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Recent Patents on Anti-Cancer Drug Discovery

Editor-in-Chief

ISSN (Print): 1574-8928
ISSN (Online): 2212-3970

Research Article

PSMA PET/MR is a New Imaging Option for Identifying Glioma Recurrence and Predicting Prognosis

Author(s): Min Xiong, Zhenghe Chen, Chao Zhou, Xiaochun Yang, Wanming Hu, Yongluo Jiang, Rongliang Zheng, Wei Fan*, Yonggao Mou* and Xiaoping Lin*

Volume 19, Issue 3, 2024

Published on: 19 June, 2023

Page: [383 - 395] Pages: 13

DOI: 10.2174/1574892818666230519150401

Price: $65

Abstract

Background: Glioma is characterized by a high recurrence rate, while the results of the traditional imaging methods (including magnetic resonance imaging, MRI) to distinguish recurrence from treatment-related changes (TRCs) are poor. Prostate-specific membrane antigen (PSMA) (US10815200B2, Deutsches Krebsforschungszentrum, German Cancer Research Center) is a type II transmembrane glycoprotein overexpressed in glioma vascular endothelium, and it is a promising target for imaging and therapy.

Objective: The study aimed to assess the performance of PSMA positron emission tomography/ magnetic resonance (PET/MR) for diagnosing recurrence and predicting prognosis in glioma patients.

Materials and Methods: Patients suspected of glioma recurrence who underwent 18F-PSMA-1007 PET/MR were prospectively enrolled. Eight metabolic parameters and fifteen texture features of the lesion were extracted from PSMA PET/MR. The ability of PSMA PET/MR to diagnose glioma recurrence was investigated and compared with conventional MRI. The diagnostic agreement was assessed using Cohen κ scores and the predictive parameters of PSMA PET/MR were obtained. Kaplan-Meier method and Cox proportional hazard model were used to analyze recurrence- free survival (RFS) and overall survival (OS). Finally, the expression of PSMA was analyzed by immunohistochemistry (IHC).

Results: Nineteen patients with a mean age of 48.11±15.72 were assessed. The maximum tumorto- parotid ratio (TPRmax) and texture features extracted from PET and T1-weighted contrast enhancement (T1-CE) MR showed differences between recurrence and TRCs (all p <0.05). PSMA PET/MR and conventional MRI exhibited comparable power in diagnosing recurrence with specificity and PPV of 100%. The interobserver concordance was fair between the two modalities (κ = 0.542, p = 0.072). The optimal cutoffs of metabolic parameters, including standardized uptake value (SUV, SUVmax, SUVmean, and SUVpeak) and TPRmax for predicting recurrence were 3.35, 1.73, 1.99, and 0.17 respectively, with the area under the curve (AUC) ranging from 0.767 to 0.817 (all p <0.05). In grade 4 glioblastoma (GBM) patients, SUVmax, SUVmean, SUVpeak, TBRmax, TBRmean, and TPRmax showed improved performance of AUC (0.833-0.867, p <0.05). Patients with SUVmax, SUVmean, or SUVpeak more than the cutoff value had significantly shorter RFS (all p <0.05). In addition, patients with SUVmean, SUVpeak, or TPRmax more than the cutoff value had significantly shorter OS (all p <0.05). PSMA expression of glioma vascular endothelium was observed in ten (10/11, 90.9%) patients with moderate-to-high levels in all GBM cases (n = 6/6, 100%).

Conclusion: This primitive study shows multiparameter PSMA PET/MR to be useful in identifying glioma (especially GBM) recurrence by providing excellent tumor background comparison, tumor heterogeneity, recurrence prediction and prognosis information, although it did not improve the diagnostic performance compared to conventional MRI. Further and larger studies are required to define its potential clinical application in this setting.

Keywords: PSMA PET/MR, glioma, recurrence, MRI, texture feature, prognosis.

[1]
Jiang T, Nam DH, Ram Z, et al. Clinical practice guidelines for the management of adult diffuse gliomas. Cancer Lett 2021; 499: 60-72.
[http://dx.doi.org/10.1016/j.canlet.2020.10.050] [PMID: 33166616]
[2]
Jiang T, Tang G-F, Lin Y, et al. Prevalence estimates for primary brain tumors in China: A multi-center cross-sectional study. Chin Med J 2011; 124(17): 2578-83.
[http://dx.doi.org/10.3760/cma.j.issn.0366-6999.2011.17.003] [PMID: 22040406]
[3]
Van de Wiele C, Sathekge M, de Spiegeleer B, de Jonghe P, Beels L, Maes A. PSMA-targeting positron emission agents for imaging solid tumors other than non-prostate carcinoma: A systematic review. Int J Mol Sci 2019; 20(19): 4886.
[http://dx.doi.org/10.3390/ijms20194886] [PMID: 31581638]
[4]
Xia L, Fang C, Chen G, Sun C. Relationship between the extent of resection and the survival of patients with low-grade gliomas: A systematic review and meta-analysis. BMC Cancer 2018; 18(1): 48.
[http://dx.doi.org/10.1186/s12885-017-3909-x] [PMID: 29306321]
[5]
Mankoff DA. A definition of molecular imaging. J Nucl Med 2007; 48(6): 18N-, 21N.
[PMID: 17536102]
[6]
Fink JR, Muzi M, Peck M, Krohn KA. Multimodality brain tumor imaging: MR imaging, PET, and PET/MR imaging. J Nucl Med 2015; 56(10): 1554-61.
[http://dx.doi.org/10.2967/jnumed.113.131516] [PMID: 26294301]
[7]
Pyatigorskaya N, Sgard B, Bertaux M, Yahia-Cherif L, Kas A. Can FDG-PET/MR help to overcome limitations of sequential MRI and PET-FDG for differential diagnosis between recurrence/progression and radionecrosis of high-grade gliomas? J Neuroradiol 2021; 48(3): 189-94.
[http://dx.doi.org/10.1016/j.neurad.2020.08.003] [PMID: 32858062]
[8]
Pellerin A, Khalifé M, Sanson M, et al. Simultaneously acquired PET and ASL imaging biomarkers may be helpful in differentiating progression from pseudo-progression in treated gliomas. Eur Radiol 2021; 31(10): 7395-405.
[http://dx.doi.org/10.1007/s00330-021-07732-0] [PMID: 33787971]
[9]
Lundemann M, Munck af Rosenschöld P, Muhic A, et al. Feasibility of multi-parametric PET and MRI for prediction of tumour recurrence in patients with glioblastoma. Eur J Nucl Med Mol Imaging 2019; 46(3): 603-13.
[http://dx.doi.org/10.1007/s00259-018-4180-3] [PMID: 30276440]
[10]
Jens C, Martin S, Klaus K, et al. 18f-tagged inhibitors of prostate specific membrane antigen (psma) and their use as imaging agents for prostate cancer. US10815200B2, 2016.
[11]
Nomura N, Pastorino S, Jiang P, et al. Prostate specific membrane antigen (PSMA) expression in primary gliomas and breast cancer brain metastases. Cancer Cell Int 2014; 14(1): 26.
[http://dx.doi.org/10.1186/1475-2867-14-26] [PMID: 24645697]
[12]
Stopa B M, Crowley J, Juhász C, Rogers C M, Witcher M R, Kiser J W. Prostate-specific membrane antigen as target for neuroimaging of central nervous system tumors. Mol Imaging 2022; 2022: 5358545.
[http://dx.doi.org/10.1155/2022/5358545]
[13]
Sasikumar A, Kashyap R, Joy A, et al. Utility of 68Ga-PSMA-11 PET/CT in imaging of glioma-a pilot study. Clin Nucl Med 2018; 43(9): e304-9.
[http://dx.doi.org/10.1097/RLU.0000000000002175] [PMID: 29939953]
[14]
Mayerhoefer ME, Materka A, Langs G, et al. Introduction to radiomics. J Nucl Med 2020; 61(4): 488-95.
[http://dx.doi.org/10.2967/jnumed.118.222893] [PMID: 32060219]
[15]
Lohmann P, Kocher M, Ceccon G, et al. Combined FET PET/MRI radiomics differentiates radiation injury from recurrent brain metastasis. Neuroimage Clin 2018; 20: 537-42.
[http://dx.doi.org/10.1016/j.nicl.2018.08.024] [PMID: 30175040]
[16]
Jadvar H, Calais J, Fanti S, et al. Appropriate use criteria for prostate-specific membrane antigen PET imaging. J Nucl Med 2022; 63(1): 59-68.
[http://dx.doi.org/10.2967/jnumed.121.263262] [PMID: 34593595]
[17]
Pauleit D, Floeth F, Hamacher K, et al. O-(2-[18F]fluoroethyl)-L-tyrosine PET combined with MRI improves the diagnostic assessment of cerebral gliomas. Brain 2005; 128(3): 678-87.
[http://dx.doi.org/10.1093/brain/awh399] [PMID: 15689365]
[18]
van Griethuysen JJM, Fedorov A, Parmar C, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res 2017; 77(21): e104-7.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-0339] [PMID: 29092951]
[19]
Radiomic Features. Available From: https://pyradiomics.readthedocs.io/en/latest/features.html [Accessed on : May 14].
[20]
Chang SS, Reuter VE, Heston WD, Bander NH, Grauer LS, Gaudin PB. Five different anti-prostate-specific membrane antigen (PSMA) antibodies confirm PSMA expression in tumor-associated neovasculature. Cancer Res 1999; 59(13): 3192-8.http://dx.doi.org/
[PMID: 10397265]
[21]
Saffar H, Noohi M, Tavangar SM, Saffar H, Azimi S. Expression of prostate-specific membrane antigen (PSMA) in brain glioma and its correlation with tumor grade. Iran J Pathol 2018; 13(1): 45-53.
[http://dx.doi.org/10.30699/ijp.2019.89854.1849] [PMID: 29731795]
[22]
Wernicke AG, Edgar MA, Lavi E, et al. Prostate-specific membrane antigen as a potential novel vascular target for treatment of glioblastoma multiforme. Arch Pathol Lab Med 2011; 135(11): 1486-9.
[http://dx.doi.org/10.5858/arpa.2010-0740-OA] [PMID: 22032578]
[23]
Schwenck J, Tabatabai G, Skardelly M, et al. In vivo visualization of prostate-specific membrane antigen in glioblastoma. Eur J Nucl Med Mol Imaging 2015; 42(1): 170-1.
[http://dx.doi.org/10.1007/s00259-014-2921-5] [PMID: 25293865]
[24]
Unterrainer M, Niyazi M, Ruf V, Bartenstein P, Albert NL. The endothelial prostate-specific membrane antigen is highly expressed in gliosarcoma and visualized by [68Ga]-PSMA-11 PET: A theranostic outlook for brain tumor patients? Neuro-oncol 2017; 19(12): 1698-9.
[http://dx.doi.org/10.1093/neuonc/nox172] [PMID: 29045711]
[25]
Kunikowska J, Kuliński R, Muylle K, Koziara H, Królicki L. 68Ga-prostate-specific membrane antigen-11 PET/CT. Clin Nucl Med 2020; 45(1): 11-8.
[http://dx.doi.org/10.1097/RLU.0000000000002806] [PMID: 31663868]
[26]
Stopa B M, Juhász C, Mittal S. Comparison of amino acid PET to advanced and emerging MRI techniques for neurooncology imaging: A systematic review of the recent studies. Mol Imaging 2021; 2021: 8874078.
[http://dx.doi.org/10.1155/2021/8874078]
[27]
Sasikumar A, Joy A, Pillai MRA, et al. Diagnostic value of 68Ga PSMA-11 PET/CT imaging of brain tumors-preliminary analysis. Clin Nucl Med 2017; 42(1): e41-8.
[http://dx.doi.org/10.1097/RLU.0000000000001451] [PMID: 27846000]
[28]
Akgun E, Akgun MY, Selçuk HH, Uzan M, Sayman HB. 68Ga PSMA PET/MR in the differentiation of low and high grade gliomas: Is 68Ga PSMA PET/MRI useful to detect brain gliomas? Eur J Radiol 2020; 130(109199): 109199.
[http://dx.doi.org/10.1016/j.ejrad.2020.109199] [PMID: 32763474]
[29]
Kläsner B, Buchmann N, Gempt J, Ringel F, Lapa C, Krause BJ. Early [18F] FET-PET in gliomas after surgical resection: comparison with MRI and histopathology. PLoS One 2015; 10(10): e0141153.
[http://dx.doi.org/10.1371/journal.pone.0141153] [PMID: 26502297]
[30]
Pan D, Rong X, Chen D, et al. Mortality of early treatment for radiation-induced brain necrosis in head and neck cancer survivors: A multicentre, retrospective, registry-based cohort study. EClinicalMedicine 2022; 52: 101618.
[http://dx.doi.org/10.1016/j.eclinm.2022.101618]
[31]
Cui M, Zorrilla-Veloz RI, Hu J, Guan B, Ma X. Diagnostic accuracy of PET for differentiating true glioma progression from post treatment-related changes: A systematic review and meta-analysis. Front Neurol 2021; 12(572): 671867.
[http://dx.doi.org/10.3389/fneur.2021.671867] [PMID: 34093419]
[32]
Salas Fragomeni RA, Menke JR, Holdhoff M, et al. Prostate-specific membrane antigen-targeted imaging with [18F]DCFPyL in high-grade gliomas. Clin Nucl Med 2017; 42(10): e433-5.
[http://dx.doi.org/10.1097/RLU.0000000000001769]
[33]
Marafi F, Sasikumar A, Fathallah W, Esmail A. 18F-PSMA 1007 brain PET/CT imaging in glioma recurrence. Clin Nucl Med 2020; 45(1): e61-2.
[http://dx.doi.org/10.1097/RLU.0000000000002668] [PMID: 31162269]
[34]
Giesel FL, Hadaschik B, Cardinale J, et al. F-18 labelled PSMA-1007: Biodistribution, radiation dosimetry and histopathological validation of tumor lesions in prostate cancer patients. Eur J Nucl Med Mol Imaging 2017; 44(4): 678-88.
[http://dx.doi.org/10.1007/s00259-016-3573-4] [PMID: 27889802]
[35]
Giesel FL, Cardinale J, Schäfer M, et al. 18F-Labelled PSMA-1007 shows similarity in structure, biodistribution and tumour uptake to the theragnostic compound PSMA-617. Eur J Nucl Med Mol Imaging 2016; 43(10): 1929-30.
[http://dx.doi.org/10.1007/s00259-016-3447-9] [PMID: 27342416]
[36]
Giesel FL, Knorr K, Spohn F, et al. Detection efficacy of 18F-PSMA-1007 PET/CT in 251 patients with biochemical recurrence of prostate cancer after radical prostatectomy. J Nucl Med 2019; 60(3): 362-8.
[http://dx.doi.org/10.2967/jnumed.118.212233] [PMID: 30042163]
[37]
Kuten J, Fahoum I, Savin Z, et al. Head-to-head comparison of 68Ga-PSMA-11 with 18F-PSMA-1007 PET/CT in staging prostate cancer using histopathology and immunohistochemical analysis as a reference standard. J Nucl Med 2020; 61(4): 527-32.
[http://dx.doi.org/10.2967/jnumed.119.234187] [PMID: 31562225]
[38]
Dijkgraaf I, Boerman OC. Radionuclide imaging of tumor angiogenesis. Cancer Biother Radiopharm 2009; 24(6): 637-47.
[http://dx.doi.org/10.1089/cbr.2009.0694] [PMID: 20025543]
[39]
Pàez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15(3): 220-31.
[http://dx.doi.org/10.1016/j.ccr.2009.01.027] [PMID: 19249680]
[40]
Bodei L, Herrmann K, Schöder H, Scott AM, Lewis JS. Radiotheranostics in oncology: current challenges and emerging opportunities. Nat Rev Clin Oncol 2022; 19(8): 534-50.
[http://dx.doi.org/10.1038/s41571-022-00652-y] [PMID: 35725926]
[41]
Kumar A, Ballal S, Yadav MP, et al. 177Lu-/68Ga-PSMA theranostics in recurrent glioblastoma multiforme. Clin Nucl Med 2020; 45(12): e512-3.
[http://dx.doi.org/10.1097/RLU.0000000000003142] [PMID: 32558721]

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