The Potential Role of PSMA-Targeted PET in Salivary Gland Malignancies: An Updated Systematic Review
Abstract
1. Introduction
2. Materials and Methods
2.1. Protocol
2.2. Literature Search Strategy and Information Sources
2.3. Eligibility Criteria
2.4. Selection Process
2.5. Data Collection Process and Data Extraction
2.6. Quality Assessment (Risk of Bias Assessment)
3. Results
3.1. Literature Search and Study Selection
3.2. Study Characteristics
3.3. Risk of Bias and Applicability
3.4. Results of Individual Studies
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Atallah, S.; Casiraghi, O.; Fakhry, N.; Wassef, M.; Uro-Coste, E.; Espitalier, F.; Sudaka, A.; Kaminsky, M.C.; Dakpe, S.; Digue, L.; et al. A Prospective Multicentre REFCOR Study of 470 Cases of Head and Neck Adenoid Cystic Carcinoma: Epidemiology and Prognostic Factors. Eur. J. Cancer 2020, 130, 241–249. [Google Scholar] [CrossRef]
- Spiro, R.H.; Huvos, A.G.; Strong, E.W. Adenoid Cystic Carcinoma of Salivary Origin. A Clinicopathologic Study of 242 Cases. Am. J. Surg. 1974, 128, 512–520. [Google Scholar] [CrossRef]
- Lloyd, S.; Yu, J.B.; Wilson, L.D.; Decker, R.H. Determinants and Patterns of Survival in Adenoid Cystic Carcinoma of the Head and Neck, Including an Analysis of Adjuvant Radiation Therapy. Am. J. Clin. Oncol. 2011, 34, 76–81. [Google Scholar] [CrossRef] [PubMed]
- Lorini, L.; Ardighieri, L.; Bozzola, A.; Romani, C.; Bignotti, E.; Buglione, M.; Guerini, A.; Lombardi, D.; Deganello, A.; Tomasoni, M.; et al. Prognosis and Management of Recurrent and/or Metastatic Head and Neck Adenoid Cystic Carcinoma. Oral Oncol. 2021, 115, 105213. [Google Scholar] [CrossRef] [PubMed]
- Colevas, A.D.; Yom, S.S.; Pfister, D.G.; Spencer, S.; Adelstein, D.; Adkins, D.; Brizel, D.M.; Burtness, B.; Busse, P.M.; Caudell, J.J.; et al. NCCN Guidelines Insights: Head and Neck Cancers, Version 1.2018. J. Natl. Compr. Cancer Netw. 2018, 16, 479–490. [Google Scholar] [CrossRef]
- Laurie, S.A.; Ho, A.L.; Fury, M.G.; Sherman, E.; Pfister, D.G. Systemic Therapy in the Management of Metastatic or Locally Recurrent Adenoid Cystic Carcinoma of the Salivary Glands: A Systematic Review. Lancet Oncol. 2011, 12, 815–824. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Luo, Y.; Li, M.; Yan, H.; Sun, M.; Fan, T. Management of Salivary Gland Carcinomas—A Review. Oncotarget 2017, 8, 3946–3956. [Google Scholar] [CrossRef]
- de Keizer, B.; Krijger, G.C.; Ververs, F.T.; van Es, R.J.J.; de Bree, R.; Willems, S. 68Ga-PSMA PET-CT Imaging of Metastatic Adenoid Cystic Carcinoma. Nucl. Med. Mol. Imaging 2017, 51, 360–361. [Google Scholar] [CrossRef]
- Klein Nulent, T.J.W.; Valstar, M.H.; Smit, L.A.; Smeele, L.E.; Zuithoff, N.P.A.; de Keizer, B.; de Bree, R.; van Es, R.J.J.; Willems, S.M. Prostate-Specific Membrane Antigen (PSMA) Expression in Adenoid Cystic Carcinoma of the Head and Neck. BMC Cancer 2020, 20, 519. [Google Scholar] [CrossRef]
- Song, H.; Sgouros, G. Alpha and Beta Radiation for Theragnostics. PET Clin. 2024, 19, 307–323. [Google Scholar] [CrossRef]
- Sadeghi, R.; Treglia, G. Systematic Reviews and Meta-Analyses of Diagnostic Studies: A Practical Guideline. Clin. Transl. Imaging 2017, 5, 83–87. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef] [PubMed]
- QUADAS-2: A Revised Tool for the Quality Assessment of Diagnostic Accuracy Studies|Annals of Internal Medicine. Available online: https://www.acpjournals.org/doi/10.7326/0003-4819-155-8-201110180-00009 (accessed on 21 August 2022).
- Klein Nulent, T.J.W.; van Es, R.J.J.; Krijger, G.C.; de Bree, R.; Willems, S.M.; de Keizer, B. Prostate-Specific Membrane Antigen PET Imaging and Immunohistochemistry in Adenoid Cystic Carcinoma- a Preliminary Analysis. Eur. J. Nucl. Med. Mol. Imaging 2017, 44, 1614–1621. [Google Scholar] [CrossRef] [PubMed]
- van Boxtel, W.; Lütje, S.; van Engen-van Grunsven, I.C.H.; Verhaegh, G.W.; Schalken, J.A.; Jonker, M.A.; Nagarajah, J.; Gotthardt, M.; van Herpen, C.M.L. 68Ga-PSMA-HBED-CC PET/CT Imaging for Adenoid Cystic Carcinoma and Salivary Duct Carcinoma: A Phase 2 Imaging Study. Theranostics 2020, 10, 2273–2283. [Google Scholar] [CrossRef] [PubMed]
- Klein Nulent, T.J.W.; van Es, R.J.J.; Willems, S.M.; Braat, A.J.A.T.; Devriese, L.A.; de Bree, R.; de Keizer, B. First Experiences with 177Lu-PSMA-617 Therapy for Recurrent or Metastatic Salivary Gland Cancer. EJNMMI Res. 2021, 11, 126. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Zhou, M.; Zang, J.; Jiang, Y.; Chen, X.; Zhu, Z.; Chen, X. A Pilot Study of 68 Ga-PSMA-617 PET/CT Imaging and 177Lu-EB-PSMA-617 Radioligand Therapy in Patients with Adenoid Cystic Carcinoma. EJNMMI Res. 2022, 12, 52. [Google Scholar] [CrossRef] [PubMed]
- Civan, C.; Kasper, S.; Berliner, C.; Fragoso-Costa, P.; Grünwald, V.; Pogorzelski, M.; Schaarschmidt, B.M.; Lang, S.; Kersting, D.; Nader, M.; et al. PSMA-Directed Imaging and Therapy of Salivary Gland Tumors: A Single-Center Retrospective Study. J. Nucl. Med. 2023, 64, 372–378. [Google Scholar] [CrossRef] [PubMed]
- Shamim, S.A.; Kumar, N.; Arora, G.; Kumar, D.; Pathak, A.; Thakkar, A.; Sikka, K.; Singh, C.A.; Kakkar, A.; Bhalla, A.S. Comparison of 68Ga-PSMA-HBED-CC and 18F-FDG PET/CT in the Evaluation of Adenoid Cystic Carcinoma—A Prospective Study. Clin. Nucl. Med. 2023, 48, e509. [Google Scholar] [CrossRef] [PubMed]
- Sartor, O.; de Bono, J.; Chi, K.N.; Fizazi, K.; Herrmann, K.; Rahbar, K.; Tagawa, S.T.; Nordquist, L.T.; Vaishampayan, N.; El-Haddad, G.; et al. Lutetium-177-PSMA-617 for Metastatic Castration-Resistant Prostate Cancer. N. Engl. J. Med. 2021, 385, 1091–1103. [Google Scholar] [CrossRef]
- Hofman, M.S.; Lawrentschuk, N.; Francis, R.J.; Tang, C.; Vela, I.; Thomas, P.; Rutherford, N.; Martin, J.M.; Frydenberg, M.; Shakher, R.; et al. Prostate-Specific Membrane Antigen PET-CT in Patients with High-Risk Prostate Cancer before Curative-Intent Surgery or Radiotherapy (proPSMA): A Prospective, Randomised, Multicentre Study. Lancet 2020, 395, 1208–1216. [Google Scholar] [CrossRef]
- Rizzo, A.; Racca, M.; Dall’Armellina, S.; Delgado Bolton, R.C.; Albano, D.; Dondi, F.; Bertagna, F.; Annunziata, S.; Treglia, G. Potential Role of PSMA-Targeted PET in Thyroid Malignant Disease: A Systematic Review. Diagnostics 2023, 13, 564. [Google Scholar] [CrossRef]
- Rizzo, A.; Racca, M.; Albano, D.; Dondi, F.; Bertagna, F.; Annunziata, S.; Treglia, G. Can PSMA-Targeting Radiopharmaceuticals Be Useful for Detecting Hepatocellular Carcinoma Using Positron Emission Tomography? An Updated Systematic Review and Meta-Analysis. Pharmaceuticals 2022, 15, 1368. [Google Scholar] [CrossRef] [PubMed]
- Rizzo, A.; Racca, M.; Dall’Armellina, S.; Rescigno, P.; Banna, G.L.; Albano, D.; Dondi, F.; Bertagna, F.; Annunziata, S.; Treglia, G. The Emerging Role of PET/CT with PSMA-Targeting Radiopharmaceuticals in Clear Cell Renal Cancer: An Updated Systematic Review. Cancers 2023, 15, 355. [Google Scholar] [CrossRef]
- Conway, R.E.; Rojas, C.; Alt, J.; Nováková, Z.; Richardson, S.M.; Rodrick, T.C.; Fuentes, J.L.; Richardson, N.H.; Attalla, J.; Stewart, S.; et al. Prostate-Specific Membrane Antigen (PSMA)-Mediated Laminin Proteolysis Generates a pro-Angiogenic Peptide. Angiogenesis 2016, 19, 487–500. [Google Scholar] [CrossRef]
- Ruhlmann, V.; Poeppel, T.D.; Veit, J.; Nagarajah, J.; Umutlu, L.; Hoffmann, T.K.; Bockisch, A.; Herrmann, K.; Sauerwein, W. Diagnostic Accuracy of 18F-FDG PET/CT and MR Imaging in Patients with Adenoid Cystic Carcinoma. BMC Cancer 2017, 17, 887. [Google Scholar] [CrossRef] [PubMed]
- Gilardi, L.; Airò Farulla, L.S.; Demirci, E.; Clerici, I.; Omodeo Salè, E.; Ceci, F. Imaging Cancer-Associated Fibroblasts (CAFs) with FAPi PET. Biomedicines 2022, 10, 523. [Google Scholar] [CrossRef]
- Kratochwil, C.; Flechsig, P.; Lindner, T.; Abderrahim, L.; Altmann, A.; Mier, W.; Adeberg, S.; Rathke, H.; Röhrich, M.; Winter, H.; et al. 68Ga-FAPI PET/CT: Tracer Uptake in 28 Different Kinds of Cancer. J. Nucl. Med. 2019, 60, 801–805. [Google Scholar] [CrossRef]
- Chen, H.; Zhao, L.; Ruan, D.; Pang, Y.; Hao, B.; Dai, Y.; Wu, X.; Guo, W.; Fan, C.; Wu, J.; et al. Usefulness of [68Ga]Ga-DOTA-FAPI-04 PET/CT in Patients Presenting with Inconclusive [18F]FDG PET/CT Findings. Eur. J. Nucl. Med. Mol. Imaging 2021, 48, 73–86. [Google Scholar] [CrossRef] [PubMed]
- Rizzo, A.; Racca, M.; Garrou, F.; Fenocchio, E.; Pellegrino, L.; Albano, D.; Dondi, F.; Bertagna, F.; Annunziata, S.; Treglia, G. Diagnostic Performance of Positron Emission Tomography with Fibroblast-Activating Protein Inhibitors in Gastric Cancer: A Systematic Review and Meta-Analysis. Int. J. Mol. Sci. 2023, 24, 10136. [Google Scholar] [CrossRef]
- Röhrich, M.; Syed, M.; Liew, D.P.; Giesel, F.L.; Liermann, J.; Choyke, P.L.; Wefers, A.K.; Ritz, T.; Szymbara, M.; Schillings, L.; et al. 68Ga-FAPI-PET/CT Improves Diagnostic Staging and Radiotherapy Planning of Adenoid Cystic Carcinomas-Imaging Analysis and Histological Validation. Radiother. Oncol. 2021, 160, 192–201. [Google Scholar] [CrossRef]
- Verena, A.; Zhang, Z.; Kuo, H.-T.; Merkens, H.; Zeisler, J.; Wilson, R.; Bendre, S.; Wong, A.A.W.L.; Bénard, F.; Lin, K.-S. Synthesis and Preclinical Evaluation of Three Novel 68Ga-Labeled Bispecific PSMA/FAP-Targeting Tracers for Prostate Cancer Imaging. Molecules 2023, 28, 1088. [Google Scholar] [CrossRef] [PubMed]
- Taralli, S.; Martino, A.; Cancellieri, A.; Calandriello, L.; Lococo, F.; Caldarella, C. Adenoid Cystic Carcinoma of the Parotid Gland: A First Case Report on 11C-Methionine PET/CT Detection of Histologically Confirmed Pulmonary Metastases. Acta Oncol. 2022, 61, 669–671. [Google Scholar] [CrossRef] [PubMed]
- Toubaru, S.; Yoshikawa, K.; Ohashi, S.; Tanimoto, K.; Hasegawa, A.; Kawaguchi, K.; Saga, T.; Kamada, T. Accuracy of Methionine-PET in Predicting the Efficacy of Heavy-Particle Therapy on Primary Adenoid Cystic Carcinomas of the Head and Neck. Radiat. Oncol. 2013, 8, 143. [Google Scholar] [CrossRef]
- Tan, B.F.; Tan, W.C.C.; Wang, F.Q.; Lechner, M.; Schartinger, V.H.; Tan, D.S.W.; Loke, K.S.H.; Nei, W.L. PSMA PET Imaging and Therapy in Adenoid Cystic Carcinoma and Other Salivary Gland Cancers: A Systematic Review. Cancers 2022, 14, 3585. [Google Scholar] [CrossRef] [PubMed]
First Authors [Ref.] | Year | Country | Study Design/Number of Involved Centers | Funding Sources |
---|---|---|---|---|
Kein Nulent et al. [14] | 2017 | The Netherlands | Single center/Retrospective | None declared |
Van Boxtel et al. [15] | 2020 | The Netherlands | Single center/Prospective | Dutch Salivary Gland Cancer Platform and the ACC Research Foundation |
Klein Nulent et al. [16] | 2021 | The Netherlands | Single center/Retrospective | None declared |
Wang et al. [17] | 2022 | China | Single center/Prospective | Several funding sources disclosed |
Civan et al. [18] | 2023 | Germany | Single center/Retrospective | Several funding sources disclosed |
Shamim et al. [19] | 2024 | India | Single center/Prospective | None declared |
First Authors [Ref.] | Sample Size (No. of Patients) | Mean/Median Age (Years) | Gender (Male %) | Clinical Setting (No. Patients) | Location of Primary Tumor (No. of Patients) | SGM Subtype (No. of Patients) | Comparative Imaging |
---|---|---|---|---|---|---|---|
Kein Nulent et al. [14] | 9 | Median: 54 | 44% | 9 Restaging | 4 Parotid 3 Palate 2 Nasal cavity | 9 ACC | [18F]FDG PET/CT; CT |
Van Boxtel et al. [15] | 25 | Median ACC: 58 Median SDC: 70 | 84% | 25 Restaging | 22 Salivary gland 1 Trachea 1 Bronchus 1 Bartholin gland | 15 ACC 10 SDC | CT; MRI |
Klein Nulent et al. [16] | 6 | Median: 39 | 50% | 6 Restaging | 3 Parotid 1 Submandibular 1 Hard palate 1 Cheek mucosa | 4 ACC 1 Adenocarcinoma 1 Acinic cell carcinoma | Not available |
Wang et al. [17] | 30 | Mean: 43 | 50% | 1 Staging 29 Restasging | n.a. | 30 ACC | [18F]FDG PET/CT |
Civan et al. [18] | 28 | Median: 59 | 39% | 2 Staging 26 Restaging | 8 Parotid 7 Submandibular 3 Sublingual 10 Minor SG | 24 ACC 2 Adenocarcinoma 1 Acinic cell carcinoma 1 Sebaceous carcinoma | CT |
Shamim et al. [19] | 17 | Mean: 44 | 41% | 4 Staging 13 Restaging | 5 Paranasal sinuses 5 Hard palate 3 Parotid 2 Submandibular 1 Nasopharynx 1 Oropharynx | 17 ACC | [18F]FDG PET/CT |
First Authors [Ref.] | Tracer | Hybrid Imaging | Administered Activity | Uptake Time (Minutes) | Image Analysis |
---|---|---|---|---|---|
Kein Nulent et al. [14] | [68Ga]Ga-PSMA-11 | PET/CT | 2 MBq/kg | 60 | Qualitative; Semiquantitative (SUVmax) |
Van Boxtel et al. [15] | [68Ga]Ga-PSMA-11 | PET/CT | 3 MBq/kg | 60 | Qualitative; Semiquantitative (SUVmax; TBR) |
Klein Nulent et al. [16] * | [68Ga]Ga-PSMA-11 | PET/CT | 2 MBq/kg | 60 | Qualitative; Semiquantitative (SUVmax) |
Wang et al. [17] ** | [68Ga]Ga-PSMA-617 | PET/CT | 1.8–2.2 MBq/kg | 50-60 | Qualitative; Semiquantitative (SUVmax) |
Civan et al. [18] ** | [68Ga]Ga-PSMA-11 [18F]PSMA-1007 | PET/CT | [68Ga]Ga-PSMA-11: 116 MBq [18F]PSMA-1007: 281 MBq | [68Ga]Ga-PSMA-11: 63 [18F]PSMA-1007: 98 | Qualitative; Semiquantitative (SUVmax) |
Shamim et al. [19] | [68Ga]Ga-PSMA-11 | PET/CT | 111–185 MBq | 45 | Qualitative; Semiquantitative (SUVmax; TBR) |
First Authors [Ref.] | Disease Sites Other than SG. | Lesions SUVmax | Immunohistochemistry for PSMA | Detection Rate | Stage Migration (No. Patient) | Outcome |
---|---|---|---|---|---|---|
Klein Nulent et al. [14] | Lymph node Lung Bone Liver Peritoneum Meninges | Different sites ranging from 2.04 to 12.97 | Staining on tumor cells ranging from 5 to 90% | Per patient: 89% | Upstaging 4/9 | PSMA-PET could detect local recurrence and distant metastases in ACC patients. |
Van Boxtel et al. [15] | Lymph node Lung Pleura Pericardium Bone Liver Brain Subcutaneous | Different sites ranging from 0.3 to 30.2 | ACC: tumor cells ranging from 0 to 90%; tumor-associated neovasculature: 0/11 samples. SDC: tumor cells 0%; tumor-associated neovasculature: 8/9 samples. | Per patient ACC: 93% Per patient SDC: 40% | Upstaging: 2/15 ACC; 0/15 SDC | PSMA-PET added diagnostic value in some of the ACC patients compared to CT. |
Klein Nulent et al. [16] | Lymph node Lung Bone Liver | Different sites ranging from 3.5 to 12.5 | Staining for PSMA ranging from 5% to 95% | Per patient: 100% | Not available | When PSMA expression is sufficient, PSMA-targeted RLT may improve symptoms and induce a PR or SD in one-third of patients. |
Wang et al. [17] | Lymph node Lung BoneLiver | Primary tumor: 9.8 Local recurrence: 10.4 Distant metastases: 4.1 | Not available | Per patient: 90% | Not available | PSMA-PET is a valuable tool for diagnosing and staging ACC. Combined with FDG PET, it can improve diagnostic performance. |
Civan et al. [18] | Lymph node Lung Bone | not available | Not available | Per patient: 96% | Upstaging: 3/28 | PSMA PET/CT upstaged about one-third of SGM patients compared to CT. |
Shamim et al. [19] | Lymph nodes Lung Bone Liver Brain Bone | Primary tumor: 4.8 Different sites ranging from 1.8 to 8.1 | Not available | Pet patient: 100% | Upstaging 2/17 | PSMA PET/CT may have a theragnostic role in ACC patients and can detect additional metastatic sites compared to FDG PET. |
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Rizzo, A.; Albano, D.; Elisei, F.; Racca, M.; Dondi, F.; Annunziata, S.; Cuzzocrea, M.; Bertagna, F.; Treglia, G. The Potential Role of PSMA-Targeted PET in Salivary Gland Malignancies: An Updated Systematic Review. Diagnostics 2024, 14, 1516. https://doi.org/10.3390/diagnostics14141516
Rizzo A, Albano D, Elisei F, Racca M, Dondi F, Annunziata S, Cuzzocrea M, Bertagna F, Treglia G. The Potential Role of PSMA-Targeted PET in Salivary Gland Malignancies: An Updated Systematic Review. Diagnostics. 2024; 14(14):1516. https://doi.org/10.3390/diagnostics14141516
Chicago/Turabian StyleRizzo, Alessio, Domenico Albano, Federica Elisei, Manuela Racca, Francesco Dondi, Salvatore Annunziata, Marco Cuzzocrea, Francesco Bertagna, and Giorgio Treglia. 2024. "The Potential Role of PSMA-Targeted PET in Salivary Gland Malignancies: An Updated Systematic Review" Diagnostics 14, no. 14: 1516. https://doi.org/10.3390/diagnostics14141516
APA StyleRizzo, A., Albano, D., Elisei, F., Racca, M., Dondi, F., Annunziata, S., Cuzzocrea, M., Bertagna, F., & Treglia, G. (2024). The Potential Role of PSMA-Targeted PET in Salivary Gland Malignancies: An Updated Systematic Review. Diagnostics, 14(14), 1516. https://doi.org/10.3390/diagnostics14141516