Utility of liver surface-guided encirclement of hepatoduodenal ligament for the Pringle maneuver in minimally invasive repeat liver resection

Table 1 Clinicopathological characteristics and perioperative outcomes of minimally invasive repeat liver resection, median (range)/n (%)

Variable	Overall, n = 72	Initial group, n = 15	LSEH group, n = 57	P value
Age (years)	70 (37-86)	68 (57-86)	70 (37-86)	0.803
Male sex	55 (76.4)	13 (86.7)	42 (73.7)	0.495
Diagnosis
HCC	35 (48.6)	8 (53.3)	27 (47.4)	1.000
CRLM	35 (48.6)	7 (46.7)	28 (49.1)
ICC	1 (1.3)	0 (0)	1 (1.7)
HCC with hepatolithiasis	1 (1.3)	0 (0)	1 (1.7)
Number of histories of liver resection
1	55 (76.4)	12 (80.0)	43 (75.4)	0.604
≥ 2	17 (23.6)	3 (20.0)	14 (24.6)
History of open liver resection	20 (28.2)	9 (60.0)	11 (19.6)	0.004
History of anatomical resection	18 (25.0)	1 (6.7)	17 (29.8)	0.095
History of multiple liver resection	22 (30.5)	3 (20.0)	19 (33.3)	0.529
Previous liver resection involving S1/4/5/6	50 (69.4)	9 (60.0)	41 (71.8)	0.368
Anti-adhesion barrier use in prior liver resection	54 (75.0)	9 (60.0)	45 (78.9)	0.180
Types of surgical approach of MISRLR
Laparoscopic	63 (87.5)	15 (100)	48 (84.2)	0.189
Robotic	9 (12.5)	0 (0)	9 (15.8)
Number of recurrent tumors at MISRLR
Single	56 (77.8)	14 (93.3)	44 (77.2)
Multiple	15 (22.2)	1 (6.7)	14 (22.8)	0.786
Recurrent tumor diameter (mm)	18.0 (5.0-70.0)	15.0 (8.0-40.0)	20.0 (5.0-70.0)	0.273
Type of MISRLR
Partial liver resection	57 (79.2)	13 (86.7)	44 (77.2)	0.368
Sectionectomy	2 (2.8)	0 (0)	2 (3.5)
Left lateral sectionectomy	3 (4.2)	0 (0)	3 (5.3)
Segmentectomy	10 (13.9)	2 (13.3)	8 (14.0)
Pringle maneuver	57 (79.2)	5 (33.3)	52 (91.2)	< 0.001
Open conversion	2 (2.8)	1 (6.7)	1 (1.8)	0.376
Operative time (minutes)	331.5 (170-719)	243.0 (170-719)	345.0 (178-700)	0.276
Blood loss (mL)	70 (0-3200)	40 (0-3200)	72 (0-1887)	0.670
Postoperative hospital stay (days)	8 (5-43)	8 (6-43)	8 (5-39)	0.128
Morbidity: ≥ Clavien-Dindo III	4 (5.6)	1 (6.7)	3 (5.3)	1.000
30-day mortality	0 (0)	0 (0)	0 (0)	1.000
In-hospital mortality	0 (0)	0 (0)	0 (0)	1.000

HCC: Hepatocellular carcinoma; CRLM: Colorectal liver metastasis; ICC: Intrahepatic cholangiocarcinoma; MISRLR: Minimally invasive repeat liver resection; LSEH: Liver surface-guided encirclement of hepatoduodenal ligament.

Table 2 Details of cases with Pringle taping failure

Group	Age	Sex	Diagnosis	MISRLR	Previous liver resection ≥ 2	Previous history of O- liver resection	Previous liver resection	Previous history of multi-liver resection	Previous history of anatomical resection	Previous history of other surgery	Size	Operative time	Blood loss	Morbidity, Clavien-Dindo ≥ III	Post operative hospital stay
Initial	65	M	CRLM	Lap-PH (S3)	0	1	O-multiple PH (S4, 5, 7, 8)	1	0	None	10	215	0	None	6
Initial	68	M	HCC	Lap-PH (S2)	0	1	O-PH (S7)	0	0	None	8	170	0	None	9
Initial	68	M	HCC	Lap-PH (S6)	1	1	O-PH (S7), Lap-PH (S2)	1	0	None	20	220	40	None	8
Initial	71	M	CRLM	Lap-PH (S4)	0	1	O-PH (S6/7)	0	0	LAC-S	20	236	100	None	8
Initial	83	F	HCC	Lap-PH (S4)	1	1	O-PH (S1), O-PH (S8)	1	0	None	11	243	30	None	21
Initial	86	M	HCC	Lap-PH (S5)	0	1	O-left hemi hepatectomy	0	1	None	20	254	200	None	16
Initial	67	M	CRLM	Lap-PH (S6)	0	1	Op-LLS + multiple PH (S6, 7, 8)	1	1	None	15	532	865	None	8
Initial	57	M	CRLM	Lap-PH (S2)	0	1	O-PH (S6, 8)	1	0	LAR	35	240	0	None	7
Initial	63	M	CRLM	Lap-PH (S2)	0	1	O-multiple PH (S2, 3, 4, 5, 6, 7)	1	0	None	15	330	0	None	8
LSEH	70	F	CRLM	Lap-PH (S3)	1	0	Lap-Segmentectomy (S7), Lap-PH (6, 8)	1	1	None	50	268	0	None	11
LSEH	74	M	Hepatolithiasis	Lap-PH (S3)	0	0	Lap-PH (S5)	0	0	O-total gastrectomy with splenectomy; O-choledocoduodenostomy	20	234	100	None	6
LSEH	78	M	HCC	Lap-PH (S3)	1	0	Lap-right anterior sectionectomy, Lap-segmentectomy (S8)	1	1	None	10	257	80	None	7
LSEH	79	M	HCC	Lap-PH (S5)	1	0	Lap-LLS, Lap-multiple PH (S4, 5, 7, 8)	1	1	Lap-cholecystectomy	10	399	1680	None	12
LSEH	68	M	HCC	Robot-PH (S3)	0	0	Lap-PH (S3, 5)	1	0	None	5	328	0	None	8

MISRLR: Minimally invasive repeat liver resection; LSEH: Liver surface-guided encirclement of hepatoduodenal ligament; M: Male; F: Female; HCC: Hepatocellular carcinoma; CRLM: Colorectal liver metastasis; Lap: Laparoscopic; PH: Partial hepatectomy; S: Sigmoidectomy; 1: Yes; 0: No; LLS: Left lateral segmentectomy; LAC: Laparoscopy-assisted colectomy; LAR: Low anterior resection; O: Open.

Table 3 Clinicopathological characteristics and perioperative outcomes of cases with history of open liver, median (range)/n (%)

Variable	Initial group, n = 9	LSEH group, n = 11	P value
Age, years	68 (57-86)	70 (58-80)	0.939
Male sex	8 (88.9)	9 (81.8)	1.000
HCC
History of anatomical resection	1 (11.1)	6 (54.5)	0.070
History of multiple liver resection	3 (33.3)	5 (45.5)	0.670
Previous liver resection involved S1/4/5/6	6 (66.7)	8 (72.7)	1.000
Number of histories of liver resection ≥ 2	2 (22.2)	4 (36.4)	0.642
Anti-adhesion barrier use in prior liver resection	6 (66.7)	9 (81.8)	0.617
Recurrent tumor diameter, mm	15 (8-35)	20 (6-40)	0.219
Approaches of MISRLR
Laparoscopic	9 (100)	10 (90.9)	1.000
Robotic	0 (0)	1 (9.1)	0.219
Types of MISRLR
Partial hepatectomy	9 (100)	6 (54.5)	0.068
Sectionectomy	0 (0)	0 (0)
Left lateral sectionectomy	0 (0)	2 (18.2)
Segmentectomy	0 (0)	3 (27.3)
Pringle maneuver	0 (0)	11 (100)	< 0.001
Open conversion	0	0	NA
Blood loss, mL	30 (0-865)	90 (2-1005)	0.195
Operative time in minutes	240 (170-532)	379 (213-644)	0.026
Morbidity: ≥ Clavien-Dindo III	0	0	NA
Postoperative hospital stay, days	8 (6-21))	8 (6-13)	0.531
30-day mortality	0	0	NA
In-hospital mortality	0	0	NA

HCC: Hepatocellular carcinoma; LSEH: Liver surface-guided encirclement of hepatoduodenal ligament; MISRLR: Minimally invasive repeat liver resection; NA: Not available.

Table 4 Potential factors associated with the Pringle taping failure after introduction of liver surface-guided encirclement of hepatoduodenal ligament technique, n (%)

Factors	LSEH technique		P value
	Failure, n = 5	Success, n = 52
Male sex	4 (80.0)	38 (73.1)	1.000
HCC	3 (60.0)	24 (46.2)	0.660
History of anatomical resection	2 (40.0)	15 (28.8)	0.629
Previous liver resection number
1	1 (20.0)	32 (61.5)	0.151
≥ 2	4 (80.0)	20 (38.4)
Three or more liver resections	3 (60.0)	11 (21.2)	0.089
History of open liver resection	0 (0)	11 (21.6)	0.571
Previously S1/4/5/6 resected	5 (100)	36 (69.2)	0.308
Anti-adhesion barrier use in previous liver resection	4 (80.0)	41 (78.8)	1.000
Approach
Laparoscopic	4 (80.0)	44 (84.6)	1.000
Robotic	1 (20.0)	8 (15.4)

HCC: Hepatocellular carcinoma; LSEH: Liver surface-guided encirclement of hepatoduodenal ligament.

Table 5 Review of the literature of minimally invasive repeat liver resection

Ref.	Country	Year	Period	n	Lap/Robo	HCC	History of OLx	Percentage, %	Partial Lx	Percentage, %	Pringle	Percentage, %	Open conv	Percentage, %
Belli et al[22]	Italy	2009	2004-2008	12	Lap	HCC only	4	33.3	4	33.3	0	0	1	8.3
Goh et al[24]	Singapore	2019	2015-2017	20	Lap (18)/Robo (2)	HCC only		65.0	11	55.0	0	0	4	20.0
Ogawa et al[34]	Japan	2020	2014-2018	28	Lap	HCC only	NR	NA	8	28.6	5	17.9	0	0
Mohan et al[48]	Singapore	2020	2012-2019	33	Lap (31)/Robo (2)	HCC included	NR	NA	NR	NA	5	15.2	2	6.1
Chen et al[32]	China	2021	2017-2018	57	Lap	HCC only	52	91.2	48	84.2	6	10.5	6	10.5
Takase et al[28]	Japan	2021	2010-2019	58	Lap	HCC only	14	24.1	50	86.2	33	56.9	0	0
Shen et al[35]	China	2022	2010-2020	48	Lap	HCC included	19	39.6	18	37.5	14	29.2	3	6.3
Mori et al[36]	Japan	2022	2016-2021	62	Lap	HCC included	7	11.3	35	56.5	35	56.5	3	4.8
Inoue et al[29]	Japan	2022	2010-2018	63	Lap	HCC included	30	47.6	59	93.7	19	30.2	6	9.5
Onda et al[37]	Japan	2023	2020-2022	43	Lap	HCC included	29	67.4	36	83.7	35	81.4	3	7.0
Our (LSEH/total)	Japan	2025	2017-2024	72	Lap (63)/Robo (9)	HCC included	11/20	18.8/28.2	44/57	77.2/77.8	52/57	91.7/79.2	1/2	1.8/2.8

Lap: Laparoscopic; Robo: Robotic; HCC: Hepatocellular carcinoma; OLx: Open liver resection; NA: Not available; Lx: Liver resection; NR: Not reported; LSEH: Liver surface-guided encirclement of hepatoduodenal ligament; Open conv: Open conversion.