Textbook oncologic outcomes following pancreatoduodenectomy in patients with pancreatic adenocarcinoma: A high-volume center study

Table 1 Demographic data and clinical characteristics of open pancreaticoduodenectomy and laparoscopic pancreaticoduodenectomy patients, mean ± SD/n (%)

Characteristic	LPD (n = 144)	OPD (n = 144)	Total (n = 288)	P value
Sex (male)	84 (58.3)	87 (60.4)	171 (59.4)	0.719
Age (years)	59.6 ± 8.3	58.5 ± 9.2	59.1 ± 8.8	0.307
BMI (kg/m2)	21.9 ± 2.4	21.9 ± 3.0	21.9 ± 2.7	0.987
Diabetes	17 (11.8)	18 (12.5)	35 (12.2)	0.857
Cardiovascular disease	32 (22.2)	31 (21.5)	63 (21.9)	0.887
ASA score
I	9 (6.2)	8 (5.6)	17 (5.9)	0.955
II	92 (63.9)	94 (65.3)	186 (64.6)
III	43 (29.9)	42 (29.2)	85 (29.5)
Neutrophil count (× 109/L), median (IQR)	3.4 (2.6, 4.3)	3.2 (2.6, 4.7)	3.4 (2.6, 4.4)	0.937
Lymphocyte count (× 109/L), median (IQR)	1.3 (1.1, 1.7)	1.3 (1.0, 1.7)	1.3 (1.0, 1.7)	0.661
Mononuclear cell count (× 109/L), median (IQR)	0.4 (0.4, 0.6)	0.5 (0.4, 0.6)	0.5 (0.4, 0.6)	0.293
Platelet count (× 109/L), median (IQR)	211.0 (167.0, 266.5)	218.5 (181.5, 259.5)	214.0 (176.0, 265.0)	0.529
Serum albumin (g/L), median (IQR)	38.5 (36.5, 40.8)	38.0 (35.6, 40.4)	38.2 (35.9, 40.5)	0.155
PLR, median (IQR)	160.5 (120.0, 216.4)	161.7 (124.6, 226.3)	160.8 (123.1, 222.2)	0.659
NLR, median (IQR)	2.5 (1.8, 3.4)	2.6 (1.8, 3.7)	2.6 (1.8, 3.4)	0.517
PNI, median (IQR)	45.6 (42.2, 48.3)	45.0 (42.3, 48.0)	45.4 (42.2, 48.1)	0.371
SII, median (IQR)	516.9 (363.3, 780.5)	549.4 (354.5, 836.6)	535.5 (359.5, 809.5)	0.557
NPS, median (IQR)	2.0 (2.0, 3.0)	3.0 (2.0, 3.0)	2.0 (2.0, 3.0)	0.240
CONUT score, median (IQR)	2.0 (1.0, 3.0)	2.0 (1.0, 3.0)	2.0 (1.0, 3.0)	1.000
ALT (U/L), median (IQR)	124.5 (43.0, 266.5)	115.0 (52.5, 245.0)	118.5 (50.0, 254.5)	0.558
AST (U/L), median (IQR)	82.0 (36.0, 188.0)	77.0 (36.5, 140.0)	78.0 (36.0, 165.5)	0.548
ALP (U/L), median (IQR)	254.0 (119.5, 454.5)	296.0 (143.5, 476.0)	277.0 (131.5, 462.0)	0.331
γ-GT (U/L), median (IQR)	460.5 (134.0, 764.0)	463.0 (141.5, 908.0)	462.5 (136.0, 832.0)	0.494
TBIL (μmol/L), median (IQR)	100.1 (17.9, 203.2)	123.2 (34.5, 198.2)	118.5 (24.2, 201.2)	0.373
DBIL (μmol/L), median (IQR)	85.0 (9.9, 163.7)	109.3 (24.5, 162.4)	95.4 (16.0, 163.6)	0.397
Serum total cholesterol level (mmol/L), median (IQR)	4.5 (3.8, 5.3)	4.8 (3.7, 6.0)	4.6 (3.8, 5.7)	0.293
CA19-9 (U/mL), median (IQR)	122.7 (37.2, 361.9)	147.1 (36.8, 579.2)	141.3 (37.0, 416.1)	0.156
CEA (ng/mL), median (IQR)	2.8 (1.8, 4.0)	3.3 (2.1, 5.3)	3.0 (2.0, 4.7)	0.013a

^aP < 0.05.

OPD: Open pancreaticoduodenectomy; LPD: Laparoscopic pancreaticoduodenectomy; ASA: American Society of Anesthesiologists; BMI: Body mass index; PLR: Platelet to lymphocyte ratio; NLR: Neutrophil to lymphocyte ratio; IQR: Interquartile range; SII: Systemic immune inflammation index; PNI: Prognostic nutritional index; NPS: Naples prognostic score; CONUT: Controlling nutritional status; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; ALP: Alkaline phosphatase; γ-GT: γ-glutamyl transferase; TBIL: Total bilirubin; DBIL: Direct bilirubin; CA19-9: Carbohydrate antigen 19-9; CEA: Carcinoembryonic antigen.

Table 2 Perioperative outcomes and survival data of open pancreaticoduodenectomy and laparoscopic pancreaticoduodenectomy, n (%)

Characteristic	LPD (n = 144)	OPD (n = 144)	Total (n = 288)	P value
Preoperative biliary drainage	83 (57.6)	80 (55.6)	163 (56.6)	0.721
Tumor size (cm), median (IQR)	2.8 (2.0, 3.2)	3.0 (2.0, 3.2)	3.0 (2.0, 3.2)	0.766
Degree of tumor differentiation
High	7 (4.9)	10 (6.9)	17 (5.9)	0.889
Low	49 (34)	50 (34.7)	99 (34.4)
Moderate	87 (60.4)	83 (57.6)	170 (59)
Undifferentiated	1 (0.7)	1 (0.7)	2 (0.7)
T stage
T1	44 (30.6)	39 (27.1)	83 (28.8)	0.772
T2	90 (62.5)	94 (65.3)	184 (63.9)
T3	8 (5.6)	7 (4.9)	15 (5.2)
T4	2 (1.4)	4 (2.8)	6 (2.1)
N stage
N0	94 (65.3)	91 (63.2)	185 (64.2)	0.364
N1	37 (25.7)	45 (31.2)	82 (28.5)
N2	13 (9)	8 (5.6)	21 (7.3)
M stage
M0	142 (98.6)	142 (98.6)	284 (98.6)	1.000
M1	2 (1.4)	2 (1.4)	4 (1.4)
Operation time (min), median (IQR)	330.0 (280.0, 400.5)	370.0 (283.5, 440.0)	350.0 (281.5, 429.5)	0.216
Bile leakage	9 (6.2)	4 (2.8)	13 (4.5)	0.156
Postoperative abdominal infection	10 (6.9)	8 (5.6)	18 (6.2)	0.626
POPF	23 (16)	48 (33.3)	71 (24.7)	< 0.001a
DGE	41 (28.5)	110 (76.4)	151 (52.4)	< 0.001a
PPH	16 (11.1)	12 (8.3)	28 (9.7)	0.426
Gastrointestinal fistula	0 (0)	2 (1.4)	2 (0.7)	0.156
Liver failure	1 (0.7)	3 (2.1)	4 (1.4)	0.314
Kidney failure	0 (0)	1 (0.7)	1 (0.3)	0.316
Lung infection	0 (0)	5 (3.5)	5 (1.7)	0.024a
Clavien-Dindo classification
I	98 (68.1)	64 (44.4)	162 (56.2)	0.225
II	24 (16.7)	62 (43.1)	86 (29.9)
III	3 (2.1)	4 (2.8)	7 (2.4)
IV	15 (10.4)	13 (9)	28 (9.7)
V	4 (2.8)	1 (0.7)	5 (1.7)
Length of stay (days), median (IQR)	20.0 (16.0, 25.5)	22.0 (16.0, 27.0)	21.0 (16.0, 26.0)	0.052
Overall survival time (months), median (IQR)	15.4 (9.0, 24.2)	14.5 (8.1, 22.0)	15.1 (8.8, 23.2)	0.134
TOO	45 (31.2)	33 (22.9)	78 (27.1)	0.112

^aP < 0.05.

OPD: Open pancreaticoduodenectomy; LPD: Laparoscopic pancreaticoduodenectomy; IQR: Interquartile range; POPF: Postoperative pancreatic fistula; DGE: Delayed gastric emptying; PPH: Postpancreatectomy hemorrhage; TOO: Textbook oncologic outcome.

Table 3 Univariate and multivariable logistic regression analysis of textbook oncologic outcome achievement in the laparoscopic pancreaticoduodenectomy cohort

Variables	Univariate analysis		Multivariate analysis
	OR (95%CI)	P value	OR (95%CI)	P value
Sex (male)	0.74 (0.36-1.51)	0.412
Age (≥ 60 years)	0.63 (0.31-1.29)	0.210
BMI (kg/m2)
≥ 18.5, < 24	Reference
< 18.5	0.58 (0.11-2.94)	0.510
≥ 24	0.77 (0.31-1.92)	0.579
Diabetes	1.64 (0.58-4.63)	0.350
Cardiovascular disease	0.83 (0.35-1.97)	0.666
ASA
I	Reference
II	0.30 (0.07-1.20)	0.089
III	0.43 (0.10-1.84)	0.254
Serum albumin (≥ 37.95 g/L)	3.03 (1.38-6.65)	0.006a	2.65 (1.00-7.00)	0.050
PLR (≥ 174.2)	0.59 (0.28-1.21)	0.150
NLR (≥ 1.61)	0.34 (0.14-0.82)	0.016a	0.42 (0.14-1.26)	0.121
PNI (≥ 48.83)	3.09 (1.36-7.02)	0.007a	1.91 (0.67-5.51)	0.228
CONUT score
≤ 3	Reference
≥ 4	0.55 (0.23-1.32)	0.181
SII (≥ 484.09)	0.64 (0.31-1.30)	0.217
NPS (≥ 3)	0.81 (0.40-1.65)	0.558
ALT (≥ 254.5 U/L)	2.48 (1.15-5.33)	0.020a	2.28 (0.88-5.89)	0.090
AST (≥ 133.5 U/L)	1.67 (0.81-3.45)	0.162
ALP (≥ 105.5 U/L)	0.65 (0.29-1.50)	0.314
γ-GT (≥ 657 U/L)	1.60 (0.77-3.32)	0.204
TBIL (≥ 63.2 μmol/L)	0.57 (0.28-1.17)	0.126
DBIL (≥ 35.15 μmol/L)	0.50 (0.24-1.03)	0.059
Serum total cholesterol level (≥ 5.59 mmol/L)	2.41 (1.07-5.42)	0.033a	2.29 (0.84-6.29)	0.107
CA19-9 (≥ 37 U/mL)	0.70 (0.32-1.57)	0.389
CEA (≥ 5 ng/mL)	1.89 (0.81-4.41)	0.143
Preoperative biliary drainage	0.77 (0.38-1.58)	0.481
Tumor size (cm)	0.98 (0.70-1.38)	0.910
T stage
T1	Reference
T2	1.02 (0.47-2.21)	0.963
T3 and T4	0.54 (0.10-2.86)	0.465
N stage
N0	Reference
N1	1.08 (0.48-2.43)	0.861
N2	1.00 (0.28-3.50)	0.995
M stage
M0	Reference
M1	2.23 (0.14-36.43)	0.574
Degree of tumor differentiation	Reference
High and moderate	Reference
Low and undifferentiated	1.40 (0.67-2.90)	0.371
Clavien-Dindo classification
I	Reference
II and above	0.18 (0.06-0.49)	< 0.001a	0.22 (0.07-0.68)	0.008a
Length of stay (days)	0.91 (0.86-0.97)	0.002a	0.94 (0.88-1.00)	0.048a

^aP < 0.05.

OR: Odds ratio; CI: Confidence interval; ASA: American Society of Anesthesiologists; BMI: Body mass index; PLR: Platelet to lymphocyte ratio; NLR: Neutrophil to lymphocyte ratio; PNI: Prognostic nutritional index; CONUT: Controlling nutritional status; SII: Systemic immune inflammation index; NPS: Naples prognostic score; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; ALP: Alkaline phosphatase; γ-GT: γ-glutamyl transferase; TBIL: Total bilirubin; DBIL: Direct bilirubin; CA19-9: Carbohydrate antigen 19-9; CEA: Carcinoembryonic antigen.

Table 4 Univariate and multivariable logistic regression analysis of textbook oncologic outcome achievement in the open pancreaticoduodenectomy cohort

Variables	Univariate analysis		Multivariate analysis
	OR (95%CI)	P value	OR (95%CI)	P value
Sex (male)	1.19 (0.53-2.67)	0.667
Age (≥ 60 years)	0.70 (0.32-1.53)	0.369
BMI (kg/m2)
≥ 18.5, < 24	Reference
< 18.5	0.26 (0.06-1.20)	0.084
≥ 24	0.52 (0.20-1.34)	0.176
Diabetes	1.35 (0.44-4.10)	0.601
Cardiovascular disease	1.22 (0.49-3.07)	0.666
ASA
I	Reference
II	0.39 (0.09-1.81)	0.231
III	0.67 (0.14-3.24)	0.615
Serum albumin (≥ 37.35 g/L)	1.58 (0.70-3.57)	0.271
PLR (≥ 121.56)	2.45 (0.79-7.57)	0.121
NLR (≥ 3.76)	1.50 (0.63-3.55)	0.362
PNI (≥ 49.38)	2.40 (0.94-6.14)	0.068
CONUT score
≤ 4	Reference
≥ 5	2.24 (0.75-6.73)	0.149
SII (≥ 873.70)	1.98 (0.82-4.80)	0.131
NPS (≥ 3)	0.83 (0.38-1.81)	0.638
ALT (≥ 170.50 U/L)	0.53 (0.22-1.27)	0.154
AST (≥ 77.50 U/L)	0.42 (0.19-0.96)	0.040a	0.39 (0.16-0.92)	0.031a
ALP (≥ 410.50 U/L)	0.67 (0.28-1.57)	0.353
γ-GT (≥ 488 U/L)	1.72 (0.78-3.77)	0.177
TBIL (≥ 148.90 μmol/L)	1.38 (0.63-3.01)	0.418
DBIL (≥ 108.40 μmol/L)	1.43 (0.65-3.14)	0.369
Serum total cholesterol level (≥ 4.84 mmol/L)	0.62 (0.28-1.36)	0.230
CA19-9 (≥ 37 U/mL)	0.42 (0.18-0.97)	0.043a	0.47 (0.19-1.17)	0.104
CEA (≥ 5 ng/mL)	0.93 (0.39-2.21)	0.862
Preoperative biliary drainage	1.83 (0.81-4.12)	0.146
Tumor size (cm)	0.90 (0.60-1.33)	0.584
T stage
T1	Reference
T2	0.73 (0.31-1.77)	0.491
T3 and T4	1.66 (0.40-6.88)	0.487
N stage
N0	Reference
N1	0.51 (0.20-1.31)	0.162
N2	0.93 (0.18-4.93)	0.933
M stage
M0	Reference
M1	3.44 (0.21-56.51)	0.387
Degree of tumor differentiation
High and moderate	Reference
Low and undifferentiated	0.74 (0.32-1.71)	0.485
Clavien-Dindo classification
I	Reference
II and above	0.30 (0.13-0.69)	0.004a	0.32 (0.13-0.78)	0.012a
Length of stay (days)	0.95 (0.90-0.99)	0.028a	0.96 (0.92-1.02)	0.185

^aP < 0.05.

OR: Odds ratio; CI: Confidence interval; ASA: American Society of Anesthesiologists; BMI: Body mass index; PLR: Platelet to lymphocyte ratio; NLR: Neutrophil to lymphocyte ratio; PNI: Prognostic nutritional index; CONUT: Controlling nutritional status; SII: Systemic immune inflammation index; NPS: Naples prognostic score; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; ALP: Alkaline phosphatase; γ-GT: γ-glutamyl transferase; TBIL: Total bilirubin; DBIL: Direct bilirubin; CA19-9: Carbohydrate antigen 19-9; CEA: Carcinoembryonic antigen.