Skip to main content

Advertisement

Log in

PET/MRI imaging in neuroendocrine neoplasm

  • Special Section: PET/MR
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Molecular imaging plays a vital role in the management of neuroendocrine neoplasms (NENs). Somatostatin receptor (SSTR) PET is critical for evaluating NENs, ascertaining peptide receptor radionuclide therapy (PRRT) eligibility, and treatment response. SSTR-PET/MRI can provide a one-stop-shop multiparametric evaluation of NENs. The acquisition of complementary imaging information in PET/MRI has distinct advantages over PET/CT and MR imaging acquisitions. The purpose of this manuscript is to provide a comprehensive overview of PET/MRI and a current review of recent PET/MRI advances in the diagnosis, staging, treatment, and surveillance of NENs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Ambrosini, V., et al., Consensus on molecular imaging and theranostics in neuroendocrine neoplasms. Eur J Cancer, 2021. 146: p. 56–73.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Taal, B.G. and O. Visser, Epidemiology of neuroendocrine tumours. Neuroendocrinology, 2004. 80 Suppl 1: p. 3–7.

    Article  PubMed  CAS  Google Scholar 

  3. Oronsky, B., et al., Nothing But NET: A Review of Neuroendocrine Tumors and Carcinomas. Neoplasia, 2017. 19(12): p. 991–1002.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Rajamohan, N., et al., PET/CT and PET/MRI in neuroendocrine neoplasms. Abdom Radiol (NY), 2022.

  5. Crona, J. and B. Skogseid, GEP- NETS UPDATE: Genetics of neuroendocrine tumors. Eur J Endocrinol, 2016. 174(6): p. R275–90.

    Article  PubMed  CAS  Google Scholar 

  6. Xu, Z., et al., Epidemiologic Trends of and Factors Associated With Overall Survival for Patients With Gastroenteropancreatic Neuroendocrine Tumors in the United States. JAMA Network Open, 2021. 4(9): p. e2124750.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kawasaki, K., M. Fujii, and T. Sato, Gastroenteropancreatic neuroendocrine neoplasms: genes, therapies and models. Dis Model Mech, 2018. 11(2).

  8. Rindi, G., G. Petrone, and F. Inzani, The 2010 WHO classification of digestive neuroendocrine neoplasms: a critical appraisal four years after its introduction. Endocr Pathol, 2014. 25(2): p. 186–92.

    Article  PubMed  CAS  Google Scholar 

  9. Yang, M., et al., Evaluation of the World Health Organization 2010 grading system in surgical outcome and prognosis of pancreatic neuroendocrine tumors. Pancreas, 2014. 43(7): p. 1003–8.

    Article  PubMed  Google Scholar 

  10. Morin, E., et al., Hormone profiling, WHO 2010 grading, and AJCC/UICC staging in pancreatic neuroendocrine tumor behavior. Cancer Med, 2013. 2(5): p. 701–11.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Liu, T.C., et al., Comparison of WHO Classifications (2004, 2010), the Hochwald grading system, and AJCC and ENETS staging systems in predicting prognosis in locoregional well-differentiated pancreatic neuroendocrine tumors. Am J Surg Pathol, 2013. 37(6): p. 853–9.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Zamora, V., et al., Immunohistochemical expression of somatostatin receptors in digestive endocrine tumours. Dig Liver Dis, 2010. 42(3): p. 220–5.

    Article  PubMed  CAS  Google Scholar 

  13. Pirasteh, A., et al., PET/MRI for neuroendocrine tumors: a match made in heaven or just another hype? Clin Transl Imaging, 2019. 7(6): p. 405–413.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jawlakh, H., et al., 68Ga-DOTATOC-PET/MRI and 11C-5-HTP-PET/MRI are superior to 68Ga-DOTATOC-PET/CT for neuroendocrine tumour imaging. Journal of Neuroendocrinology, 2021. 33(6): p. e12981.

    Article  PubMed  CAS  Google Scholar 

  15. Ehman, E.C., et al., PET/MRI: Where might it replace PET/CT? J Magn Reson Imaging, 2017. 46(5): p. 1247–1262.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Galgano, S.J., et al., Applications of PET/MRI in Abdominopelvic Oncology. Radiographics, 2021. 41(6): p. 1750–1765.

    Article  PubMed  Google Scholar 

  17. Miles, K.A., S.A. Voo, and A.M. Groves, Additional clinical value for PET/MRI in oncology: moving beyond simple diagnosis. Journal of Nuclear Medicine, 2018. 59(7): p. 1028–1032.

    Article  PubMed  CAS  Google Scholar 

  18. Cabello, J. and S.I. Ziegler, Advances in PET/MR instrumentation and image reconstruction. Br J Radiol, 2018. 91(1081): p. 20160363.

    Article  PubMed  Google Scholar 

  19. Hope, T.A., et al., Simultaneous (68)Ga-DOTA-TOC PET/MRI with gadoxetate disodium in patients with neuroendocrine tumor. Abdom Imaging, 2015. 40(6): p. 1432–40.

    Article  PubMed  Google Scholar 

  20. Panda, A., et al., PET/Magnetic Resonance Imaging Applications in Abdomen and Pelvis. Magn Reson Imaging Clin N Am, 2020. 28(3): p. 369–380.

    Article  PubMed  Google Scholar 

  21. Catana, C., Motion correction options in PET/MRI. Semin Nucl Med, 2015. 45(3): p. 212–23.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lalush, D.S., Magnetic Resonance-Derived Improvements in PET Imaging. Magn Reson Imaging Clin N Am, 2017. 25(2): p. 257–272.

    Article  PubMed  Google Scholar 

  23. Fuin, N., et al., Concurrent Respiratory Motion Correction of Abdominal PET and Dynamic Contrast-Enhanced-MRI Using a Compressed Sensing Approach. J Nucl Med, 2018. 59(9): p. 1474–1479.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Izquierdo-Garcia, D., et al., Comparison of MR-based attenuation correction and CT-based attenuation correction of whole-body PET/MR imaging. Eur J Nucl Med Mol Imaging, 2014. 41(8): p. 1574–84.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Martinez-Möller, A., et al., Workflow and scan protocol considerations for integrated whole-body PET/MRI in oncology. Journal of Nuclear Medicine, 2012. 53(9): p. 1415–1426.

    Article  PubMed  Google Scholar 

  26. Martin, S., et al., Neuroendocrine neoplasm imaging: protocols by site of origin. Abdominal Radiology, 2022: p. 1–15.

  27. Choi, S.J., et al., Diagnostic value of [(68)Ga]Ga-DOTA-labeled-somatostatin analogue PET/MRI for detecting liver metastasis in patients with neuroendocrine tumors: a systematic review and meta-analysis. Eur Radiol, 2022. 32(7): p. 4628–4637.

    Article  PubMed  CAS  Google Scholar 

  28. Berzaczy, D., et al., 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, 2017. 42(9): p. 669–674.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Sawicki, L.M., et al., Evaluation of 68Ga-DOTATOC PET/MRI for whole-body staging of neuroendocrine tumours in comparison with 68Ga-DOTATOC PET/CT. European Radiology, 2017. 27(10): p. 4091–4099.

    Article  PubMed  Google Scholar 

  30. Schreiter, N.F., et al., Evaluation of the potential of PET–MRI fusion for detection of liver metastases in patients with neuroendocrine tumours. Eur Radiol, 2012. 22(2): p. 458–67.

    Article  PubMed  Google Scholar 

  31. Hayoz, R., et al., The combination of hepatobiliary phase with Gd-EOB-DTPA and DWI is highly accurate for the detection and characterization of liver metastases from neuroendocrine tumor. Eur Radiol, 2020. 30(12): p. 6593–6602.

    Article  PubMed  CAS  Google Scholar 

  32. Tirumani, S.H., et al., Value of hepatocellular phase imaging after intravenous gadoxetate disodium for assessing hepatic metastases from gastroenteropancreatic neuroendocrine tumors: comparison with other MRI pulse sequences and with extracellular agent. Abdominal Radiology, 2018. 43(9): p. 2329–2339.

    Article  PubMed  Google Scholar 

  33. Morse, B., et al., Magnetic Resonance Imaging of Neuroendocrine Tumor Hepatic Metastases: Does Hepatobiliary Phase Imaging Improve Lesion Conspicuity and Interobserver Agreement of Lesion Measurements? Pancreas, 2017. 46(9).

  34. Seith, F., et al., Fast non-enhanced abdominal examination protocols in PET/MRI for patients with neuroendocrine tumors (NET): comparison to multiphase contrast-enhanced PET/CT. La radiologia medica, 2018. 123(11): p. 860–870.

    Article  PubMed  Google Scholar 

  35. Alshaima Alshammari, M.M., Rizwan Syed, Evangelia Skoura, Sofia Michopoulou, Fulvio Zaccagna, Jamshed Bomanji, Francesco Fraioli, Impact of Integrated Whole Body 68Ga PET/MR Imaging in Comparison with 68Ga PET/CT in Lesions Detection and Diagnosis of Suspected Neuroendocrine Tumours. American Journal of Internal Medicine, 2019. 7(4).

  36. Barachini, O., et al., The impact of 18F-FDOPA-PET/MRI image fusion in detecting liver metastasis in patients with neuroendocrine tumors of the gastrointestinal tract. BMC Med Imaging, 2020. 20(1): p. 22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Beiderwellen, K., et al., Hybrid imaging of the bowel using PET/MR enterography: Feasibility and first results. European Journal of Radiology, 2016. 85(2): p. 414–421.

    Article  PubMed  Google Scholar 

  38. Saleh, M., et al., New frontiers in imaging including radiomics updates for pancreatic neuroendocrine neoplasms. Abdom Radiol (NY), 2022. 47(9): p. 3078–3100.

    Article  PubMed  Google Scholar 

  39. Adams, L.C., et al., Quantitative 3D Assessment of (68)Ga-DOTATOC PET/MRI with Diffusion-Weighted Imaging to Assess Imaging Markers for Gastroenteropancreatic Neuroendocrine Tumors: Preliminary Results. J Nucl Med, 2020. 61(7): p. 1021–1027.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Weber, M., et al., Textural analysis of hybrid DOTATOC-PET/MRI and its association with histological grading in patients with liver metastases from neuroendocrine tumors. Nucl Med Commun, 2020. 41(4): p. 363–369.

    Article  PubMed  CAS  Google Scholar 

  41. Bruckmann, N.M., et al., Correlation between contrast enhancement, standardized uptake value (SUV), and diffusion restriction (ADC) with tumor grading in patients with therapy-naive neuroendocrine neoplasms using hybrid (68)Ga-DOTATOC PET/MRI. Eur J Radiol, 2021. 137: p. 109588.

    Article  PubMed  Google Scholar 

  42. Mapelli, P., et al., (68)Ga-DOTATOC PET/MR imaging and radiomic parameters in predicting histopathological prognostic factors in patients with pancreatic neuroendocrine well-differentiated tumours. Eur J Nucl Med Mol Imaging, 2022. 49(7): p. 2352–2363.

    Article  PubMed  CAS  Google Scholar 

  43. Remes, S.M., et al., Immunohistochemical Expression of Somatostatin Receptor Subtypes in a Panel of Neuroendocrine Neoplasias. J Histochem Cytochem, 2019. 67(10): p. 735–743.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Reubi, J.C., Somatostatin and other Peptide receptors as tools for tumor diagnosis and treatment. Neuroendocrinology, 2004. 80 Suppl 1: p. 51–6.

    Article  PubMed  CAS  Google Scholar 

  45. Pauwels, E., et al., Somatostatin receptor PET ligands - the next generation for clinical practice. Am J Nucl Med Mol Imaging, 2018. 8(5): p. 311–331.

    PubMed  PubMed Central  CAS  Google Scholar 

  46. Johnbeck, C.B., et al., Head-to-Head Comparison of (64)Cu-DOTATATE and (68)Ga-DOTATOC PET/CT: A Prospective Study of 59 Patients with Neuroendocrine Tumors. J Nucl Med, 2017. 58(3): p. 451–457.

    Article  PubMed  CAS  Google Scholar 

  47. Yang, J., et al., Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: a meta-analysis. Acta Radiol, 2014. 55(4): p. 389–98.

    Article  PubMed  Google Scholar 

  48. Mayerhoefer, M.E., et al., Gadoxetate-enhanced versus diffusion-weighted MRI for fused Ga-68-DOTANOC PET/MRI in patients with neuroendocrine tumours of the upper abdomen. Eur Radiol, 2013. 23(7): p. 1978–85.

    Article  PubMed  Google Scholar 

  49. Nicolas, G.P., et al., Sensitivity Comparison of (68)Ga-OPS202 and (68)Ga-DOTATOC PET/CT in Patients with Gastroenteropancreatic Neuroendocrine Tumors: A Prospective Phase II Imaging Study. J Nucl Med, 2018. 59(6): p. 915–921.

    Article  PubMed  CAS  Google Scholar 

  50. Mittra, E.S., Neuroendocrine Tumor Therapy: (177)Lu-DOTATATE. AJR Am J Roentgenol, 2018. 211(2): p. 278–285.

    Article  PubMed  Google Scholar 

  51. Park, S., et al., Somatostatin Receptor Imaging and Theranostics: Current Practice and Future Prospects. J Nucl Med, 2021. 62(10): p. 1323–1329.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Werner, R.A., et al., SSTR-RADS Version 1.0 as a Reporting System for SSTR PET Imaging and Selection of Potential PRRT Candidates: A Proposed Standardization Framework. J Nucl Med, 2018. 59(7): p. 1085–1091.

  53. Werner, R.A., et al., High Interobserver Agreement for the Standardized Reporting System SSTR-RADS 1.0 on Somatostatin Receptor PET/CT. J Nucl Med, 2021. 62(4): p. 514–520.

  54. Garin, E., et al., Predictive value of 18F-FDG PET and somatostatin receptor scintigraphy in patients with metastatic endocrine tumors. J Nucl Med, 2009. 50(6): p. 858–64.

    Article  PubMed  CAS  Google Scholar 

  55. Hindie, E., The NETPET Score: Combining FDG and Somatostatin Receptor Imaging for Optimal Management of Patients with Metastatic Well-Differentiated Neuroendocrine Tumors. Theranostics, 2017. 7(5): p. 1159–1163.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Chan, D.L., et al., Dual Somatostatin Receptor/FDG PET/CT Imaging in Metastatic Neuroendocrine Tumours: Proposal for a Novel Grading Scheme with Prognostic Significance. Theranostics, 2017. 7(5): p. 1149–1158.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Shah, M.H., et al., Neuroendocrine and Adrenal Tumors, Version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw, 2021. 19(7): p. 839–868.

  58. Hope, T.A., et al., NANETS/SNMMI Consensus Statement on Patient Selection and Appropriate Use of (177)Lu-DOTATATE Peptide Receptor Radionuclide Therapy. J Nucl Med, 2020. 61(2): p. 222–227.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Roll, W., et al., Imaging and liquid biopsy in the prediction and evaluation of response to PRRT in neuroendocrine tumors: implications for patient management. Eur J Nucl Med Mol Imaging, 2021. 48(12): p. 4016–4027.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Malczewska, A., et al., The clinical applications of a multigene liquid biopsy (NETest) in neuroendocrine tumors. Adv Med Sci, 2020. 65(1): p. 18–29.

    Article  PubMed  CAS  Google Scholar 

  61. Galgano, S.J., et al., Imaging of Neuroendocrine Neoplasms: Monitoring Treatment Response-AJR Expert Panel Narrative Review. AJR Am J Roentgenol, 2022. 218(5): p. 767–780.

    Article  PubMed  Google Scholar 

  62. Modlin, I.M., et al., The NETest: The Clinical Utility of Multigene Blood Analysis in the Diagnosis and Management of Neuroendocrine Tumors. Endocrinol Metab Clin North Am, 2018. 47(3): p. 485–504.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Modlin, I.M., et al., The clinical utility of a novel blood-based multi-transcriptome assay for the diagnosis of neuroendocrine tumors of the gastrointestinal tract. Am J Gastroenterol, 2015. 110(8): p. 1223–32.

    Article  PubMed  CAS  Google Scholar 

  64. Oberg, K., et al., A meta-analysis of the accuracy of a neuroendocrine tumor mRNA genomic biomarker (NETest) in blood. Ann Oncol, 2020. 31(2): p. 202–212.

    Article  PubMed  CAS  Google Scholar 

  65. Modlin, I.M., et al., Molecular Genomic Assessment Using a Blood-based mRNA Signature (NETest) is Cost-effective and Predicts Neuroendocrine Tumor Recurrence With 94% Accuracy. Ann Surg, 2021. 274(3): p. 481–490.

    Article  PubMed  Google Scholar 

  66. Modlin, I.M., et al., Early Identification of Residual Disease After Neuroendocrine Tumor Resection Using a Liquid Biopsy Multigenomic mRNA Signature (NETest). Ann Surg Oncol, 2021. 28(12): p. 7506–7517.

    Article  PubMed  Google Scholar 

  67. Kaewput, C., S. Suppiah, and S. Vinjamuri, Correlation between Standardized Uptake Value of (68)Ga-DOTA-NOC Positron Emission Tomography/Computed Tomography and Pathological Classification of Neuroendocrine Tumors. World J Nucl Med, 2018. 17(1): p. 34–40.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Teker, F. and U. Elboga, Is SUVmax a useful marker for progression-free survival in patients with metastatic GEP-NET receiving (177)Lu-DOTATATE therapy? Hell J Nucl Med, 2021. 24(2): p. 122–131.

    PubMed  Google Scholar 

  69. Carlsen, E.A., et al., (64)Cu-DOTATATE PET/CT and Prediction of Overall and Progression-Free Survival in Patients with Neuroendocrine Neoplasms. J Nucl Med, 2020. 61(10): p. 1491–1497.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Thuillier, P., et al., Diagnostic performance of a whole-body dynamic 68GA-DOTATOC PET/CT acquisition to differentiate physiological uptake of pancreatic uncinate process from pancreatic neuroendocrine tumor. Medicine (Baltimore), 2020. 99(33): p. e20021.

    Article  PubMed  CAS  Google Scholar 

  71. Broski, S.M., et al., Clinical PET/MRI: 2018 Update. AJR Am J Roentgenol, 2018. 211(2): p. 295–313.

    Article  PubMed  Google Scholar 

  72. Giesel, F.L., et al., Comparison of neuroendocrine tumor detection and characterization using DOTATOC-PET in correlation with contrast enhanced CT and delayed contrast enhanced MRI. Eur J Radiol, 2012. 81(10): p. 2820–5.

    Article  PubMed  CAS  Google Scholar 

  73. Samarin, A., et al., PET/MR imaging of bone lesions--implications for PET quantification from imperfect attenuation correction. Eur J Nucl Med Mol Imaging, 2012. 39(7): p. 1154–60.

    Article  PubMed  Google Scholar 

  74. Antoch, G., et al., Whole-body dual-modality PET/CT and whole-body MRI for tumor staging in oncology. JAMA, 2003. 290(24): p. 3199–206.

    Article  PubMed  CAS  Google Scholar 

  75. Mayerhoefer, M.E., et al., 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, 2020. 47(1): p. 51–60.

    Article  PubMed  CAS  Google Scholar 

  76. Alshammari, A. and M. Masoomi, Impact of Integrated Whole Body 68Ga PET/MR Imaging in Comparison with 68Ga PET/CT in Lesions Detection and Diagnosis of Suspected Neuroendocrine Tumours. 2019.

Download references

Funding

No financial support/funding.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to this paper with the conception and design of the study, literature review and analysis, drafting and critical revision and editing, and final approval of the final version.

Corresponding author

Correspondence to Luis Calimano-Ramirez.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Virarkar, M.K., Montanarella, M., Itani, M. et al. PET/MRI imaging in neuroendocrine neoplasm. Abdom Radiol 48, 3585–3600 (2023). https://doi.org/10.1007/s00261-022-03757-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-022-03757-1

Keywords

Navigation