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

Abstract

BACKGROUND

Repeated application of the Pringle maneuver is a key obstacle to safe minimally invasive repeat liver resection (MISRLR). However, limited technical guidance is available.

AIM

To study the utility of newly developed Pringle taping method guided by liver surface in MISRLR.

METHODS

We retrospectively reviewed 72 cases of MISRLR performed by a single surgeon at two centers from August 2015 to July 2024. Beginning in October 2019, a liver surface-guided encirclement of hepatoduodenal ligament (LSEH) was used for repeat Pringle taping. Perioperative outcomes including Pringle taping success, operative time, blood loss, conversion rate, morbidity, and mortality were assessed.

RESULTS

Laparoscopic and robotic approaches were used in 63 patients and 9 patients, respectively. The median operative time, blood loss, and hospital stay were 331.5 minutes, 70 mL, and 8 days, respectively. Open conversion occurred in two cases (2.8%) due to severe adhesions and right renal vein injury. Clavien-Dindo grade ≥ III complications occurred in 5.6% of cases with no mortality. Anti-adhesion barriers were used in 54 patients (75.0%). LSEH was attempted in 57 cases, improving Pringle taping success from 33.0% to 91.4% (P < 0.001). LSEH succeeded in all patients with prior open liver resection (n = 11). Among 6 patients in whom LSEH failed, 3 patients (50.0%) had undergone a third liver resection, and 1 patient had a history of distal gastrectomy with choledochoduodenostomy.

CONCLUSION

The newly developed LSEH technique for Pringle taping in MISRLR was feasible, enhancing safety and reproducibility even in patients with a history of open liver resection.

Core Tip: We demonstrated an effective, reproducible technique for repeat Pringle maneuver in challenging minimally invasive repeat liver resection (MISRLR). We retrospectively evaluated 72 patients who underwent MISRLR and examined the impact of a modified Pringle taping technique guided by the caudate lobe of the liver as an anatomical landmark. A marked improvement in success rate of Pringle taping from 33.0% to 91.4% occurred following this modification with low morbidity and no mortality. Thus, the proposed method may enhance both safety and reproducibility in MISRLR, particularly for patients with a history of open liver resection.

INTRODUCTION

Liver resection is an effective, potentially curative treatment for both primary and metastatic liver cancers, including hepatocellular carcinoma, intrahepatic cholangiocarcinoma, and colorectal liver metastasis. It holds a central place in current treatment guidelines and recommendations[1-3]. Nevertheless, recurrence rates remain high, often exceeding 50%, even after successful resection in patients with colorectal liver metastasis or hepatocellular carcinoma[4-7]. Repeat liver resections have shown good outcomes and are performed increasingly, aided by multidisciplinary management of recurrent disease, advances in chemotherapy, improved imaging, and refinements in surgical technique[8,9].

Minimally invasive liver resection (MILR), including laparoscopic, hybrid, and robotic approaches, has been adopted increasingly for the management of liver tumors. Its feasibility and safety are well established, and it is now implemented widely as a standard surgical strategy in selected patients[10-12]. A meta-analysis and systematic review showed that MILR was associated with more favorable perioperative outcomes compared with the open approach[13]. Nevertheless, detailed descriptions of the surgical techniques involved remain limited. Repeat liver resection is inherently more technically demanding because of postoperative adhesions, displacement of anatomical landmarks, and deformation of the liver that together can lead to longer operative times, increased blood loss, and higher morbidity[14].

Over time, various technical and instrumental innovations have accompanied the evolution of MILR[12,15-17]. Among these minimizing intraoperative hemorrhage remains a central goal. Although energy devices for parenchymal transection have advanced considerably, hepatic blood flow occlusion using the Pringle maneuver is still frequently required in MILR. In minimally invasive repeat liver resection (MISRLR), particularly after a prior open major liver resection, performing the Pringle maneuver can be technically challenging because of dense adhesions around the hepatic hilum[18]. In this report we present the short-term outcomes of MISRLR incorporating a technical modification of the Pringle maneuver designed to address these challenges.

MATERIALS AND METHODS

Patients

We conducted a retrospective review of a prospectively maintained database to identify consecutive patients who underwent repeat laparoscopic or robotic liver resection at Nippon Medical School Chiba Hokuso and Nippon Medical School Hospital between April 2015 and July 2024 that were performed or supervised by the same surgeon (Kawano Y). During this period 360 patients underwent MILR of whom 72 (15.0%) underwent repeat laparoscopic or robotic liver resection. The first 15 cases adopted the conventional Pringle taping method, directly encircling the hepatoduodenal ligament from the foramen of Winslow (initial group). In October 2019 we introduced liver surface-guided encirclement of hepatoduodenal ligament (LSEH) that was adopted in 57 cases (LSEH group). Perioperative outcomes after this modification were evaluated including Pringle maneuver success rate, procedure time, blood loss, conversion rate, morbidity, and mortality. Postoperative complications were classified according to the Clavien-Dindo system. This retrospective study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the Ethics Review Committee of Nippon Medical School, No. 30-03-1107.

Routine liver resection procedure

The patients were positioned supine for resection of lesions in the left lobe or in a semi-left lateral decubitus position for lesions in the right lobe. The first trocar was inserted at the umbilicus using the open method. A flexible laparoscope was used, and carbon dioxide pneumoperitoneum was established and maintained at 10 mmHg. Five ports were inserted under direct vision with placement depending on the tumor location. Intraoperative ultrasonography was routinely performed to confirm tumor location and its relationship to adjacent hepatic vasculature. To reduce intraoperative bleeding the head-elevated position was used, and anesthesiologists maintained low central venous pressure and tidal volume.

We attempted the Pringle maneuver in every case. The maneuver was performed in cycles of 15 minutes of clamping followed by 5 minutes of reperfusion; the clamping time was extended to 20 minutes when indocyanine green test results were within the normal range. For anatomical liver resection surgical stapling devices were used to transect the Glissonean pedicles and hepatic veins. Hepatic parenchymal transection was performed with an ultrasonic surgical aspirator (CUSA; Integra Life Sciences Inc., Princeton, NJ, United States), laparoscopic ultrasonic coagulation shears (Harmonic 1100; Ethicon Endo-Surgery, Inc., Cincinnati, OH, United States), and a soft coagulation system with the VIO3 electrosurgical system (Erbe Elektromedizin GmbH, Tübingen, Germany). Vessels over 5 mm in diameter on the cut surface were divided using clips (Hem-o-Lok; Teleflex Medical, Morrisville, NC, United States or Challenger Ti-P; Aesculap AG, Tuttlingen, Germany) and laparoscopic ultrasonic coagulation shears.

The resected specimen was retrieved using a reinforced laparoscopic retrieval bag (EndoCatch Gold or EndoCatch; Medtronic, Minneapolis, MN, United States). Intrahepatic artery, portal vein, and hepatic vein flow were routinely assessed with Doppler ultrasonography during resection and before abdominal closure. Anti-adhesion barriers (AdSpray; Terumo Corporation, Tokyo, Japan, or Interceed; Ethicon, Inc., Somerville, NJ, United States) were routinely applied around the hepatoduodenal ligament, lesser omentum, duodenum, and remnant liver surfaces to facilitate future hepatectomy if required. Initial and repeat liver resections were performed in the same manner as described above.

LSEH technique for the preparation of a repeat Pringle maneuver

The practical, safe steps performed for securing the Pringle maneuver in MISRLR are illustrated in Figure 1. First, Rouviere’s sulcus was identified, guided by the gallbladder, or if the gallbladder had been excised by the gallbladder bed. The caudate process could be seen dorsal to Rouviere’s sulcus with the inferior vena cava (IVC) situated dorsal to the caudate process. After confirming Rouviere’s sulcus the caudate process was dissected carefully to expose its outer membrane. Dorsal or lateral dissection was avoided to prevent injury to the IVC or right renal vein.

Figure 1.

Schema of liver surface-guided encirclement of hepatoduodenal ligament. A: Approach from the right side; B: Approach from the left side. IVC: Inferior vena cava.

Once Spiegel’s lobe was visualized, the IVC on its dorsal side was confirmed. Encirclement of the hepatoduodenal ligament could then be performed safely by introducing an Encircler (Niti-on; Funabashi, Chiba, Japan) or a similar device such as the Endo Retract Mini (Medtronic, Minneapolis, MN, United States) from the right side (Figure 1A) or left side (Figure 1B) of the hepatoduodenal mesentery, depending on which is easier, passing ventral to the IVC[19,20]. The tape attached to the instrument tip was then divided, and the Pringle maneuver was applied using the Rummel tourniquet technique with a silicon tube[21]. If the duodenum was adherent to the hepatoduodenal ligament, adhesiolysis was performed before applying the Pringle maneuver. Hepatic inflow control was routinely confirmed with intraoperative Doppler ultrasonography. The principles of the Pringle taping method were consistent for both the laparoscopic and robotic approaches. A step-by-step description of the technique is provided in Video.

Statistical analysis

All statistical analyses were performed using EZR, a modified version of R Commander. The χ² test or Fisher’s exact test was used to compare categorical variables, depending on their distribution. For continuous variables differences between groups were assessed with Student’s t-test; if values were not normally distributed, the Mann-Whitney U test was applied. Two-sided P values < 0.05 were considered statistically significant.

RESULTS

Patient characteristics and perioperative outcomes

The patients’ clinicopathological characteristics are summarized in Table 1. A laparoscopic approach was used in 63 patients and a robotic approach in 9 patients. The overall median procedure duration, blood loss, and postoperative hospital stay were 331.5 minutes, 70 mL, and 8 days, respectively. No postoperative mortality occurred during the study period. Age, sex, diagnosis, and the number of liver resections were comparable between the two groups. A history of open liver resection was significantly more common in the initial group. The success rate of hepatoduodenal ligament taping improved markedly from 33.0% to 91.4% after the modification (P < 0.001). The tumor size and procedural approach did not differ between the groups. The open conversion rate comprised 1 case in each group due to right renal vein injury in the initial group and severe abdominal adhesions in the LSEH group. Both were unrelated to the success of Pringle taping. The median operative time, blood loss, postoperative hospital stay, and incidence of postoperative complications classified as Clavien-Dindo grade ≥ III were comparable between the groups.

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.

Cases of Pringle taping failure

Among the initial 15 cases, all 9 instances of Pringle maneuver failure occurred in patients with a history of open liver resection (Table 2). By contrast after introduction of the technical modification, Pringle taping was successfully completed in all 11 patients with a history of open liver resection (Table 3). Details of the 5 patients in whom LSEH could not be performed are summarized in Table 2.

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.

Factors other than a history of open liver resection associated with Pringle taping failure after the modification

Despite the technical modification Pringle taping failed in 5 cases. Comparison between the failure and success groups showed no significant differences in diagnosis, previous tumor characteristics, or procedural variations. However, the number of prior liver resections may be related to the success rate of Pringle taping (P = 0.089; Table 4).

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.

DISCUSSION

Laparoscopic liver resection is widely performed for patients with liver tumors, driven by advances in laparoscopic surgical techniques and devices[15]. With the continued development of surgical instruments, refinement of techniques, and accumulation of surgical experience, the indications for laparoscopic liver resection have expanded to include recurrent liver tumors worldwide[13,22-24]. A recent systematic review and meta-analysis demonstrated that laparoscopic repeat liver resection (LRLR) is feasible and achieves favorable short-term outcomes for recurrent liver malignancies compared with open repeat liver resection[25-27]. However, because of the nature of redo surgery, adhesions around the liver often make repeat LRLR technically challenging, leading to prolonged operative times, increased blood loss, and a higher likelihood of conversion to hand-assisted laparoscopic surgery or open surgery[18,28-31]. In this context the Pringle maneuver remains one of the key factors in ensuring the feasibility and successful completion of MISRLR.

The LSEH technique is not intended as a modification of the Pringle maneuver, but rather as a preparatory step before vascular control with a tourniquet or clamps. It was developed following a major venous injury to the right renal vein that occurred during Pringle taping in the early period of MISRLR without a learning curve. From this complication we learned how to avoid disorientation that could lead to major vascular injury around the hepatoduodenal ligament in cases with severe adhesions. We also re-recognized the importance of the caudate lobe, particularly its liver surface, as a reliable anatomical landmark to prevent unintentional dorsal dissection when separating adhesions around the hepatoduodenal ligament. However, to date there have been no descriptions in the literature regarding tips for safely performing repeat Pringle taping. Interestingly, the LSEH technique can sometimes also be effective even during open repeat liver resection.

In this study we demonstrated the feasibility of MISRLR with the LSEH technique. Our perioperative results including a low open conversion rate were comparable with those previously reported in the literature (Table 5)[32-37]. We also outlined a structured and reproducible approach to performing the Pringle maneuver during MISRLR, guided meticulously by anatomical landmarks, particularly the liver surface of the caudate lobe. This method achieved a high success rate in our cohort. By contrast a review of the current MISRLR literature revealed substantial variability in reported success rates, ranging from 5% to 100%. This variation underscores the need for explicit emphasis on this concept in surgical training and education. While some authors have argued against the routine use of the Pringle maneuver, we advocate for its judicious application in MISRLR, particularly in repeat procedures given its potential to enhance operative safety and hemostatic control especially in cases involving larger or anatomical resections.

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.

Postoperative adhesion is a major obstacle to repeat liver resection because it can complicate subsequent surgeries and adversely affect patient outcomes[18,38]. A history of the Pringle maneuver itself may contribute to severe adhesions around the hepatoduodenal ligament. Although MISRLR after open liver resection is feasible in selected patients, it remains generally challenging. From the era of open repeat resections, we have routinely applied anti-adhesive barriers around the hepatoduodenal ligament. Similarly, in our MILR procedures we consider anti-adhesion barriers essential and apply them around the hepatoduodenal ligament, gallbladder or gallbladder bed, the duodenum, and the lesser omentum with future repeat liver resections in mind. We speculate that this practice contributed positively to the success of dissection around the hepatoduodenal ligament for Pringle taping.

Before and after modification of the Pringle taping method, the background characteristics of the failure group showed different tendencies. In the initial series all cases of Pringle taping failure occurred in patients who had undergone prior open liver resection. Inoue et al[29] reported that prior use of the Pringle maneuver significantly increased surgical difficulty and was associated with a high open conversion rate. Although the learning curve may have influenced outcomes, our technical modification enabled safer Pringle taping and allowed completion of surgeries without open conversion. Nakada et al[39] also noted that in addition to previous liver resection, liver cirrhosis classified as Child-Pugh B may increase the difficulty of Pringle taping, and they employed a precoagulation technique as an alternative when the Pringle maneuver was not feasible. When taping is difficult, vascular clamping instruments can be an option. Onda et al[40] reported that a vertical Satinsky clamp may be useful in laparoscopic repeat resections even in relatively small series. We likewise prepare extracorporeal vascular clamps for the Pringle maneuver; if these cannot be used successfully, open conversion should be considered.

Robotic liver resection has begun to spread in clinical practice, demonstrating reduced blood loss and shorter hospital stays[41-43]. Robotic repeat liver resections are also being explored in early clinical experience. We have introduced robotic liver resection for repeat cases, building on our experience with LRLR and the LSEH technique. Recently successful robotic major or complex repeat liver resections have been reported in case studies, highlighting advantages such as magnification for improved anatomical visualization of the hepatic hilum and the articulating function of robotic instruments, which facilitate precise manipulation even within a narrow operative field[44-46]. Vancoillie et al[47] reported that robotic repeat liver resection yielded favorable outcomes in terms of blood loss and length of hospitalization compared with LRLR. Additionally, camera rotation was noted to be effective in dissecting adhesions on the parietal peritoneum to access the liver.

The first limitation of this study was its retrospective design with a relatively small sample size. However, it was conducted at two centers. In addition, selection bias between the two groups may have been present due to the study period of MISRLR, heterogeneous diagnoses (Supplementary Table 1), and variations in minimally invasive techniques (Supplementary Table 2). These factors may partly explain why the cases with Pringle taping failure did not show worse outcomes (Supplementary Table 3). Second, we did not compare MISRLR with open repeat liver resection although many groups have reported the non-inferiority of MISRLR. Third, we could not discuss the oncologic benefits here as the study was designed primarily as a feasibility study focused on technical development. Finally, we did not classify the severity of adhesions around the hepatoduodenal ligament because the degree of adhesion is difficult to assess objectively. The routine use of anti-adhesion barriers in our practice also may have already minimized the impact of adhesion. Further research addressing these issues is needed with long-term outcomes for 5 year-period. Nevertheless, we believe our LSEH technique may contribute to implementation of safe repeat liver resection.

CONCLUSION

The newly developed taping method, LSEH, for the repeat Pringle maneuver may serve as a valuable adjunct in facilitating MISRLR with a high success rate of Pringle taping and low rate of open conversion. Good outcomes were even observed in patients with a history of open liver resection, and it could be particularly beneficial for extended repeat resections. Greater caution is warranted in patients undergoing a third or subsequent liver resection or upper gastrointestinal surgery. Further study is required to clarify the LSEH technique.

Data sharing statement

There is no additional data available.