Japanese Journal of Radiology

, Volume 35, Issue 5, pp 242–253 | Cite as

Is the combination of MR and CT findings useful in determining the tumor grade of pancreatic neuroendocrine tumors?

  • Fumihito ToshimaEmail author
  • Dai Inoue
  • Takahiro Komori
  • Kotaro Yoshida
  • Norihide Yoneda
  • Tetsuya Minami
  • Osamu Matsui
  • Hiroko Ikeda
  • Toshifumi Gabata
Original Article



To retrospectively elucidate the findings useful in determining the tumor grade of pancreatic neuroendocrine tumors (PNETs) by combined assessment of magnetic resonance (MR) and dynamic computed tomography (CT) images.

Materials and methods

Eighty-nine patients with PNETs (96 lesions) were included, and classified as G1, 59; G2, 29; and G3, 8 lesions. Image analysis included lesion diameter, shape, enhancement pattern on arterial phase (AP) and delayed phase CT images, calcification, cystic portion, main pancreatic duct dilatation, signal-intensity on T1-, T2-weighted MR images, and appearance of apparent diffusion coefficient (ADC).


Significant differences among G1, G2, and G3 groups were noted in tumor maximal diameter (p < 0.0001), shape (p < 0.0001), enhancement pattern on AP image (p < 0.0001), cystic portion (p = 0.012), and ADC finding. In multivariate analysis, ADC finding was the independent factor (p = 0.002). The combination findings of low ADC ratio (ADC value of the lesion/ADC value of the parenchyma <0.94), not homogeneous hyper-attenuation, lobulated shape, and hyper-intensity on T2-weighted image were suggestive of G2 or G3 with a probability of 100%. Conversely, all lesions with high ADC ratio and small size (≤25 mm) belonged to the G1 group.


Combined assessment of MR and CT findings could improve the prediction of tumor grading in PNETs.


Pancreatic neuroendocrine tumors Neuroendocrine tumors G1 Neuroendocrine tumors G2 Neuroendocrine carcinoma Magnetic resonance imaging (MRI) Computed tomography (CT) 



The authors state that this work has not received any funding.

Conflict of interest

The authors declare no conflict of interest associated with this manuscript.


  1. 1.
    Hruban RH, Pitman MB, Klimstra DS. Tumors of the pancreas. AFIP atlas of tumor pathology. 4th series fascicle 6. Washington: American Registry of Pathology; 2007.Google Scholar
  2. 2.
    Sahani DV, Bonaffini PA, Del Castillo CF, Blake MA. Gastroenteropancreatic neuroendocrine tumors: role of imaging in diagnosis and management. Radiology. 2013;266:38–61.CrossRefPubMedGoogle Scholar
  3. 3.
    Klimstra DS, Arnold R, Capella, et al. Neuroendocrine neoplasms of the pancreas. In: Bosman F, Carneiro F, Hruban RH, Theise ND, editors. WHO classification of tumours of the digestive system. 4th ed. Lyon: IARC Press; 2010. p. 322–6.Google Scholar
  4. 4.
    Rindi G. The ENETS guidelines: the new TNM classification system. Tumori. 2010;96:806–9.PubMedGoogle Scholar
  5. 5.
    Rindi G, Klöppel G, Alhman H, et al. TNM staging of foregut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2006;449:395–401.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Rindi G, Klöppel G, Couvelard A, et al. TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2007;451:757–62.CrossRefPubMedGoogle Scholar
  7. 7.
    Rindi G, Falconi M, Klersy C, et al. TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst. 2012;10:764–77.CrossRefGoogle Scholar
  8. 8.
    Ekeblad S, Skogseid B, Dunder K, Öberg K, Eriksson B. Prognostic factors and survival in 324 patients with pancreatic endocrine tumor treated at a single institution. Clin Cancer Res. 2008;14:7798–803.CrossRefPubMedGoogle Scholar
  9. 9.
    Bettini R, Partelli S, Boninsegna L, et al. Tumor size correlates with malignancy in nonfunctioning pancreatic endocrine tumor. Surgery. 2011;150:75–82.CrossRefPubMedGoogle Scholar
  10. 10.
    Takumi K, Fukukura Y, Higashi M, et al. Pancreatic neuroendocrine tumors: correlation between the contrast-enhanced computed tomography features and the pathological tumor grade. Eur J Radiol. 2015;84:1436–43.CrossRefPubMedGoogle Scholar
  11. 11.
    d’Assignies G, Couvelard A, Bahrami S, et al. Pancreatic endocrine tumors: tumor blood flow assessed with perfusion CT reflects angiogenesis and correlates with prognostic factors. Radiology. 2009;250:407–16.CrossRefPubMedGoogle Scholar
  12. 12.
    Rodallec M, Vilgrain V, Couvelard A, et al. Endocrine pancreatic tumours and helical CT: contrast enhancement is correlated with microvascular density, histoprognostic factors and survival. Pancreatology. 2006;6:77–85.CrossRefPubMedGoogle Scholar
  13. 13.
    Luo Y, Dong Z, Chen J, et al. Pancreatic neuroendocrine tumours: correlation between MSCT features and pathological classification. Eur Radiol. 2014;24:2945–52.CrossRefPubMedGoogle Scholar
  14. 14.
    Kim DW, Kim HJ, Kim KW, et al. Neuroendocrine neoplasms of the pancreas at dynamic enhanced CT: comparison between grade 3 neuroendocrine carcinoma and grade 1/2 neuroendocrine tumour. Eur Radiol. 2015;25:1375–83.CrossRefPubMedGoogle Scholar
  15. 15.
    Manfredi R, Bonatti M, Mantovani W, et al. Non-hyperfunctional neuroendocrine tumours of the pancreas: MR imaging appearance and correlation with their biological behavior. Eur Radiol. 2013;23:3029–39.CrossRefPubMedGoogle Scholar
  16. 16.
    Wang Y, Chen ZE, Yaghmai V, et al. Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging. 2011;33:1071–9.CrossRefPubMedGoogle Scholar
  17. 17.
    Jang KM, Kim SH, Lee SJ, Choi D. The value of gadoxetic acid-enhanced and diffusion-weighted MRI for prediction of grading of pancreatic neuroendocrine tumors. Acta Radiol. 2014;55:140–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Kim JH, Eun HW, Kim YJ, Han JK, Choi BI. Staging accuracy of MR for pancreatic neuroendocrine tumor and imaging findings according to the tumor grade. Abdom Imaging. 2013;38:1106–14.CrossRefPubMedGoogle Scholar
  19. 19.
    Hwang EJ, Lee JM, Yoon JH, et al. Intravoxel incoherent motion diffusion-weighted imaging of pancreatic neuroendocrine tumor: prediction of the histologic grade using pure diffusion coefficient and tumor size. Invest Radiol. 2014;49:392–402.CrossRefGoogle Scholar
  20. 20.
    Lewis RB, Lattin GE Jr, Paal E. Pancreatic endocrine tumors: radiologic-clinicopathologic correlation. RadioGraphics. 2010;30:1445–64.CrossRefPubMedGoogle Scholar
  21. 21.
    Rösch T, Lightdale CJ, Botet JF, et al. Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med. 1992;326:1721–6.CrossRefPubMedGoogle Scholar
  22. 22.
    Gouya H, Vignaux O, Augui J, et al. CT, endoscopic sonography, and a combined protocol for preoperative evaluation of pancreatic insulinomas. AJR Am J Roentgenol. 2003;181:987–92.CrossRefPubMedGoogle Scholar
  23. 23.
    Ardengh JC, de Paulo GA, Ferrari AP. EUS-guided FNA in the diagnosis of pancreatic neuroendocrine tumors before surgery. Gastrointest Endosc. 2004;60:378–84.CrossRefPubMedGoogle Scholar
  24. 24.
    Figueiredo FA, Giovannini M, Monges G, et al. EUS-FNA predicts 5-year survival in pancreatic endocrine tumors. Gastrointest Endosc. 2009;70:907–14.CrossRefPubMedGoogle Scholar
  25. 25.
    Yang Z, Tang LH, Klimstra DS. Effect of tumor heterogeneity on the assessment of Ki67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol. 2011;35:853–60.CrossRefPubMedGoogle Scholar
  26. 26.
    Hill JS, McPhee JT, McDade TP, et al. Pancreatic neuroendocrine tumors: the impact of surgical resection on survival. Cancer. 2009;115:741–51.CrossRefPubMedGoogle Scholar
  27. 27.
    Falconi M, Bartsch DK, Eriksson B, 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;95:120–34.CrossRefPubMedGoogle Scholar
  28. 28.
    National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology. Neuroendocrine tumors 2015 version 1. [National Comprehensive Cancer Network Web site]. Accessed 30 Jan 2015.
  29. 29.
    La Rosa S, Klersy C, Uccella S, et al. Improved histologic and clinicopathologic criteria for prognostic evaluation of pancreatic endocrine tumors. Hum Pathol. 2009;40:30–40.CrossRefPubMedGoogle Scholar

Copyright information

© Japan Radiological Society 2017

Authors and Affiliations

  • Fumihito Toshima
    • 1
    Email author
  • Dai Inoue
    • 1
  • Takahiro Komori
    • 1
  • Kotaro Yoshida
    • 1
  • Norihide Yoneda
    • 1
  • Tetsuya Minami
    • 1
  • Osamu Matsui
    • 1
  • Hiroko Ikeda
    • 2
  • Toshifumi Gabata
    • 1
  1. 1.Department of RadiologyKanazawa University Graduate School of Medical ScienceKanazawaJapan
  2. 2.Department of PathologyKanazawa University Graduate School of Medical ScienceKanazawaJapan

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