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Comparison of [68Ga]Ga-FAPI and [18F]FDG uptake in patients with gastric signet-ring-cell carcinoma: a multicenter retrospective study

  • Gastrointestinal
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Abstract

Objective

In this study, we investigated the role of [68Ga]Ga-FAPI PET imaging in the detection of primary and metastatic gastric signet-ring-cell carcinoma (GSRCC) and compared with [18F]FDG PET.

Methods

This retrospective multicenter analysis included 34 patients with histologically confirmed GSRCCs from four medical centers. The maximum standard uptake value (SUVmax), tumor-to-background ratio (TBR), and diagnostic accuracy were compared between the two modalities. [18F]FDG and [68Ga]Ga-FAPI uptakes were compared by using the Wilcoxon signed-rank test. McNemar’s test was used to compare the diagnostic accuracy between the two techniques.

Results

Data were analyzed from 27 paired PET/CT and 7 paired PET/MRI scans for 34 GSRCC patients (16 men and 18 women) who had a median age of 51 years (range: 25–85 years). [68Ga]Ga-FAPI PET showed higher SUVmax and TBR values than did [18F]FDG PET in the primary tumors (SUVmax: 5.2 vs. 2.2, p = 0.001; TBR: 7.6 vs. 1.3, p < 0.001), involved lymph nodes (SUVmax: 6.8 vs. 2.5, p < 0.001; TBR: 5.8 vs. 1.3, p < 0.001), and bone and visceral metastases (SUVmax: 6.5 vs. 2.4, p < 0.001; TBR: 6.3 vs. 1.3, p < 0.001). In diagnostic performance, [68Ga]Ga-FAPI PET exhibited higher sensitivity than [18F]FDG PET for detecting primary tumors (73% [16/22] vs. 18% [4/22], p < 0.001), local recurrences (100% [7/7] vs. 29% [2/7], p = 0.071), lymph node metastases (77% [59/77] vs. 23% [18/77], p < 0.001), and distant metastases (93% [207/222] vs. 39% [86/222], p < 0.001).

Conclusion

The results from this multicenter retrospective analysis justify the clinical use of [68Ga]Ga-FAPI tracers for GSRCC diagnosis and staging.

Key Points

[68Ga]Ga-FAPI PET/CT is a promising imaging modality for the detection of primary and metastatic disease and has implications for TNM staging in GSRCC.

In this multicenter study of 34 patients with GSRCC, [68Ga]Ga-FAPI PET exhibited greater radiotracer uptake, tumor-to-background ratios, and diagnostic accuracy than [18F]FDG PET for detecting primary/recurrent tumors and metastatic lesions.

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Abbreviations

AJCC:

American Joint Committee on Cancer

BM:

Bone metastases

FAPIs:

Fibroblast activation protein inhibitors

FDG:

Fluorodeoxy-D-glucose

GMP:

Good manufacturing practices

GSRCC:

Gastric signet-ring-cell carcinoma

IQR:

Interquartile range

LM:

Liver metastases

LNM:

Lymph node metastases

LNs:

Lymph nodes

LR:

Local recurrence

Mets:

Metastases

PC:

Peritoneal carcinomatosis

PD:

Progressive disease

PET:

Positron emission tomography

PT:

Primary tumor

SUVmax :

Maximum standardized uptake value

TBR:

Tumor-to-background ratio

TNM staging:

Tumor, node, and metastasis staging

UCM:

Uncommon metastases

References

  1. Pernot S, Voron T, Perkins G, Lagorce-Pages C, Berger A, Taieb J (2015) Signet-ring cell carcinoma of the stomach: impact on prognosis and specific therapeutic challenge. World J Gastroenterol 21:11428–11438

    Article  CAS  Google Scholar 

  2. Erickson LA (2017) Gastric signet ring cell carcinoma. Mayo Clin Proc 92:e95–e96

    Article  Google Scholar 

  3. Kao YC, Fang WL, Wang RF et al (2019) Clinicopathological differences in signet ring cell adenocarcinoma between early and advanced gastric cancer. Gastric Cancer 22:255–263

    Article  CAS  Google Scholar 

  4. Bosch KD, Chicklore S, Cook GJ et al (2020) Staging FDG PET-CT changes management in patients with gastric adenocarcinoma who are eligible for radical treatment. Eur J Nucl Med Mol Imaging 47:759–767

    Article  Google Scholar 

  5. Shimada H, Okazumi S, Koyama M, Murakami K (2011) Japanese Gastric Cancer Association Task Force for Research Promotion: clinical utility of (1)(8)F-fluoro-2-deoxyglucose positron emission tomography in gastric cancer. A systematic review of the literature. Gastric Cancer 14:13–21

    Article  Google Scholar 

  6. Herrmann K, Ott K, Buck AK et al (2007) Imaging gastric cancer with PET and the radiotracers 18F-FLT and 18F-FDG: a comparative analysis. J Nucl Med 48:1945–1950

    Article  CAS  Google Scholar 

  7. Garin-Chesa P, Old LJ, Rettig WJ (1990) Cell surface glycoprotein of reactive stromal fibroblasts as a potential antibody target in human epithelial cancers. Proc Natl Acad Sci U S A 87:7235–7239

    Article  CAS  Google Scholar 

  8. Lindner T, Loktev A, Altmann A et al (2018) Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J Nucl Med 59:1415–1422

    Article  CAS  Google Scholar 

  9. Giesel FL, Kratochwil C, Lindner T et al (2019) (68)Ga-FAPI PET/CT: biodistribution and preliminary dosimetry estimate of 2 DOTA-containing FAP-targeting agents in patients with various cancers. J Nucl Med 60:386–392

    Article  CAS  Google Scholar 

  10. Kratochwil C, Flechsig P, Lindner T et al (2019) (68)Ga-FAPI PET/CT: tracer uptake in 28 different kinds of cancer. J Nucl Med 60:801–805

    Article  CAS  Google Scholar 

  11. Chen H, Pang Y, Wu J et al (2020) Comparison of [(68)Ga]Ga-DOTA-FAPI-04 and [(18)F] FDG PET/CT for the diagnosis of primary and metastatic lesions in patients with various types of cancer. Eur J Nucl Med Mol Imaging 47:1820–1832

    Article  Google Scholar 

  12. Pang Y, Zhao L, Luo Z et al (2021) Comparison of (68)Ga-FAPI and (18)F-FDG uptake in gastric, duodenal, and colorectal cancers. Radiology 298:393–402

    Article  Google Scholar 

  13. Kuten J, Levine C, Shamni O et al (2022) Head-to-head comparison of [(68)Ga]Ga-FAPI-04 and [(18)F]-FDG PET/CT in evaluating the extent of disease in gastric adenocarcinoma. Eur J Nucl Med Mol Imaging 49:743–750

    Article  CAS  Google Scholar 

  14. Fu L, Huang S, Wu H et al (2022) Superiority of [(68)Ga]Ga-FAPI-04/[(18)F]FAPI-42 PET/CT to [(18)F]FDG PET/CT in delineating the primary tumor and peritoneal metastasis in initial gastric cancer. Eur Radiol. https://doi.org/10.1007/s00330-022-08743-1

  15. Qin C, Shao F, Gai Y et al (2022) (68)Ga-DOTA-FAPI-04 PET/MR in the evaluation of gastric carcinomas: comparison with (18)F-FDG PET/CT. J Nucl Med 63:81–88

    Article  CAS  Google Scholar 

  16. Pang Y, Huang H, Fu L, Zhao L, Chen H (2020) 68Ga-FAPI PET/CT detects gastric signet-ring cell carcinoma in a patient previously treated for prostate cancer. Clin Nucl Med 45:632–635

    Article  Google Scholar 

  17. Fan C, Guo W, Su G, Chen B, Chen H (2021) Widespread metastatic gastric signet-ring cell carcinoma shown by 68Ga-FAPI PET/CT. Clin Nucl Med 46:e78–e79

    Article  Google Scholar 

  18. Alan-Selcuk N, Ergen S, Demirci E, Ocak M, Kabasakal L (2021) ([68)Ga]DOTA-FAPI-04 PET/CT imaging in a case of a signet ring cell carcinoma of stomach. Eur J Nucl Med Mol Imaging 48:4523–4524

    Article  Google Scholar 

  19. Guo YH, Yang MF (2021) Comparison of 18F-AlF-NOTA-FAPI and 18F-FDG imaging in a patient with gastric signet-ring cell carcinoma. Clin Nucl Med 46:929–930

    Article  Google Scholar 

  20. Dondi F, Albano D, Giubbini R, Bertagna F (2021) 18F-FDG PET and PET/CT for the evaluation of gastric signet ring cell carcinoma: a systematic review. Nucl Med Commun 42:1293–1300

    Article  CAS  Google Scholar 

  21. Altini C, Niccoli Asabella A, Di Palo A et al (2015) 18F-FDG PET/CT role in staging of gastric carcinomas: comparison with conventional contrast enhancement computed tomography. Medicine (Baltimore) 94:e864

    Article  CAS  Google Scholar 

  22. Jiang D, Chen X, You Z et al (2022) Comparison of [(68) Ga]Ga-FAPI-04 and [(18)F]-FDG for the detection of primary and metastatic lesions in patients with gastric cancer: a bicentric retrospective study. Eur J Nucl Med Mol Imaging 49:732–742

    Article  CAS  Google Scholar 

  23. Roncati L, Manenti A, Barbolini G, Maiorana A (2018) Deep inside of gastric signet-ring cell carcinoma. Neoplasma 65:579–584

    Article  CAS  Google Scholar 

  24. Kwon KJ, Shim KN, Song EM et al (2014) Clinicopathological characteristics and prognosis of signet ring cell carcinoma of the stomach. Gastric Cancer 17:43–53

    Article  Google Scholar 

  25. Oh HH, Lee SE, Choi IS et al (2011) The peak-standardized uptake value (P-SUV) by preoperative positron emission tomography-computed tomography (PET-CT) is a useful indicator of lymph node metastasis in gastric cancer. J Surg Oncol 104:530–533

    Article  Google Scholar 

  26. Gundogan C, Komek H, Can C et al (2022) Comparison of 18F-FDG PET/CT and 68Ga-FAPI-04 PET/CT in the staging and restaging of gastric adenocarcinoma. Nucl Med Commun 43:64–72

    Article  Google Scholar 

  27. Shang Q, Zhao L, Pang Y, Meng T, Chen H (2022) Differentiation of reactive lymph nodes and tumor metastatic lymph nodes with 68Ga-FAPI PET/CT in a patient with squamous cell lung cancer. Clin Nucl Med 47:458–461

    Article  Google Scholar 

  28. Chen S, Chen Z, Zou G et al (2022) Accurate preoperative staging with [(68)Ga]Ga-FAPI PET/CT for patients with oral squamous cell carcinoma: a comparison to 2-[(18)F]FDG PET/CT. Eur Radiol. https://doi.org/10.1007/s00330-022-08686-7

  29. Shang Q, Zhao L, Pang Y, Yu Y, Chen H (2022) 68Ga-FAPI PET/CT distinguishes the reactive lymph nodes from tumor metastatic lymph nodes in a patient with nasopharyngeal carcinoma. Clin Nucl Med 47:367–368

    Article  Google Scholar 

  30. Kinoshita T, Kinoshita T, Saiura A, Esaki M, Sakamoto H, Yamanaka T (2015) Multicentre analysis of long-term outcome after surgical resection for gastric cancer liver metastases. Br J Surg 102:102–107

    Article  CAS  Google Scholar 

  31. Zhao L, Chen S, Chen S et al (2021) (68)Ga-fibroblast activation protein inhibitor PET/CT on gross tumour volume delineation for radiotherapy planning of oesophageal cancer. Radiother Oncol 158:55–61

    Article  CAS  Google Scholar 

  32. Syed M, Flechsig P, Liermann J et al (2020) Fibroblast activation protein inhibitor (FAPI) PET for diagnostics and advanced targeted radiotherapy in head and neck cancers. Eur J Nucl Med Mol Imaging 47:2836–2845

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank all the researchers and patients at the four different institutions for their great help in this investigation.

Funding

This study has received funding from the National Natural Science Foundation of China (grant #82071963) and the Key Medical and Health Projects in Xiamen (grant #3502Z20191104).

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Authors

Corresponding authors

Correspondence to Haojun Chen, Fang Xie, Jing Wang or Long Sun.

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This scientific guarantor of this publication is Haojun Chen, MD, PhD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

Authors Haojun Chen and Yizhen Pang kindly provided statistical advice for this manuscript.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• multicenter study

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Chen, H., Pang, Y., Li, J. et al. Comparison of [68Ga]Ga-FAPI and [18F]FDG uptake in patients with gastric signet-ring-cell carcinoma: a multicenter retrospective study. Eur Radiol 33, 1329–1341 (2023). https://doi.org/10.1007/s00330-022-09084-9

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