Imaging evaluation of immunotherapy for hepatocellular carcinoma_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Yun , HUANG Zixing ,  SONG Bin

Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

SONG Bin, Email: cjr.songbin@vip.163.com

Keywords：

hepatocellular carcinoma; immunotherapy; computed tomography; magnetic resonance imaging; ultrasound; positron emission computed tomography-computed tomography

DOI：

10.7507/1007-9424.201806043

Video：

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Objective To analyze and summarize advantages, disadvantages, and limitations of present imaging techniques in assessing efficacy of immunotherapy for patient with hepatocellular carcinoma in order to provide strong evidence for drug therapy evaluation and clinical decision-making for it. Method The relevant literatures about imaging evaluation of immunotherapy for hepatocellular carcinoma were collected to make a review, then analyze and summarize the value of different imaging techniques. Results The immunotherapy, characterized by the noninvasive, high specificity and good curative effect, had been playing an important role in the treatment of hepatocellular carcinoma in recent years. The imaging techniques currently used to assess the immunotherapy results of hepatocellular carinoma mainly included the CT, MRI, ultrasound, and nuclear medicine, which could be used to better evaluate the effectiveness of immunotherapy. It was very important for screening of the patients’ treatment options and judging of the survival and prognosis. The most of the evaluation indicators were based on the anatomic evaluation criteria and it had some certain limitations in evaluating the immunotherapy efficacy of patient with hepatocellular carcinoma. Conclusions As an emerging biological therapy, immunotherapy has gradually become a hotspot in diagnosis and treatment of hepatocellular carcinoma in future. Present imaging techniques and evaluation criteria have certain limitations. More multifunctional imaging indicators need to be improved and developed so as to provide strong evidence for drug therapy evaluation and clinical decision of patient with hepatocellular carcinoma.

Citation： ZHANG Yun, HUANG Zixing, SONG Bin. Imaging evaluation of immunotherapy for hepatocellular carcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2018, 25(7): 867-872. doi: 10.7507/1007-9424.201806043 Copy

1.	World Health Organization. Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/pages/online.aspx [Accessed on 31 August, 2014].
2.	Zheng ZX, Zheng RS, Zhang SW, et al. Colorectal cancer incidence and mortality in China, 2010. Asian Pac J Cancer Prev, 2014, 15(19): 8455-8460.
3.	Shields A, Reddy KR. Hepatocellular carcinoma: current treatment strategies. Curr Treat Options Gastroenterol, 2005, 8(6): 457-466.
4.	叶胜龙. 肝癌的非手术治疗. 中华肝脏病杂志, 2006, 14(7): 558-560.
5.	Chiriva-Internati M, Grizzi F, Wachtel MS, et al. Biological treatment for liver tumor and new potential biomarkers. Dig Dis Sci, 2008, 53(3): 836-843.
6.	Kelly PN. The cancer immunotherapy revolution. Science, 2018, 359(6382): 1344-1345.
7.	Kudo M. Immuno-oncology in hepatocellular carcinoma: 2017 update. Oncology, 2017, 93 Suppl 1: 147-159.
8.	Yaghmai V, Besa C, Kim E, et al. Imaging assessment of hepatocellular carcinoma response to locoregional and systemic therapy. AJR Am J Roentgenol, 2013, 201(1): 80-96.
9.	Solinas C, Porcu M, Hlavata Z, et al. Critical features and challenges associated with imaging in patients undergoing cancer immunotherapy. Crit Rev Oncol Hematol, 2017, 120: 13-21.
10.	Chen J, Ji T, Zhao J, et al. Sorafenib-resistant hepatocellular carcinoma stratified by phosphorylated ERK activates PD-1 immune checkpoint. Oncotarget, 2016, 7(27): 41274-41284.
11.	Sawada Y, Yoshikawa T, Fujii S, et al. Remarkable tumor lysis in a hepatocellular carcinoma patient immediately following glypican-3-derived peptide vaccination: an autopsy case. Hum Vaccin Immunother, 2013, 9(6): 1228-1233.
12.	Cui J, Wang N, Zhao H, et al. Combination of radiofrequency ablation and sequential cellular immunotherapy improves progression-free survival for patients with hepatocellular carcinoma. Int J Cancer, 2014, 134(2): 342-351.
13.	彭诗云. 肝癌靶向治疗的功能影像学评价现状. 中国医学影像学杂志, 2017, 25(2): 151-154.
14.	Pitton MB, Kloeckner R, Herber S, et al. MRI versus 64-row MDCT for diagnosis of hepatocellular carcinoma. World J Gastroenterol, 2009, 15(48): 6044-6051.
15.	Purysko AS, Remer EM, Coppa CP, et al. LI-RADS: A case-based review of the new categorization of liver findings in patients with end-stage liver disease. Radiographics, 2012, 32(7): 1995-1998.
16.	Burrel M, Llovet JM, Ayuso C, et al. MRI angiography is superior to helical CT for detection of HCC prior to liver transplantation: an explant correlation. Hepatology, 2003, 38(4): 1034-1042.
17.	Khalili K, Kim TK, Jang HJ, et al. Optimization of imaging diagnosis of 1—2 cm hepatocellular carcinoma: an analysis of diagnostic performance and resource utilization. J Hepatol, 2011, 54(4): 723-728.
18.	Ayuso C, Rimola J, García-Criado A. Imaging of HCC. Abdom Imaging, 2012, 37(2): 215-230.
19.	Maataoui A, Qian J, Vossoughi D, et al. Transarterial chemoembolization alone and in combination with other therapies: a comparative study in an animal HCC model. Eur Radiol, 2005, 15(1): 127-133.
20.	El Ansary M, Mogawer S, Elhamid SA, et al. Immunotherapy by autologous dendritic cell vaccine in patients with advanced HCC. J Cancer Res Clin Oncol, 2013, 139(1): 39-48.
21.	Marinelli S, Salvatore V, Baron Toaldo M, et al. Evaluation of the impact of transient interruption of antiangiogenic treatment using ultrasound-based techniques in a murine model of hepatocellular carcinoma. BMC Cancer, 2014, 14: 403.
22.	Wahl RL, Jacene H, Kasamon Y, et al. From RECIST to PERCIST: Evolving considerations for PET response criteria in solid tumors. J Nucl Med, 2009, 50 Suppl 1: 122S-150S.
23.	Perng P, Marcus C, Subramaniam RM. ¹⁸F-FDG PET/CT and melanoma: staging, immune modulation and mutation-targeted therapy assessment, and prognosis. AJR Am J Roentgenol, 2015, 205(2): 259-270.
24.	Higuchi M, Owada Y, Inoue T, et al. FDG-PET in the evaluation of response to nivolumab in recurrent non-small-cell lung cancer. World J Surg Oncol, 2016, 14(1): 238.
25.	Song MJ, Bae SH, Yoo IeR, et al. Predictive value of ¹⁸F-fluorodeoxyglucose PET/CT for transarterial chemolipiodolization of hepatocellular carcinoma. World J Gastroenterol, 2012, 18(25): 3215-3222.
26.	Torizuka T, Tamaki N, Inokuma T, et al. Value of fluorine-18-FDG-PET to monitor hepatocellular carcinoma after interventional therapy. J Nucl Med, 1994, 35(12): 1965-1969.
27.	Delbeke D, Martin WH, Sandler MP, et al. Evaluation of benign vs malignant hepatic lesions with positron emission tomography. Arch Surg, 1998, 133(5): 510-515.
28.	Trojan J, Schroeder O, Raedle J, et al. Fluorine-18 FDG positron emission tomography for imaging of hepatocellular carcinoma. Am J Gastroenterol, 1999, 94(11): 3314-3319.
29.	Gilles R, de Geus-Oei LF, Mulders PF, et al. Immunotherapy response evaluation with ¹⁸F-FDG-PET in patients with advanced stage renal cell carcinoma. World J Urol, 2013, 31(4): 841-846.
30.	World Health Organization. WHO handbook for reporting results of cancer treatment. Geneva: World Health Organization, 1979.
31.	Duffaud F, Therasse P. New guidelines to evaluate the response to treatment in solid tumors. Bull Cancer, 2000, 87(12): 881-886.
32.	Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer, 2009, 45(2): 228-247.
33.	Bruix J, Sherman M, Llovet JM, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol, 2001, 35(3): 421-430.
34.	Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis, 2010, 30(1): 52-60.
35.	Choi H, Charnsangavej C, de Castro Faria S, et al. CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings. AJR Am J Roentgenol, 2004, 183(6): 1619-1628.
36.	Wolchok JD, Hoos A, O’Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res, 2009, 15(23): 7412-7420.
37.	Nishino M, Guo M, Jackman DM, et al. CT tumor volume measurement in advanced non-small-cell lung cancer: Performance characteristics of an emerging clinical tool. Acad Radiol, 2011, 18(1): 54-62.
38.	Seymour L, Bogaerts J, Perrone A, et al. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol, 2017, 18(3): e143-e152.
39.	Eleneen Y, Colen RR. Cancer imaging in immunotherapy. Adv Exp Med Biol, 2017, 995: 141-153.
40.	Tazdait M, Mezquita L, Lahmar J, et al. Patterns of responses in metastatic NSCLC during PD-1 or PDL-1 inhibitor therapy: Comparison of RECIST 1.1, irRECIST and iRECIST criteria. Eur J Cancer, 2018, 88: 38-47.
41.	Kiryu S, Akai H, Nojima M, et al. Impact of hepatocellular carcinoma heterogeneity on computed tomography as a prognostic indicator. Sci Rep, 2017, 7(1): 12689.
42.	Zhou W, Zhang L, Wang K, et al. Malignancy characterization of hepatocellular carcinomas based on texture analysis of contrast-enhanced MR images. J Magn Reson Imaging, 2017, 45(5): 1476-1484.
43.	Bakr S, Echegaray S, Shah R, et al. Noninvasive radiomics signature based on quantitative analysis of computed tomography images as a surrogate for microvascular invasion in hepatocellular carcinoma: a pilot study. J Med Imaging (Bellingham), 2017, 4(4): 041303.
44.	Fu S, Chen S, Liang C, et al. Texture analysis of intermediate-advanced hepatocellular carcinoma: prognosis and patients’ selection of transcatheter arterial chemoembolization and sorafenib. Oncotarget, 2017, 8(23): 37855-37865.
45.	王茹, 杨晓莹, 王克英, 等. 纹理分析对经动脉化学栓塞治疗术后肝癌复发的评价. 中华肝脏病杂志, 2017, 25(3): 200-204.
46.	Imai Y, Katayama K, Hori M, et al. Prospective comparison of Gd-EOB-DTPA-Enhanced MRI with dynamic CT for detecting recurrence of HCC after radiofrequency ablation. Liver Cancer, 2017, 6(4): 349-359.
47.	Yang SH, Lin J, Lu F, et al. Evaluation of antiangiogenic and antiproliferative effects of sorafenib by sequential histology and intravoxel incoherent motion diffusion-weighted imaging in an orthotopic hepatocellular carcinoma xenograft model. J Magn Reson Imaging, 2017, 45(1): 270-280.

1. World Health Organization. Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/pages/online.aspx [Accessed on 31 August, 2014].
2. Zheng ZX, Zheng RS, Zhang SW, et al. Colorectal cancer incidence and mortality in China, 2010. Asian Pac J Cancer Prev, 2014, 15(19): 8455-8460.
3. Shields A, Reddy KR. Hepatocellular carcinoma: current treatment strategies. Curr Treat Options Gastroenterol, 2005, 8(6): 457-466.
4. 叶胜龙. 肝癌的非手术治疗. 中华肝脏病杂志, 2006, 14(7): 558-560.
5. Chiriva-Internati M, Grizzi F, Wachtel MS, et al. Biological treatment for liver tumor and new potential biomarkers. Dig Dis Sci, 2008, 53(3): 836-843.
6. Kelly PN. The cancer immunotherapy revolution. Science, 2018, 359(6382): 1344-1345.
7. Kudo M. Immuno-oncology in hepatocellular carcinoma: 2017 update. Oncology, 2017, 93 Suppl 1: 147-159.
8. Yaghmai V, Besa C, Kim E, et al. Imaging assessment of hepatocellular carcinoma response to locoregional and systemic therapy. AJR Am J Roentgenol, 2013, 201(1): 80-96.
9. Solinas C, Porcu M, Hlavata Z, et al. Critical features and challenges associated with imaging in patients undergoing cancer immunotherapy. Crit Rev Oncol Hematol, 2017, 120: 13-21.
10. Chen J, Ji T, Zhao J, et al. Sorafenib-resistant hepatocellular carcinoma stratified by phosphorylated ERK activates PD-1 immune checkpoint. Oncotarget, 2016, 7(27): 41274-41284.
11. Sawada Y, Yoshikawa T, Fujii S, et al. Remarkable tumor lysis in a hepatocellular carcinoma patient immediately following glypican-3-derived peptide vaccination: an autopsy case. Hum Vaccin Immunother, 2013, 9(6): 1228-1233.
12. Cui J, Wang N, Zhao H, et al. Combination of radiofrequency ablation and sequential cellular immunotherapy improves progression-free survival for patients with hepatocellular carcinoma. Int J Cancer, 2014, 134(2): 342-351.
13. 彭诗云. 肝癌靶向治疗的功能影像学评价现状. 中国医学影像学杂志, 2017, 25(2): 151-154.
14. Pitton MB, Kloeckner R, Herber S, et al. MRI versus 64-row MDCT for diagnosis of hepatocellular carcinoma. World J Gastroenterol, 2009, 15(48): 6044-6051.
15. Purysko AS, Remer EM, Coppa CP, et al. LI-RADS: A case-based review of the new categorization of liver findings in patients with end-stage liver disease. Radiographics, 2012, 32(7): 1995-1998.
16. Burrel M, Llovet JM, Ayuso C, et al. MRI angiography is superior to helical CT for detection of HCC prior to liver transplantation: an explant correlation. Hepatology, 2003, 38(4): 1034-1042.
17. Khalili K, Kim TK, Jang HJ, et al. Optimization of imaging diagnosis of 1—2 cm hepatocellular carcinoma: an analysis of diagnostic performance and resource utilization. J Hepatol, 2011, 54(4): 723-728.
18. Ayuso C, Rimola J, García-Criado A. Imaging of HCC. Abdom Imaging, 2012, 37(2): 215-230.
19. Maataoui A, Qian J, Vossoughi D, et al. Transarterial chemoembolization alone and in combination with other therapies: a comparative study in an animal HCC model. Eur Radiol, 2005, 15(1): 127-133.
20. El Ansary M, Mogawer S, Elhamid SA, et al. Immunotherapy by autologous dendritic cell vaccine in patients with advanced HCC. J Cancer Res Clin Oncol, 2013, 139(1): 39-48.
21. Marinelli S, Salvatore V, Baron Toaldo M, et al. Evaluation of the impact of transient interruption of antiangiogenic treatment using ultrasound-based techniques in a murine model of hepatocellular carcinoma. BMC Cancer, 2014, 14: 403.
22. Wahl RL, Jacene H, Kasamon Y, et al. From RECIST to PERCIST: Evolving considerations for PET response criteria in solid tumors. J Nucl Med, 2009, 50 Suppl 1: 122S-150S.
23. Perng P, Marcus C, Subramaniam RM. ¹⁸F-FDG PET/CT and melanoma: staging, immune modulation and mutation-targeted therapy assessment, and prognosis. AJR Am J Roentgenol, 2015, 205(2): 259-270.
24. Higuchi M, Owada Y, Inoue T, et al. FDG-PET in the evaluation of response to nivolumab in recurrent non-small-cell lung cancer. World J Surg Oncol, 2016, 14(1): 238.
25. Song MJ, Bae SH, Yoo IeR, et al. Predictive value of ¹⁸F-fluorodeoxyglucose PET/CT for transarterial chemolipiodolization of hepatocellular carcinoma. World J Gastroenterol, 2012, 18(25): 3215-3222.
26. Torizuka T, Tamaki N, Inokuma T, et al. Value of fluorine-18-FDG-PET to monitor hepatocellular carcinoma after interventional therapy. J Nucl Med, 1994, 35(12): 1965-1969.
27. Delbeke D, Martin WH, Sandler MP, et al. Evaluation of benign vs malignant hepatic lesions with positron emission tomography. Arch Surg, 1998, 133(5): 510-515.
28. Trojan J, Schroeder O, Raedle J, et al. Fluorine-18 FDG positron emission tomography for imaging of hepatocellular carcinoma. Am J Gastroenterol, 1999, 94(11): 3314-3319.
29. Gilles R, de Geus-Oei LF, Mulders PF, et al. Immunotherapy response evaluation with ¹⁸F-FDG-PET in patients with advanced stage renal cell carcinoma. World J Urol, 2013, 31(4): 841-846.
30. World Health Organization. WHO handbook for reporting results of cancer treatment. Geneva: World Health Organization, 1979.
31. Duffaud F, Therasse P. New guidelines to evaluate the response to treatment in solid tumors. Bull Cancer, 2000, 87(12): 881-886.
32. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer, 2009, 45(2): 228-247.
33. Bruix J, Sherman M, Llovet JM, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol, 2001, 35(3): 421-430.
34. Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis, 2010, 30(1): 52-60.
35. Choi H, Charnsangavej C, de Castro Faria S, et al. CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings. AJR Am J Roentgenol, 2004, 183(6): 1619-1628.
36. Wolchok JD, Hoos A, O’Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res, 2009, 15(23): 7412-7420.
37. Nishino M, Guo M, Jackman DM, et al. CT tumor volume measurement in advanced non-small-cell lung cancer: Performance characteristics of an emerging clinical tool. Acad Radiol, 2011, 18(1): 54-62.
38. Seymour L, Bogaerts J, Perrone A, et al. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol, 2017, 18(3): e143-e152.
39. Eleneen Y, Colen RR. Cancer imaging in immunotherapy. Adv Exp Med Biol, 2017, 995: 141-153.
40. Tazdait M, Mezquita L, Lahmar J, et al. Patterns of responses in metastatic NSCLC during PD-1 or PDL-1 inhibitor therapy: Comparison of RECIST 1.1, irRECIST and iRECIST criteria. Eur J Cancer, 2018, 88: 38-47.
41. Kiryu S, Akai H, Nojima M, et al. Impact of hepatocellular carcinoma heterogeneity on computed tomography as a prognostic indicator. Sci Rep, 2017, 7(1): 12689.
42. Zhou W, Zhang L, Wang K, et al. Malignancy characterization of hepatocellular carcinomas based on texture analysis of contrast-enhanced MR images. J Magn Reson Imaging, 2017, 45(5): 1476-1484.
43. Bakr S, Echegaray S, Shah R, et al. Noninvasive radiomics signature based on quantitative analysis of computed tomography images as a surrogate for microvascular invasion in hepatocellular carcinoma: a pilot study. J Med Imaging (Bellingham), 2017, 4(4): 041303.
44. Fu S, Chen S, Liang C, et al. Texture analysis of intermediate-advanced hepatocellular carcinoma: prognosis and patients’ selection of transcatheter arterial chemoembolization and sorafenib. Oncotarget, 2017, 8(23): 37855-37865.
45. 王茹, 杨晓莹, 王克英, 等. 纹理分析对经动脉化学栓塞治疗术后肝癌复发的评价. 中华肝脏病杂志, 2017, 25(3): 200-204.
46. Imai Y, Katayama K, Hori M, et al. Prospective comparison of Gd-EOB-DTPA-Enhanced MRI with dynamic CT for detecting recurrence of HCC after radiofrequency ablation. Liver Cancer, 2017, 6(4): 349-359.
47. Yang SH, Lin J, Lu F, et al. Evaluation of antiangiogenic and antiproliferative effects of sorafenib by sequential histology and intravoxel incoherent motion diffusion-weighted imaging in an orthotopic hepatocellular carcinoma xenograft model. J Magn Reson Imaging, 2017, 45(1): 270-280.

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