Abstract
Purpose
To evaluate the current literature on technical feasibility and diagnostic value of PET/MRI in management of patients with neuroendocrine tumors (NETs).
Methods
A systematic literature search of the PubMed/MEDLINE database identified studies that evaluated the role of simultaneous PET/MRI for the evaluation of neuroendocrine tumors in human subjects. Exclusion criteria included studies lacking simultaneous PET/MRI, absence of other than attenuation-correction MRI pulse sequences, and case reports. No data-pooling or statistical analysis was performed due to the small number of articles and heterogeneity of the methodologies.
Results
From the 21 identified articles, five were included, which demonstrated successful technical feasibility of simultaneous PET/MRI through various imaging protocols in a total of 105 patients. All articles demonstrated equal or superior detection of liver lesions by PET/MRI over PET/CT. While one study reported superior detection of bone lesions by PET/MRI, two demonstrated favorable detection by PET/CT. Two studies demonstrated superiority of PET/CT in detection of nodal metastases; three studies reported the pitfall of PET/MRI in detection of lung lesion.
Conclusion
The current literature reports successful technical feasibility of PET/MRI for imaging of NETs. While whole-body PET/CT in conjunction with an abdominal MRI may serve as a comprehensive approach for baseline staging, follow-up with PET/MRI may be preferred for those with liver-only disease. Another possible role for PET/MRI is to provide a multiparametric approach to follow-up of response to treatment. With further advances in MRI imaging acquisitions and post-processing techniques, PET/MRI may become more applicable to a broader group of patients with NETs, and possibly the imaging modality of choice for this patient population.
Similar content being viewed by others
References
Modlin IM, Sandor A (1997) An analysis of 8305 cases of carcinoid tumors. Cancer 79(4):813–829
Ter-Minassian M, Chan JA, Hooshmand SM, Brais LK, Daskalova A, Heafield R, Buchanan L, Qian ZR, Fuchs CS, Lin X, Christiani DC, Kulke MH (2013) Clinical presentation, recurrence, and survival in patients with neuroendocrine tumors: results from a prospective institutional database. Endocr Relat Cancer 20(2):187–196. https://doi.org/10.1530/ERC-12-0340
Pape UF, Berndt U, Muller-Nordhorn J, Bohmig M, Roll S, Koch M, Willich SN, Wiedenmann B (2008) Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours. Endocr Relat Cancer 15(4):1083–1097. https://doi.org/10.1677/ERC-08-0017
Sadowski SM, Neychev V, Millo C, Shih J, Nilubol N, Herscovitch P, Pacak K, Marx SJ, Kebebew E (2016) Prospective study of 68Ga-DOTATATE positron emission tomography/computed tomography for detecting gastro-entero-pancreatic neuroendocrine tumors and unknown primary sites. J Clin Oncol 34(6):588–596. https://doi.org/10.1200/JCO.2015.64.0987
Delle Fave G, O’Toole D, Sundin A, Taal B, Ferolla P, Ramage JK, Ferone D, Ito T, Weber W, Zheng-Pei Z, De Herder WW, Pascher A, Ruszniewski P, Vienna Consensus Conference p (2016) ENETS consensus guidelines update for gastroduodenal neuroendocrine neoplasms. Neuroendocrinology 103(2):119–124. https://doi.org/10.1159/000443168
Niederle B, Pape UF, Costa F, Gross D, Kelestimur F, Knigge U, Oberg K, Pavel M, Perren A, Toumpanakis C, O’Connor J, O’Toole D, Krenning E, Reed N, Kianmanesh R, Vienna Consensus Conference p (2016) ENETS consensus guidelines update for neuroendocrine neoplasms of the Jejunum and Ileum. Neuroendocrinology 103(2):125–138. https://doi.org/10.1159/000443170
Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, Kos-Kudla B, Kwekkeboom D, Rindi G, Kloppel G, Reed N, Kianmanesh R, Jensen RT, Vienna Consensus Conference p (2016) ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology 103(2):153–171. https://doi.org/10.1159/000443171
O’Toole D, Kianmanesh R, Caplin M (2016) ENETS 2016 consensus guidelines for the management of patients with digestive neuroendocrine tumors: an update. Neuroendocrinology 103(2):117–118. https://doi.org/10.1159/000443169
Pavel M, O’Toole D, Costa F, Capdevila J, Gross D, Kianmanesh R, Krenning E, Knigge U, Salazar R, Pape UF, Oberg K, Vienna Consensus Conference p (2016) ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology 103(2):172–185. https://doi.org/10.1159/000443167
Ramage JK, De Herder WW, Delle Fave G, Ferolla P, Ferone D, Ito T, Ruszniewski P, Sundin A, Weber W, Zheng-Pei Z, Taal B, Pascher A, Vienna Consensus Conference p (2016) ENETS consensus guidelines update for colorectal neuroendocrine neoplasms. Neuroendocrinology 103(2):139–143. https://doi.org/10.1159/000443166
Dromain C, de Baere T, Lumbroso J, Caillet H, Laplanche A, Boige V, Ducreux M, Duvillard P, Elias D, Schlumberger M, Sigal R, Baudin E (2005) Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy, computed tomography, and magnetic resonance imaging. J Clin Oncol 23(1):70–78. https://doi.org/10.1200/JCO.2005.01.013
Schraml C, Schwenzer NF, Sperling O, Aschoff P, Lichy MP, Muller M, Brendle C, Werner MK, Claussen CD, Pfannenberg C (2013) Staging of neuroendocrine tumours: comparison of [(6)(8)Ga]DOTATOC multiphase PET/CT and whole-body MRI. Cancer Imaging 13:63–72. https://doi.org/10.1102/1470-7330.2013.0007
Carlbom L, Caballero-Corbalan J, Granberg D, Sorensen J, Eriksson B, Ahlstrom H (2017) Whole-body MRI including diffusion-weighted MRI compared with 5-HTP PET/CT in the detection of neuroendocrine tumors. Ups J Med Sci 122(1):43–50. https://doi.org/10.1080/03009734.2016.1248803
Farchione A, Rufini V, Brizi MG, Iacovazzo D, Larghi A, Massara RM, Petrone G, Poscia A, Treglia G, De Marinis L, Giordano A, Rindi G, Bonomo L (2016) Evaluation of the added value of diffusion-weighted imaging to conventional magnetic resonance imaging in pancreatic neuroendocrine tumors and comparison with 68Ga-DOTANOC positron emission tomography/computed tomography. Pancreas 45(3):345–354. https://doi.org/10.1097/MPA.0000000000000461
Flechsig P, Zechmann CM, Schreiweis J, Kratochwil C, Rath D, Schwartz LH, Schlemmer HP, Kauczor HU, Haberkorn U, Giesel FL (2015) Qualitative and quantitative image analysis of CT and MR imaging in patients with neuroendocrine liver metastases in comparison to (68)Ga-DOTATOC PET. Eur J Radiol 84(8):1593–1600. https://doi.org/10.1016/j.ejrad.2015.04.009
Etchebehere EC, de Oliveira Santos A, Gumz B, Vicente A, Hoff PG, Corradi G, Ichiki WA, de Almeida Filho JG, Cantoni S, Camargo EE, Costa FP (2014) 68Ga-DOTATATE PET/CT, 99mTc-HYNIC-octreotide SPECT/CT, and whole-body MR imaging in detection of neuroendocrine tumors: a prospective trial. J Nucl Med 55(10):1598–1604. https://doi.org/10.2967/jnumed.114.144543
Armbruster M, Zech CJ, Sourbron S, Ceelen F, Auernhammer CJ, Rist C, Haug A, Singnurkar A, Reiser MF, Sommer WH (2014) Diagnostic accuracy of dynamic gadoxetic-acid-enhanced MRI and PET/CT compared in patients with liver metastases from neuroendocrine neoplasms. J Magn Resonance Imaging 40(2):457–466. https://doi.org/10.1002/jmri.24363
Armbruster M, Sourbron S, Haug A, Zech CJ, Ingrisch M, Auernhammer CJ, Nikolaou K, Paprottka PM, Rist C, Reiser MF, Sommer WH (2014) Evaluation of neuroendocrine liver metastases: a comparison of dynamic contrast-enhanced magnetic resonance imaging and positron emission tomography/computed tomography. Invest Radiol 49(1):7–14. https://doi.org/10.1097/RLI.0b013e3182a4eb4a
Klinaki I, Al-Nahhas A, Soneji N, Win Z (2013) 68 Ga DOTATATE PET/CT uptake in spinal lesions and MRI correlation on a patient with neuroendocrine tumor: potential pitfalls. Clin Nucl Med 38(12):e449–e453. https://doi.org/10.1097/RLU.0b013e31827a2325
Schmid-Tannwald C, Schmid-Tannwald CM, Morelli JN, Neumann R, Haug AR, Jansen N, Nikolaou K, Schramm N, Reiser MF, Rist C (2013) 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(6):897–907. https://doi.org/10.1007/s00259-013-2371-5
Giesel FL, Kratochwil C, Mehndiratta A, Wulfert S, Moltz JH, Zechmann CM, Kauczor HU, Haberkorn U, Ley S (2012) Comparison of neuroendocrine tumor detection and characterization using DOTATOC-PET in correlation with contrast enhanced CT and delayed contrast enhanced MRI. Eur J Radiol 81(10):2820–2825. https://doi.org/10.1016/j.ejrad.2011.11.007
Froling V, Denecke T, Pollinger A, Schreiter NF (2010) Detection of a neuroendocrine differentiated cystic pancreatic lesion by gallium-68-DOTATOC-PET/CT with inconclusive MRI, CT and ultrasound diagnosis. Rofo 182(2):175–177. https://doi.org/10.1055/s-0028-1109828
Schreiter NF, Nogami M, Steffen I, Pape UF, Hamm B, Brenner W, Rottgen R (2012) Evaluation of the potential of PET-MRI fusion for detection of liver metastases in patients with neuroendocrine tumours. Eur Radiol 22(2):458–467. https://doi.org/10.1007/s00330-011-2266-4
Treglia G, Bongiovanni M, Giovanella L (2014) Rare sinonasal small cell neuroendocrine carcinoma evaluated by F-18-FDG PET/MRI. Endocrine 47(2):654–655. https://doi.org/10.1007/s12020-014-0190-5
Paola M, De Cobelli F, Picchio M (2019) PET/MRI in neuroendocrine tumours: blessings and curses. Curr Radiopharm 12(2):96–97. https://doi.org/10.2174/1874471012999190404151701
Mayerhoefer ME, Ba-Ssalamah A, Weber M, Mitterhauser M, Eidherr H, Wadsak W, Raderer M, Trattnig S, Herneth A, Karanikas G (2013) Gadoxetate-enhanced versus diffusion-weighted MRI for fused Ga-68-DOTANOC PET/MRI in patients with neuroendocrine tumours of the upper abdomen. Eur Radiol 23(7):1978–1985. https://doi.org/10.1007/s00330-013-2785-2
Gaertner FC, Beer AJ, Souvatzoglou M, Eiber M, Furst S, Ziegler SI, Brohl F, Schwaiger M, Scheidhauer K (2013) Evaluation of feasibility and image quality of 68 Ga-DOTATOC positron emission tomography/magnetic resonance in comparison with positron emission tomography/computed tomography in patients with neuroendocrine tumors. Invest Radiol 48(5):263–272. https://doi.org/10.1097/RLI.0b013e31828234d0
Beiderwellen KJ, Poeppel TD, Hartung-Knemeyer V, Buchbender C, Kuehl H, Bockisch A, Lauenstein TC (2013) Simultaneous 68Ga-DOTATOC PET/MRI in patients with gastroenteropancreatic neuroendocrine tumors: initial results. Invest Radiol 48(5):273–279. https://doi.org/10.1097/RLI.0b013e3182871a7f
Hope TA, Pampaloni MH, Nakakura E, VanBrocklin H, Slater J, Jivan S, Aparici CM, Yee J, Bergsland E (2015) Simultaneous (68)Ga-DOTA-TOC PET/MRI with gadoxetate disodium in patients with neuroendocrine tumor. Abdom Imaging 40(6):1432–1440. https://doi.org/10.1007/s00261-015-0409-9
Berzaczy D, Giraudo C, Haug AR, Raderer M, Senn D, Karanikas G, Weber M, Mayerhoefer ME (2017) Whole-Body 68Ga-DOTANOC PET/MRI versus 68Ga-DOTANOC PET/CT in patients with neuroendocrine tumors: a prospective study in 28 patients. Clin Nucl Med 42(9):669–674. https://doi.org/10.1097/RLU.0000000000001753
Sawicki LM, Deuschl C, Beiderwellen K, Ruhlmann V, Poeppel TD, Heusch P, Lahner H, Fuhrer D, Bockisch A, Herrmann K, Forsting M, Antoch G, Umutlu L (2017) Evaluation of (68)Ga-DOTATOC PET/MRI for whole-body staging of neuroendocrine tumours in comparison with (68)Ga-DOTATOC PET/CT. Eur Radiol 27(10):4091–4099. https://doi.org/10.1007/s00330-017-4803-2
Seith F, Schraml C, Reischl G, Nikolaou K, Pfannenberg C, la Fougere C, Schwenzer N (2018) Fast non-enhanced abdominal examination protocols in PET/MRI for patients with neuroendocrine tumors (NET): comparison to multiphase contrast-enhanced PET/CT. Radiol Med 123(11):860–870. https://doi.org/10.1007/s11547-018-0917-0
Wang X, Pirasteh A, Brugarolas J, Rofsky NM, Lenkinski RE, Pedrosa I, Madhuranthakam AJ (2018) Whole-body MRI for metastatic cancer detection using T2 -weighted imaging with fat and fluid suppression. Magn Reson Med 80(4):1402–1415. https://doi.org/10.1002/mrm.27117
Riihimaki M, Hemminki A, Sundquist K, Sundquist J, Hemminki K (2016) The epidemiology of metastases in neuroendocrine tumors. Int J Cancer 139(12):2679–2686. https://doi.org/10.1002/ijc.30400
Cieszanowski A, Lisowska A, Dabrowska M, Korczynski P, Zukowska M, Grudzinski IP, Pacho R, Rowinski O, Krenke R (2016) MR imaging of pulmonary nodules: detection rate and accuracy of size estimation in comparison to computed tomography. PLoS ONE 11(6):e0156272. https://doi.org/10.1371/journal.pone.0156272
Strosberg J, El-Haddad G, Wolin E, Hendifar A, Yao J, Chasen B, Mittra E, Kunz PL, Kulke MH, Jacene H, Bushnell D, O’Dorisio TM, Baum RP, Kulkarni HR, Caplin M, Lebtahi R, Hobday T, Delpassand E, Van Cutsem E, Benson A, Srirajaskanthan R, Pavel M, Mora J, Berlin J, Grande E, Reed N, Seregni E, Oberg K, Lopera Sierra M, Santoro P, Thevenet T, Erion JL, Ruszniewski P, Kwekkeboom D, Krenning E, Investigators N-T (2017) Phase 3 trial of (177)Lu-dotatate for midgut neuroendocrine tumors. N Engl J Med 376(2):125–135. https://doi.org/10.1056/NEJMoa1607427
Mayerhoefer ME, Prosch H, Beer L, Tamandl D, Beyer T, Hoeller C, Berzaczy D, Raderer M, Preusser M, Hochmair M, Kiesewetter B, Scheuba C, Ba-Ssalamah A, Karanikas G, Kesselbacher J, Prager G, Dieckmann K, Polterauer S, Weber M, Rausch I, Brauner B, Eidherr H, Wadsak W, Haug AR (2019) PET/MRI versus PET/CT in oncology: a prospective single-center study of 330 examinations focusing on implications for patient management and cost considerations. Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-019-04452-y
Funding
This research was funded in part through the United States National Institute of Health/National Cancer Institute (NIH/NCI) Cancer Center Support Grant P30 CA008748.
Author information
Authors and Affiliations
Contributions
AP: literature search and review, manuscript writing and editing, content planning, material collection. CR: literature search and review, manuscript writing and editing. MEM: literature search and review, manuscript writing and editing. RGG: manuscript writing and editing, content planning, material collection. SML: manuscript editing, content planning. LB: literature review, manuscript writing editing, content planning.
Corresponding author
Ethics declarations
Conflict of interest
Ali Pirasteh: Nothing to disclose. Christopher Riedl: Nothing to disclose. Marius Erik Mayerhoefer: Speaker honoraria from Siemens Healthcare and Bristol-Myers Squibb and research support from Siemens Healthcare. Romina Grazia Giancipoli: Nothing to disclose. Steven Mark Larson: receiving commercial research grants from Genentech, Inc., WILEX AG, Telix Pharmaceuticals Limited, and Regeneron Pharmaceuticals, Inc.; holding ownership interest/equity in Voreyda Theranostics Inc. and Elucida Oncology Inc., and holding stock in ImaginAb, Inc. SML is the inventor and owner of issued patents both currently unlicensed and licensed by MSK to Samus Therapeutics, Inc., Y-mAbs Therapeutics Inc., and Elucida Oncology, Inc. SML is or has served as a consultant to Cynvec LLC, Eli Lilly & Co., Prescient Therapeutics Limited, Advanced Innovative Partners, LLC, Gerson Lehrman Group, Progenics Pharmaceuticals, Inc., and Janssen Pharmaceuticals, Inc. Lisa Bodei: Consultancy and speaker for AAA and Ipsen; consultancy for Curium.
Human rights and animal welfare
This review article does not contain any imaging studies with human or animal subjects performed by the authors solely for the purposes of this review. The provided images are from exams performed for the purposes of clinical care at the authors’ institution (Memorial Sloan Kettering Cancer Center), and not with the prospective intention of being utilized for this review. No Institutional Review Board approval or patient consent was required for the purposes of this literature review. All patient information was handled according the United States Health Insurance and Accountability Act.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pirasteh, A., Riedl, C., Mayerhoefer, M.E. et al. PET/MRI for neuroendocrine tumors: a match made in heaven or just another hype?. Clin Transl Imaging 7, 405–413 (2019). https://doi.org/10.1007/s40336-019-00344-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40336-019-00344-1