023;43(12):2762–2775. doi:10.1111/liv.15719
  • Pinyol R, Montal R, Bassaganyas L, et al. Molecular predictors of prevention of recurrence in HCC with sorafenib as adjuvant treatment and prognostic factors in the Phase 3 STORM trial. Gut. 2019;68(6):1065–1075. doi:10.1136/gutjnl-2018-316408
  • Montironi C, Castet F, Haber PK, et al. Inflamed and non-inflamed classes of HCC: a revised immunogenomic classification. Gut. 2023;72(1):129–140. doi:10.1136/gutjnl-2021-325918
  • Zeng Q, Klein C, Caruso S, et al. Artificial intelligence predicts immune and inflammatory gene signatures directly from hepatocellular carcinoma histology. J Hepatol. 2022;77(1):116–127. doi:10.1016/j.jhep.2022.01.018
  • Schmauch B, Romagnoni A, Pronier E, et al. A deep learning model to predict RNA-Seq expression of tumours from whole slide images. Nat Commun. 2020;11(1):3877. doi:10.1038/s41467-020-17678-4
  • Calderaro J, Seraphin TP, Luedde T, Simon TG. Artificial intelligence for the prevention and clinical management of hepatocellular carcinoma. J Hepatol. 2022;76(6):1348–1361. doi:10.1016/j.jhep.2022.01.014
  • Su K, Wang F, Li X, et al. Effect of external beam radiation therapy versus transcatheter arterial chemoembolization for non-diffuse hepatocellular carcinoma (≥ 5 cm): a multicenter experience over a ten-year period. Front Immunol. 2023;14:1265959. doi:10.3389/fimmu.2023.1265959
  • Li H, Wu Z, Chen J, et al. External radiotherapy combined with sorafenib has better efficacy in unresectable hepatocellular carcinoma: a systematic review and meta-analysis. Clin Exp Med. 2023;23(5):1537–1549. doi:10.1007/s10238-022-00972-4
  • Li H, Su K, Guo L, et al. PD-1 inhibitors combined with antiangiogenic therapy with or without transarterial chemoembolization in the treatment of hepatocellular carcinoma: a propensity matching analysis. J Hepatocell Carcinoma. 2023;10:1257–1266. doi:10.2147/JHC.S415843
  • Reig M, Forner A, Rimola J, et al. BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol. 2022;76(3):681–693. doi:10.1016/j.jhep.2021.11.018
  • Hack SP, Spahn J, Chen M, et al. IMbrave 050: a of atezolizumab plus bevacizumab in high-risk hepatocellular carcinoma after curative resection or ablation. Future Oncol. 2020;16(15):975–989. doi:10.2217/fon-2020-0162
  • Jung S-M, Kim JM, Choi G-S, et al. Characteristics of early recurrence after curative liver resection for solitary hepatocellular carcinoma. J Gastrointest Surg. 2019;23:304–311.
  • Roayaie S, Schwartz JD, Sung MW, et al. Recurrence of hepatocellular carcinoma after liver transplant: patterns and prognosis. Liver Transpl. 2004;10:534–540. doi:10.1002/lt.20128
  • Parfitt JR, Marotta P, Alghamdi M, et al. Recurrent hepatocellular carcinoma after transplantation: use of a pathological score on explanted livers to predict recurrence. Liver Transpl. 2007;13:543–551. doi:10.1002/lt.21078
  • Ochiai T, Ikoma H, Okamoto K, Kokuba Y, Sonoyama T, Otsuji E. Clinicopathologic features and risk factors for extrahepatic recurrences of hepatocellular carcinoma after curative resection. World J Surg. 2012;36:136–143. doi:10.1007/s00268-011-1317-y
  • Shah SA, Tan JCC, McGilvray ID, et al. Does microvascular invasion affect outcomes after liver transplantation for HCC? A histopathological analysis of 155 consecutive explants. J Gastrointest Surg. 2007;11:464–471. doi:10.1007/s11605-006-0033-7
  • Yamamoto Y, et al. Post-hepatectomy survival in advanced hepatocellular carcinoma with portal vein tumor thrombosis. World J Gastroenterol. 2015;21(1):246–253. doi:10.3748/wjg.v21.i1.246
  • Du Z-G, Wei Y-G, Chen K-F, Li B. Risk factors associated with early and late recurrence after curative resection of hepatocellular carcinoma: a single institution’s experience with 398 consecutive patients. Hepatobiliary Pancreat Dis Int. 2014;13(2):153–161. doi:10.1016/S1499-3872(14)60025-4
  • Goh BKP, Teo J-Y, Chan C-Y, et al. Importance of tumor size as a prognostic factor after partial liver resection for solitary hepatocellular carcinoma: implications on the current AJCC staging system. J Surg Oncol. 2016;113(1):89–93. doi:10.1002/jso.24099
  • Oba A, Takahashi S, Kato Y, et al. Usefulness of resection for hepatocellular carcinoma with macroscopic bile duct tumor thrombus. Anticancer Res. 2014;34(8):4367–4372.
  • Lin S-H, Eng H-L, Liu Y-W, et al. Characteristics and prognosis of patients with large well-differentiated hepatocellular carcinoma who have undergone resection. Am J Surg. 2022;223(2):339–345. doi:10.1016/j.amjsurg.2021.03.065
  • Zavaglia C, De Carlis L, Alberti AB, et al. Predictors of long-term survival after liver transplantation for hepatocellular carcinoma. Am J Gastroenterol. 2005;100(12):2708–2716. doi:10.1111/j.1572-0241.2005.00289.x
  • Zhang H, Yuan S-X, Dai S-Y, et al. Tumor size does not independently affect long-term survival after curative resection of solitary hepatocellular carcinoma without macroscopic vascular invasion. World J Surg. 2014;38(4):947–957. doi:10.1007/s00268-013-2365-2
  • Lim C, Mise Y, Sakamoto Y, et al. Above 5 cm, size does not matter anymore in patients with hepatocellular carcinoma. World JSurg. 2014;38(11):2910–2918. doi:10.1007/s00268-014-2704-y
  • Silva JPM, Coelho FF, Cassenote AJF, et al. Preoperative inflammatory markers as prognostic predictors after hepatocellular carcinoma resection: data from a western referral center. BMC Surg. 2022;22(1):329. doi:10.1186/s12893-022-01779-6
  • Shimada M, Rikimaru T, Hamatsu T, et al. The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg. 2001;182(2):177–182. doi:10.1016/S0002-9610(01)00682-1