Imaging characteristics of gallium-68 labeled fibroblast activation protein inhibitor-positron emission tomography/magnetic resonance imaging in liver fibrosis and liver tumor_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

FENG Liwen ,  XIAO Guangqin

Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, P. R. China;

Corresponding author：

XIAO Guangqin, Email: xiaoguangqin1021@163.com

Keywords：

liver fibrosis; liver tumor; fibroblast activation protein inhibitor; positron emission tomography; magnetic resonance imaging

DOI：

10.7507/1007-9424.202110120

Video：

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Objective To investigate the imaging characteristics of gallium-68 labeled fibroblast activation protein inhibitor (⁶⁸Ga-FAPI)-positron emission tomography/magnetic resonance (PET/MR) imaging in patients with liver fibrosis or liver tumor. Methods Thirteen patients with suspected liver tumor who underwent ⁶⁸Ga-FAPI-PET/MR examination from May 2020 to April 2021 were retrospectively analyzed. Maximum standard uptake value (SUVmax) was investigated. All patients underwent liver surgery or biopsy. Scheuer scoring system was used to evaluate the liver fibrosis. The imaging characteristics of liver fibrosis or liver tumor were analyzed. Results The liver fibrosis was confirmed in 6 patients, including 1 case of S2, 2 cases of S3, and 3 cases of S4. Among them, 4 patients had increased uptake of ⁶⁸Ga-FAPI, with patchy or diffuse abnormal concentration of liver, and the SUVmax was 7.9±3.1. The liver imaging of the other 2 patients with liver fibrosis showed no obvious radioactive concentration. In addition, 2 patients were diagnosed with hepatocellular carcinoma, its SUVmax was 7.2 and 6.1; 1 patient was diagnosed with hepatobiliary duct carcinoma and its SUVmax was 13.8. Moreover, increased uptake of ⁶⁸Ga-FAPI was observed in 4 patients with metastatic liver cancer, with SUVmax of 6.7±2.7. Conclusion Both liver fibrosis and liver tumor are suitable for ⁶⁸Ga-FAPI-PET/MR examination, which have different imaging characteristics.

Citation： FENG Liwen, XIAO Guangqin. Imaging characteristics of gallium-68 labeled fibroblast activation protein inhibitor-positron emission tomography/magnetic resonance imaging in liver fibrosis and liver tumor. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(5): 607-612. doi: 10.7507/1007-9424.202110120 Copy

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2.	曾志萍, 郭津生. 肝纤维化发生机制及治疗研究进展. 世界华人消化杂志, 2017, 25(7): 569-575.
3.	Lin E, Zou B, Zeng G, et al. The impact of liver fibrosis on microvascular invasion and prognosis of hepatocellular carcinoma with a solitary nodule: a Surveillance, Epidemiology, and End Results (SEER) database analysis. Ann Transl Med, 2021, 9(16): 1310. doi: 10.21037/atm-21-3731.
4.	张原青, 郭津生. 乙型肝炎病毒促进肝细胞性肝癌发生的机制. 中华肝脏病杂志, 2016, 24(2): 152-156.
5.	马海芬, 肖维华, 虞继红, 等. FAP和MMP-9在人乙肝相关性肝纤维化分级及肝癌中的表达意义. 浙江临床医学, 2019, 21(12): 1695-1697.
6.	Siveke JT. Fibroblast-activating protein: targeting the roots of the tumor microenvironment. J Nucl Med, 2018, 59(9): 1412-1414.
7.	Baglieri J, Brenner DA, Kisseleva T. The role of fibrosis and liver-associated fibroblasts in the pathogenesis of hepatocellular carcinoma. Int J Mol Sci, 2019, 20(7): 1723. doi: 10.3390/ijms20071723.
8.	Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer, 2016, 16(9): 582-598.
9.	Zhou Y, Yang X, Liu H, et al. Value of [⁶⁸Ga]Ga-FAPI-04 imaging in the diagnosis of renal fibrosis. Eur J Nucl Med Mol Imaging, 2021, 48(11): 3493-3501.
10.	Schmidkonz C, Rauber S, Atzinger A, et al. Disentangling inflammatory from fibrotic disease activity by fibroblast activation protein imaging. Ann Rheum Dis, 2020, 79(11): 1485-1491.
11.	Zhao L, Gu J, Fu K, et al. ⁶⁸Ga-FAPI PET/CT in assessment of liver nodules in a cirrhotic patient. Clin Nucl Med, 2020, 45(10): e430-e432. doi: 10.1097/RLU.0000000000003015.
12.	Qin C, Shao F, Gai Y, et al. ⁶⁸Ga-DOTA-FAPI-04 PET/MR in the evaluation of gastric carcinomas: comparison with ¹⁸F-FDG PET/CT. J Nucl Med, 2022, 63(1): 81-88.
13.	Qin C, Liu F, Huang J, et al. A head-to-head comparison of ⁶⁸Ga-DOTA-FAPI-04 and ¹⁸F-FDG PET/MR in patients with nasopharyngeal carcinoma: a prospective study. Eur J Nucl Med Mol Imaging, 2021, 48(10): 3228-3237.
14.	Pang Y, Zhao L, Luo Z, et al. Comparison of ⁶⁸Ga-FAPI and ¹⁸F-FDG uptake in gastric, duodenal, and colorectal cancers. Radiology, 2021, 298(2): 393-402.
15.	Wang H, Zhu W, Ren S, et al. ⁶⁸Ga-FAPI-04 versus ¹⁸F-FDG PET/CT in the detection of hepatocellular carcinoma. Front Oncol, 2021, 11: 693640. doi: 10.3389/fonc.2021.693640.
16.	倪妙琪, 吴爽, 金晨, 等. ⁶⁸Ga-FAPI PET/CT在恶性肿瘤中的临床应用. 国际放射医学核医学杂志, 2021, 45(5): 307-312.
17.	Calais J, Mona CE. Will FAPI PET/CT replace FDG PET/CT in the next decade? Point—An important diagnostic, phenotypic, and biomarker role. AJR Am J Roentgenol, 2021, 216(2): 305-306.
18.	Shi X, Xing H, Yang X, et al. Comparison of PET imaging of activated fibroblasts and ¹⁸F-FDG for diagnosis of primary hepatic tumours: a prospective pilot study. Eur J Nucl Med Mol Imaging, 2021, 48(5): 1593-1603.
19.	邢海群, 朱文佳, 董诚岩, 等. 肝胆肿瘤患者⁶⁸Ga-FAPI-04 PET显像的内照射剂量及分布研究. 中华放射医学与防护杂志, 2021, 41(4): 293-298.
20.	Şahin E, Elboğa U, Çelen YZ, et al. Comparison of ⁶⁸Ga-DOTA-FAPI and ¹⁸FDG PET/CT imaging modalities in the detection of liver metastases in patients with gastrointestinal system cancer. Eur J Radiol, 2021, 142: 109867. doi: 10.1016/j.ejrad.2021.109867.
21.	Desmet VJ, Gerber M, Hoofnagle JH, et al. Classification of chronic hepatitis: diagnosis, grading and staging. Hepatology, 1994, 19(6): 1513-1520.
22.	Qin C, Song Y, Liu X, et al. Increased uptake of ⁶⁸Ga-DOTA-FAPI-04 in bones and joints: metastases and beyond. Eur J Nucl Med Mol Imaging, 2022, 49(2): 709-720.
23.	Zhang X, Song W, Qin C, et al. Non-malignant findings of focal ⁶⁸Ga-FAPI-04 uptake in pancreas. Eur J Nucl Med Mol Imaging, 2021, 48(8): 2635-2641.
24.	Gao H, Zhu F, Wang M, et al. Preoperatively staging liver fibrosis using noninvasive method in hepatitis B virus-infected hepatocellular carcinoma patients. Oncotarget, 2017, 8(3): 4289-4300.
25.	Xiao G, Zhu S, Xiao X, et al. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology, 2017, 66(5): 1486-1501.
26.	俞晓春, 胡旭姣, 章家青, 等. HA、Ⅳ-C、APRI及Fib-4对乙型肝炎后肝纤维化的诊断效果. 检验医学, 2019, 34(6): 539-542.

1. Beschin A, De Baetselier P, Van Ginderachter JA. Contribution of myeloid cell subsets to liver fibrosis in parasite infection. J Pathol, 2013, 229(2): 186-197.
2. 曾志萍, 郭津生. 肝纤维化发生机制及治疗研究进展. 世界华人消化杂志, 2017, 25(7): 569-575.
3. Lin E, Zou B, Zeng G, et al. The impact of liver fibrosis on microvascular invasion and prognosis of hepatocellular carcinoma with a solitary nodule: a Surveillance, Epidemiology, and End Results (SEER) database analysis. Ann Transl Med, 2021, 9(16): 1310. doi: 10.21037/atm-21-3731.
4. 张原青, 郭津生. 乙型肝炎病毒促进肝细胞性肝癌发生的机制. 中华肝脏病杂志, 2016, 24(2): 152-156.
5. 马海芬, 肖维华, 虞继红, 等. FAP和MMP-9在人乙肝相关性肝纤维化分级及肝癌中的表达意义. 浙江临床医学, 2019, 21(12): 1695-1697.
6. Siveke JT. Fibroblast-activating protein: targeting the roots of the tumor microenvironment. J Nucl Med, 2018, 59(9): 1412-1414.
7. Baglieri J, Brenner DA, Kisseleva T. The role of fibrosis and liver-associated fibroblasts in the pathogenesis of hepatocellular carcinoma. Int J Mol Sci, 2019, 20(7): 1723. doi: 10.3390/ijms20071723.
8. Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer, 2016, 16(9): 582-598.
9. Zhou Y, Yang X, Liu H, et al. Value of [⁶⁸Ga]Ga-FAPI-04 imaging in the diagnosis of renal fibrosis. Eur J Nucl Med Mol Imaging, 2021, 48(11): 3493-3501.
10. Schmidkonz C, Rauber S, Atzinger A, et al. Disentangling inflammatory from fibrotic disease activity by fibroblast activation protein imaging. Ann Rheum Dis, 2020, 79(11): 1485-1491.
11. Zhao L, Gu J, Fu K, et al. ⁶⁸Ga-FAPI PET/CT in assessment of liver nodules in a cirrhotic patient. Clin Nucl Med, 2020, 45(10): e430-e432. doi: 10.1097/RLU.0000000000003015.
12. Qin C, Shao F, Gai Y, et al. ⁶⁸Ga-DOTA-FAPI-04 PET/MR in the evaluation of gastric carcinomas: comparison with ¹⁸F-FDG PET/CT. J Nucl Med, 2022, 63(1): 81-88.
13. Qin C, Liu F, Huang J, et al. A head-to-head comparison of ⁶⁸Ga-DOTA-FAPI-04 and ¹⁸F-FDG PET/MR in patients with nasopharyngeal carcinoma: a prospective study. Eur J Nucl Med Mol Imaging, 2021, 48(10): 3228-3237.
14. Pang Y, Zhao L, Luo Z, et al. Comparison of ⁶⁸Ga-FAPI and ¹⁸F-FDG uptake in gastric, duodenal, and colorectal cancers. Radiology, 2021, 298(2): 393-402.
15. Wang H, Zhu W, Ren S, et al. ⁶⁸Ga-FAPI-04 versus ¹⁸F-FDG PET/CT in the detection of hepatocellular carcinoma. Front Oncol, 2021, 11: 693640. doi: 10.3389/fonc.2021.693640.
16. 倪妙琪, 吴爽, 金晨, 等. ⁶⁸Ga-FAPI PET/CT在恶性肿瘤中的临床应用. 国际放射医学核医学杂志, 2021, 45(5): 307-312.
17. Calais J, Mona CE. Will FAPI PET/CT replace FDG PET/CT in the next decade? Point—An important diagnostic, phenotypic, and biomarker role. AJR Am J Roentgenol, 2021, 216(2): 305-306.
18. Shi X, Xing H, Yang X, et al. Comparison of PET imaging of activated fibroblasts and ¹⁸F-FDG for diagnosis of primary hepatic tumours: a prospective pilot study. Eur J Nucl Med Mol Imaging, 2021, 48(5): 1593-1603.
19. 邢海群, 朱文佳, 董诚岩, 等. 肝胆肿瘤患者⁶⁸Ga-FAPI-04 PET显像的内照射剂量及分布研究. 中华放射医学与防护杂志, 2021, 41(4): 293-298.
20. Şahin E, Elboğa U, Çelen YZ, et al. Comparison of ⁶⁸Ga-DOTA-FAPI and ¹⁸FDG PET/CT imaging modalities in the detection of liver metastases in patients with gastrointestinal system cancer. Eur J Radiol, 2021, 142: 109867. doi: 10.1016/j.ejrad.2021.109867.
21. Desmet VJ, Gerber M, Hoofnagle JH, et al. Classification of chronic hepatitis: diagnosis, grading and staging. Hepatology, 1994, 19(6): 1513-1520.
22. Qin C, Song Y, Liu X, et al. Increased uptake of ⁶⁸Ga-DOTA-FAPI-04 in bones and joints: metastases and beyond. Eur J Nucl Med Mol Imaging, 2022, 49(2): 709-720.
23. Zhang X, Song W, Qin C, et al. Non-malignant findings of focal ⁶⁸Ga-FAPI-04 uptake in pancreas. Eur J Nucl Med Mol Imaging, 2021, 48(8): 2635-2641.
24. Gao H, Zhu F, Wang M, et al. Preoperatively staging liver fibrosis using noninvasive method in hepatitis B virus-infected hepatocellular carcinoma patients. Oncotarget, 2017, 8(3): 4289-4300.
25. Xiao G, Zhu S, Xiao X, et al. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology, 2017, 66(5): 1486-1501.
26. 俞晓春, 胡旭姣, 章家青, 等. HA、Ⅳ-C、APRI及Fib-4对乙型肝炎后肝纤维化的诊断效果. 检验医学, 2019, 34(6): 539-542.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Imaging characteristics of gallium-68 labeled fibroblast activation protein inhibitor-positron emission tomography/magnetic resonance imaging in liver fibrosis and liver tumor

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