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CC BY-NC-ND 4.0 · Journal of Clinical Interventional Radiology ISVIR 2020; 4(02): 088-097
DOI: 10.1055/s-0040-1708579
Review Article

Response Assessment Following Image-Guided Therapy of Hepatocellular Carcinoma

Pankaj Gupta
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Naveen Kalra
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Ajay Gulati
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Vishnu Dev
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Ujjwal Gorsi
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Sreedhara B. Cheluvashetty
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Praveen Kumar-M
2   Department of Pharmacology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Ajay Duseja
3   Department of Hepatology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Virendra Singh
3   Department of Hepatology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Radha K. Dhiman
3   Department of Hepatology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
,
Manavjit Singh Sandhu
1   Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
› Author Affiliations Financial Disclosure None.
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Abstract

Image-guided locoregional therapies have an important role in the management of patients with hepatocellular carcinoma (HCC). Recent advances in the ablative as well as endovascular therapies have expanded the role of interventional radiologists in the treatment of HCC. Following image-guided therapy, an accurate response assessment is vital. Knowledge regarding normal postprocedure changes and subtle signs of residual or recurrent disease is important. In this review, we discuss various response evaluation criteria currently employed for HCC. We also discuss the postprocedure imaging features suggestive of residual disease or recurrence and imaging biomarkers for response assessment.

Keywords

ablative therapies - hepatocellular carcinoma - response


Publication History

Article published online:
01 July 2020

© .

Thieme Medical and Scientific Publishers Private Ltd.
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  • References

  • 1 GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016; 388 (10053) 1459-1544
    CrossrefPubMedGoogle Scholar
  • 2 European Association for the Study of the Liver. Electronic address easloffice@easloffice.eu, European Association for the Study of the Liver. Management of hepatocellular carcinoma. J Hepatol 2018; 69 (01) 182-236
    CrossrefPubMedGoogle Scholar
  • 3 Kielar A, Fowler KJ, Lewis S. et al. Locoregional therapies for hepatocellular carcinoma and the new LI-RADS treatment response algorithm. Abdom Radiol (NY) 2018; 43 (01) 218-230
    CrossrefPubMedGoogle Scholar
  • 4 Kalra N, Gupta P, Chawla Y, Khandelwal N. Locoregional treatment for hepatocellular carcinoma: the best is yet to come. World J Radiol 2015; 7 (10) 306-318
    CrossrefPubMedGoogle Scholar
  • 5 Gupta P, Kalra N, Shyamkumar NK, et al. Indian Society of Vascular and Interventional Radiology Expert Consensus Statements for Ablation in Hepatocellular Carcinoma: Part I. J Clin Interv Radiol ISVIR 2020. [in press]
    PubMed
  • 6 Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 2010; 30 (01) 52-60
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Yaghmai V, Besa C, Kim E, Gatlin JL, Siddiqui NA, Taouli B. Imaging assessment of hepatocellular carcinoma response to locoregional and systemic therapy. AJR Am J Roentgenol 2013; 201 (01) 80-96
    CrossrefPubMedGoogle Scholar
  • 8 European Association For The Study Of The Liver , European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012; 56 (04) 908-943
    CrossrefPubMedGoogle Scholar
  • 9 Keppke AL, Salem R, Reddy D. et al. Imaging of hepatocellular carcinoma after treatment with yttrium-90 microspheres. AJR Am J Roentgenol 2007; 188 (03) 768-775
    CrossrefPubMedGoogle Scholar
  • 10 Kubota K, Hisa N, Nishikawa T. et al. Evaluation of hepatocellular carcinoma after treatment with transcatheter arterial chemoembolization: comparison of Lipiodol-CT, power Doppler sonography, and dynamic MRI. Abdom Imaging 2001; 26 (02) 184-190
    CrossrefPubMedGoogle Scholar
  • 11 Lim HS, Jeong YY, Kang HK, Kim JK, Park JG. Imaging features of hepatocellular carcinoma after transcatheter arterial chemoembolization and radiofrequency ablation. AJR Am J Roentgenol 2006; 187 (04) W341-9
    CrossrefPubMedGoogle Scholar
  • 12 Takayasu K, Arii S, Matsuo N. et al. Comparison of CT findings with resected specimens after chemoembolization with iodized oil for hepatocellular carcinoma. AJR Am J Roentgenol 2000; 175 (03) 699-704
    CrossrefPubMedGoogle Scholar
  • 13 Kim HC, Chung JW, Lee W, Jae HJ, Park JH. Recognizing extrahepatic collateral vessels that supply hepatocellular carcinoma to avoid complications of transcatheter arterial chemoembolization. Radiographics 2005; 25 (Suppl. 01) S25-S39
    CrossrefPubMedGoogle Scholar
  • 14 Young S, Taylor AJ, Sanghvi T. Post locoregional therapy treatment imaging in hepatocellular carcinoma patients: a literature-based review. J Clin Transl Hepatol 2018; 6 (02) 189-197
    CrossrefPubMedGoogle Scholar
  • 15 Kloeckner R, Otto G, Biesterfeld S, Oberholzer K, Dueber C, Pitton MB. MDCT versus MRI assessment of tumor response after transarterial chemoembolization for the treatment of hepatocellular carcinoma. Cardiovasc Intervent Radiol 2010; 33 (03) 532-540
    CrossrefPubMedGoogle Scholar
  • 16 Bisseret D, Ronot M, Abdel-Rehim M. et al. Intratumoral gas in hepatocellular carcinoma following transarterial chemoembolization: associated factors and clinical impact. J Vasc Interv Radiol 2013; 24 (11) 1623-1631
    CrossrefPubMedGoogle Scholar
  • 17 Sieghart W, Hucke F, Pinter M. et al. The ART of decision making: retreatment with transarterial chemoembolization in patients with hepatocellular carcinoma. Hepatology 2013; 57 (06) 2261-2273
    CrossrefPubMedGoogle Scholar
  • 18 Semaan S, Makkar J, Lewis S, Chatterji M, Kim E, Taouli B. Imaging of hepatocellular carcinoma response after 90Y radioembolization. AJR Am J Roentgenol 2017; 209 (05) W263-W276
    CrossrefPubMedGoogle Scholar
  • 19 Dromain C, de Baere T, Elias D. et al. Hepatic tumors treated with percutaneous radio-frequency ablation: CT and MR imaging follow-up. Radiology 2002; 223 (01) 255-262
    CrossrefPubMedGoogle Scholar
  • 20 Sironi S, Livraghi T, Meloni F. De Cobelli F, Ferrero C, Del Maschio A. Small hepatocellular carcinoma treated with percutaneous RF ablation: MR imaging follow-up. AJR Am J Roentgenol 1999; 173 (05) 1225-1229
    CrossrefPubMedGoogle Scholar
  • 21 Kim YS, Rhim H, Lim HK. Imaging after radiofrequency ablation of hepatic tumors. Semin Ultrasound CT MR 2009; 30 (02) 49-66
    CrossrefPubMedGoogle Scholar
  • 22 Park MH, Rhim H, Kim YS, Choi D, Lim HK, Lee WJ. Spectrum of CT findings after radiofrequency ablation of hepatic tumors. Radiographics 2008; 28 (02) 379-390, discussion 390–392
    CrossrefPubMedGoogle Scholar
  • 23 Nakazawa T, Kokubu S, Shibuya A. et al. Radiofrequency ablation of hepatocellular carcinoma: correlation between local tumor progression after ablation and ablative margin. AJR Am J Roentgenol 2007; 188 (02) 480-488
    CrossrefPubMedGoogle Scholar
  • 24 Chiang J, Cristescu M, Lee MH. et al. Effects of microwave ablation on arterial and venous vasculature after treatment of hepatocellular carcinoma. Radiology 2016; 281 (02) 617-624
    CrossrefPubMedGoogle Scholar
  • 25 Shyn PB, Mauri G, Alencar RO. et al. Percutaneous imaging-guided cryoablation of liver tumors: predicting local progression on 24-hour MRI. AJR Am J Roentgenol 2014; 203 (02) W181-91
    CrossrefPubMedGoogle Scholar
  • 26 Kalra N, Gupta P, Gorsi U. et al. Irreversible electroporation for unresectable hepatocellular carcinoma: initial experience. Cardiovasc Intervent Radiol 2019; 42 (04) 584-590
    CrossrefPubMedGoogle Scholar
  • 27 Padia SA, Johnson GE, Yeung RS, Park JO, Hippe DS, Kogut MJ. Irreversible electroporation in patients with hepatocellular carcinoma: immediate versus delayed findings at MR imaging. Radiology 2016; 278 (01) 285-294
    CrossrefPubMedGoogle Scholar
  • 28 Zhang LJ, Peng J, Wu SY. et al. Liver virtual non-enhanced CT with dual-source, dual-energy CT: a preliminary study. Eur Radiol 2010; 20 (09) 2257-2264
    CrossrefPubMedGoogle Scholar
  • 29 Altenbernd J, Heusner TA, Ringelstein A, Ladd SC, Forsting M, Antoch G. Dual-energy-CT of hypervascular liver lesions in patients with HCC: investigation of image quality and sensitivity. Eur Radiol 2011; 21 (04) 738-743
    CrossrefPubMedGoogle Scholar
  • 30 Lee SH, Lee JM, Kim KW. et al. Dual-energy computed tomography to assess tumor response to hepatic radiofrequency ablation: potential diagnostic value of virtual noncontrast images and iodine maps. Invest Radiol 2011; 46 (02) 77-84
    CrossrefPubMedGoogle Scholar
  • 31 Zhang L, Wang N, Mao J. et al. Dual-energy CT-derived volumetric iodine concentration for the assessment of therapeutic response after microwave ablation in a rabbit model with intrahepatic VX2 tumor. J Vasc Interv Radiol 2018; 29 (10) 1455-1461
    CrossrefPubMedGoogle Scholar
  • 32 Mohamed AM, Louka AL, Ghazee AF. The role of diffusion weighted MR imaging in assessment of hepatocellular carcinoma after radiofrequency ablation. The Egyptian Journal of Hospital Medicine 2017; 68: 1339-1341
    CrossrefPubMedGoogle Scholar
  • 33 Mannelli L, Kim S, Hajdu CH, Babb JS, Clark TW, Taouli B. Assessment of tumor necrosis of hepatocellular carcinoma after chemoembolization: diffusion-weighted and contrast-enhanced MRI with histopathologic correlation of the explanted liver. AJR Am J Roentgenol 2009; 193 (04) 1044-1052
    CrossrefPubMedGoogle Scholar
  • 34 Kamel IR, Liapi E, Reyes DK, Zahurak M, Bluemke DA, Geschwind JF. Unresectable hepatocellular carcinoma: serial early vascular and cellular changes after transarterial chemoembolization as detected with MR imaging. Radiology 2009; 250 (02) 466-473
    CrossrefPubMedGoogle Scholar
  • 35 Deng J, Miller FH, Rhee TK. et al. Diffusion-weighted MR imaging for determination of hepatocellular carcinoma response to yttrium-90 radioembolization. J Vasc Interv Radiol 2006; 17 (07) 1195-1200
    CrossrefPubMedGoogle Scholar
  • 36 Kamel IR, Reyes DK, Liapi E, Bluemke DA, Geschwind JF. Functional MR imaging assessment of tumor response after 90Y microsphere treatment in patients with unresectable hepatocellular carcinoma. J Vasc Interv Radiol 2007; 18 (1 Pt 1) 49-56
    CrossrefPubMedGoogle Scholar
  • 37 Goshima S, Kanematsu M, Kondo H. et al. Evaluating local hepatocellular carcinoma recurrence post-transcatheter arterial chemoembolization: is diffusion-weighted MRI reliable as an indicator?. J Magn Reson Imaging 2008; 27 (04) 834-839
    CrossrefPubMedGoogle Scholar
  • 38 Yuan Z, Ye XD, Dong S. et al. Role of magnetic resonance diffusion-weighted imaging in evaluating response after chemoembolization of hepatocellular carcinoma. Eur J Radiol 2010; 75 (01) e9-e14
    CrossrefPubMedGoogle Scholar
  • 39 Mannelli L, Kim S, Hajdu CH, Babb JS, Taouli B. Serial diffusion-weighted MRI in patients with hepatocellular carcinoma: prediction and assessment of response to transarterial chemoembolization. Preliminary experience. Eur J Radiol 2013; 82 (04) 577-582
    CrossrefPubMedGoogle Scholar
  • 40 Lu TL, Becce F, Bize P, Denys A, Meuli R, Schmidt S. Assessment of liver tumor response by high-field (3 T) MRI after radiofrequency ablation: short- and mid-term evolution of diffusion parameters within the ablation zone. Eur J Radiol 2012; 81 (09) e944-e950
    CrossrefPubMedGoogle Scholar
  • 41 Bonekamp S, Jolepalem P, Lazo M, Gulsun MA, Kiraly AP, Kamel IR. Hepatocellular carcinoma: response to TACE assessed with semiautomated volumetric and functional analysis of diffusion-weighted and contrast-enhanced MR imaging data. Radiology 2011; 260 (03) 752-761
    CrossrefPubMedGoogle Scholar
  • 42 Ye XD, Yuan Z, Zhang J, Yuan Z. Radiological biomarkers for assessing response to locoregional therapies in hepatocellular carcinoma: From morphological to functional imaging (Review). (Review). Oncol Rep 2017; 37 (03) 1337-1346
    CrossrefPubMedGoogle Scholar
  • 43 Tamandl D, Waneck F, Sieghart W. et al. Early response evaluation using CT-perfusion one day after transarterial chemoembolization for HCC predicts treatment response and long-term disease control. Eur J Radiol 2017; 90: 73-80
    CrossrefPubMedGoogle Scholar
  • 44 Chen G, Ma DQ, He W, Zhang BF, Zhao LQ. Computed tomography perfusion in evaluating the therapeutic effect of transarterial chemoembolization for hepatocellular carcinoma. World J Gastroenterol 2008; 14 (37) 5738-5743
    CrossrefPubMedGoogle Scholar
  • 45 Rathmann N, Kara K, Budjan J. et al. Parenchymal liver blood volume and dynamic volume perfusion CT measurements of hepatocellular carcinoma in patients undergoing transarterial chemoembolization. Anticancer Res 2017; 37 (10) 5681-5685
    PubMedGoogle Scholar
  • 46 Zhu AX, Holalkere NS, Muzikansky A, Horgan K, Sahani DV. Early antiangiogenic activity of bevacizumab evaluated by computed tomography perfusion scan in patients with advanced hepatocellular carcinoma. Oncologist 2008; 13 (02) 120-125
    CrossrefPubMedGoogle Scholar
  • 47 Ippolito D, Bonaffini PA, Ratti L. et al. Hepatocellular carcinoma treated with transarterial chemoembolization: dynamic perfusion-CT in the assessment of residual tumor. World J Gastroenterol 2010; 16 (47) 5993-6000
    PubMedGoogle Scholar
  • 48 Marquez HP, Puippe G, Mathew RP, Alkadhi H, Pfammatter T, Fischer MA. CT perfusion for early response evaluation of radiofrequency ablation of focal liver lesions: first experience. Cardiovasc Intervent Radiol 2017; 40 (01) 90-98
    CrossrefPubMedGoogle Scholar
  • 49 Claudon M, Dietrich CF, Choi BI. et al. World Federation for Ultrasound in Medicine; European Federation of Societies for Ultrasound. Guidelines and good clinical practice recommendations for Contrast Enhanced Ultrasound (CEUS) in the liver - update 2012: A WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultrasound Med Biol 2013; 39 (02) 187-210
    CrossrefPubMedGoogle Scholar
  • 50 Liu M, Lin MX, Lu MD. et al. Comparison of contrast-enhanced ultrasound and contrast-enhanced computed tomography in evaluating the treatment response to transcatheter arterial chemoembolization of hepatocellular carcinoma using modified RECIST. Eur Radiol 2015; 25 (08) 2502-2511
    CrossrefPubMedGoogle Scholar
  • 51 Zhong J, Su Z, Zhang Y. et al. Contrast-enhanced ultrasonography versus contrast-enhanced computed tomography for assessment of residual tumor from hepatocellular carcinoma treated with transarterial chemoembolization: a meta-analysis. J Ultrasound Med 2018; 37 (08) 1881-1890
    CrossrefPubMedGoogle Scholar
  • 52 Zheng SG, Xu HX, Lu MD. et al. Role of contrast-enhanced ultrasound in follow-up assessment after ablation for hepatocellular carcinoma. World J Gastroenterol 2013; 19 (06) 855-865
    CrossrefPubMedGoogle Scholar
  • 53 Catalano O, Izzo F, Vallone P. et al. Integrating contrast-enhanced sonography in the follow-up algorithm of hepatocellular carcinoma treated with radiofrequency ablation: single cancer center experience. Acta Radiol 2015; 56 (02) 133-142
    CrossrefPubMedGoogle Scholar
  • 54 Kaufmann S, Schulze M, Spira D, Horger M. Comparison of volume perfusion computed tomography and contrast-enhanced ultrasound for assessment of therapeutic effect of transarterial chemoembolization in patients with hepatocellular carcinoma: a preliminary report. Acta Radiol 2016; 57 (01) 8-12
    CrossrefPubMedGoogle Scholar
  • 55 Zhan Y, Zhou F, Yu X. et al. Quantitative dynamic contrast-enhanced ultrasound may help predict the outcome of hepatocellular carcinoma after microwave ablation. Int J Hyperthermia 2019; 35 (01) 105-111
    CrossrefPubMedGoogle Scholar
  • 56 Young H, Baum R, Cremerius U, Herholz K, Hoekstra O, Lammertsma AA, Pruim J, Price P. European Organization for Research and Treatment of Cancer (EORTC) PET Study Group. Measurement of clinical and subclinical tumour response using [18F]-fluorodeoxyglucose and positron emission tomography: Review and 1999 EORTC recommendations. Eur J Cancer 1999; 35: 1773-1782
    CrossrefPubMedGoogle Scholar
  • 57 Kim SH, Won KS, Choi BW. et al. Usefulness of F-18 FDG PET/CT in the evaluation of early treatment response after interventional therapy for hepatocellular carcinoma. Nucl Med Mol Imaging 2012; 46 (02) 102-110
    CrossrefPubMedGoogle Scholar
  • 58 Jreige M, Mitsakis P, Van Der Gucht A. et al. 18F-FDG PET/CT predicts survival after90Y transarterial radioembolization in unresectable hepatocellular carcinoma. Eur J Nucl Med Mol Imaging 2017; 44 (07) 1215-1222
    CrossrefPubMedGoogle Scholar
  • 59 Yuan Z, Li WT, Ye XD, Zhu HY, Peng WJ. Novel functional magnetic resonance imaging biomarkers for assessing response to therapy in hepatocellular carcinoma. Clin Transl Oncol 2014; 16 (07) 599-605
    CrossrefPubMedGoogle Scholar
  • 60 Kwee SA, Sato MM, Kuang Y. et al. [18F]Fluorocholine PET/CT imaging of liver cancer: radiopathologic correlation with tissue phospholipid profiling. Mol Imaging Biol 2017; 19 (03) 446-455
    CrossrefPubMedGoogle Scholar
  • 61 Yuan Z, Ye XD, Dong S, Xu LC, Xiao XS. Evaluation of early imaging response after chemoembolization of hepatocellular carcinoma by phosphorus-31 magnetic resonance spectroscopy-initial experience. J Vasc Interv Radiol 2011; 22 (08) 1166-1173
    CrossrefPubMedGoogle Scholar
  • 62 Lee JE, Jang JY, Jeong SW. et al. Diagnostic value for extrahepatic metastases of hepatocellular carcinoma in positron emission tomography/computed tomography scan. World J Gastroenterol 2012; 18 (23) 2979-2987
    CrossrefPubMedGoogle Scholar
  • 63 Kloth C, Thaiss WM, Kärgel R. et al. Evaluation of texture analysis parameter for response prediction in patients with hepatocellular carcinoma undergoing drug-eluting bead transarterial chemoembolization (DEB-TACE) using biphasic contrast-enhanced CT image data: correlation with liver perfusion CT. Acad Radiol 2017; 24 (11) 1352-1363
    CrossrefPubMedGoogle Scholar
  • 64 Kim J, Choi SJ, Lee SH, Lee HY, Park H. Predicting survival using pretreatment CT for patients with hepatocellular carcinoma treated with transarterial chemoembolization: comparison of models using radiomics. AJR Am J Roentgenol 2018; 211 (05) 1026-1034
    CrossrefPubMedGoogle Scholar
  • 65 Shan QY, Hu HT, Feng ST. et al. CT-based peritumoral radiomics signatures to predict early recurrence in hepatocellular carcinoma after curative tumor resection or ablation. Cancer Imaging 2019; 19 (01) 11
    CrossrefPubMedGoogle Scholar
  • 66 Donati OF, Hany TF, Reiner CS. et al. Value of retrospective fusion of PET and MR images in detection of hepatic metastases: comparison with 18F-FDG PET/CT and Gd-EOB-DTPA-enhanced MRI. J Nucl Med 2010; 51 (05) 692-699
    CrossrefPubMedGoogle Scholar