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Open Access 05-09-2024 | Hepatocellular Carcinoma | Magnetic Resonance

MRI-based prediction of the need for wide resection margins in patients with single hepatocellular carcinoma

Authors: Yanshu Wang, Yali Qu, Chongtu Yang, Yuanan Wu, Hong Wei, Yun Qin, Jie Yang, Tianying Zheng, Jie Chen, Roberto Cannella, Federica Vernuccio, Maxime Ronot, Weixia Chen, Bin Song, Hanyu Jiang

Published in: European Radiology

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Abstract

Objectives

To develop an MRI-based score that enables individualized predictions of the survival benefit of wide over narrow resection margins.

Materials and methods

This single-center retrospective study (December 2011 to May 2022) included consecutive patients who underwent curative-intent resection for single Barcelona Clinic Liver Cancer (BCLC) 0/A HCC and preoperative contrast-enhanced MRI. In patients with narrow resection margins, preoperative demographic, laboratory, and MRI variables independently associated with early recurrence-free survival (RFS) were identified using Cox regression analyses, which were employed to develop a predictive score (named “MARGIN”). Survival outcomes were compared between wide and narrow resection margins in a propensity-score matched cohort for the score-stratified low- and high-risk groups, respectively.

Results

Four hundred nineteen patients (median age, 54 years; 361 men) were included, 282 (67.3%) undergoing narrow resection margins. In patients with narrow resection margins, age, alpha-fetoprotein (AFP) > 400 ng/mL, protein induced by vitamin K absence or antagonist-II (PIVKA-II) > 200 mAU/mL, radiological involvement of liver capsule, and infiltrative appearance were associated with early RFS (p values, 0.002–0.04) and formed the MARGIN score with a testing dataset C-index of 0.75 (95% CI: 0.65–0.84). In the matched cohort, wide resection margin was associated with improved early RFS rate for the high-risk group (MARGIN score ≥ − 1.3; 71.1% vs 41.0%; p = 0.02), but not for the low-risk group (MARGIN score < − 1.3; 79.7% vs 76.1%; p = 0.36).

Conclusion

In patients with single BCLC 0/A HCC, the MARGIN score may serve as promising decision-making to indicate the need for wide resection margins.

Clinical relevance statement

The MARGIN score has the potential to identify patients who would benefit more from wide resection margins than narrow resection margins, improving the postoperative survival of patients with single BCLC 0/A hepatocellular carcinoma (HCC).

Key Points

  • Age, AFP, PIVKA-II, radiological involvement of liver capsule, and infiltrative appearance were associated with early RFS and formed the MARGIN score.
  • The MARGIN score achieved a testing dataset C-index of 0.75.
  • Wide resection margins were associated with improved early RFS for the high-risk group, but not for the low-risk group.

Graphical Abstract

Appendix
Available only for authorised users
Literature
1.
go back to reference Singal AG, Kanwal F, Llovet JM (2023) Global trends in hepatocellular carcinoma epidemiology: implications for screening, prevention and therapy. Nat Rev Clin Oncol 20:864–884CrossRefPubMed Singal AG, Kanwal F, Llovet JM (2023) Global trends in hepatocellular carcinoma epidemiology: implications for screening, prevention and therapy. Nat Rev Clin Oncol 20:864–884CrossRefPubMed
2.
go back to reference Lin YJ, Ho CM (2021) Is the rationale of anatomical liver resection for hepatocellular carcinoma universally adoptable? A hypothesis-driven review. Medicina (Kaunas) 57:131 Lin YJ, Ho CM (2021) Is the rationale of anatomical liver resection for hepatocellular carcinoma universally adoptable? A hypothesis-driven review. Medicina (Kaunas) 57:131
3.
go back to reference Zhang EL, Cheng Q, Huang ZY et al (2021) Revisiting surgical strategies for hepatocellular carcinoma with microvascular invasion. Front Oncol 11:691354CrossRefPubMedPubMedCentral Zhang EL, Cheng Q, Huang ZY et al (2021) Revisiting surgical strategies for hepatocellular carcinoma with microvascular invasion. Front Oncol 11:691354CrossRefPubMedPubMedCentral
4.
go back to reference Shi M, Guo RP, Lin XJ et al (2007) Partial hepatectomy with wide versus narrow resection margin for solitary hepatocellular carcinoma: a prospective randomized trial. Ann Surg 245:36–43CrossRefPubMedPubMedCentral Shi M, Guo RP, Lin XJ et al (2007) Partial hepatectomy with wide versus narrow resection margin for solitary hepatocellular carcinoma: a prospective randomized trial. Ann Surg 245:36–43CrossRefPubMedPubMedCentral
5.
go back to reference Yang P, Si A, Yang J et al (2019) A wide-margin liver resection improves long-term outcomes for patients with HBV-related hepatocellular carcinoma with microvascular invasion. Surgery 165:721–730CrossRefPubMed Yang P, Si A, Yang J et al (2019) A wide-margin liver resection improves long-term outcomes for patients with HBV-related hepatocellular carcinoma with microvascular invasion. Surgery 165:721–730CrossRefPubMed
6.
go back to reference Nitta H, Allard MA, Sebagh M et al (2021) Ideal surgical margin to prevent early recurrence after hepatic resection for hepatocellular carcinoma. World J Surg 45:1159–1167CrossRefPubMed Nitta H, Allard MA, Sebagh M et al (2021) Ideal surgical margin to prevent early recurrence after hepatic resection for hepatocellular carcinoma. World J Surg 45:1159–1167CrossRefPubMed
7.
go back to reference Kobayashi N, Aramaki O, Midorikawa Y et al (2020) Impact of marginal resection for hepatocellular carcinoma. Surgery Today 50:1471–1479CrossRefPubMed Kobayashi N, Aramaki O, Midorikawa Y et al (2020) Impact of marginal resection for hepatocellular carcinoma. Surgery Today 50:1471–1479CrossRefPubMed
8.
go back to reference Michelakos T, Kontos F, Sekigami Y et al (2021) Hepatectomy for solitary hepatocellular carcinoma: resection margin width does not predict survival. J Gastrointest Surg 25:1727–1735CrossRefPubMed Michelakos T, Kontos F, Sekigami Y et al (2021) Hepatectomy for solitary hepatocellular carcinoma: resection margin width does not predict survival. J Gastrointest Surg 25:1727–1735CrossRefPubMed
9.
go back to reference Zhou Z, Qi L, Mo Q et al (2021) Effect of surgical margin on postoperative prognosis in patients with solitary hepatocellular carcinoma: a propensity score matching analysis. J Cancer 12:4455–4462CrossRefPubMedPubMedCentral Zhou Z, Qi L, Mo Q et al (2021) Effect of surgical margin on postoperative prognosis in patients with solitary hepatocellular carcinoma: a propensity score matching analysis. J Cancer 12:4455–4462CrossRefPubMedPubMedCentral
10.
go back to reference Lin Y, Xu J, Hong J et al (2022) Prognostic impact of surgical margin in hepatectomy on patients with hepatocellular carcinoma: a meta-analysis of observational studies. Front Surg 9:810479CrossRefPubMedPubMedCentral Lin Y, Xu J, Hong J et al (2022) Prognostic impact of surgical margin in hepatectomy on patients with hepatocellular carcinoma: a meta-analysis of observational studies. Front Surg 9:810479CrossRefPubMedPubMedCentral
11.
go back to reference Li Y, Li PP, Sun DP et al (2022) One- versus two-stage partial hepatectomy for large resectable solitary hepatocellular carcinomas determined preoperatively to have a narrow resection margin: a propensity score matching analysis. Hepatobiliary Surg Nutr 11:662–674CrossRefPubMedPubMedCentral Li Y, Li PP, Sun DP et al (2022) One- versus two-stage partial hepatectomy for large resectable solitary hepatocellular carcinomas determined preoperatively to have a narrow resection margin: a propensity score matching analysis. Hepatobiliary Surg Nutr 11:662–674CrossRefPubMedPubMedCentral
12.
go back to reference Chen B, Wu JX, Cheng SH et al (2021) Phase 2 study of adjuvant radiotherapy following narrow-margin hepatectomy in patients with HCC. Hepatology 74:2595–2604CrossRefPubMed Chen B, Wu JX, Cheng SH et al (2021) Phase 2 study of adjuvant radiotherapy following narrow-margin hepatectomy in patients with HCC. Hepatology 74:2595–2604CrossRefPubMed
13.
go back to reference Tsilimigras DI, Sahara K, Moris D et al (2020) Effect of surgical margin width on patterns of recurrence among patients undergoing R0 hepatectomy for T1 hepatocellular carcinoma: an international multi-institutional analysis. J Gastrointest Surg 24:1552–1560CrossRefPubMed Tsilimigras DI, Sahara K, Moris D et al (2020) Effect of surgical margin width on patterns of recurrence among patients undergoing R0 hepatectomy for T1 hepatocellular carcinoma: an international multi-institutional analysis. J Gastrointest Surg 24:1552–1560CrossRefPubMed
14.
go back to reference Marques F, Ghallab M, Vibert E et al (2022) Prognostic impact of surgical margins for hepatocellular carcinoma according to preoperative alpha-fetoprotein level. HPB (Oxford) 24:848–856CrossRefPubMed Marques F, Ghallab M, Vibert E et al (2022) Prognostic impact of surgical margins for hepatocellular carcinoma according to preoperative alpha-fetoprotein level. HPB (Oxford) 24:848–856CrossRefPubMed
15.
go back to reference Park JH, Kim DH, Kim SH et al (2018) The clinical implications of liver resection margin size in patients with hepatocellular carcinoma in terms of positron emission tomography positivity. World J Surg 42:1514–1522CrossRefPubMed Park JH, Kim DH, Kim SH et al (2018) The clinical implications of liver resection margin size in patients with hepatocellular carcinoma in terms of positron emission tomography positivity. World J Surg 42:1514–1522CrossRefPubMed
16.
go back to reference Zhou KQ, Sun YF, Cheng JW et al (2020) Effect of surgical margin on recurrence based on preoperative circulating tumor cell status in hepatocellular carcinoma. EBioMedicine 62:103107CrossRefPubMedPubMedCentral Zhou KQ, Sun YF, Cheng JW et al (2020) Effect of surgical margin on recurrence based on preoperative circulating tumor cell status in hepatocellular carcinoma. EBioMedicine 62:103107CrossRefPubMedPubMedCentral
17.
go back to reference Cha SW, Sohn JH, Kim SH et al (2020) Interaction between the tumor microenvironment and resection margin in different gross types of hepatocellular carcinoma. J Gastroenterol Hepatol 35:648–653CrossRefPubMed Cha SW, Sohn JH, Kim SH et al (2020) Interaction between the tumor microenvironment and resection margin in different gross types of hepatocellular carcinoma. J Gastroenterol Hepatol 35:648–653CrossRefPubMed
18.
go back to reference Ueno M, Hayami S, Shigekawa Y et al (2015) Prognostic impact of surgery and radiofrequency ablation on single nodular HCC ⩽ 5 cm: cohort study based on serum HCC markers. J Hepatol 63:1352–1359CrossRefPubMed Ueno M, Hayami S, Shigekawa Y et al (2015) Prognostic impact of surgery and radiofrequency ablation on single nodular HCC ⩽ 5 cm: cohort study based on serum HCC markers. J Hepatol 63:1352–1359CrossRefPubMed
19.
go back to reference Fan W, Zhu B, Yue S et al (2023) Identifying optimal candidates for post-TIPS patients with HCC undergoing TACE: a multicenter observational study. Eur Radiol 33:2809–2820CrossRefPubMed Fan W, Zhu B, Yue S et al (2023) Identifying optimal candidates for post-TIPS patients with HCC undergoing TACE: a multicenter observational study. Eur Radiol 33:2809–2820CrossRefPubMed
20.
go back to reference Lee S, Kang TW, Song KD et al (2021) Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg 273:564–571CrossRefPubMed Lee S, Kang TW, Song KD et al (2021) Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg 273:564–571CrossRefPubMed
21.
go back to reference Bossuyt PM, Reitsma JB, Bruns DE et al (2015) STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. Radiology 277:826–832CrossRefPubMed Bossuyt PM, Reitsma JB, Bruns DE et al (2015) STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. Radiology 277:826–832CrossRefPubMed
23.
go back to reference Jiang H, Yang C, Chen Y et al (2023) Development of a model including MRI features for predicting advanced-stage recurrence of hepatocellular carcinoma after liver resection. Radiology 309:e230527CrossRefPubMed Jiang H, Yang C, Chen Y et al (2023) Development of a model including MRI features for predicting advanced-stage recurrence of hepatocellular carcinoma after liver resection. Radiology 309:e230527CrossRefPubMed
24.
go back to reference Wei H, Yang T, Chen J et al (2022) Prognostic implications of CT/MRI LI-RADS in hepatocellular carcinoma: State of the art and future directions. Liver Int 42:2131–2144CrossRefPubMed Wei H, Yang T, Chen J et al (2022) Prognostic implications of CT/MRI LI-RADS in hepatocellular carcinoma: State of the art and future directions. Liver Int 42:2131–2144CrossRefPubMed
25.
go back to reference Ronot M, Chernyak V, Burgoyne A et al (2023) Imaging to predict prognosis in hepatocellular carcinoma: current and future perspectives. Radiology 307:e221429CrossRefPubMed Ronot M, Chernyak V, Burgoyne A et al (2023) Imaging to predict prognosis in hepatocellular carcinoma: current and future perspectives. Radiology 307:e221429CrossRefPubMed
26.
go back to reference Chan AWH, Zhong J, Berhane S et al (2018) Development of pre and post-operative models to predict early recurrence of hepatocellular carcinoma after surgical resection. J Hepatol 69:1284–1293CrossRefPubMed Chan AWH, Zhong J, Berhane S et al (2018) Development of pre and post-operative models to predict early recurrence of hepatocellular carcinoma after surgical resection. J Hepatol 69:1284–1293CrossRefPubMed
27.
go back to reference Moons KG, Altman DG, Reitsma JB et al (2015) Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med 162:W1–W73CrossRefPubMed Moons KG, Altman DG, Reitsma JB et al (2015) Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med 162:W1–W73CrossRefPubMed
28.
go back to reference Wang H, Yu H, Qian YW et al (2020) Impact of surgical margin on the prognosis of early hepatocellular carcinoma (≤ 5 cm): a propensity score matching analysis. Front Med 7:139 Wang H, Yu H, Qian YW et al (2020) Impact of surgical margin on the prognosis of early hepatocellular carcinoma (≤ 5 cm): a propensity score matching analysis. Front Med 7:139
29.
go back to reference Ding DY, Liu L, Lin KY et al (2023) Perioperative and long-term survival outcomes of laparoscopic versus open hepatectomy for BCLC stage A large hepatocellular carcinoma patients in difficult segments: a two-centre, propensity score matching analysis. Front Oncol 13:1095357CrossRefPubMedPubMedCentral Ding DY, Liu L, Lin KY et al (2023) Perioperative and long-term survival outcomes of laparoscopic versus open hepatectomy for BCLC stage A large hepatocellular carcinoma patients in difficult segments: a two-centre, propensity score matching analysis. Front Oncol 13:1095357CrossRefPubMedPubMedCentral
30.
go back to reference Hayward RA, Kent DM, Vijan S et al (2006) Multivariable risk prediction can greatly enhance the statistical power of clinical trial subgroup analysis. BMC Med Res Methodol 6:18CrossRefPubMedPubMedCentral Hayward RA, Kent DM, Vijan S et al (2006) Multivariable risk prediction can greatly enhance the statistical power of clinical trial subgroup analysis. BMC Med Res Methodol 6:18CrossRefPubMedPubMedCentral
31.
go back to reference Reig M, Forner A, Rimola J et al (2022) BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol 76:681–693CrossRefPubMed Reig M, Forner A, Rimola J et al (2022) BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol 76:681–693CrossRefPubMed
32.
go back to reference Rhee H, Chung T, Yoo JE et al (2020) Gross type of hepatocellular carcinoma reflects the tumor hypoxia, fibrosis, and stemness-related marker expression. Hepatol Int 14:239–248CrossRefPubMed Rhee H, Chung T, Yoo JE et al (2020) Gross type of hepatocellular carcinoma reflects the tumor hypoxia, fibrosis, and stemness-related marker expression. Hepatol Int 14:239–248CrossRefPubMed
33.
go back to reference Liu K, Zheng H, Sui X et al (2023) Microwave ablation versus surgical resection for subcapsular hepatocellular carcinoma: a propensity score-matched study of long-term therapeutic outcomes. Eur Radiol 33:1938–1948CrossRefPubMed Liu K, Zheng H, Sui X et al (2023) Microwave ablation versus surgical resection for subcapsular hepatocellular carcinoma: a propensity score-matched study of long-term therapeutic outcomes. Eur Radiol 33:1938–1948CrossRefPubMed
34.
go back to reference Lee IC, Huang JY, Chen TC et al (2021) Evolutionary learning-derived clinical-radiomic models for predicting early recurrence of hepatocellular carcinoma after resection. Liver Cancer 10:572–582CrossRefPubMedPubMedCentral Lee IC, Huang JY, Chen TC et al (2021) Evolutionary learning-derived clinical-radiomic models for predicting early recurrence of hepatocellular carcinoma after resection. Liver Cancer 10:572–582CrossRefPubMedPubMedCentral
35.
go back to reference Cao X, Yang H, Luo X et al (2023) A Cox nomogram for assessing recurrence free survival in hepatocellular carcinoma following surgical resection using dynamic contrast-enhanced MRI radiomics. J Magn Reson Imaging 58:1930–1941CrossRefPubMed Cao X, Yang H, Luo X et al (2023) A Cox nomogram for assessing recurrence free survival in hepatocellular carcinoma following surgical resection using dynamic contrast-enhanced MRI radiomics. J Magn Reson Imaging 58:1930–1941CrossRefPubMed
36.
go back to reference Galgano SJ, Smith EN (2023) LI-RADS version 2018 for MRI and CT: interreader agreement in real-world practice. Radiology 307:e231212CrossRefPubMed Galgano SJ, Smith EN (2023) LI-RADS version 2018 for MRI and CT: interreader agreement in real-world practice. Radiology 307:e231212CrossRefPubMed
37.
go back to reference Liu JW, Zhuang GK, Bai SL et al (2023) The comparison of surgical margins and type of hepatic resection for hepatocellular carcinoma with microvascular invasion. Oncologist 28:e1043–e1051CrossRefPubMedPubMedCentral Liu JW, Zhuang GK, Bai SL et al (2023) The comparison of surgical margins and type of hepatic resection for hepatocellular carcinoma with microvascular invasion. Oncologist 28:e1043–e1051CrossRefPubMedPubMedCentral
Metadata
Title
MRI-based prediction of the need for wide resection margins in patients with single hepatocellular carcinoma
Authors
Yanshu Wang
Yali Qu
Chongtu Yang
Yuanan Wu
Hong Wei
Yun Qin
Jie Yang
Tianying Zheng
Jie Chen
Roberto Cannella
Federica Vernuccio
Maxime Ronot
Weixia Chen
Bin Song
Hanyu Jiang
Publication date
05-09-2024
Publisher
Springer Berlin Heidelberg
Published in
European Radiology
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-024-11043-5