Skip to main content
SpringerLink
Log in

Pancreatic neuroendocrine tumors: tailoring imaging to specific clinical scenarios

  • Special Section: Neuroendocrine Neoplasms
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

The clinical and imaging presentation of pancreatic neuroendocrine tumors (PanNETs) is variable and depends on tumor grade, stage, and functional status. This degree of variability combined with a multitude of treatment options and imaging modalities results in complexity when choosing the most appropriate imaging studies across various clinical scenarios. While various guidelines exist in the management and evaluation of PanNETs, there is an overall lack of consensus and detail regarding optimal imaging guidelines and protocols. This manuscript aims to fill gaps where current guidelines may lack specificity regarding the choice of the most appropriate imaging study in the diagnosis, treatment planning, monitoring, and surveillance of PanNETs under various clinical scenarios.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. McKenna LR, Edil BH. Update on pancreatic neuroendocrine tumors. Gland Surg. 2014;3(4):258-75. doi: https://doi.org/10.3978/j.issn.2227-684X.2014.06.03.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, et al. One hundred years after "carcinoid": epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26(18):3063-72. doi: https://doi.org/10.1200/JCO.2007.15.4377

    Article  PubMed  Google Scholar 

  3. Westrick RJ, Eitzman DT. Plasminogen activator inhibitor-1 in vascular thrombosis. Curr Drug Targets. 2007;8(9):966-1002. doi: https://doi.org/10.2174/138945007781662328.

    Article  PubMed  Google Scholar 

  4. https://www.cancer.org/cancer/pancreatic-neuroendocrine-tumor/about/key-statistics.html. Accessed 4/4/2022.

  5. Lawrence B, Gustafsson BI, Chan A, Svejda B, Kidd M, Modlin IM. The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am. 2011;40(1):1-18, vii. doi: https://doi.org/10.1016/j.ecl.2010.12.005.

    Article  PubMed  Google Scholar 

  6. Lewis RB, Lattin GE, Jr., Paal E. Pancreatic endocrine tumors: radiologic-clinicopathologic correlation. Radiographics. 2010;30(6):1445-64. doi: https://doi.org/10.1148/rg.306105523.

    Article  PubMed  Google Scholar 

  7. Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, et al. ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology. 2016;103(2):153-71. doi: https://doi.org/10.1159/000443171.

    Article  CAS  PubMed  Google Scholar 

  8. Capelli P, Fassan M, Scarpa A. Pathology - grading and staging of GEP-NETs. Best Pract Res Clin Gastroenterol. 2012;26(6):705-17. doi: https://doi.org/10.1016/j.bpg.2013.01.003.

    Article  PubMed  Google Scholar 

  9. Gastrointestinal Pathology Study Group of Korean Society of P, Cho MY, Kim JM, Sohn JH, Kim MJ, Kim KM, et al. Current Trends of the Incidence and Pathological Diagnosis of Gastroenteropancreatic Neuroendocrine Tumors (GEP-NETs) in Korea 2000-2009: Multicenter Study. Cancer Res Treat. 2012;44(3):157-65. doi: https://doi.org/10.4143/crt.2012.44.3.157.

    Article  Google Scholar 

  10. Halfdanarson TR, Rabe KG, Rubin J, Petersen GM. Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol. 2008;19(10):1727-33. doi: https://doi.org/10.1093/annonc/mdn351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hope TA, Bergsland EK, Bozkurt MF, Graham M, Heaney AP, Herrmann K, et al. Appropriate Use Criteria for Somatostatin Receptor PET Imaging in Neuroendocrine Tumors. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2018;59(1):66-74. doi: https://doi.org/10.2967/jnumed.117.202275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. https://www.nccn.org/professionals/physician_gls/pdf/neuroendocrine_blocks.pdf. Accessed 01/04/2022.

  13. Howe JR, Merchant NB, Conrad C, Keutgen XM, Hallet J, Drebin JA, et al. The North American Neuroendocrine Tumor Society Consensus Paper on the Surgical Management of Pancreatic Neuroendocrine Tumors. Pancreas. 2020;49(1):1-33. doi: https://doi.org/10.1097/MPA.0000000000001454.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sundin A, Arnold R, Baudin E, Cwikla JB, Eriksson B, Fanti S, et al. ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: Radiological, Nuclear Medicine & Hybrid Imaging. Neuroendocrinology. 2017;105(3):212-44. doi: https://doi.org/10.1159/000471879.

    Article  CAS  PubMed  Google Scholar 

  15. Galgano SJ, Iravani A, Bodei L, El-Haddad G, Hofman MS, Kong G. Imaging of Neuroendocrine Neoplasms: Monitoring Treatment Response-AJR Expert Panel Narrative Review. AJR Am J Roentgenol. 2022. doi: https://doi.org/10.2214/AJR.21.27159.

    Article  PubMed  Google Scholar 

  16. Rockall AG, Reznek RH. Imaging of neuroendocrine tumours (CT/MR/US). Best Pract Res Clin Endocrinol Metab. 2007;21(1):43-68. doi: https://doi.org/10.1016/j.beem.2007.01.003.

    Article  CAS  PubMed  Google Scholar 

  17. Almeida RR, Lo GC, Patino M, Bizzo B, Canellas R, Sahani DV. Advances in Pancreatic CT Imaging. AJR Am J Roentgenol. 2018;211(1):52-66. doi: https://doi.org/10.2214/AJR.17.18665.

    Article  PubMed  Google Scholar 

  18. Kambadakone AR, Fung A, Gupta RT, Hope TA, Fowler KJ, Lyshchik A, et al. LI-RADS technical requirements for CT, MRI, and contrast-enhanced ultrasound. Abdom Radiol (NY). 2018;43(1):56-74. doi: https://doi.org/10.1007/s00261-017-1325-y.

    Article  PubMed  Google Scholar 

  19. Tamm EP, Bhosale P, Lee JH, Rohren EM. State-of-the-art Imaging of Pancreatic Neuroendocrine Tumors. Surg Oncol Clin N Am. 2016;25(2):375-400. doi: https://doi.org/10.1016/j.soc.2015.11.007.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Chiti G, Grazzini G, Cozzi D, Danti G, Matteuzzi B, Granata V, et al. Imaging of Pancreatic Neuroendocrine Neoplasms. International Journal of Environmental Research and Public Health. 2021;18(17):8895.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Kuo EJ, Salem RR. Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol. 2013;20(9):2815-21. doi: https://doi.org/10.1245/s10434-013-3005-7.

    Article  PubMed  Google Scholar 

  22. Sadot E, Reidy-Lagunes DL, Tang LH, Do RK, Gonen M, D'Angelica MI, et al. Observation versus Resection for Small Asymptomatic Pancreatic Neuroendocrine Tumors: A Matched Case-Control Study. Ann Surg Oncol. 2016;23(4):1361-70. doi: https://doi.org/10.1245/s10434-015-4986-1.

    Article  PubMed  Google Scholar 

  23. Lee LC, Grant CS, Salomao DR, Fletcher JG, Takahashi N, Fidler JL, et al. Small, nonfunctioning, asymptomatic pancreatic neuroendocrine tumors (PNETs): role for nonoperative management. Surgery. 2012;152(6):965-74. doi: https://doi.org/10.1016/j.surg.2012.08.038.

    Article  PubMed  Google Scholar 

  24. Wild D, Bomanji JB, Benkert P, Maecke H, Ell PJ, Reubi JC, et al. Comparison of 68Ga-DOTANOC and 68Ga-DOTATATE PET/CT within patients with gastroenteropancreatic neuroendocrine tumors. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2013;54(3):364-72. doi: https://doi.org/10.2967/jnumed.112.111724.

    Article  CAS  PubMed  Google Scholar 

  25. Ambrosini V, Campana D, Bodei L, Nanni C, Castellucci P, Allegri V, et al. 68Ga-DOTANOC PET/CT clinical impact in patients with neuroendocrine tumors. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2010;51(5):669-73. doi: https://doi.org/10.2967/jnumed.109.071712.

    Article  PubMed  Google Scholar 

  26. Naswa N, Sharma P, Soundararajan R, Karunanithi S, Nazar AH, Kumar R, et al. Diagnostic performance of somatostatin receptor PET/CT using 68Ga-DOTANOC in gastrinoma patients with negative or equivocal CT findings. Abdom Imaging. 2013;38(3):552-60. doi: https://doi.org/10.1007/s00261-012-9925-z.

    Article  PubMed  Google Scholar 

  27. Falconi M, Bartsch DK, Eriksson B, Kloppel G, Lopes JM, O'Connor JM, et al. ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms of the digestive system: well-differentiated pancreatic non-functioning tumors. Neuroendocrinology. 2012;95(2):120-34. doi: https://doi.org/10.1159/000335587.

    Article  CAS  PubMed  Google Scholar 

  28. 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(1):80-7. doi: https://doi.org/10.1007/s12020-012-9631-1.

    Article  CAS  PubMed  Google Scholar 

  29. Jung JG, Lee KT, Woo YS, Lee JK, Lee KH, Jang KT, et al. Behavior of Small, Asymptomatic, Nonfunctioning Pancreatic Neuroendocrine Tumors (NF-PNETs). Medicine (Baltimore). 2015;94(26):e983. doi: https://doi.org/10.1097/MD.0000000000000983.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Partelli S, Cirocchi R, Crippa S, Cardinali L, Fendrich V, Bartsch DK, et al. Systematic review of active surveillance versus surgical management of asymptomatic small non-functioning pancreatic neuroendocrine neoplasms. Br J Surg. 2017;104(1):34-41. doi: https://doi.org/10.1002/bjs.10312.

    Article  CAS  PubMed  Google Scholar 

  31. Dromain C, Baere Td, Lumbroso J, Caillet H, Laplanche A, Boige V, et al. Detection of Liver Metastases From Endocrine Tumors: A Prospective Comparison of Somatostatin Receptor Scintigraphy, Computed Tomography, and Magnetic Resonance Imaging. Journal of Clinical Oncology. 2005;23(1):70-8. doi: https://doi.org/10.1200/jco.2005.01.013.

    Article  PubMed  Google Scholar 

  32. Nigri G, Petrucciani N, Debs T, Mangogna LM, Crovetto A, Moschetta G, et al. Treatment options for PNET liver metastases: a systematic review. World J Surg Oncol. 2018;16(1):142. doi: https://doi.org/10.1186/s12957-018-1446-y.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Haider M, Jiang BG, Parker JA, Bullock AJ, Goehler A, Tsai LL. Use of MRI and Ga-68 DOTATATE for the detection of neuroendocrine liver metastases. Abdom Radiol (NY). 2022;47(2):586-95. doi: https://doi.org/10.1007/s00261-021-03341-z.

    Article  PubMed  Google Scholar 

  34. Bodei L, Sundin A, Kidd M, Prasad V, Modlin IM. The status of neuroendocrine tumor imaging: from darkness to light? Neuroendocrinology. 2015;101(1):1-17. doi: https://doi.org/10.1159/000367850.

    Article  CAS  PubMed  Google Scholar 

  35. Hayoz R, Vietti-Violi N, Duran R, Knebel JF, Ledoux JB, Dromain C. 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):6593-602. doi: https://doi.org/10.1007/s00330-020-06930-6.

    Article  CAS  PubMed  Google Scholar 

  36. Morse B, Jeong D, Thomas K, Diallo D, Strosberg JR. 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):1219-24. doi: https://doi.org/10.1097/MPA.0000000000000920.

    Article  PubMed  Google Scholar 

  37. Hermanek P, Wittekind C. Residual tumor (R) classification and prognosis. Semin Surg Oncol. 1994;10(1):12-20. doi: https://doi.org/10.1002/ssu.2980100105.

    Article  CAS  PubMed  Google Scholar 

  38. Jilesen AP, van Eijck CH, in't Hof KH, van Dieren S, Gouma DJ, van Dijkum EJ. Postoperative Complications, In-Hospital Mortality and 5-Year Survival After Surgical Resection for Patients with a Pancreatic Neuroendocrine Tumor: A Systematic Review. World J Surg. 2016;40(3):729-48. doi: https://doi.org/10.1007/s00268-015-3328-6.

    Article  PubMed  Google Scholar 

  39. Singh S, Chan DL, Moody L, Liu N, Fischer HD, Austin PC, et al. Recurrence in Resected Gastroenteropancreatic Neuroendocrine Tumors. JAMA Oncol. 2018;4(4):583-5. doi: https://doi.org/10.1001/jamaoncol.2018.0024.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Jackson T, Darwish M, Cho E, Nagatomo K, Osman H, Jeyarajah DR. 68Ga-DOTATATE PET/CT compared to standard imaging in metastatic neuroendocrine tumors: a more sensitive test to detect liver metastasis? Abdom Radiol (NY). 2021;46(7):3179-83. doi: https://doi.org/10.1007/s00261-021-02990-4.

    Article  PubMed  Google Scholar 

  41. Frilling A, Modlin IM, Kidd M, Russell C, Breitenstein S, Salem R, et al. Recommendations for management of patients with neuroendocrine liver metastases. Lancet Oncol. 2014;15(1):e8-21. doi: https://doi.org/10.1016/S1470-2045(13)70362-0.

    Article  PubMed  Google Scholar 

  42. Ronot M, Clift AK, Baum RP, Singh A, Kulkarni HR, Frilling A, et al. Morphological and Functional Imaging for Detecting and Assessing the Resectability of Neuroendocrine Liver Metastases. Neuroendocrinology. 2018;106(1):74-88. doi: https://doi.org/10.1159/000479293.

    Article  CAS  PubMed  Google Scholar 

  43. Spina JC, Hume I, Pelaez A, Peralta O, Quadrelli M, Garcia Monaco R. Expected and Unexpected Imaging Findings after (90)Y Transarterial Radioembolization for Liver Tumors. Radiographics. 2019;39(2):578-95. doi: https://doi.org/10.1148/rg.2019180095.

    Article  PubMed  Google Scholar 

  44. Sadowski SM, Neychev V, Millo C, Shih J, Nilubol N, Herscovitch P, et al. Prospective Study of 68Ga-DOTATATE Positron Emission Tomography/Computed Tomography for Detecting Gastro-Entero-Pancreatic Neuroendocrine Tumors and Unknown Primary Sites. J Clin Oncol. 2016;34(6):588-96. doi: https://doi.org/10.1200/JCO.2015.64.0987.

    Article  CAS  PubMed  Google Scholar 

  45. Fujimori N, Miki M, Lee L, Matsumoto K, Takamatsu Y, Takaoka T, et al. Natural history and clinical outcomes of pancreatic neuroendocrine neoplasms based on the WHO 2017 classification; a single-center experience of 30 years. Pancreatology. 2020;20(4):709-15. doi: https://doi.org/10.1016/j.pan.2020.04.003.

    Article  PubMed  Google Scholar 

  46. Kwekkeboom DJ, de Herder WW, Kam BL, van Eijck CH, van Essen M, Kooij PP, et al. Treatment with the radiolabeled somatostatin analog [177 Lu-DOTA 0,Tyr3]octreotate: toxicity, efficacy, and survival. J Clin Oncol. 2008;26(13):2124-30. doi: https://doi.org/10.1200/JCO.2007.15.2553.

    Article  CAS  PubMed  Google Scholar 

  47. Braat A, Kappadath SC, Ahmadzadehfar H, Stothers CL, Frilling A, Deroose CM, et al. Radioembolization with (90)Y Resin Microspheres of Neuroendocrine Liver Metastases: International Multicenter Study on Efficacy and Toxicity. Cardiovasc Intervent Radiol. 2019;42(3):413-25. doi: https://doi.org/10.1007/s00270-018-2148-0.

    Article  CAS  PubMed  Google Scholar 

  48. Zhang P, Yu J, Li J, Shen L, Li N, Zhu H, et al. Clinical and Prognostic Value of PET/CT Imaging with Combination of (68)Ga-DOTATATE and (18)F-FDG in Gastroenteropancreatic Neuroendocrine Neoplasms. Contrast Media Mol Imaging. 2018;2018:2340389. doi: https://doi.org/10.1155/2018/2340389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mapelli P, Partelli S, Salgarello M, Doraku J, Muffatti F, Schiavo Lena M, et al. Dual Tracer 68Ga-DOTATOC and 18F-FDG PET Improve Preoperative Evaluation of Aggressiveness in Resectable Pancreatic Neuroendocrine Neoplasms. Diagnostics (Basel). 2021;11(2). doi: https://doi.org/10.3390/diagnostics11020192.

    Article  PubMed  Google Scholar 

  50. Alevroudis E, Spei ME, Chatziioannou SN, Tsoli M, Wallin G, Kaltsas G, et al. Clinical Utility of (18)F-FDG PET in Neuroendocrine Tumors Prior to Peptide Receptor Radionuclide Therapy: A Systematic Review and Meta-Analysis. Cancers (Basel). 2021;13(8). doi: https://doi.org/10.3390/cancers13081813.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all members of the Society of Abdominal Radiology Disease-Focused Panel on Neuroendocrine Tumors (SAR-NET-DFP).

Author information

Authors and Affiliations

  1. Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd, St. Louis, MO, 63110, USA

    Katerina S. Konstantinoff & Malak Itani

  2. Department of Radiology, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX, 77030, USA

    Ajaykumar C. Morani & Priya R. Bhosale

  3. Department of Radiology and Biomedical Imaging, The University of California, San Francisco, 185 Berry Street Lobby 6, San Francisco, CA, 94107, USA

    Thomas A. Hope

  4. Department of Radiology, Michigan Medicine, 1500 E Medical Center Dr, Ann Arbor, MI, 48109, USA

    Isaac R. Francis

  5. Department of Radiology, Mayo Clinic Hospital, 5777 E. Mayo Blvd, Phoenix, AZ, 85054, USA

    Motoyo Yano

  6. Department of Radiology, University of Washington, 1959 NE Pacific St, Seattle, WA, 98195, USA

    Amir Iravani

  7. Department of Internal Medicine, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO, 63110, USA

    Nikolaos A. Trikalinos

Authors
  1. Katerina S. Konstantinoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ajaykumar C. Morani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas A. Hope
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Priya R. Bhosale
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isaac R. Francis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Motoyo Yano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Amir Iravani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nikolaos A. Trikalinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Malak Itani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Malak Itani.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests that are related to the work submitted for publication.

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

Konstantinoff, K.S., Morani, A.C., Hope, T.A. et al. Pancreatic neuroendocrine tumors: tailoring imaging to specific clinical scenarios. Abdom Radiol 48, 1843–1853 (2023). https://doi.org/10.1007/s00261-022-03737-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-022-03737-5

Keywords

Search

Navigation