Korean Journal of Radiology

  • 제24권3호
  • /
  • Pages.190-203
  • /
  • 2023
  • /
  • 1229-6929(pISSN)
  • /
  • 2005-8330(eISSN)
대한영상의학회 (The Korean Society of Radiology)
권호 표지
DOI QR코드

DOI QR Code

Targetoid Primary Liver Malignancy in Chronic Liver Disease: Prediction of Postoperative Survival Using Preoperative MRI Findings and Clinical Factors

  • So Hyun Park (Department of Radiology, Gil Medical Center, Gachon University College of Medicine) ;
  • Subin Heo (Department of Radiology, Ajou University Hospital) ;
  • Bohyun Kim (Department of Radiology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Jungbok Lee (Department of Clinical Epidemiology and Biostatistics, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Ho Joong Choi (Department of Surgery, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Pil Soo Sung (Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Joon-Il Choi (Department of Radiology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea)
  • 투고 : 2022.02.24
  • 심사 : 2022.11.23
  • 발행 : 2023.03.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective: We aimed to assess and validate the radiologic and clinical factors that were associated with recurrence and survival after curative surgery for heterogeneous targetoid primary liver malignancies in patients with chronic liver disease and to develop scoring systems for risk stratification. Materials and Methods: This multicenter retrospective study included 197 consecutive patients with chronic liver disease who had a single targetoid primary liver malignancy (142 hepatocellular carcinomas, 37 cholangiocarcinomas, 17 combined hepatocellular carcinoma-cholangiocarcinomas, and one neuroendocrine carcinoma) identified on preoperative gadoxetic acid-enhanced MRI and subsequently surgically removed between 2010 and 2017. Of these, 120 patients constituted the development cohort, and 77 patients from separate institution served as an external validation cohort. Factors associated with recurrence-free survival (RFS) and overall survival (OS) were identified using a Cox proportional hazards analysis, and risk scores were developed. The discriminatory power of the risk scores in the external validation cohort was evaluated using the Harrell C-index. The Kaplan-Meier curves were used to estimate RFS and OS for the different risk-score groups. Results: In RFS model 1, which eliminated features exclusively accessible on the hepatobiliary phase (HBP), tumor size of 2-5 cm or > 5 cm, and thin-rim arterial phase hyperenhancement (APHE) were included. In RFS model 2, tumors with a size of > 5 cm, tumor in vein (TIV), and HBP hypointense nodules without APHE were included. The OS model included a tumor size of > 5 cm, thin-rim APHE, TIV, and tumor vascular involvement other than TIV. The risk scores of the models showed good discriminatory performance in the external validation set (C-index, 0.62-0.76). The scoring system categorized the patients into three risk groups: favorable, intermediate, and poor, each with a distinct survival outcome (all log-rank p < 0.05). Conclusion: Risk scores based on rim arterial enhancement pattern, tumor size, HBP findings, and radiologic vascular invasion status may help predict postoperative RFS and OS in patients with targetoid primary liver malignancies.

키워드

과제정보

This study was supported by the National Research Foundation of Korea (NRF) grant funded by the Ministry of Science and ICT, Korea (NRF-2022R1F1A1071409).

참고문헌

  1. Llovet JM, Kelley RK, Villanueva A, Singal AG, Pikarsky E, Roayaie S, et al. Hepatocellular carcinoma. Nat Rev Dis Primers 2021;7:6 
  2. American College of Radiology. LI-RADS® CT/MRI. acr.org Web site. https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/LI-RADS-CT-MRI-v2018. Accessed February 27, 2021 
  3. Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the study of liver diseases. Hepatology 2018;68:723-750  https://doi.org/10.1002/hep.29913
  4. European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182-236  https://doi.org/10.1016/j.jhep.2018.03.019
  5. Kim DH, Choi SH, Park SH, Kim KW, Byun JH, Kim SY, et al. Liver imaging reporting and data system category M: a systematic review and meta-analysis. Liver Int 2020;40:1477-1487  https://doi.org/10.1111/liv.14420
  6. Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 2018;67:358-380  https://doi.org/10.1002/hep.29086
  7. Kim SS, Lee S, Choi JY, Lim JS, Park MS, Kim MJ. Diagnostic performance of the LR-M criteria and spectrum of LI-RADS imaging features among primary hepatic carcinomas. Abdom Radiol (NY) 2020;45:3743-3754  https://doi.org/10.1007/s00261-020-02562-y
  8. Sammon J, Fischer S, Menezes R, Hosseini-Nik H, Lewis S, Taouli B, et al. MRI features of combined hepatocellular-cholangiocarcinoma versus mass forming intrahepatic cholangiocarcinoma. Cancer Imaging 2018;18:8 
  9. Park HJ, Kim YK, Cha DI, Ko SE, Kim S, Lee ES, et al. Targetoid hepatic observations on gadoxetic acid-enhanced MRI using LI-RADS version 2018: emphasis on hepatocellular carcinomas assigned to the LR-M category. Clin Radiol 2020;75:478.e13-478.e23  https://doi.org/10.1016/j.crad.2020.01.002
  10. Choi SH, Lee SS, Park SH, Kim KM, Yu E, Park Y, et al. LI-RADS classification and prognosis of primary liver cancers at gadoxetic acid-enhanced MRI. Radiology 2019;290:388-397  https://doi.org/10.1148/radiol.2018181290
  11. An C, Kim DW, Park YN, Chung YE, Rhee H, Kim MJ. Single hepatocellular carcinoma: preoperative MR imaging to predict early recurrence after curative resection. Radiology 2015;276:433-443  https://doi.org/10.1148/radiol.15142394
  12. An C, Park S, Chung YE, Kim DY, Kim SS, Kim MJ, et al. Curative resection of single primary hepatic malignancy: liver imaging reporting and data system category LR-M portends a worse prognosis. AJR Am J Roentgenol 2017;209:576-583  https://doi.org/10.2214/AJR.16.17478
  13. Jeon SK, Joo I, Lee DH, Lee SM, Kang HJ, Lee KB, et al. Combined hepatocellular cholangiocarcinoma: LI-RADS v2017 categorisation for differential diagnosis and prognostication on gadoxetic acid-enhanced MR imaging. Eur Radiol 2019;29:373-382  https://doi.org/10.1007/s00330-018-5605-x
  14. Shin J, Lee S, Kim SS, Chung YE, Choi JY, Park MS, et al. Characteristics and early recurrence of hepatocellular carcinomas categorized as LR-M: comparison with those categorized as LR-4 or 5. J Magn Reson Imaging 2021;54:1446-1454  https://doi.org/10.1002/jmri.27650
  15. Ariizumi S, Kitagawa K, Kotera Y, Takahashi Y, Katagiri S, Kuwatsuru R, et al. A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci 2011;18:575-585  https://doi.org/10.1007/s00534-010-0369-y
  16. Cho ES, Choi JY. MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol 2015;16:449-464  https://doi.org/10.3348/kjr.2015.16.3.449
  17. Sakon M, Nagano H, Nakamori S, Dono K, Umeshita K, Murakami T, et al. Intrahepatic recurrences of hepatocellular carcinoma after hepatectomy: analysis based on tumor hemodynamics. Arch Surg 2002;137:94-99  https://doi.org/10.1001/archsurg.137.1.94
  18. Kim KA, Kim MJ, Jeon HM, Kim KS, Choi JS, Ahn SH, et al. Prediction of microvascular invasion of hepatocellular carcinoma: usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. J Magn Reson Imaging 2012;35:629-634  https://doi.org/10.1002/jmri.22876
  19. Toyoda H, Kumada T, Tada T, Niinomi T, Ito T, Sone Y, et al. Non-hypervascular hypointense nodules detected by Gd-EOB-DTPA-enhanced MRI are a risk factor for recurrence of HCC after hepatectomy. J Hepatol 2013;58:1174-1180  https://doi.org/10.1016/j.jhep.2013.01.030
  20. Kim DK, An C, Chung YE, Choi JY, Lim JS, Park MS, et al. Hepatobiliary versus extracellular MRI contrast agents in hepatocellular carcinoma detection: hepatobiliary phase features in relation to disease-free survival. Radiology 2019;293:594-604  https://doi.org/10.1148/radiol.2019190414
  21. Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO classification of tumours of the digestive system. Geneva: World Health Organization, 2010 
  22. Fowler KJ, Potretzke TA, Hope TA, Costa EA, Wilson SR. LI-RADS M (LR-M): definite or probable malignancy, not specific for hepatocellular carcinoma. Abdom Radiol (NY) 2018;43:149-157  https://doi.org/10.1007/s00261-017-1196-2
  23. Min JH, Kim JM, Kim YK, Kim H, Choi GS, Kang TW, et al. A modified LI-RADS: targetoid tumors with enhancing capsule can be diagnosed as HCC instead of LR-M lesions. Eur Radiol 2022;32:912-922  https://doi.org/10.1007/s00330-021-08124-0
  24. Cannella R, Fraum TJ, Ludwig DR, Borhani AA, Tsung A, Furlan A, et al. Targetoid appearance on T2-weighted imaging and signs of tumor vascular involvement: diagnostic value for differentiating HCC from other primary liver carcinomas. Eur Radiol 2021;31:6868-6878  https://doi.org/10.1007/s00330-021-07743-x
  25. Motosugi U, Murakami T, Lee JM, Fowler KJ, Heiken JP, Sirlin CB; LI-RADS HBA Working Group. Recommendation for terminology: nodules without arterial phase hyperenhancement and with hepatobiliary phase hypointensity in chronic liver disease. J Magn Reson Imaging 2018;48:1169-1171  https://doi.org/10.1002/jmri.26515
  26. Bae JS, Lee JM, Yoon JH, Jang S, Chung JW, Lee KB, et al. How to best detect portal vein tumor thrombosis in patients with hepatocellular carcinoma meeting the Milan criteria: gadoxetic acid-enhanced MRI versus contrast-enhanced CT. Liver Cancer 2020;9:293-307  https://doi.org/10.1159/000505191
  27. Punt CJ, Buyse M, Kohne CH, Hohenberger P, Labianca R, Schmoll HJ, et al. Endpoints in adjuvant treatment trials: a systematic review of the literature in colon cancer and proposed definitions for future trials. J Natl Cancer Inst 2007;99:998-1003  https://doi.org/10.1093/jnci/djm024
  28. Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AX, et al. Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 2008;100:698-711  https://doi.org/10.1093/jnci/djn134
  29. Liu Y, Yang T, Wei YW. What is the difference between overall survival, recurrence-free survival and time-to-recurrence? Br J Surg 2020;107:e634 
  30. Yang H, Bae SH, Nam H, Lee HL, Lee SW, Yoo SH, et al. A risk prediction model for hepatocellular carcinoma after hepatitis B surface antigen seroclearance. J Hepatol 2022;77:632-641  https://doi.org/10.1016/j.jhep.2022.03.032
  31. Park SY, Park JE, Kim H, Park SH. Review of statistical methods for evaluating the performance of survival or other time-to-event prediction models (from conventional to deep learning approaches). Korean J Radiol 2021;22:1697-1707  https://doi.org/10.3348/kjr.2021.0223
  32. Rhee H, An C, Kim HY, Yoo JE, Park YN, Kim MJ. Hepatocellular carcinoma with irregular rim-like arterial phase hyperenhancement: more aggressive pathologic features. Liver Cancer 2019;8:24-40  https://doi.org/10.1159/000488540
  33. Park SH, Lee SS, Yu E, Kang HJ, Park Y, Kim SY, et al. Combined hepatocellular-cholangiocarcinoma: gadoxetic acid-enhanced MRI findings correlated with pathologic features and prognosis. J Magn Reson Imaging 2017;46:267-280  https://doi.org/10.1002/jmri.25568
  34. Rhee H, Cho ES, Nahm JH, Jang M, Chung YE, Baek SE, et al. Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol 2021;74:109-121  https://doi.org/10.1016/j.jhep.2020.08.013
  35. Kim B, Won JH, Kim J, Kwon Y, Cho HJ, Huh J, et al. Hepatic arterial infusion chemotherapy for advanced hepatocellular carcinoma: radiologic and clinical factors predictive of survival. AJR Am J Roentgenol 2021;216:1566-1573  https://doi.org/10.2214/AJR.20.23213
  36. Min JH, Kim YK, Choi SY, Kang TW, Lee SJ, Kim JM, et al. Intrahepatic mass-forming cholangiocarcinoma: arterial enhancement patterns at MRI and prognosis. Radiology 2019;290:691-699  https://doi.org/10.1148/radiol.2018181485
  37. Joo I, Kim SY, Kang TW, Kim YK, Park BJ, Lee YJ, et al. Radiologic-pathologic correlation of hepatobiliary phase hypointense nodules without arterial phase hyperenhancement at gadoxetic acid-enhanced MRI: a multicenter study. Radiology 2020;296:335-345  https://doi.org/10.1148/radiol.2020192275
  38. Hyodo T, Murakami T, Imai Y, Okada M, Hori M, Kagawa Y, et al. Hypovascular nodules in patients with chronic liver disease: risk factors for development of hypervascular hepatocellular carcinoma. Radiology 2013;266:480-490  https://doi.org/10.1148/radiol.12112677
  39. Kang Y, Lee JM, Kim SH, Han JK, Choi BI. Intrahepatic mass-forming cholangiocarcinoma: enhancement patterns on gadoxetic acid-enhanced MR images. Radiology 2012;264:751-760  https://doi.org/10.1148/radiol.12112308
  40. Rodriguez-Peralvarez M, Luong TV, Andreana L, Meyer T, Dhillon AP, Burroughs AK. A systematic review of microvascular invasion in hepatocellular carcinoma: diagnostic and prognostic variability. Ann Surg Oncol 2013;20:325-339  https://doi.org/10.1245/s10434-012-2513-1
  41. Bai DS, Zhang C, Chen P, Jin SJ, Jiang GQ. The prognostic correlation of AFP level at diagnosis with pathological grade, progression, and survival of patients with hepatocellular carcinoma. Sci Rep 2017;7:12870