Summary
Nuclear medicine has been implicated in the diagnosis and treatment of endocrine disorders for several decades. With recent development of PET tracers, functional imaging now plays a major role in endocrine tumors enabling with high performance to their localization, characterization, and staging. Besides 18F-FDG, which may be used in the management and follow-up of endocrine tumors, new tracers have emerged, such as 18F-DOPA for neuroendocrine tumors (NETs) (medullary thyroid carcinoma, pheochromocytomas and paragangliomas and well-differentiated NETs originating from the midgut) and 18F-Choline in the field of primary hyperparathyroidism. Moreover, some peptides such as somatostatin analogs can also be used for peptide receptor radionuclide therapy. In this context, Gallium-68 labeled somatostatin analogs (68Ga-SSA) can help to tailor therapeutic choices and follow the response to treatment in the so-called “theranostic” approach. This review emphasizes the usefulness of these three novel PET tracers (18F-Choline, 18F-FDOPA, and 68Ga-SSA) for primary hyperparathyroidism and neuroendocrine tumors.
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References
R. Boellaard, R. Delgado-Bolton, W.J.G. Oyen et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur. J. Nucl. Med Mol. Imaging 42, 328–354 (2015). https://doi.org/10.1007/s00259-014-2961-x
V. Cuccurullo, G.D. Di Stasio, L. Evangelista, G. Castoria, L. Mansi, Biochemical and pathophysiological premises to positron emission tomography with Choline radiotracers. J. Cell. Physiol. 232, 270–275 (2017). https://doi.org/10.1002/jcp.25478
C. Lussey-Lepoutre, E. Hindié, F. Montravers et al. The current role of 18F-FDOPA PET for neuroendocrine tumor imaging. Médecine Nucl. 40, 20–30 (2016). https://doi.org/10.1016/j.mednuc.2016.01.003
J.J.M. Teunissen, D.J. Kwekkeboom, R. Valkema, E.P. Krenning, Nuclear medicine techniques for the imaging and treatment of neuroendocrine tumours. Endocr. Relat. Cancer 18(Suppl 1), S27–S51 (2011). https://doi.org/10.1530/ERC-10-0282
I.M. Modlin, K. Oberg, D.C. Chung et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 9, 61–72 (2008). https://doi.org/10.1016/S1470-2045(07)70410-2
J.-Y. Scoazec, A. Couvelard, Ppour le réseau TENpath (réseau national d’expertise pour le diagnostic anatomopathologique des tumeurs neuroendocrines malignes de l’adulte, sporadiques et familiales). [The new WHO classification of digestive neuroendocrine tumors]. Ann. Pathol. 31, 88–92 (2011). https://doi.org/10.1016/j.annpat.2011.01.001
A. Dolcetta-Capuzzo, V. Villa, L. Albarello et al. Gastroenteric neuroendocrine neoplasms classification: comparison of prognostic models. Cancer 119, 36–44 (2013). https://doi.org/10.1002/cncr.27716
G. Klöppel, Neuroendocrine neoplasms: dichotomy, origin and classifications. Visc. Med. 33, 324–330 (2017). https://doi.org/10.1159/000481390
J. Strosberg, G. El-Haddad, E. Wolin et al. Phase 3 trial of 177Lu-Dotatate for midgut neuroendocrine tumors. N. Engl. J. Med. 376, 125–135 (2017). https://doi.org/10.1056/NEJMoa1607427
M.M. Graham, X. Gu, T. Ginader, P. Breheny, J.J. Sunderland, 68Ga-DOTATOC imaging of neuroendocrine tumors: a systematic review and metaanalysis. J. Nucl. Med. 58, 1452–1458 (2017). https://doi.org/10.2967/jnumed.117.191197
S.A. Deppen, J. Blume, A.J. Bobbey et al. 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. 57, 872–878 (2016). https://doi.org/10.2967/jnumed.115.165803
F. Montravers, D. Grahek, K. Kerrou et al. Can fluorodihydroxyphenylalanine PET replace somatostatin receptor scintigraphy in patients with digestive endocrine tumors? J. Nucl. Med. 47, 1455–1462 (2006)
A. Imperiale, E. Rust, S. Gabriel et al. 18F-fluorodihydroxyphenylalanine PET/CT in patients with neuroendocrine tumors of unknown origin: relation to tumor origin and differentiation. J. Nucl. Med. 55, 367–372 (2014). https://doi.org/10.2967/jnumed.113.126896
M. Fani, G.P. Nicolas, D. Wild, Somatostatin receptor antagonists for imaging and therapy. J. Nucl. Med. 58(Suppl 2), 61S–66S (2017). https://doi.org/10.2967/jnumed.116.186783
G.P. Nicolas, N. Schreiter, F. Kaul et al. Sensitivity comparison of 68Ga-OPS202 and 68Ga-DOTATOC PET/CT in patients with gastroenteropancreatic neuroendocrine tumors: a prospective phase II imaging study. J. Nucl. Med. 59, 915–921 (2018). https://doi.org/10.2967/jnumed.117.199760
T.R. Halfdanarson, K.G. Rabe, J. Rubin, G.M. Petersen, Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann. Oncol. J. Eur. Soc. Med Oncol. 19, 1727–1733 (2008). https://doi.org/10.1093/annonc/mdn351
H. Ahlström, B. Eriksson, M. Bergström, P. Bjurling, B. Långström, K. Oberg, Pancreatic neuroendocrine tumors: diagnosis with PET. Radiology 195, 333–337 (1995). https://doi.org/10.1148/radiology.195.2.7724749
F. Montravers, K. Kerrou, V. Nataf et al. Impact of fluorodihydroxyphenylalanine-18F positron emission tomography on management of adult patients with documented or occult digestive endocrine tumors. J. Clin. Endocrinol. Metab. 94, 1295–1301 (2009). https://doi.org/10.1210/jc.2008-1349
O.C. Neels, K.P. Koopmans, P.L. Jager et al. Manipulation of [11C]-5-hydroxytryptophan and 6-[18F]fluoro-3,4-dihydroxy-L-phenylalanine accumulation in neuroendocrine tumor cells. Cancer Res. 68, 7183–7190 (2008). https://doi.org/10.1158/0008-5472.CAN-08-0095
S. Kauhanen, M. Seppänen, P. Nuutila, Premedication with carbidopa masks positive finding of insulinoma and beta-cell hyperplasia in [(18)F]-dihydroxy-phenyl-alanine positron emission tomography. J. Clin. Oncol. Oncol. 26, 5307–5308 (2008). https://doi.org/10.1200/JCO.2008.18.8581. author reply5308-5309
A. Imperiale, F. Sebag, M. Vix et al. 18F-FDOPA PET/CT imaging of insulinoma revisited. Eur. J. Nucl. Med. Mol. Imaging 42, 409–418 (2015). https://doi.org/10.1007/s00259-014-2943-z
A. Imperiale, T. Bahougne, B. Goichot, P. Bachellier, D. Taïeb, I.J. Namer, Dynamic 18F-FDOPA PET findings after carbidopa premedication in 2 adult patients with insulinoma-related hyperinsulinemic hypoglycemia. Clin. Nucl. Med. 40, 682–684 (2015). https://doi.org/10.1097/RLU.0000000000000686
A. Imperiale, P. Addeo, G. Averous, I.J. Namer, P. Bachellier, Solid pseudopapillary pancreatic tumor mimicking a neuroendocrine neoplasm on 18F-FDOPA PET/CT. J. Clin. Endocrinol. Metab. 98, 2643–2644 (2013). https://doi.org/10.1210/jc.2013-1942
R. Kumar, P. Sharma, P. Garg et al. Role of (68)Ga-DOTATOC PET-CT in the diagnosis and staging of pancreatic neuroendocrine tumours. Eur. Radiol. 21, 2408–2416 (2011). https://doi.org/10.1007/s00330-011-2199-y
C. Schmid-Tannwald, C.M. Schmid-Tannwald, J.N. Morelli et al. Comparison of abdominal MRI with diffusion-weighted imaging to 68Ga-DOTATATE PET/CT in detection of neuroendocrine tumors of the pancreas. Eur. J. Nucl. Med. Mol. Imaging 40, 897–907 (2013). https://doi.org/10.1007/s00259-013-2371-5
P. Sharma, S. Arora, V.S. Dhull et al. Evaluation of (68)Ga-DOTANOC PET/CT imaging in a large exclusive population of pancreatic neuroendocrine tumors. Abdom. Imaging 40, 299–309 (2015). https://doi.org/10.1007/s00261-014-0219-5
P. Sharma, S. Arora, S. Karunanithi et al. Somatostatin receptor based PET/CT imaging with 68Ga-DOTA-Nal3-octreotide for localization of clinically and biochemically suspected insulinoma. Q J. Nucl. Med Mol. Imaging 60, 69–76 (2016)
V. Prasad, A. Sainz-Esteban, R. Arsenic et al. Role of (68)Ga somatostatin receptor PET/CT in the detection of endogenous hyperinsulinaemic focus: an explorative study. Eur. J. Nucl. Med. Mol. Imaging 43, 1593–1600 (2016). https://doi.org/10.1007/s00259-016-3331-7
J. Bertherat, F. Tenenbaum, K. Perlemoine et al. Somatostatin receptors 2 and 5 are the major somatostatin receptors in insulinomas: an in vivo and in vitro study. J. Clin. Endocrinol. Metab. 88, 5353–5360 (2003). https://doi.org/10.1210/jc.2002-021895
Y. Luo, Q. Pan, S. Yao et al. Glucagon-like peptide-1 receptor PET/CT with 68Ga-NOTA-exendin-4 for detecting localized insulinoma: a prospective cohort study. J. Nucl. Med. 57, 715–720 (2016). https://doi.org/10.2967/jnumed.115.167445
E. Christ, D. Wild, S. Ederer et al. Glucagon-like peptide-1 receptor imaging for the localisation of insulinomas: a prospective multicentre imaging study. Lancet Diabetes Endocrinol. 1, 115–122 (2013). https://doi.org/10.1016/S2213-8587(13)70049-4
K. Antwi, M. Fani, T. Heye et al. Comparison of glucagon-like peptide-1 receptor (GLP-1R) PET/CT, SPECT/CT and 3T MRI for the localisation of occult insulinomas: evaluation of diagnostic accuracy in a prospective crossover imaging study. Eur. J. Nucl. Med. Mol. Imaging 45, 2318–2327 (2018). https://doi.org/10.1007/s00259-018-4101-5
A. Haug, C.J. Auernhammer, B. Wängler et al. Intraindividual comparison of 68Ga-DOTA-TATE and 18F-DOPA PET in patients with well-differentiated metastatic neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 36, 765–770 (2009). https://doi.org/10.1007/s00259-008-1030-8
D. Putzer, M. Gabriel, D. Kendler et al. Comparison of (68)Ga-DOTA-Tyr(3)-octreotide and (18)F-fluoro-L-dihydroxyphenylalanine positron emission tomography in neuroendocrine tumor patients. Q J. Nucl. Med Mol. Imaging 54, 68–75 (2010)
N. Naswa, P. Sharma, R. Soundararajan et al. Diagnostic performance of somatostatin receptor PET/CT using 68Ga-DOTANOC in gastrinoma patients with negative or equivocal CT findings. Abdom. Imaging 38, 552–560 (2013). https://doi.org/10.1007/s00261-012-9925-z
M. Anlauf, B. Sipos, I. Boeck et al. [Neuroendocrine neoplasms of the distal jejunum and ileum]. Pathology 35, 283–293 (2014). https://doi.org/10.1007/s00292-013-1888-5. quiz 294
S. Balogova, J.-N. Talbot, V. Nataf et al. 18F-fluorodihydroxyphenylalanine vs other radiopharmaceuticals for imaging neuroendocrine tumours according to their type. Eur. J. Nucl. Med. Mol. Imaging 40, 943–966 (2013). https://doi.org/10.1007/s00259-013-2342-x
K.P. Koopmans, E.G.E. de Vries, I.P. Kema et al. Staging of carcinoid tumours with 18F-DOPA PET: a prospective, diagnostic accuracy study. Lancet Oncol. 7, 728–734 (2006). https://doi.org/10.1016/S1470-2045(06)70801-4
H. Ilhan, W.P. Fendler, C.C. Cyran et al. Impact of (68)Ga-DOTATATE PET/CT on the surgical management of primary neuroendocrine tumors of the pancreas or ileum. Ann. Surg. Oncol. 22, 164–171 (2015). https://doi.org/10.1245/s10434-014-3981-2
V. Ambrosini, P. Tomassetti, P. Castellucci et al. Comparison between 68Ga-DOTA-NOC and 18F-DOPA PET for the detection of gastro-entero-pancreatic and lung neuro-endocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 35, 1431–1438 (2008). https://doi.org/10.1007/s00259-008-0769-2
T. Binderup, U. Knigge, A. Loft et al. Functional imaging of neuroendocrine tumors: a head-to-head comparison of somatostatin receptor scintigraphy, 123I-MIBG scintigraphy, and 18F-FDG PET. J. Nucl. Med.51, 704–712 (2010). https://doi.org/10.2967/jnumed.109.069765
T.H. Tan, C.Y. Boey, B.N. Lee, Impact of 68Ga-DOTA-peptide PET/CT on the management of gastrointestinal neuroendocrine tumour (GI-NET): Malaysian National Referral Centre Experience. Nucl. Med. Mol. Imaging 52, 119–124 (2018). https://doi.org/10.1007/s13139-017-0496-3
T. Belhocine, J. Foidart, P. Rigo et al. Fluorodeoxyglucose positron emission tomography and somatostatin receptor scintigraphy for diagnosing and staging carcinoid tumours: correlations with the pathological indexes p53 and Ki-67. Nucl. Med. Commun. 23, 727–734 (2002)
E. Rust, F. Hubele, E. Marzano et al. Nuclear medicine imaging of gastro-entero-pancreatic neuroendocrine tumors. The key role of cellular differentiation and tumor grade: from theory to clinical practice. Cancer Imaging. 12, 173–184 (2012). https://doi.org/10.1102/1470-7330.2012.0026
R. Abgral, S. Leboulleux, D. Déandreis et al. Performance of (18)fluorodeoxyglucose-positron emission tomography and somatostatin receptor scintigraphy for high Ki67 ( ≥ 10%) well-differentiated endocrine carcinoma staging. J. Clin. Endocrinol. Metab. 96, 665–671 (2011). https://doi.org/10.1210/jc.2010-2022
G. Luo, Z. Liu, M. Guo et al. (18)F-FDG PET/CT can be used to detect non-functioning pancreatic neuroendocrine tumors. Int. J. Oncol. 45, 1531–1536 (2014). https://doi.org/10.3892/ijo.2014.2570
S. Partelli, M. Rinzivillo, A. Maurizi et al. The role of combined Ga-DOTANOC and (18)FDG PET/CT in the management of patients with pancreatic neuroendocrine tumors. Neuroendocrinology 100, 293–299 (2014). https://doi.org/10.1159/000368609
E. Garin, F. Le Jeune, A. Devillers et al. Predictive value of 18F-FDG PET and somatostatin receptor scintigraphy in patients with metastatic endocrine tumors. J. Nucl. Med. 50, 858–864 (2009). https://doi.org/10.2967/jnumed.108.057505
M. Bucau, A. Laurent-Bellue, N. Poté et al. 18F-FDG uptake in well-differentiated neuroendocrine tumors correlates with both Ki-67 and VHL pathway inactivation. Neuroendocrinology 106, 274–282 (2018). https://doi.org/10.1159/000480239
E.M. Tabaksblat, S.W. Langer, U. Knigge et al. Diagnosis and treatment of bronchopulmonary neuroendocrine tumours: state of the art. Acta Oncol. Stockh. Swed. 55, 3–14 (2016). https://doi.org/10.3109/0284186X.2015.1067715
B.I. Gustafsson, M. Kidd, A. Chan, M.V. Malfertheiner, I.M. Modlin, Bronchopulmonary neuroendocrine tumors. Cancer 113, 5–21 (2008). https://doi.org/10.1002/cncr.23542
C. Ansquer, D. Taieb, F. Montravers, F. Tenenbaum, PET imaging with 68 gallium labelled somatostatin analogues in the evaluation of neuroendocrine tumours (NETs). http://www.em-consulte.com/en/article/963107. Accessed 16 June 2018.
M.F. Bozkurt, I. Virgolini, S. Balogova 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 44, 1588–1601 (2017). https://doi.org/10.1007/s00259-017-3728-y
M. Rodrigues, T. Traub-Weidinger, S. Li, B. Ibi, I. Virgolini, Comparison of 111In-DOTA-DPhe1-Tyr3-octreotide and 111In-DOTA-lanreotide scintigraphy and dosimetry in patients with neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 33, 532–540 (2006). https://doi.org/10.1007/s00259-005-0020-3
V. Ambrosini, P. Castellucci, D. Rubello et al. 68Ga-DOTA-NOC: a new PET tracer for evaluating patients with bronchial carcinoid. Nucl. Med. Commun. 30, 281–286 (2009). https://doi.org/10.1097/MNM.0b013e32832999c1
G. Treglia, P. Castaldi, G. Rindi, A. Giordano, V. Rufini, Diagnostic performance of Gallium-68 somatostatin receptor PET and PET/CT in patients with thoracic and gastroenteropancreatic neuroendocrine tumours: a meta-analysis. Endocrine 42, 80–87 (2012). https://doi.org/10.1007/s12020-012-9631-1
K. Oberg, Molecular imaging radiotherapy: theranostics for personalized patient management of neuroendocrine tumors (NETs). Theranostics 2, 448–458 (2012). https://doi.org/10.7150/thno.3931
I. Kayani, B.G. Conry, A.M. Groves et al. A comparison of 68Ga-DOTATATE and 18F-FDG PET/CT in pulmonary neuroendocrine tumors. J. Nucl. Med. 50, 1927–1932 (2009). https://doi.org/10.2967/jnumed.109.066639
T. Jindal, A. Kumar, B. Venkitaraman et al. Evaluation of the role of [18F]FDG-PET/CT and [68Ga]DOTATOC-PET/CT in differentiating typical and atypical pulmonary carcinoids. Cancer Imaging 11, 70–75 (2011). https://doi.org/10.1102/1470-7330.2011.0010
B. Venkitaraman, S. Karunanithi, A. Kumar, G.C. Khilnani, R. Kumar, Role of 68Ga-DOTATOC PET/CT in initial evaluation of patients with suspected bronchopulmonary carcinoid. Eur. J. Nucl. Med. Mol. Imaging 41, 856–864 (2014). https://doi.org/10.1007/s00259-013-2659-5
N. Pandit, M. Gonen, L. Krug, S.M. Larson, Prognostic value of [18F]FDG-PET imaging in small cell lung cancer. Eur. J. Nucl. Med. Mol. Imaging 30, 78–84 (2003). https://doi.org/10.1007/s00259-002-0937-8
U.-F. Pape, A. Perren, B. Niederle et al. ENETS Consensus Guidelines for the management of patients with neuroendocrine neoplasms from the jejuno-ileum and the appendix including goblet cell carcinomas. Neuroendocrinology 95, 135–156 (2012). https://doi.org/10.1159/000335629
G. Capurso, M. Rinzivillo, R. Bettini, L. Boninsegna, G. Delle Fave, M. Falconi, Systematic review of resection of primary midgut carcinoid tumour in patients with unresectable liver metastases. Br. J. Surg. 99, 1480–1486 (2012). https://doi.org/10.1002/bjs.8842
M.D. Miljković, M. Girotra, R.R. Abraham, R.B. Erlich, Novel medical therapies of recurrent and metastatic gastroenteropancreatic neuroendocrine tumors. Dig. Dis. Sci. 57, 9–18 (2012). https://doi.org/10.1007/s10620-011-1854-0
V. Prasad, V. Ambrosini, M. Hommann, D. Hoersch, S. Fanti, R.P. Baum, Detection of unknown primary neuroendocrine tumours (CUP-NET) using (68)Ga-DOTA-NOC receptor PET/CT. Eur. J. Nucl. Med. Mol. Imaging 37, 67–77 (2010). https://doi.org/10.1007/s00259-009-1205-y
N. Naswa, P. Sharma, A. Kumar et al. 68Ga-DOTANOC PET/CT in patients with carcinoma of unknown primary of neuroendocrine origin. Clin. Nucl. Med. 37, 245–251 (2012). https://doi.org/10.1097/RLU.0b013e31823ea730
O. Alonso, M. Rodríguez-Taroco, E. Savio, C. Bentancourt, J.P. Gambini, H. Engler, 68)Ga-DOTATATE PET/CT in the evaluation of patients with neuroendocrine metastatic carcinoma of unknown origin. Ann. Nucl. Med. 28, 638–645 (2014). https://doi.org/10.1007/s12149-014-0856-3
G. Treglia, C. Aktolun, A. Chiti et al. The 2015 Revised American Thyroid Association guidelines for the management of medullary thyroid carcinoma: the “evidence-based” refusal to endorse them by EANM due to the “not evidence-based” marginalization of the role of Nuclear Medicine. Eur. J. Nucl. Med. Mol. Imaging 43, 1486–1490 (2016). https://doi.org/10.1007/s00259-016-3404-7
S. Leboulleux, E. Baudin, J.-P. Travagli, M. Schlumberger, Medullary thyroid carcinoma. Clin. Endocrinol. (Oxf.). 61, 299–310 (2004). https://doi.org/10.1111/j.1365-2265.2004.02037.x
A.L. Giraudet, D. Vanel, S. Leboulleux et al. Imaging medullary thyroid carcinoma with persistent elevated calcitonin levels. J. Clin. Endocrinol. Metab. 92, 4185–4190 (2007). https://doi.org/10.1210/jc.2007-1211
G. Treglia, P. Castaldi, M.F. Villani et al. Comparison of 18F-DOPA, 18F-FDG and 68Ga-somatostatin analogue PET/CT in patients with recurrent medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 39, 569–580 (2012). https://doi.org/10.1007/s00259-011-2031-6
A.R. Romero-Lluch, J.I. Cuenca-Cuenca, R. Guerrero-Vázquez et al. Diagnostic utility of PET/CT with 18F-DOPA and 18F-FDG in persistent or recurrent medullary thyroid carcinoma: the importance of calcitonin and carcinoembryonic antigen cutoff. Eur. J. Nucl. Med. Mol. Imaging 44, 2004–2013 (2017). https://doi.org/10.1007/s00259-017-3759-4
H.H.G. Verbeek, J.T.M. Plukker, K.P. Koopmans et al. Clinical relevance of 18F-FDG PET and 18F-DOPA PET in recurrent medullary thyroid carcinoma. J. Nucl. Med. 53, 1863–1871 (2012). https://doi.org/10.2967/jnumed.112.105940
F. Caobelli, A. Chiaravalloti, L. Evangelista et al. Predictive and prognostic value of 18F-DOPA PET/CT in patients affected by recurrent medullary carcinoma of the thyroid. Ann. Nucl. Med. 32, 7–15 (2018). https://doi.org/10.1007/s12149-017-1213-0
A. Archier, C. Heimburger, C. Guerin et al. 18)F-DOPA PET/CT in the diagnosis and localization of persistent medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 43, 1027–1033 (2016). https://doi.org/10.1007/s00259-015-3227-y
A. Sesti, M. Mayerhoefer, M. Weber et al. Relevance of calcitonin cut-off in the follow-up of medullary thyroid carcinoma for conventional imaging and 18-fluorine-fluorodihydroxyphenylalanine PET. Anticancer Res. 34, 6647–6654 (2014)
S. Kauhanen, C. Schalin-Jäntti, M. Seppänen et al. Complementary roles of 18F-DOPA PET/CT and 18F-FDG PET/CT in medullary thyroid cancer. J. Nucl. Med. 52, 1855–1863 (2011). https://doi.org/10.2967/jnumed.111.094771
M. Luster, W. Karges, K. Zeich et al. Clinical value of 18-fluorine-fluorodihydroxyphenylalanine positron emission tomography/computed tomography in the follow-up of medullary thyroid carcinoma. Thyroid 20, 527–533 (2010). https://doi.org/10.1089/thy.2009.0342
M.C. Marzola, M.R. Pelizzo, M. Ferdeghini et al. Dual PET/CT with (18)F-DOPA and (18)F-FDG in metastatic medullary thyroid carcinoma and rapidly increasing calcitonin levels: comparison with conventional imaging. Eur. J. Surg. Oncol. 36, 414–421 (2010). https://doi.org/10.1016/j.ejso.2010.01.001
M. Beheshti, S. Pöcher, R. Vali et al. The value of 18F-DOPA PET-CT in patients with medullary thyroid carcinoma: comparison with 18F-FDG PET-CT. Eur. Radiol. 19, 1425–1434 (2009). https://doi.org/10.1007/s00330-008-1280-7
K.P. Koopmans, J.W.B. de Groot, J.T.M. Plukker et al. 18F-dihydroxyphenylalanine PET in patients with biochemical evidence of medullary thyroid cancer: relation to tumor differentiation. J. Nucl. Med. 49, 524–531 (2008). https://doi.org/10.2967/jnumed.107.047720
B. Beuthien-Baumann, A. Strumpf, J. Zessin, J. Bredow, J. Kotzerke, Diagnostic impact of PET with 18F-FDG, 18F-DOPA and 3-O-methyl-6-[18F]fluoro-DOPA in recurrent or metastatic medullary thyroid carcinoma. Eur. J. Nucl. Med. Mol. Imaging 34, 1604–1609 (2007). https://doi.org/10.1007/s00259-007-0425-2
S. Hoegerle, C. Altehoefer, N. Ghanem, I. Brink, E. Moser, E. Nitzsche, 18F-DOPA positron emission tomography for tumour detection in patients with medullary thyroid carcinoma and elevated calcitonin levels. Eur. J. Nucl. Med. 28, 64–71 (2001)
G. Treglia, V. Rufini, M. Salvatori, A. Giordano, L. Giovanella, PET imaging in recurrent medullary thyroid carcinoma. Int. J. Mol. Imaging 2012, 324686 (2012). https://doi.org/10.1155/2012/324686
K. Slavikova, F. Montravers, G. Treglia et al. What is currently the best radiopharmaceutical for the hybrid PET/CT detection of recurrent medullary thyroid carcinoma? Curr. Radiopharm. 6, 96–105 (2013)
M. Soussan, V. Nataf, K. Kerrou et al. Added value of early 18F-FDOPA PET/CT acquisition time in medullary thyroid cancer. Nucl. Med. Commun. 33, 775–779 (2012). https://doi.org/10.1097/MNM.0b013e3283543304
S.A. Wells, S.L. Asa, H. Dralle et al. Revised American Thyroid Association guidelines for the management of medullary thyroid carcinoma. Thyroid J. Am. Thyroid Assoc. 25, 567–610 (2015). https://doi.org/10.1089/thy.2014.0335
American Thyroid Association Guidelines Task Force, R.T. Kloos, C. Eng et al. Medullary thyroid cancer: management guidelines of the American Thyroid Association. Thyroid J. Am. Thyroid Assoc. 19, 565–612 (2009). https://doi.org/10.1089/thy.2008.0403
A. Oudoux, P.-Y. Salaun, C. Bournaud et al. Sensitivity and prognostic value of positron emission tomography with F-18-fluorodeoxyglucose and sensitivity of immunoscintigraphy in patients with medullary thyroid carcinoma treated with anticarcinoembryonic antigen-targeted radioimmunotherapy. J. Clin. Endocrinol. Metab. 92, 4590–4597 (2007). https://doi.org/10.1210/jc.2007-0938
J. Barbet, L. Campion, F. Kraeber-Bodéré, J.-F. Chatal; GTE Study Group, Prognostic impact of serum calcitonin and carcinoembryonic antigen doubling-times in patients with medullary thyroid carcinoma. J. Clin. Endocrinol. Metab. 90, 6077–6084 (2005). https://doi.org/10.1210/jc.2005-0044
K. Pacak, S.H. Tella, Pheochromocytoma and Paraganglioma. ed. by L.J. De Groot, G. Chrousos, K. Dungan et al. Endotext. (MDText.com, Inc., South Dartmouth (MA), 2000). http://www.ncbi.nlm.nih.gov/books/NBK481899/. Accessed 12 June 2018.
L. Amar, A. Servais, A.-P. Gimenez-Roqueplo, F. Zinzindohoue, G. Chatellier, P.-F. Plouin, Year of diagnosis, features at presentation, and risk of recurrence in patients with pheochromocytoma or secreting paraganglioma. J. Clin. Endocrinol. Metab. 90, 2110–2116 (2005). https://doi.org/10.1210/jc.2004-1398
R.A. DeLellis, R.V. Lloyd, P.U. Heitz, World Health Organization classification of tumours pathology & genetics. Tumours Endocr. Organs. 151–155 (2004).
J. Favier, L. Amar, A.-P. Gimenez-Roqueplo, Paraganglioma and phaeochromocytoma: from genetics to personalized medicine. Nat. Rev. Endocrinol. 11, 101–111 (2015). https://doi.org/10.1038/nrendo.2014.188
D. Taïeb, K. Pacak, Molecular imaging and theranostic approaches in pheochromocytoma and paraganglioma. Cell Tissue Res. 372, 393–401 (2018). https://doi.org/10.1007/s00441-018-2791-4
D. Taïeb, H.J. Timmers, E. Hindié et al., EANM 2012 guidelines for radionuclide imaging of phaeochromocytoma and paraganglioma. Eur. J. Nucl. Med. Mol. Imaging 39, 1977–1995 (2012). https://doi.org/10.1007/s00259-012-2215-8
F. Pacini, M.G. Castagna, L. Brilli, G. Pentheroudakis; ESMO Guidelines Working Group, Thyroid cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 23(Suppl 7), vii110–vii119 (2012). https://doi.org/10.1093/annonc/mds230
G. Treglia, F. Cocciolillo, C. de Waure et al. Diagnostic performance of 18F-dihydroxyphenylalanine positron emission tomography in patients with paraganglioma: a meta-analysis. Eur. J. Nucl. Med. Mol. Imaging 39, 1144–1153 (2012). https://doi.org/10.1007/s00259-012-2087-y
S. Hoegerle, N. Ghanem, C. Altehoefer et al. 18F-DOPA positron emission tomography for the detection of glomus tumours. Eur. J. Nucl. Med. Mol. Imaging 30, 689–694 (2003). https://doi.org/10.1007/s00259-003-1115-3
Timmers HJLM, C.C. Chen, J.A. Carrasquillo et al. Comparison of 18F-fluoro-L-DOPA, 18F-fluoro-deoxyglucose, and 18F-fluorodopamine PET and 123I-MIBG scintigraphy in the localization of pheochromocytoma and paraganglioma. J. Clin. Endocrinol. Metab. 94, 4757–4767 (2009). https://doi.org/10.1210/jc.2009-1248
I. Janssen, C.C. Chen, D. Taieb et al. 68Ga-DOTATATE PET/CT in the localization of head and neck paragangliomas compared with other functional imaging modalities and CT/MRI. J. Nucl. Med. 57, 186–191 (2016). https://doi.org/10.2967/jnumed.115.161018
A. Archier, A. Varoquaux, P. Garrigue et al. Prospective comparison of (68)Ga-DOTATATE and (18)F-FDOPA PET/CT in patients with various pheochromocytomas and paragangliomas with emphasis on sporadic cases. Eur. J. Nucl. Med. Mol. Imaging 43, 1248–1257 (2016). https://doi.org/10.1007/s00259-015-3268-2
A. Kroiss, D. Putzer, A. Frech et al. A retrospective comparison between 68Ga-DOTA-TOC PET/CT and 18F-DOPA PET/CT in patients with extra-adrenal paraganglioma. Eur. J. Nucl. Med. Mol. Imaging 40, 1800–1808 (2013). https://doi.org/10.1007/s00259-013-2548-y
I. Janssen, E.M. Blanchet, K. Adams et al. Superiority of [68Ga]-DOTATATE PET/CT to other functional imaging modalities in the localization of SDHB-associated metastatic pheochromocytoma and paraganglioma. Clin. Cancer Res. 21, 3888–3895 (2015). https://doi.org/10.1158/1078-0432.CCR-14-2751
C. Lepoutre-Lussey, C. Caramella, F. Bidault et al. Screening in asymptomatic SDHx mutation carriers: added value of 18F-FDG PET/CT at initial diagnosis and 1-year follow-up. Eur. J. Nucl. Med. Mol. Imaging 42, 868–876 (2015). https://doi.org/10.1007/s00259-015-3003-z
J.P. Bilezikian, L. Bandeira, A. Khan, N.E. Cusano, Hyperparathyroidism. Lancet Lond. Engl. 391, 168–178 (2018). https://doi.org/10.1016/S0140-6736(17)31430-7
J.P. Bilezikian, M.L. Brandi, R. Eastell et al. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the Fourth International Workshop. J. Clin. Endocrinol. Metab. 99, 3561–3569 (2014). https://doi.org/10.1210/jc.2014-1413
A.A. Khan, D.A. Hanley, R. Rizzoli et al. Primary hyperparathyroidism: review and recommendations on evaluation, diagnosis, and management. A Canadian and international consensus. Osteoporos. Int J. Establ Result Coop. Eur. Found. Osteoporos. Natl. Osteoporos. Found. USA 28, 1–19 (2017). https://doi.org/10.1007/s00198-016-3716-2
A.M. Laird, S.K. Libutti, Minimally invasive parathyroidectomy versus bilateral neck exploration for primary hyperparathyroidism. Surg. Oncol. Clin. N. Am. 25, 103–118 (2016). https://doi.org/10.1016/j.soc.2015.08.012
J.M. Ruda, C.S. Hollenbeak, B.C. Stack, A systematic review of the diagnosis and treatment of primary hyperparathyroidism from 1995 to 2003. Otolaryngol. Head Neck Surg. 132, 359–372 (2005). https://doi.org/10.1016/j.otohns.2004.10.005
C.-Y. Lo, B.H. Lang, W.F. Chan, A.W.C. Kung, K.S.L. Lam, A prospective evaluation of preoperative localization by technetium-99m sestamibi scintigraphy and ultrasonography in primary hyperparathyroidism. Am. J. Surg. 193, 155–159 (2007). https://doi.org/10.1016/j.amjsurg.2006.04.020
C. Ansquer, E. Mirallié, T. Carlier, H. Abbey-Huguenin, F. Aubron, F. Kraeber-Bodéré, Preoperative localization of parathyroid lesions. Value of 99mTc-MIBI tomography and factors influencing detection. Nukl. Nucl. Med. 47, 158–162 (2008)
T. Carlier, A. Oudoux, E. Mirallié et al. 99mTc-MIBI pinhole SPECT in primary hyperparathyroidism: comparison with conventional SPECT, planar scintigraphy and ultrasonography. Eur. J. Nucl. Med. Mol. Imaging 35, 637–643 (2008). https://doi.org/10.1007/s00259-007-0625-9
T. Cazaentre, F. Clivaz, F. Triponez, False-positive result in 18F-fluorocholine PET/CT due to incidental and ectopic parathyroid hyperplasia. Clin. Nucl. Med. 39, e328–e330 (2014). https://doi.org/10.1097/RLU.0b013e3182a77b62
M. Hodolic, V. Huchet, S. Balogova et al. Incidental uptake of (18)F-fluorocholine (FCH) in the head or in the neck of patients with prostate cancer. Radiol. Oncol. 48, 228–234 (2014). https://doi.org/10.2478/raon-2013-0075
P. Mapelli, E. Busnardo, P. Magnani et al. Incidental finding of parathyroid adenoma with 11C-choline PET/CT. Clin. Nucl. Med. 37, 593–595 (2012). https://doi.org/10.1097/RLU.0b013e31824c5ffc
M. Orevi, N. Freedman, E. Mishani, M. Bocher, O. Jacobson, Y. Krausz, Localization of parathyroid adenoma by 11C-choline PET/CT: preliminary results. Clin. Nucl. Med. 39, 1033–1038 (2014). https://doi.org/10.1097/RLU.0000000000000607
L. Lezaic, S. Rep, M.J. Sever, T. Kocjan, M. Hocevar, J. Fettich, 18F-Fluorocholine PET/CT for localization of hyperfunctioning parathyroid tissue in primary hyperparathyroidism: a pilot study. Eur. J. Nucl. Med. Mol. Imaging 41, 2083–2089 (2014). https://doi.org/10.1007/s00259-014-2837-0
M. Hocevar, L. Lezaic, S. Rep et al. Focused parathyroidectomy without intraoperative parathormone testing is safe after pre-operative localization with 18F-Fluorocholine PET/CT. Eur. J. Surg. Oncol. J. Eur. Soc. Surg. Oncol. Br. Assoc. Surg. Oncol. 43, 133–137 (2017). https://doi.org/10.1016/j.ejso.2016.09.016
N. Thanseer, S.K. Bhadada, A. Sood et al. Comparative effectiveness of ultrasonography, 99mTc-Sestamibi, and 18F-Fluorocholine PET/CT in detecting parathyroid adenomas in patients with primary hyperparathyroidism. Clin. Nucl. Med. 42, e491–e497 (2017). https://doi.org/10.1097/RLU.0000000000001845
S. Rep, M. Hocevar, J. Vaupotic, U. Zdesar, K. Zaletel, L. Lezaic, 18F-choline PET/CT for parathyroid scintigraphy: significantly lower radiation exposure of patients in comparison to conventional nuclear medicine imaging approaches. J. Radiol. Prot. 38, 343–356 (2018). https://doi.org/10.1088/1361-6498/aaa86f
A.O.J. Bergenfelz, G. Wallin, S. Jansson et al. Results of surgery for sporadic primary hyperparathyroidism in patients with preoperatively negative sestamibi scintigraphy and ultrasound. Langenbecks Arch. Surg. 396, 83–90 (2011). https://doi.org/10.1007/s00423-010-0724-0
B.M. Dy, M.L. Richards, B.J. Vazquez, G.B. Thompson, D.R. Farley, C.S. Grant, Primary hyperparathyroidism and negative Tc99 sestamibi imaging: to operate or not? Ann. Surg. Oncol. 19, 2272–2278 (2012). https://doi.org/10.1245/s10434-012-2325-3
L. Michaud, A. Burgess, V. Huchet et al. Is 18F-fluorocholine-positron emission tomography/computerized tomography a new imaging tool for detecting hyperfunctioning parathyroid glands in primary or secondary hyperparathyroidism? J. Clin. Endocrinol. Metab. 99, 4531–4536 (2014). https://doi.org/10.1210/jc.2014-2821
L. Michaud, S. Balogova, A. Burgess et al. A pilot comparison of 18F-fluorocholine PET/CT, ultrasonography and 123I/99mTc-sestaMIBI dual-phase dual-isotope scintigraphy in the preoperative localization of hyperfunctioning parathyroid glands in primary or secondary hyperparathyroidism: influence of thyroid anomalies. Medicine (Baltimore) 94, e1701 (2015). https://doi.org/10.1097/MD.0000000000001701
S. Grimaldi, J. Young, P. Kamenicky et al., Challenging pre-surgical localization of hyperfunctioning parathyroid glands in primary hyperparathyroidism: the added value of 18F-Fluorocholine PET/CT. Eur. J. Nucl. Med. Mol. Imaging. (2018). https://doi.org/10.1007/s00259-018-4018-z
S. Rep, L. Lezaic, T. Kocjan et al. Optimal scan time for evaluation of parathyroid adenoma with [(18)F]-fluorocholine PET/CT. Radiol. Oncol. 49, 327–333 (2015). https://doi.org/10.1515/raon-2015-0016
W.P. Kluijfhout, W.M.C.M. Vorselaars, S.A.M. van den Berk et al. Fluorine-18 fluorocholine PET-CT localizes hyperparathyroidism in patients with inconclusive conventional imaging: a multicenter study from the Netherlands. Nucl. Med. Commun. 37, 1246–1252 (2016). https://doi.org/10.1097/MNM.0000000000000595
W.P. Kluijfhout, J.D. Pasternak, J.E. Gosnell et al. 18F fluorocholine PET/MR imaging in patients with primary hyperparathyroidism and inconclusive conventional imaging: a prospective pilot study. Radiology 284, 460–467 (2017). https://doi.org/10.1148/radiol.2016160768
E. Quak, D. Blanchard, B. Houdu et al. F18-choline PET/CT guided surgery in primary hyperparathyroidism when ultrasound and MIBI SPECT/CT are negative or inconclusive: the APACH1 study. Eur. J. Nucl. Med. Mol. Imaging 45, 658–666 (2018). https://doi.org/10.1007/s00259-017-3911-1
M. Beheshti, L. Hehenwarter, Z. Paymani et al. 18F-Fluorocholine PET/CT in the assessment of primary hyperparathyroidism compared with 99mTc-MIBI or 99mTc-tetrofosmin SPECT/CT: a prospective dual-centre study in 100 patients. Eur. J. Nucl. Med. Mol. Imaging 45, 1762–1771 (2018). https://doi.org/10.1007/s00259-018-3980-9
S. Fischli, I. Suter-Widmer, B.T. Nguyen et al. The significance of 18F-Fluorocholine-PET/CT as localizing imaging technique in patients with primary hyperparathyroidism and negative conventional imaging. Front. Endocrinol. 8, 380 (2017). https://doi.org/10.3389/fendo.2017.00380
G.F. Huber, M. Hüllner, C. Schmid et al. Benefit of 18F-fluorocholine PET imaging in parathyroid surgery. Eur. Radiol. 28, 2700–2707 (2018). https://doi.org/10.1007/s00330-017-5190-4
C. Amadou, G. Bera, M. Ezziane et al., 18F-Fluorocholine PET/CT and parathyroid 4D computed tomography for primary hyperparathyroidism: the challenge of reoperative patients. World J. Surg. (2019). https://doi.org/10.1007/s00268-019-04910-6
O. Koulouri, N. Kandasamy, A.C. Hoole et al. Successful treatment of residual pituitary adenoma in persistent acromegaly following localisation by 11C-methionine PET co-registered with MRI. Eur. J. Endocrinol. 175, 485–498 (2016). https://doi.org/10.1530/EJE-16-0639
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Bergeret, S., Charbit, J., Ansquer, C. et al. Novel PET tracers: added value for endocrine disorders. Endocrine 64, 14–30 (2019). https://doi.org/10.1007/s12020-019-01895-z
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DOI: https://doi.org/10.1007/s12020-019-01895-z