Fast non-enhanced abdominal examination protocols in PET/MRI for patients with neuroendocrine tumors (NET): comparison to multiphase contrast-enhanced PET/CT
To evaluate fast non-enhanced protocols for abdominal PET/MRI in comparison to contrast-enhanced PET/CT with somatostatin receptor (SSR)-specific radiotracers regarding effectiveness of lesion detection in NET patients.
This was a retrospective analysis of 29 patients (12 male, 57 ± 13 years) who underwent PET/CT and subsequently PET/MRI at the same day. Two readers evaluated independently four PET/MRI setups: (I) PET + T2 Half Fourier Acquisition Single Shot Turbo Spin Echo (T2 HASTE), (II) PET + T2 HASTE + T2-weighted spin-echo sequence (T2 TSE), III) PET + T2 HASTE + Diffusion Weighted Imaging (DWI) and (IV) PET + T2 HASTE + T2 TSE + DWI. A consensus reading of PET/MRI and PET/CT including follow-up examinations served as the reference standard for lesion-based analysis. Lesion sizes were assessed.
Setup IV provided comparable overall detection rates as PET/CT in both readers: PET/MRI 91.5%/92.9% versus 89.7% in PET/CT. In liver and bone lesions (mean diameter: 1.9 and 1.5 cm), PET/MRI was equal or superior to PET/CT: 98%/98% versus 85% in PET/CT; 100%/95% versus 100% in PET/CT, but inferior in pancreatic lesions, small bowel lesions and lymph node metastases (mean diameter: 1.3, 0.5 and 1.8 cm).
A non-enhanced MR protocol comprising T2 HASTE, T2 TSE and DWI for SSR-PET/MRI seems to provide comparable effectiveness in lesions detection as multiphase contrast-enhanced PET/CT. It might, therefore, serve as valid alternative, e.g., for follow-up examinations in patients with unresectable NET and kidney failure.
KeywordsPET/MRI Neuroendocrine tumors Somatostatin receptor-specific radiotracers
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
The patient population included 9 patients as a part of a larger, prospectively conducted study which was designed as a feasibility study for PET/MRI. This study was approved by the German Federal Institute for Drugs and Medical Devices as well as the local ethics committee. Written informed consent was obtained from all patients concerning both examinations and the scientific evaluation of their data. So far, the data of those 9 patients have not been included in any study comparing the diagnostic accuracy of both modalities. 20 patients underwent a clinically indicated PET/MRI subsequently to PET/CT. From those patients, written informed consent was obtained for the additional PET/MRI examination. Regarding the retrospective scientific evaluation of the pseudonymized data, the local ethics committee waived informed consent.
- 6.Belousova E, Karmazanovsky G, Kriger A, Kalinin D, Mannelli L, Glotov A, Karelskaya N, Paklina O, Kaldarov A (2017) Contrast-enhanced MDCT in patients with pancreatic neuroendocrine tumours: correlation with histological findings and diagnostic performance in differentiation between tumour grades. Clin Radiol 72(2):150–158. https://doi.org/10.1016/j.crad.2016.10.021 Epub 2016 Nov 1024 CrossRefPubMedGoogle Scholar
- 7.Kwekkeboom DJ, de Herder WW, Kam BL, van Eijck CH, van Essen M, Kooij PP, Feelders RA, van Aken MO, Krenning EP (2008) Treatment with the radiolabeled somatostatin analog [177 Lu-DOTA 0, Tyr3]octreotate: toxicity, efficacy, and survival. J Clin Oncol Off J Am Soc Clin Oncol 26(13):2124–2130. https://doi.org/10.1200/jco.2007.15.2553 CrossRefGoogle Scholar
- 9.Sun W, Lipsitz S, Catalano P, Mailliard JA, Haller DG (2005) Phase II/III study of doxorubicin with fluorouracil compared with streptozocin with fluorouracil or dacarbazine in the treatment of advanced carcinoid tumors: Eastern Cooperative Oncology Group Study E1281. J Clin Oncol Off J Am Soc Clin Oncol 23(22):4897–4904. https://doi.org/10.1200/jco.2005.03.616 CrossRefGoogle Scholar
- 13.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 Off J Am Soc Clin Oncol 23(1):70–78. https://doi.org/10.1200/jco.2005.01.013 CrossRefGoogle Scholar
- 14.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 Off Publ Int Cancer Imaging Soc 13:63–72. https://doi.org/10.1102/1470-7330.2013.0007 CrossRefGoogle Scholar
- 16.Berzaczy D, Giraudo C, Haug AR, Raderer M, Senn D, Karanikas G, Weber M, Mayerhoefer ME (2017) Whole-Body 68 Ga-DOTANOC PET/MRI Versus 68 Ga-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 CrossRefPubMedPubMedCentralGoogle Scholar
- 17.Guckel B, Gatidis S, Enck P, Schafer J, Bisdas S, Pfannenberg C, Schwenzer N (2015) Patient comfort during positron emission tomography/magnetic resonance and positron emission tomography/computed tomography examinations: subjective assessments with visual analog scales. Invest Radiol 50(10):726–732. https://doi.org/10.1097/rli.0000000000000177 CrossRefPubMedGoogle Scholar
- 18.Taron J, Schraml C, Pfannenberg C, Reimold M, Schwenzer N, Nikolaou K, Martirosian P, Seith F (2018) Simultaneous multislice diffusion-weighted imaging in whole-body positron emission tomography/magnetic resonance imaging for multiparametric examination in oncological patients. Eur Radiol. https://doi.org/10.1007/s00330-017-5216-y CrossRefPubMedGoogle Scholar
- 19.Grueneisen J, Sawicki LM, Schaarschmidt BM, Suntharalingam S, von der Ropp S, Wetter A, Ruhlmann V, Quick HH, Forsting M, Umutlu L (2016) Evaluation of a fast protocol for staging lymphoma patients with integrated PET/MRI. PLoS ONE 11(6):e0157880. https://doi.org/10.1371/journal.pone.0157880 CrossRefPubMedPubMedCentralGoogle Scholar
- 20.Brogsitter C, Zophel K, Hartmann H, Schottelius M, Wester HJ, Kotzerke J (2014) Twins in spirit part II: DOTATATE and high-affinity DOTATATE–the clinical experience. Eur J Nucl Med Mol Imaging 41(6):1158–1165. https://doi.org/10.1007/s00259-014-2690-1 Epub 02014 Feb 00215 CrossRefPubMedGoogle Scholar
- 21.Hofmann M, Maecke H, Borner R, Weckesser E, Schoffski P, Oei L, Schumacher J, Henze M, Heppeler A, Meyer J, Knapp H (2001) Biokinetics and imaging with the somatostatin receptor PET radioligand (68)Ga-DOTATOC: preliminary data. Eur J Nucl Med 28(12):1751–1757. https://doi.org/10.1007/s002590100639 CrossRefPubMedGoogle Scholar
- 22.Oehmigen M, Ziegler S, Jakoby BW, Georgi JC, Paulus DH, Quick HH (2014) Radiotracer dose reduction in integrated PET/MR: implications from national electrical manufacturers association phantom studies. J Nucl Med Off Publ Soc Nucl Med 55(8):1361–1367. https://doi.org/10.2967/jnumed.114.139147 CrossRefGoogle Scholar
- 23.Krausz Y, Rubinstein R, Appelbaum L, Mishani E, Orevi M, Fraenkel M, Tshori S, Glaser B, Bocher M, Salmon A, Chisin R, Gross DJ, Freedman N (2012) Ga-68 DOTA-NOC uptake in the pancreas: pathological and physiological patterns. Clin Nucl Med 37(1):57–62. https://doi.org/10.1097/RLU.0b013e3182393404 CrossRefPubMedGoogle Scholar
- 25.Virgolini I, Ambrosini V, Bomanji JB, Baum RP, Fanti S, Gabriel M, Papathanasiou ND, Pepe G, Oyen W, De Cristoforo C, Chiti A (2010) Procedure guidelines for PET/CT tumour imaging with 68 Ga-DOTA-conjugated peptides: 68 Ga-DOTA-TOC, 68 Ga-DOTA-NOC, 68 Ga-DOTA-TATE. Eur J Nucl Med Mol Imaging 37(10):2004–2010. https://doi.org/10.1007/s00259-010-1512-3 CrossRefPubMedGoogle Scholar
- 27.d’Assignies G, Fina P, Bruno O, Vullierme MP, Tubach F, Paradis V, Sauvanet A, Ruszniewski P, Vilgrain V (2013) High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging. Radiology 268(2):390–399. https://doi.org/10.1148/radiol.13121628 CrossRefPubMedGoogle Scholar
- 28.Morani AC, Elsayes KM, Liu PS, Weadock WJ, Szklaruk J, Dillman JR, Khan A, Chenevert TL, Hussain HK (2013) Abdominal applications of diffusion-weighted magnetic resonance imaging: where do we stand. World J Radiol 5(3):68–80. https://doi.org/10.4329/wjr.v5.i3.68 CrossRefPubMedPubMedCentralGoogle Scholar
- 29.Samarin A, Hullner M, Queiroz MA, Stolzmann P, Burger IA, von Schulthess G, Veit-Haibach P (2015) 18F-FDG-PET/MR increases diagnostic confidence in detection of bone metastases compared with 18F-FDG-PET/CT. Nucl Med Commun 36(12):1165–1173. https://doi.org/10.1097/mnm.0000000000000387 CrossRefPubMedGoogle Scholar
- 30.Martinez-Moller A, Souvatzoglou M, Delso G, Bundschuh RA, Chefd’hotel C, Ziegler SI, Navab N, Schwaiger M, Nekolla SG (2009) Tissue classification as a potential approach for attenuation correction in whole-body PET/MRI: evaluation with PET/CT data. J Nucl Med Off Publ Soc Nucl Med 50(4):520–526. https://doi.org/10.2967/jnumed.108.054726 CrossRefGoogle Scholar
- 31.Seith F, Gatidis S, Schmidt H, Bezrukov I, la Fougere C, Nikolaou K, Pfannenberg C, Schwenzer N (2016) Comparison of positron emission tomography quantification using magnetic resonance- and computed tomography-based attenuation correction in physiological tissues and lesions: a whole-body positron emission tomography/magnetic resonance study in 66 patients. Invest Radiol 51(1):66–71. https://doi.org/10.1097/rli.0000000000000208 CrossRefPubMedGoogle Scholar
- 32.Paulus DH, Quick HH, Geppert C, Fenchel M, Zhan Y, Hermosillo G, Faul D, Boada F, Friedman KP, Koesters T (2015) Whole-body PET/MR imaging: quantitative evaluation of a novel model-based MR attenuation correction method including bone. J Nucl Med Off Publ Soc Nucl Med 56(7):1061–1066. https://doi.org/10.2967/jnumed.115.156000 CrossRefGoogle Scholar
- 33.Schwenzer NF, Schmidt H, Gatidis S, Brendle C, Muller M, Konigsrainer I, Claussen CD, Pfannenberg AC, Schraml C (2014) Measurement of apparent diffusion coefficient with simultaneous MR/positron emission tomography in patients with peritoneal carcinomatosis: comparison with 18F-FDG-PET. J Magn Reson imaging JMRI 40(5):1121–1128. https://doi.org/10.1002/jmri.24497 CrossRefPubMedGoogle Scholar