European Radiology

, Volume 27, Issue 4, pp 1748–1759 | Cite as

Prediction of pancreatic neuroendocrine tumour grade with MR imaging features: added value of diffusion-weighted imaging

  • Emad Lotfalizadeh
  • Maxime RonotEmail author
  • Mathilde Wagner
  • Jérôme Cros
  • Anne Couvelard
  • Marie-Pierre Vullierme
  • Wassim Allaham
  • Olivia Hentic
  • Philippe Ruzniewski
  • Valérie Vilgrain



To evaluate the value of MR imaging including diffusion-weighted imaging (DWI) for the grading of pancreatic neuroendocrine tumours (pNET).

Material and Methods

Between 2006 and 2014, all resected pNETs with preoperative MR imaging including DWI were included. Tumour grading was based on the 2010 WHO classification. MR imaging features included size, T1-w, and T2-w signal intensity, enhancement pattern, apparent (ADC) and true diffusion (D) coefficients.


One hundred and eight pNETs (mean 40 ± 33 mm) were evaluated in 94 patients (48 women, 51 %, mean age 52 ± 12). Fifty-five (51 %), 42 (39 %), and 11 (10 %) tumours were given the following grades (G): G1, G2, and G3. Mean ADC and D values were significantly lower as grade increased (ADC: 2.13 ± 0.70, 1.78 ± 0.72, and 0.86 ± 0.22 10-3 mm2/s, and D: 1.92 ± 0.70, 1.75 ± 0.74, and 0.82 ± 0.19 10-3 mm2/s G1, G2, and G3, all p < 0.001). A higher grade was associated with larger sized tumours (p < 0.001). The AUROC of ADC and D to differentiate G3 and G1-2 were 0.96 ± 0.02 and 0.95 ± 0.02. Optimal cut-off values for the identification of G3 were 1.19 10-3 mm2/s for ADC (sensitivity 100 %, specificity 92 %) and 1.04 10-3 mm2/s for D (sensitivity 82 %, specificity 92 %).


Morphological/functional MRI features of pNETS depend on tumour grade. DWI is useful for the identification of high-grade tumours.

Key Points

Morphological and functional MRI features of pNETs depend on tumour grade.

Their combination has a high predictive value for grade.

All pNETs should be explored by MR imaging including DWI.

DWI is helpful for identification of high-grade and poorly-differentiated tumours.


Neoplasm Pancreas Ki-67 Carcinoma Grading 



apparent diffusion coefficient


true diffusion coefficient


diffusion-weighted imaging


European Neuroendocrine Tumour Society




(pancreatic) neuroendocrine tumour


magnetic resonance imaging


World Health Organization



The scientific guarantor of this publication is Maxime Ronot. The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. Methodology: retrospective, diagnostic or prognostic study, performed at one institution.

Supplementary material

330_2016_4539_Fig6_ESM.gif (26 kb)
Supplemental Figure 1

Example of a G1 pNET of the head of the pancreas in a 58 yo female. MR imaging showed a small (< 2 cm) hypervascular tumour on arterial phase images (arrow in a) with high signal intensity on high b value diffusion-weighted images (b=600 s/mm2) (arrow in b), and a mean ADC value of 2.30 10-3 mm2/s (c). All features were consistent with a G1 tumour. The lesion was resected, and pathological analysis confirmed the tumour grade (Ki67 < 1%). (GIF 26 kb)

330_2016_4539_Fig7_ESM.gif (23 kb)
Supplemental Figure 1

Example of a G1 pNET of the head of the pancreas in a 58 yo female. MR imaging showed a small (< 2 cm) hypervascular tumour on arterial phase images (arrow in a) with high signal intensity on high b value diffusion-weighted images (b=600 s/mm2) (arrow in b), and a mean ADC value of 2.30 10-3 mm2/s (c). All features were consistent with a G1 tumour. The lesion was resected, and pathological analysis confirmed the tumour grade (Ki67 < 1%). (GIF 26 kb)

330_2016_4539_Fig8_ESM.gif (34 kb)
Supplemental Figure 1

Example of a G1 pNET of the head of the pancreas in a 58 yo female. MR imaging showed a small (< 2 cm) hypervascular tumour on arterial phase images (arrow in a) with high signal intensity on high b value diffusion-weighted images (b=600 s/mm2) (arrow in b), and a mean ADC value of 2.30 10-3 mm2/s (c). All features were consistent with a G1 tumour. The lesion was resected, and pathological analysis confirmed the tumour grade (Ki67 < 1%). (GIF 26 kb)

330_2016_4539_MOESM1_ESM.tif (307 kb)
High resolution image (TIF 306 kb)
330_2016_4539_MOESM2_ESM.tif (249 kb)
High resolution image (TIF 248 kb)
330_2016_4539_MOESM3_ESM.tif (371 kb)
High resolution image (TIF 370 kb)
330_2016_4539_Fig9_ESM.gif (21 kb)
Supplemental Figure 2

Proposition of classification algorithm for the prediction of tumour grade. The right hand side column represents the mean (and standard deviation) of each box. (GIF 21 kb)

330_2016_4539_MOESM4_ESM.tiff (182 kb)
High resolution image (TIFF 181 kb)
330_2016_4539_MOESM5_ESM.docx (16 kb)
ESM 1 (DOCX 15 kb)


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Copyright information

© European Society of Radiology 2016

Authors and Affiliations

  • Emad Lotfalizadeh
    • 1
  • Maxime Ronot
    • 1
    • 2
    • 3
    Email author
  • Mathilde Wagner
    • 1
    • 3
  • Jérôme Cros
    • 2
    • 4
  • Anne Couvelard
    • 2
    • 4
  • Marie-Pierre Vullierme
    • 1
  • Wassim Allaham
    • 1
  • Olivia Hentic
    • 5
  • Philippe Ruzniewski
    • 5
  • Valérie Vilgrain
    • 1
    • 2
    • 3
  1. 1.Department of RadiologyUniversity Hospitals Paris Nord Val de SeineClichyFrance
  2. 2.University Paris DiderotParisFrance
  3. 3.INSERM U1149, Centre de Recherche Biomédicale Bichat-Beaujon, CRB3ParisFrance
  4. 4.Department of PathologyUniversity Hospitals Paris Nord Val de SeineClichyFrance
  5. 5.Department of GastroenterologyUniversity Hospitals Paris Nord Val de SeineClichyFrance

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