Pancreatic neuroendocrine neoplasms: Magnetic resonance imaging features according to grade and stage

Table 1 Magnetic resonance protocol and pulse sequences: Technical parameters

Pulse sequence	Imaging plane	TR (ms)	TE (ms)	Thickness (mm)
T2w HASTE	Axial	∞	90.00	6
	Coronal	∞	90.00	6
	Para-coronal	∞	90.00	4
	Sagittal	∞	90.00	4
FsT2w RARE	Axial	2900.00	82-87	6
DWI-EPI	Axial	6000-6500	59.00	6
Chemical-shift	Axial	90-130	2.37/4.87	6
FsT1w VIBE	Axial	4.28	2.39	2-3
	Coronal	3.52	1.32	2-3
	Sagittal	3.52	1.32	2-3
2D MRCP HASTE	Multiple	∞	746.00	65-75

TR: Repetition time; TE: Time of echo; HASTE: Half-Fourier single-shot turbo spin echo; DWI-EPI: Diffusion-weighted echo-planar imaging; RARE: Rapid acquisition with relaxation enhancement; VIBE: Volume-interpolated breath-hold examination; MRCP: Magnetic resonance cholangiopancreatography.

Table 2 Comparison of qualitative features between grades and stages

Feature	Grade				ENETS TNM stage1
	Total	G12	G2-32	P value	Total	I/II2	III/IV2	P value
Location				0.094				0.059
Head	24	11 (45.8)	13 (54.2)		23	7 (30.4)	16 (69.6)
Body	25	18 (72)	7 (28)		22	14 (63.6)	8 (36.4)
Tail	6	2 (33.3)	4 (66.7)		6	4 (66.7)	2 (33.3)
Margins				< 0.001				< 0.001
Well defined	39	28 (71.8)	11 (28.2)		35	24 (68.6)	11 (31.4)
Ill defined	16	3 (18.8)	13 (81.2)		16	1 (6.2)	15 (93.8)
Vasc. infiltration				0.022	-	-	-	-
Present	7	1 (14.3)	6 (85.7)
Absent	48	30 (62.5)	18 (37.5)
Liver metastases				0.002	-	-	-	-
Present	7	0 (0)	7 (100)
Absent	48	31 (64.6)	17 (35.4)
Atrophy3				0.446				0.151
Present	13	7 (53.8)	6 (46.2)		13	4 (30.8)	9 (69.2)
Absent	36	22 (61.1)	14 (38.9)		32	17 (53.1)	15 (46.9)
MPD dilation4				0.215				0.151
Present	13	6 (46.2)	7 (53.8)		13	4 (30.8)	9 (69.2)
Absent	36	23 (63.9)	13 (36.1)		32	17 (53.1)	15 (46.9)
CBD dilation4				0.264				0.275
Present	7	2 (28.6)	5 (71.4)		7	1 (14.3)	6 (85.7)
Absent	17	9 (52.9)	8 (47.1)		16	6 (37.5)	10 (62.5)

¹Four lesions were excluded from this analysis (minimally invasive surgery without lymphadenectomy);

²Number of cases/cases in row;

³Pancreatic head/body lesions;

⁴Pancreatic head lesions. Data are presented as numbers of cases. ENETS: European Neuroendocrine Society; TNM: Tumor-nodes-metastases.

Table 3 Comparison of signal intensity between grades and European Neuroendocrine Society tumor-nodes-metastases stages

Feature	Grade				ENETS TNM stage1
	Total	G12	G2-32	P value	Total	I/II2	III/IV2	P value
T1w				0.395				0.659
Hypointense	45	27 (60)	18 (40)		42	22 (52.4)	20 (47.6)
Isointense	4	1 (25)	3 (75)		4	1 (25)	3 (75)
Hyperintense	6	3 (50)	3 (50)		5	2 (40)	3 (60)
fsT1w				0.836				0.900
Hypointense	39	23 (59)	16 (41)		37	19 (51.4)	18 (48.6)
Isointense	9	5 (55.6)	4 (44.4)		8	3 (37.5)	5 (62.5)
Hyperintense	7	3 (42.9)	4 (57.1)		6	3 (50)	3 (50)
T2w				0.937				0.274
Hypointense	16	9 (56.3)	7 (43.2)		16	8 (50)	8 (50)
Isointense	12	6 (50)	6 (50)		11	3 (27.3)	8 (72.7)
Hyperintense	27	16 (59.3)	11 (40.7)		24	14 (58.3)	10 (41.7)
fsT2w				1.000				0.318
Hypointense	13	7 (53.8)	6 (46.2)		13	5 (38.5)	8 (61.5)
Isointense	11	6 (54.5)	5 (45.5)		9	3 (33.3)	6 (66.7)
Hyperintense	31	18 (58.1)	13 (41.9)		29	17 (58.6)	12 (41.4)
Fluid areas				0.279				0.464
Present	15	7 (46.7)	8 (53.3)		15	8 (53.3)	7 (46.7)
Absent	40	24 (60)	16 (40)		38	17 (47.2)	19 (52.8)
Arterial				0.089				0.055
Hypointense	13	4 (30.8)	9 (69.2)		12	3 (25)	9 (75)
Isointense	11	8 (72.7)	3 (27.3)		9	3 (33.3)	6 (66.7)
Hyperintense	31	19 (61.3)	12 (38.7)		30	19 (63.3)	11 (36.7)
Portal				1.000				0.933
Hypointense	14	8 (57.1)	6 (42.9)		14	6 (42.9)	8 (57.1)
Isointense	13	7 (53.8)	6 (46.2)		12	6 (50)	6 (50)
Hyperintense	28	16 (57.1)	12 (42.9)		25	13 (52)	12 (48)
Delayed				0.441				0.340
Hypointense	12	6 (50)	6 (50)		11	4 (36.4)	7 (63.6)
Isointense	19	9 (47.4)	10 (52.6)		17	7 (41.2)	10 (58.8)
Hyperintense	24	16 (66.7)	8 (33.3)		23	14 (60.9)	9 (39.1)
Enhancement				0.006				0.163
Heterogeneous	25	9 (36)	16 (64)		25	10 (40)	15 (60)
Homogeneous	30	22 (73.3)	8 (26.7)		26	15 (57.7)	11 (42.3)

¹Four lesions were excluded from this analysis (minimally invasive surgery without lymphadenectomy);

²Number of cases/cases in row. ENETS: European Neuroendocrine Society; TNM: Tumor-nodes-metastases.

Table 4 Qualitative image analysis and comparison between grades and stages

	Grades				ENETS TNM stages1
	Total	G1	G2-3	P value	Total	I/II	III/IV	P value
Size (mm)	28.7 ± 20.8	22.7 ± 17.7	36.4 ± 22.1	0.017	29.9 ± 21.1	24.6 ± 19	34.9 ± 22.1	0.080
MPD caliber2 (mm)	6 ± 2	6.8 ± 2.7	5.4 ± 1	0.256	6 ± 2	7.7 ± 2.9	5.3 ± 0.9	0.038
CBD caliber3 (mm)	13.4 ± 3.9	18.3 ± 3	11.5 ± 2	0.151	13.4 ± 3.9	20.5	12.3 ± 2.6	0.034
ADCL (× 10-3 mm2/s)	1.29 ± 0.47	1.45 ± 0.53	1.09 ± 0.28	0.003	1.31 ± 0.48	1.53 ± 0.55	1.10 ± 0.25	0.001

Data are expressed as means ± SD.

¹Four lesions have been excluded from this analysis (minimally invasive surgery without lymphadenectomy);

²Pancreatic head/body lesions showing upstream MPD dilation;

³Pancreatic head lesions showing upstream CBD dilation. ENETS: European Neuroendocrine Society; TNM: Tumor-nodes-metastases.

Table 5 Diagnostic performances in the identification of G2-3 and stage III-IV pancreatic neuroendocrine neoplasms

	Feature	Diagnostic performance
		Se	Sp	PPV	NPV
Grade 2-3	Ill defined margins	54.2 (33.2-73.8)	90.3 (73.1-97.5)	81.2 (53.7-95)	71.7 (54.9-84.4)
	Vascular infiltration	29.2 (13.4-51.2)	96.7 (81.5-99.8)	87.5 (46.7-99.3)	63.8 (48.4-76.9)
	Liver metastases	25 (10.6-47)	96.7 (81.5-99.8)	85.7 (42-99.2)	62.5 (47.3-75.7)
	Heterogeneous enhancement	66.7 (44.7-83.6)	71 (51.7-85.1)	64 (42.6-81.3)	73.3 (53.8-87)
	Size > 17.5 mm	91.7 (71.5-98.5)	61.3 (42.3-77.6)	64.7 (46.5-79.7)	90.5 (68.2-98.3)
	Size > 20 mm	79.2 (57.3-92.1)	60.9 (38.8-79.5)	67.8 (47.6-83.4)	73.6 (48.6-52.4)
	ADC < 1.21 × 10-3 mm2/s	70.8 (48.7-86.6)	64.5 (45.4-80.2)	60.7 (40.7-77.9)	74.1 (53.4-88.1)
Stage III-IV	Ill defined margins	57.7 (37.2-76)	96 (77.7-99.8)	93.7 (67.7-99.7)	68.6 (50.6-82.6)
	ADC < 1.28 × 10-3 mm2/s	80.7 (60-92.7)	64 (42.6-81.3)	70 (50.4-84.6)	76.2 (52.4-90.9)

Diagnostic performances are expressed as percentages (95%CI). AUC: Area under the curve; Se: Sensitivity; Sp: Specificity; PPV: Positive predictive value; NPV: Negative predictive value.

Table 6 Combination of magnetic resonance findings for differentiating G1 from G2-3 pancreatic neuroendocrine neoplasms

Number of features	Diagnostic performance
	Se	Sp	PPV	NPV
≥ 1	100 (82.8-100)	35.5 (19.8-54.6)	54.5 (38.9-69.3)	100 (67.8-100)
≥ 2	79.2 (57.3-92.1)	80.1 (61.9-91.9)	76 (54.5-89.8)	83.3 (64.5-93.7)
≥ 3	58.3 (36.9-77.2)	93.5 (77.1-98.9)	87.5 (60.4-97.8)	74.3 (57.6-86.4)
≥ 4	20.8 (7.9-42.7)	96.7 (81.5-99.8)	83.3 (36.5-99.1)	61.2 (46.2-74.4)
≥ 5	8.3 (1.4-28.5)	96.4 (86.4-99.4)	100 (19.8-100)	58.5 (44.2-71.6)

MR findings are ill-defined margins, vascular invasion, liver metastases, size > 17.5 mm, ADC < 1.21 < 10^-3 mm²/s. Diagnostic performances are expressed as percentages (95%CI). Se: Sensitivity; Sp: Specificity; PPV: Positive predictive value; NPV: Negative predictive value.