PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms: An Umbrella Review of Published Meta-Analyses
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
3. Results
3.1. Diagnostic Performance of PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms
3.1.1. Suspected NETs
3.1.2. Thoracic and/or Gastroenteropancreatic NETs
3.1.3. Small Cell Lung Cancer (SCLC)
3.1.4. Metastatic NETs with Unknow Primary Tumor (CUP-NETs)
3.1.5. Paragangliomas (PGL)
3.1.6. Neuroblastoma (NB)
3.1.7. Recurrent Medullary Thyroid Carcinoma (rMTC)
3.1.8. Merkel Cell Carcinoma (MCC)
3.1.9. Multiple Endocrine Neoplasia (MEN) Syndromes and Ectopic Cushing Syndrome (ECS)
3.2. Prognostic Value of PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasm
3.2.1. Thoracic and/or Gastroenteropancreatic NETs
3.2.2. Small Cell Lung Cancer (SCLC)
3.3. Clinical Impact of PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms
3.3.1. Thoracic and/or Gastroenteropancreatic NETs and CUP-NETs
3.3.2. SCLC
3.4. Safety of PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms
4. Discussion
- (A)
- Diagnostic performance:
- 68Ga-SSA PET and related hybrid modalities yield high diagnostic performance in patients with suspected NETs, and in detecting thoracic and gastroenteropacreatic NETs, CUP-NETs and PGL.
- 18F-FDOPA PET and related hybrid modalities yield good diagnostic performance in patients with intestinal NETs, PGL, NB and can be a good alternative to other PET methods in these settings; 18F-FDOPA is the best PET radiopharmaceutical in detecting rMTC even if the detection rate is suboptimal.
- 68Ga-exendin-4 PET has good diagnostic accuracy in detecting insulinomas and it could be used as the preferred PET method in this setting.
- 18F-FDG PET and related hybrid modalities yield good diagnostic performance in detecting aggressive neuroendocrine neoplasms (e.g., high-grade NETs, SCLC, NB and MCC).
- (B)
- Prognostic value:
- The 68Ga-SSA PET has a recognized prognostic value in well-differentiated NETs; in these patients, a lower uptake at 68Ga-SSA PET is associated with a worse prognosis.
- The 18F-FDG PET has a recognized prognostic value in aggressive neuroendocrine neoplasms; in these patients, higher values of metabolic parameters are associated with a worse prognosis.
- (C)
- Clinical impact:
- There is a significant clinical impact of 68Ga-SSA PET and related hybrid modalities in patients with NETs.
- (D)
- Safety:
- There are no major toxicities or safety issues related to the use of PET radiopharmaceuticals in patients with neuroendocrine neoplasms.
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Appendix A
References
- Rindi, G.; Inzani, F. Neuroendocrine neoplasm update: Toward universal nomenclature. Endocr. Relat. Cancer 2020, 27, R211–R218. [Google Scholar] [CrossRef] [PubMed]
- Modlin, I.M.; Lye, K.D.; Kidd, M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer 2003, 97, 934–959. [Google Scholar] [CrossRef] [PubMed]
- Wong, R.K.S.; Metser, U.; Veit-Haibach, P. Neuroendocrine Tumors: Imaging Perspective. PET Clin. 2021, 16, 353–364. [Google Scholar] [CrossRef] [PubMed]
- Treglia, G.; Kroiss, A.S.; Piccardo, A.; Lococo, F.; Santhanam, P.; Imperiale, A. Role of positron emission tomography in thyroid and neuroendocrine tumors. Minerva Endocrinol. 2018, 43, 341–355. [Google Scholar] [CrossRef]
- Taïeb, D.; Jha, A.; Treglia, G.; Pacak, K. Molecular imaging and radionuclide therapy of pheochromocytoma and paraganglioma in the era of genomic characterization of disease subgroups. Endocr. Relat. Cancer 2019, 26, R627–R652. [Google Scholar] [CrossRef]
- Treglia, G.; Goichot, B.; Giovanella, L.; Hindié, E.; Jha, A.; Pacak, K.; Taïeb, D.; Walter, T.; Imperiale, A. Prognostic and predictive value of nuclear imaging in endocrine oncology. Endocrine 2020, 67, 9–19. [Google Scholar] [CrossRef]
- Fusar-Poli, P.; Radua, J. Ten simple rules for conducting umbrella reviews. Evid. Based Ment. Health 2018, 21, 95–100. [Google Scholar] [CrossRef] [Green Version]
- Alevroudis, E.; Spei, M.E.; Chatziioannou, S.N.; Tsoli, M.; Wallin, G.; Kaltsas, G.; Daskalakis, K. Clinical Utility of 18F-FDG PET in Neuroendocrine Tumors Prior to Peptide Receptor Radionuclide Therapy: A Systematic Review and Meta-Analysis. Cancers 2021, 13, 1813. [Google Scholar] [CrossRef]
- Barrio, M.; Czernin, J.; Fanti, S.; Ambrosini, V.; Binse, I.; Du, L.; Eiber, M.; Herrmann, K.; Fendler, W.P. The Impact of Somatostatin Receptor-Directed PET/CT on the Management of Patients with Neuroendocrine Tumor: A Systematic Review and Meta-Analysis. J. Nucl. Med. 2017, 58, 756–761. [Google Scholar] [CrossRef] [Green Version]
- Bauckneht, M.; Albano, D.; Annunziata, S.; Santo, G.; Guglielmo, P.; Frantellizzi, V.; Branca, A.; Ferrari, C.; Vento, A.; Mirabile, A.; et al. Somatostatin Receptor PET/CT Imaging for the Detection and Staging of Pancreatic NET: A Systematic Review and Meta-Analysis. Diagnostics 2020, 10, 598. [Google Scholar] [CrossRef]
- Cheng, X.; Bao, L.; Xu, Z.; Li, D.; Wang, J.; Li, Y. ¹⁸F-FDG-PET and ¹⁸F-FDG-PET/CT in the detection of recurrent or metastatic medullary thyroid carcinoma: A systematic review and meta-analysis. J. Med. Imaging Radiat. Oncol. 2012, 56, 136–142. [Google Scholar] [CrossRef]
- Christensen, T.N.; Andersen, P.K.; Langer, S.W.; Fischer, B.M.B. Prognostic Value of 18F-FDG-PET Parameters in Patients with Small Cell Lung Cancer: A Meta-Analysis and Review of Current Literature. Diagnostics 2021, 11, 174. [Google Scholar] [CrossRef]
- De Dosso, S.; Treglia, G.; Pascale, M.; Tamburello, A.; Santhanam, P.; Kroiss, A.S.; Pereira Mestre, R.; Saletti, P.; Giovanella, L. Detection rate of unknown primary tumour by using somatostatin receptor PET/CT in patients with metastatic neuroendocrine tumours: A meta-analysis. Endocrine 2019, 64, 456–468. [Google Scholar] [CrossRef]
- Deppen, S.A.; Blume, J.; Bobbey, A.J.; Shah, C.; Graham, M.M.; Lee, P.; Delbeke, D.; Walker, R.C. 68Ga-DOTATATE Compared with 111In-DTPA-Octreotide and Conventional Imaging for Pulmonary and Gastroenteropancreatic Neuroendocrine Tumors: A Systematic Review and Meta-Analysis. J. Nucl. Med. 2016, 57, 872–878. [Google Scholar] [CrossRef] [Green Version]
- Geijer, H.; Breimer, L.H. Somatostatin receptor PET/CT in neuroendocrine tumours: Update on systematic review and meta-analysis. Eur. J. Nucl. Med. Mol. Imaging 2013, 40, 1770–1780. [Google Scholar] [CrossRef]
- Han, S.; Suh, C.H.; Woo, S.; Kim, Y.J.; Lee, J.J. Performance of 68Ga-DOTA-Conjugated Somatostatin Receptor-Targeting Peptide PET in Detection of Pheochromocytoma and Paraganglioma: A Systematic Review and Metaanalysis. J. Nucl. Med. 2019, 60, 369–376. [Google Scholar] [CrossRef] [Green Version]
- Han, S.; Lee, H.S.; Woo, S.; Kim, T.H.; Yoo, C.; Ryoo, B.Y.; Ryu, J.S. Prognostic Value of 18F-FDG PET in Neuroendocrine Neoplasm: A Systematic Review and Meta-analysis. Clin. Nucl. Med. 2021, 46, 723–731. [Google Scholar] [CrossRef]
- Jiang, Y.; Hou, G.; Cheng, W. The utility of 18F-FDG and 68Ga-DOTA-Peptide PET/CT in the evaluation of primary pulmonary carcinoid: A systematic review and meta-analysis. Medicine 2019, 98, e14769. [Google Scholar] [CrossRef]
- Kan, Y.; Zhang, S.; Wang, W.; Liu, J.; Yang, J.; Wang, Z. 68Ga-somatostatin receptor analogs and 18F-FDG PET/CT in the localization of metastatic pheochromocytomas and paragangliomas with germline mutations: A meta-analysis. Acta Radiol. 2018, 59, 1466–1474. [Google Scholar] [CrossRef]
- Lee, D.Y.; Kim, Y.I. Prognostic Value of Maximum Standardized Uptake Value in 68Ga-Somatostatin Receptor Positron Emission Tomography for Neuroendocrine Tumors: A Systematic Review and Meta-analysis. Clin. Nucl. Med. 2019, 44, 777–783. [Google Scholar] [CrossRef]
- Lee, S.W.; Shim, S.R.; Jeong, S.Y.; Kim, S.J. Comparison of 5 Different PET Radiopharmaceuticals for the Detection of Recurrent Medullary Thyroid Carcinoma: A Network Meta-analysis. Clin. Nucl. Med. 2020, 45, 341–348. [Google Scholar] [CrossRef]
- Li, H.F.; Mao, H.J.; Zhao, L.; Guo, D.L.; Chen, B.; Yang, J.F. The Diagnostic Accuracy of PET(CT) in Patients With Neuroblastoma: A Meta-Analysis and Systematic Review. J. Comput. Assist. Tomogr. 2020, 44, 111–117. [Google Scholar] [CrossRef]
- Liu, X.; Li, N.; Jiang, T.; Xu, H.; Ran, Q.; Shu, Z.; Wu, J.; Li, Y.; Zhou, S.; Zhang, B. Comparison of gallium-68 somatostatin receptor and 18F-fluorodeoxyglucose positron emission tomography in the diagnosis of neuroendocrine tumours: A systematic review and meta-analysis. Hell J. Nucl. Med. 2020, 23, 188–200. [Google Scholar] [CrossRef]
- Lu, Y.Y.; Chen, J.H.; Liang, J.A.; Chu, S.; Lin, W.Y.; Kao, C.H. 18F-FDG PET or PET/CT for detecting extensive disease in small-cell lung cancer: A systematic review and meta-analysis. Nucl. Med. Commun. 2014, 35, 697–703. [Google Scholar] [CrossRef]
- Ma, H.; Kan, Y.; Yang, J.G. Clinical value of 68Ga-DOTA-SSTR PET/CT in the diagnosis and detection of neuroendocrine tumors of unknown primary origin: A systematic review and meta-analysis. Acta Radiol. 2021, 62, 1217–1228. [Google Scholar] [CrossRef]
- Martucci, F.; Pascale, M.; Valli, M.C.; Pesce, G.A.; Froesch, P.; Giovanella, L.; Richetti, A.; Treglia, G. Impact of 18F-FDG PET/CT in Staging Patients With Small Cell Lung Cancer: A Systematic Review and Meta-Analysis. Front. Med. 2020, 6, 336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nie, K.; Zhang, Y.X.; Nie, W.; Zhu, L.; Chen, Y.N.; Xiao, Y.X.; Liu, S.Y.; Yu, H. Prognostic value of metabolic tumour volume and total lesion glycolysis measured by 18F-fluorodeoxyglucose positron emission tomography/computed tomography in small cell lung cancer: A systematic review and meta-analysis. J. Med. Imaging Radiat. Oncol. 2019, 63, 84–93. [Google Scholar] [CrossRef] [Green Version]
- Piccardo, A.; Fiz, F.; Bottoni, G.; Ugolini, M.; Noordzij, W.; Trimboli, P. Head-to-head comparison between 18 F-DOPA PET/CT and 68 Ga-DOTA-peptide PET/CT in detecting intestinal neuroendocrine tumours: A systematic review and meta-analysis. Clin. Endocrinol. 2021. [Google Scholar] [CrossRef] [PubMed]
- Rufini, V.; Treglia, G.; Montravers, F.; Giordano, A. Diagnostic accuracy of [18F] DOPA PET and PET/CT in patients with neuroendocrine tumors: A meta-analysis. Clin. Trnasl. Imaging 2013, 1, 111–122. [Google Scholar] [CrossRef] [Green Version]
- Shah, R.; Garg, R.; Majmundar, M.; Purandare, N.; Malhotra, G.; Patil, V.; Ramteke-Jadhav, S.; Lila, A.; Shah, N.; Bandgar, T. Exendin-4-based imaging in insulinoma localization: Systematic review and meta-analysis. Clin. Endocrinol. 2021, 95, 354–364. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.; Poon, R.; Wong, R.; Metser, U. 68Ga PET Imaging in Patients With Neuroendocrine Tumors: A Systematic Review and Meta-analysis. Clin. Nucl. Med. 2018, 43, 802–810. [Google Scholar] [CrossRef]
- Sun, L.; Zhang, B.; Peng, R. Diagnostic Performance of 18F-FDG PET(CT) in Bone-Bone Marrow Involvement in Pediatric Neuroblastoma: A Systemic Review and Meta-Analysis. Contrast Media Mol. Imaging 2021, 2021, 8125373. [Google Scholar] [CrossRef]
- Treglia, G.; Cocciolillo, F.; Di Nardo, F.; Poscia, A.; de Waure, C.; Giordano, A.; Rufini, V. Detection rate of recurrent medullary thyroid carcinoma using fluorine-18 dihydroxyphenylalanine positron emission tomography: A meta-analysis. Acad. Radiol. 2012, 19, 1290–1299. [Google Scholar] [CrossRef]
- Treglia, G.; Castaldi, P.; Rindi, G.; Giordano, A.; Rufini, V. Diagnostic performance of Gallium-68 somatostatin receptor PET and PET/CT in patients with thoracic and gastroenteropancreatic neuroendocrine tumours: A meta-analysis. Endocrine 2012, 42, 80–87. [Google Scholar] [CrossRef]
- Treglia, G.; Cocciolillo, F.; de Waure, C.; Di Nardo, F.; Gualano, M.R.; Castaldi, P.; Rufini, V.; Giordano, A. Diagnostic performance of 18F-dihydroxyphenylalanine positron emission tomography in patients with paraganglioma: A meta-analysis. Eur. J. Nucl. Med. Mol. Imaging 2012, 39, 1144–1153. [Google Scholar] [CrossRef]
- Treglia, G.; Villani, M.F.; Giordano, A.; Rufini, V. Detection rate of recurrent medullary thyroid carcinoma using fluorine-18 fluorodeoxyglucose positron emission tomography: A meta-analysis. Endocrine 2012, 42, 535–545. [Google Scholar] [CrossRef]
- Treglia, G.; Kakhki, V.R.; Giovanella, L.; Sadeghi, R. Diagnostic performance of fluorine-18-fluorodeoxyglucose positron emission tomography in patients with Merkel cell carcinoma: A systematic review and meta-analysis. Am. J. Clin. Dermatol. 2013, 14, 437–447. [Google Scholar] [CrossRef]
- Treglia, G.; Tamburello, A.; Giovanella, L. Detection rate of somatostatin receptor PET in patients with recurrent medullary thyroid carcinoma: A systematic review and a meta-analysis. Hormones 2017, 16, 362–372. [Google Scholar] [CrossRef] [Green Version]
- Xia, J.; Zhang, H.; Hu, Q.; Liu, S.Y.; Zhang, L.Q.; Zhang, A.; Zhang, X.L.; Wang, Y.Q.; Liu, A.G. Comparison of diagnosing and staging accuracy of PET (CT) and MIBG on patients with neuroblastoma: Systemic review and meta-analysis. J. Huazhong Univ. Sci. Technol. Med. Sci. 2017, 37, 649–660. [Google Scholar] [CrossRef]
- Yang, J.; Kan, Y.; Ge, B.H.; Yuan, L.; Li, C.; Zhao, W. Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: A meta-analysis. Acta Radiol. 2014, 55, 389–398. [Google Scholar] [CrossRef]
- Zhu, D.; Wang, Y.; Wang, L.; Chen, J.; Byanju, S.; Zhang, H.; Liao, M. Prognostic value of the maximum standardized uptake value of pre-treatment primary lesions in small-cell lung cancer on 18F-FDG PET/CT: A meta-analysis. Acta Radiol. 2018, 59, 1082–1090. [Google Scholar] [CrossRef]
- July, M.; Santhanam, P.; Giovanella, L.; Treglia, G. Role of positron emission tomography imaging in Multiple Endocrine Neoplasia syndromes. Clin. Physiol. Funct. Imaging 2018, 38, 4–9. [Google Scholar] [CrossRef]
- Santhanam, P.; Taieb, D.; Giovanella, L.; Treglia, G. PET imaging in ectopic Cushing syndrome: A systematic review. Endocrine 2015, 50, 297–305. [Google Scholar] [CrossRef]
- Bozkurt, M.F.; Virgolini, I.; Balogova, S.; Beheshti, M.; Rubello, D.; Decristoforo, C.; Ambrosini, V.; Kjaer, A.; Delgado-Bolton, R.; Kunikowska, J.; et al. Guideline for PET/CT imaging of neuroendocrine neoplasms with 68Ga-DOTA-conjugated somatostatin receptor targeting peptides and 18F-DOPA. Eur. J. Nucl. Med. Mol. Imaging 2017, 44, 1588–1601. [Google Scholar] [CrossRef]
- Taïeb, D.; Hicks, R.J.; Hindié, E.; Guillet, B.A.; Avram, A.; Ghedini, P.; Timmers, H.J.; Scott, A.T.; Elojeimy, S.; Rubello, D.; et al. European Association of Nuclear Medicine Practice Guideline/Society of Nuclear Medicine and Molecular Imaging Procedure Standard 2019 for radionuclide imaging of phaeochromocytoma and paraganglioma. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 2112–2137. [Google Scholar] [CrossRef]
- Bar-Sever, Z.; Biassoni, L.; Shulkin, B.; Kong, G.; Hofman, M.S.; Lopci, E.; Manea, I.; Koziorowski, J.; Castellani, R.; Boubaker, A.; et al. Guidelines on nuclear medicine imaging in neuroblastoma. Eur. J. Nucl. Med. Mol. Imaging 2018, 45, 2009–2024. [Google Scholar] [CrossRef]
- Giovanella, L.; Treglia, G.; Iakovou, I.; Mihailovic, J.; Verburg, F.A.; Luster, M. EANM practice guideline for PET/CT imaging in medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 61–77. [Google Scholar] [CrossRef]
- Ambrosini, V.; Kunikowska, J.; Baudin, E.; Bodei, L.; Bouvier, C.; Capdevila, J.; Cremonesi, M.; de Herder, W.W.; Dromain, C.; Falconi, M.; et al. Consensus on molecular imaging and theranostics in neuroendocrine neoplasms. Eur. J. Cancer 2021, 146, 56–73. [Google Scholar] [CrossRef]
- Van Tinteren, H.; Hoekstra, O.S.; Boers, M. The need for Health Technology Assessments of PET. Eur. J. Nucl. Med. Mol. Imaging 2003, 30, 1438. [Google Scholar] [CrossRef]
- Fuchs, S.; Grössmann, N.; Ferch, M.; Busse, R.; Wild, C. Evidence-based indications for the planning of PET or PET/CT capacities are needed. Clin. Transl. Imaging 2019, 7, 65–81. [Google Scholar] [CrossRef] [Green Version]
- Froelich, M.F.; Schnitzer, M.L.; Holzgreve, A.; Gassert, F.G.; Gresser, E.; Overhoff, D.; Schwarze, V.; Fabritius, M.P.; Nörenberg, D.; von Münchhausen, N.; et al. Cost-Effectiveness Analysis of 68Ga DOTA-TATE PET/CT, 111In-Pentetreotide SPECT/CT and CT for Diagnostic Workup of Neuroendocrine Tumors. Diagnostics 2021, 11, 334. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Li, Q.; Li, L.; Wang, R.; Zou, K.; Tian, R.; Sun, X. Methodological quality of systematic reviews used in clinical practice guidelines: Focus on clinical imaging. Clin. Transl. Imaging 2021, 9, 373–382. [Google Scholar] [CrossRef]
- Yang, J.; Hao, R.; Zhu, X. Diagnostic role of 18F-dihydroxyphenylalanine positron emission tomography in patients with congenital hyperinsulinism: A meta-analysis. Nucl. Med. Commun. 2013, 34, 347–353. [Google Scholar] [CrossRef]
- Treglia, G.; Mirk, P.; Giordano, A.; Rufini, V. Diagnostic performance of fluorine-18-dihydroxyphenylalanine positron emission tomography in diagnosing and localizing the focal form of congenital hyperinsulinism: A meta-analysis. Pediatr. Radiol. 2012, 42, 1372–1379. [Google Scholar] [CrossRef]
- Blomberg, B.A.; Moghbel, M.C.; Saboury, B.; Stanley, C.A.; Alavi, A. The value of radiologic interventions and (18)F-DOPA PET in diagnosing and localizing focal congenital hyperinsulinism: Systematic review and meta-analysis. Mol. Imaging Biol. 2013, 15, 97–105. [Google Scholar] [CrossRef] [Green Version]
- Agrawal, K.; Padhy, B.M.; Meher, B.R.; Mohanty, R.R. Diagnostic utility of Ga-68 DOTA-SSTR and F-18 FDG PET/CT in the detection of culprit tumours causing osteomalacia: A systematic review and meta-analysis. Nucl. Med. Commun. 2021, 42, 646–655. [Google Scholar] [CrossRef]
- Jiang, Y.; Hou, G.; Cheng, W. Performance of 68Ga-DOTA-SST PET/CT, octreoscan SPECT/CT and 18F-FDG PET/CT in the detection of culprit tumors causing osteomalacia: A meta-analysis. Nucl. Med. Commun. 2020, 41, 370–376. [Google Scholar] [CrossRef]
- Meyer, M.; Nicod Lalonde, M.; Testart, N.; Jreige, M.; Kamani, C.; Boughdad, S.; Muoio, B.; Becce, F.; Schaefer, N.; Candrian, C.; et al. Detection Rate of Culprit Tumors Causing Osteomalacia Using Somatostatin Receptor PET/CT: Systematic Review and Meta-Analysis. Diagnostics 2019, 10, 2. [Google Scholar] [CrossRef] [Green Version]
Disease | PET Tracer | Ref. | Year | Studies (pts) Included in the Meta-Analysis | Pooled DR (95% CI) | Pooled Sensitivity (95% CI) | Pooled Specificity (95% CI) | AUC (95% CI) | Statistical Heterogeneity | Publication Bias |
---|---|---|---|---|---|---|---|---|---|---|
Suspected NETs | 68Ga-SSA | [31] | 2018 | 6 (598) | NR | pb: 91% (85–94) | pb: 94% (86–98) | NR | NR | No |
Thoracic and GEP-NETs | 68Ga-SSA | [34] | 2012 | 16 (567) | NR | pb: 93% (91–95) | pb: 91% (82–97) | pb: 0.96 | Yes | NR |
[15] | 2013 | 22 (2105) | NR | pb: 93% (91–94) | pb: 96% (95–98) | pb: 0.98 (0.95–1) | Yes | No | ||
[40] | 2014 | 10 (416) | NR | pb a: 93% (89–96) pb b: 96% (91–99) | pb a: 85% (74–93) pb b: 100% (82–100) | pb a: 0.96 pb b: 0.98 | Yes | NR | ||
[14] | 2016 | 17 (971) | NR | pb: 91% (81–96) | pb: 91% (78–96) | NR | Yes | No | ||
[23] | 2020 | 30 (3401) | NR | pb: 92% (89–95) lb: 95% (86–98) | pb: 91% (83–95) lb: 93% (83–97) | pb: 0.96 (0.94–0.98) lb: 0.98 (0.96–0.99) | Yes | Yes | ||
18F-FDOPA | [29] | 2013 | 8 (289) | NR | pb: 77% (71–82) | pb: 95% (87–98) | pb: 0.94 | Yes | NR | |
18F-FDG | [23] | 2020 | 30 (3401) | NR | pb: 70% (41–89) | pb: 97% (70–100) | pb: 0.94 (0.92–0.96) | Yes | No | |
P-NETs | 68Ga-SSA | [10] | 2020 | 18 (NR) | pb: 81% (65–90) lb: 92% (80–97) | pb: 80% (71–87) | pb: 95% (75–100) | NR | Yes | Yes |
Insulinomas | 68Ga-exendin-4 | [30] | 2021 | 16 (179) | NR | lb: 94% (NR) | lb: 83% (NR) | NR | NR | NR |
I-NETs | 68Ga-SSA | [28] | 2021 | 6 (112) | NR | pb: 88% (79–94) lb: 82% (63–94) | NR | NR | Yes | No |
18F-FDOPA | [28] | 2021 | 6 (112) | NR | pb: 83% (70–92) lb: 95% (89–99) | NR | NR | Yes | No | |
L-NETs | 68Ga-SSA | [18] | 2019 | 14 (352) | NR | pb: 90% (82–95) | NR | NR | Yes | NR |
18F-FDG | [18] | 2019 | 14 (352) | NR | pb: 71% (66–76) | NR | NR | Yes | NR | |
ED-SCLC | 18F-FDG | [24] | 2014 | 12 (369) | NR | pb: 97% (94–99) | pb: 98% (95–100) | pb: 0.98 | No | NR |
CUP-NETs | 68Ga-SSA | [13] | 2019 | 12 (383) | pb: 56% (48–63) | NR | NR | NR | Yes | No |
[25] | 2020 | 10 (484) | pb: 61% (53–69) | pb: 82% (63–92) | pb: 55% (31–77) | pb: 0.69 (0.65–0.73) | Yes | No | ||
PGL | 68Ga-SSA | [19] | 2018 | 17 (629) | NR | pb: 95% (92–97) lb: 96% (93–98) | pb: 87% (63–96) | pb: 0.88 (0.85–0.91) | Yes | No |
[16] | 2019 | 9 (215) | lb: 93% (91–95) | NR | NR | NR | No | Yes | ||
18F-FDOPA | [35] | 2012 | 11 (275) | NR | pb: 91% (87–94) lb: 79% (76–81) | pb: 95% (86–99) lb: 95% (84–99) | pb: 0.95 lb: 0.94 | Yes | NR | |
[29] | 2013 | 13 (401) | NR | pb: 92% (88–95) | pb: 92% (85–97) | pb: 0.95 | Yes | NR | ||
[16] | 2019 | 9 (215) | lb: 80% (69–88) | NR | NR | NR | No | Yes | ||
18F-FDG | [19] | 2018 | 17 (629) | NR | pb: 85% (78–91) lb: 83% (68–92) | pb: 55% (37–73) | pb: 0.78 (0.74–0.81) | Yes | No | |
[16] | 2019 | 9 (215) | lb: 74% (46–91) | NR | NR | NR | No | Yes | ||
NB | 18F-FDG | [32] | 2021 | 7 (127) | NR | pb: 78% (64–88) lb: 89% (81–94) | pb: 90% (79–97) lb: 78% (70–85) | pb: 0.94 | Yes | No |
Several | [39] | 2017 | 11 (1081) | NR | pb: 82% (75–88) lb: 90% (88–92) | pb: 70% (52–84) lb: 71% (63–79) | pb: 0.69 lb: 0.94 | No | No | |
[22] | 2020 | 11 (580) | NR | pb: 91% (86–94) | pb: 78% (66–86) | pb: 0.93 (0.90–0.95) | Yes | No | ||
rMTC | 68Ga-SSA | [38] | 2017 | 9 (152) | pb: 63% (49–77) | NR | NR | NR | Yes | NR |
18F-FDOPA | [33] | 2012 | 8 (146) | pb: 66% (58–74) lb: 71% (67–75) | NR | NR | NR | Yes | NR | |
[29] | 2013 | 8 (161) | NR | pb: 62% (54–69) | NR | NR | Yes | NR | ||
18F-FDG | [36] | 2012 | 24 (538) | pb: 59% (54–63) | NR | NR | NR | Yes | NR | |
[11] | 2012 | 15 (815) | NR | pb: 69% (64–74) | NR | NR | Yes | NR | ||
Several | [21] | 2020 | 14 (306) | NR | NR | NR | NR | Yes | No | |
MCC | 18F-FDG | [37] | 2013 | 6 (92) | NR | pb: 90% (80–96) | pb: 98% (90–100) | pb: 0.96 | No | No |
Disease | PET Tracer | Ref. | Year | Studies (pts) Included in the Meta-Analysis | Variable Assessed for Prognosis | Pooled OR for DCR (95% CI) | Pooled HR for PFS/EFS (95% CI) | Pooled HR for OS (95% CI) | Statistical Heterogeneity | Publication Bias |
---|---|---|---|---|---|---|---|---|---|---|
Thoracic and GEP-NETs | 68Ga-SSA | [20] | 2019 | 8 (474) | SUVmax | NR | 2.31 (1.34–4.0) | 2.97 (1.71–5.15) | Yes | Yes |
18F-FDG | [8] | 2021 | 12 (1492) | PET results (+/−) before PRRT | 4.85 (2.27–10.36) | 2.45 (1.48–4.04) | 2.25 (1.55–3.28) | Yes | Yes | |
[17] | 2021 | 23 (1799) | uptake (high/low) | NR | 2.84 (2.21–3.64) | 3.50 (2.75–4.45) | Yes | Yes | ||
SCLC | 18F-FDG | [41] | 2018 | 12 (1062) | metabolic parameters (SUVmax) | NR | 1.09 (1.02–1.17) | 1.13 (1.05–1.22) | No | No |
[27] | 2019 | 7 (680) | metabolic parameters (MTV, TLG) | NR | MTV: 2.78 (1.39–5.53) | MTV: 2.42 (1.46–4.03)TLG: 1.61(1.24–2.07) | Yes | NR | ||
[12] | 2021 | 19 (NR) | metabolic parameters (SUVmax, MTV) | NR | SUVmax: 1.24 (0.94–1.63) MTV: 3.22 (1.96–5.28) | SUVmax: 1.50 (1.17–1.91) MTV: 2.83 (2.00–4.01) | Yes | Yes |
Disease | PET Tracer | Ref. | Year | Studies (pts) Included in the Meta-Analysis | Pooled Change of Management (95% CI) | Statistical Heterogeneity | Publication Bias |
---|---|---|---|---|---|---|---|
Thoracic and GEP-NETs | 68Ga-SSA | [9] | 2017 | 14 (1561) | 44% (36–51) | Yes | NR |
[31] | 2018 | 9 (NR) | 45% (36–55) | Yes | NR | ||
CUP-NETs | 68Ga-SSA | [13] | 2019 | 4 (114) | 20% (9–33) | Yes | No |
SCLC | 18F-FDG | [26] | 2020 | 6 (277) | 15% (9–21) | Yes | No |
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Treglia, G.; Sadeghi, R.; Giovinazzo, F.; Galiandro, F.; Annunziata, S.; Muoio, B.; Kroiss, A.S. PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms: An Umbrella Review of Published Meta-Analyses. Cancers 2021, 13, 5172. https://doi.org/10.3390/cancers13205172
Treglia G, Sadeghi R, Giovinazzo F, Galiandro F, Annunziata S, Muoio B, Kroiss AS. PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms: An Umbrella Review of Published Meta-Analyses. Cancers. 2021; 13(20):5172. https://doi.org/10.3390/cancers13205172
Chicago/Turabian StyleTreglia, Giorgio, Ramin Sadeghi, Francesco Giovinazzo, Federica Galiandro, Salvatore Annunziata, Barbara Muoio, and Alexander Stephan Kroiss. 2021. "PET with Different Radiopharmaceuticals in Neuroendocrine Neoplasms: An Umbrella Review of Published Meta-Analyses" Cancers 13, no. 20: 5172. https://doi.org/10.3390/cancers13205172