Minimally invasive vs open pancreatectomy for nonfunctioning pancreatic neuroendocrine tumors

Table 1 Clinicopathological characteristics of resected nonfunctioning pancreatic neuroendocrine tumors

Variable	Finding
Age in yr, median (range)	56.0 (46.0–63.0)
Male, n (%)	51 (46.4)
BMI in kg/m², median (range)	24.1 (22.1–26.3)
ASA, grade, n (%)
I	30 (27.3)
II	59 (53.6)
III	21 (19.1)
Diabetes, preoperative, n (%)	20 (18.2)
Pancreatic tumor location, n (%)
Head	41 (35.7)
Neck	6 (5.2)
Body	26 (22.6)
Tail	42 (36.5)
Type of surgery, n (%)
Distal pancreatectomy	51 (46.4)
Enucleation	22 (20.0)
Central pancreatectomy	7 (6.4)
Pylorus-preservingpancreaticoduodenectomy	21 (19.1)
Total pancreatectomy	9 (8.2)
MIS or open, n (%)
MIS	62 (56.4)
Open	48 (43.6)
Post-operative length of stay in d, median (range)	11.5 (8.0–17.0)
Clavien-Dindo grade, n (%)
0: no complications	58 (52.7)
I	35 (31.8)
II	8 (7.3)
IIIa	5 (4.5)
IIIb	3 (2.7)
IVa	1 (0.9)
IVb	0 (0)
POPF by ISGPF
Grade A	47 (40.9%)
Grade B	6 (5.2%)
Grade C	0 (0%)
DGE by ISGPS
Grade A	18 (15.7%)
Grade B	1 (0.9%)
Grade C	0 (0%)
Resection margin status, n (%)
R0	97 (88.2)
R1	5 (4.5)
R2	8 (7.3)
Pathological tumor size in cm, median (range)	1.8 (1.2–3.2)
T stage by ENETS classification
T1	56 (50.9%)
T2	18 (16.4%)
T3	36 (32.7%)
T4	0 (0.0%)
N status
Negative	57 (51.9%)
Positive	9 (8.1%)
No lymphadenectomy	44 (40.0%)
Metastasis present, n (%)	5 (4.5)
2010 WHO classification grade, n (%)
G1	78 (70.9)
G2	27 (24.54)
G3	4 (3.63)
Unknown	1 (0.9)

ASA: American Society of Anesthesiologists; BMI: Body mass index; DGE: Delayed gastric emptying; ENETS: European Neuroendocrine Tumor Society; ISGPS: International Study Group on Pancreatic Surgery; ISGPF: International Study Group on Pancreatic Fistula; POPF: Post-operative pancreatic fistulae; WHO: World Health Organization.

Table 2 Clinicopathological characteristics of minimally invasive and open approaches in terms of the distal location of nonfunctioning pancreatic neuroendocrine tumors

Variable	Open approach, n = 12	MIS, n = 39	P value
Male	7 (58.3%)	19 (48.7%)	0.801
Age in yr, median (range)	58.5 (51.0-64.5)	56.0 (47.0-64.5)	0.617
BMI in kg/m², median (range)	24.6 (22.1-25.5)	24.8 (22.9-27.3)	0.418
ASA grade, n (%)			0.243
I	5 (41.7)	7 (17.9)
II	5 (41.7)	23 (59.0)
Ш	2 (16.7)	9 (23.1)
Spleen-preserving distal pancreatectomy	5 (41.7%)	26 (66.6%)
Conversion, n (%)	-	4 (10.2)
Robot-assisted	-	8 (20.5%)
Operative time as minimum, median (range)	179.0 (159.5–251.5)	216.0 (185.5–276.0)	0.105
Blood loss in cc, median (range)	175.0 (65.0–450.0)	100 (45.0–275.0)	0.093
Clavien-Dindo grade			0.729
0: no complications	7 (58.3%)	26 (66.7%)
I	4 (33.3%)	10 (25.6%)
II	1 (8.3%)	2 (5.1%)
IIIa	0 (0.0%)	1 (2.6%)
DGE by ISGPS			0.561
Grade A	0 (0.0%)	4 (10.3%)
Grade B	0 (0.0%)	0 (0.0%)
Grade C	0 (0.0%)	0 (0.0%)
POPF by ISGPF			0.805
Grade A	7 (58.3%)	20 (51.3%)
Grade B	0 (0.0%)	1 (2.6%)
Grade C	0 (0.0%)	0 (0.0%)
Post-operative length of stay in d, median (range)	14.0 (11.5-16.0)	8.0 (7.0-10.5)	< 0.001
Resection margin status			0.612
R0	12 (100.0%)	36 (92.3%)
R1	0 (0.0%)	2 (5.1%)
R2	0 (0.0%)	1 (2.6%)
Pathological tumor size in cm, median (range)	2.5 (1.4-3.9)	2.0 (1.5-3.2)	0.548
T stage by ENETS classification			0.563
T1	5 (41.7%)	20 (51.3%)
T2	2 (16.7%)	9 (23.1%)
T3	5 (41.7%)	10 (25.6%)
N stage			0.056
Negative	9 (75.0%)	38 (97.4%)
Positive	3 (25.0%)	1 (2.6%)
M stage
0	12 (100.0%)	39 (100.0%)
Nodal harvest, median (range)	0.0 (0.0-5.5)	1.0 (0.0-3.5)	0.767
2010 WHO grade			0.365
G1	7 (57.1%)	25 (64.1%)
G2	4 (42.9%)	14 (35.9%)
G3	1 (8.3%)	0 (0%)

ASA: American Society of Anesthesiologists; BMI: Body mass index; DGE: Delayed gastric emptying; ENETS: European Neuroendocrine Tumor Society; ISGPS: International Study Group on Pancreatic Surgery; ISGPF: International Study Group on Pancreatic Fistula; MIS: Minimally invasive surgery; POPF: Post-operative pancreatic fistulae; WHO: World Health Organization.

Table 3 Clinicopathological characteristics of the minimally invasive surgery and open groups in terms of the proximal location of nonfunctioning pancreatic neuroendocrine tumors

Variable	Open, n = 22	MIS, n = 15	P value
Male	11 (50.0%)	5 (33.3%)	0.505
Age in yr, median (range)	53.5 (40.0–65.0)	53.0 (43.0–65.5)	0.631
BMI in kg/m², median (range)	24.6 (22.7–27.3)	21.9 (21.1–23.4)	0.006
ASA grade, n (%)			0.069
I	6 (27.3)	0 (0.0)
II	14 (63.6)	12 (80.0)
III	2 (9.1)	3 (20.0)
Type of surgery			0.541
Central pancreatectomy	3 (13.6%)	4 (26.7%)
PPPD	14 (63.6%)	7 (46.7%)
Total pancreatectomy	5 (22.7%)	4 (26.7%)
Operative time in min, median (range)	346.0 (295.0-400.0)	512.0 (462.5-530.0)	< 0.001
Blood loss in cc, median (range)	450.0 (100.0-1020.0)	400. (175.0-450.0)	0.515
Clavien-Dindo grade			0.489
0: no complications	10 (45.5%)	4 (26.7%)
I	8 (36.4%)	5 (33.3%)
II	1 (4.5%)	3 (20.0%)
IIIa	1 (4.5%)	1 (6.7%)
IIIb	2 (9.1%)	1 (6.7%)
IV	0 (0.0%)	1 (6.7%)
DGEby ISGPS			0.457
Grade A	7 (31.8%)	5 (33.3%)
Grade B	0 (0.0%)	1 (6.7%)
Grade C	0 (0.0%)	0 (0.0%)
POPF by ISGPF			0.571
Grade A	5 (22.7%)	4 (26.7%)
Grade B	1 (4.5%)	2 (13.3%)
Grade C	0 (0.0%)	0 (0.0%)
Post-operative length of stay in d, median (range)	20.0 (14.0–30.0)	13.0 (10.5–24.5)	0.210
Resection margin status			0.505
R0	20 (90.9%)	15 (100.0%)
R1	0 (0.0%)	0 (0.0%)
R2	2 (9.1%)	0 (0.0%)
Pathological tumor size incm, median (range)	2.6 (1.5-4.5)	1.5 (1.3-2.2)	0.041
T stage by ENETs classification			0.081
T1	6 (27.3%)	8 (53.3%)
T2	5 (22.7%)	0 (0.0%)
T3	11 (50.0%)	7 (46.7%)
N stage			1.000
0	20 (90.9%)	13 (86.7%)
1	2 (9.1%)	2 (13.3%)
M stage			1.000
0	19 (86.4%)	13 (86.7%)
1	3 (13.6%)	2 (13.3%)
Nodal harvest, median (range)	7.5 (5-12)	6.0 (2.5-12.5)	0.804
2010 WHO grade			0.848
G1	16 (72.7%)	10 (66.7%)
G2	3 (13.6%)	4 (26.7%)
G3	2 (9.1%)	1 (6.7%)
Unknown	1 (4.5%)	0 (0%)

ASA: American Society of Anesthesiologists; BMI: Body mass index; DGE: Delayed gastric emptying; ENETS: European Neuroendocrine Tumour Society; ISGPS: International Study Group on Pancreatic Surgery; ISGPF: International Study Group on Pancreatic Fistula; MIS: Minimally invasive surgery; POPF: Post-operative pancreatic fistulae; PPPD: Pylorus-preserving pancreaticoduodenectomy; WHO: World Health Organization.

Table 4 Factors associated with tumor recurrence after curative resection of nonfunctioning pancreatic neuroendocrine tumors

Variable	Univariate analysis			Multivariate analysis
	HR	95%CI	P value	HR	95%CI	P value
Age > 60 yr	0.40	0.09-1.83	0.239
Male	1.95	0.62-6.16	0.254
Minimally invasive surgery	0.61	0.18-2.09	0.432	1.062	0.28-4.03	0.929
Tumor size > 2.5 cm	22.21	2.86-172.69	0.003	16.21	1.99-128.8	0.009
Positive resection margin	1.52	0.33–6.99	0.589
Poor differentiation, G3	71.55	6.43-795.75	0.001	24.429	1.99-277.95	0.017
Positive lymph node	1.93	0.42–8.83	0.398
Lympho-vascular invasion	8.77	2.75-27.93	< 0.001	3.56	0.96-13.2	0.058

HR: Hazard ratio.