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Copyright ©The Author(s) 2026. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jan 7, 2026; 32(1): 113470
Published online Jan 7, 2026. doi: 10.3748/wjg.v32.i1.113470
Utility of liver surface-guided encirclement of hepatoduodenal ligament for the Pringle maneuver in minimally invasive repeat liver resection
Yoichi Kawano, Takahiro Murokawa, Akira Hamaguchi, Takashi Ono, Takahiro Haruna, Daigo Yoshimori, Junji Ueda, Tetsuya Shimizu, Akira Matsushita, Hiroshi Yoshida, Department of Gastroenterological Surgery, Nippon Medical School, Tokyo 113-8603, Japan
Yuto Aoki, Toshiyuki Irie, Mampei Kawashima, Ryo Ga, Yukio Oshiro, Keisuke Minamimura, Yoshiharu Nakamura, Department of Gastroenterological Surgery, Nippon Medical School Chiba Hokusoh Hospital, Chiba 270-1694, Japan
Hiroyasu Furuki, Tomohiro Kanda, Department of Gastroenterological Surgery, Nippon Medical School Tama Nagayama Hospital, Tokyo 206-8512, Japan
Masato Yoshioka, Nobuhiko Taniai, Department of Gastroenterological Surgery, Nippon Medical School Musashi Kosugi Hospital, Kanagawa 211-8533, Japan
ORCID number: Takahiro Murokawa (0009-0009-8565-5973); Tetsuya Shimizu (0000-0002-5877-9526); Hiroshi Yoshida (0000-0002-2463-9023).
Co-first authors: Yoichi Kawano and Takahiro Murokawa.
Author contributions: Kawano T and Murokawa T conceived and designed the study, performed the experiments, and made equivalent and indispensable contributions to this manuscript as co-first authors; Kawano T, Murokawa T, and Aoki Y contributed to drafting the manuscript; Kawano T, Murokawa T, and Kawano Y contributed to the analysis and interpretation of data; Kawano T, Murokawa T, Taniai N, Nakamura Y, and Yoshida H contributed to the critical revision of manuscript; Murokawa T, Ga R, Hamaguchi A, Aoki Y, Ono T, Haruna T, Yoshimori D, Irie T, Furuki H, Ueda J, Shimizu T, Kawashima M, Kanda T, Oshiro Y, Minamimura K, Yoshioka M, and Matsushita A contributed to the acquisition of data. All authors read and approved the final version of the manuscript.
Institutional review board statement: The study was reviewed and approved by the Ethics Review Committee of Nippon Medical School, No. 30-03-1107.
Informed consent statement: Since this is a retrospective study, informed consent has been waived.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: There is no additional data available.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Takahiro Murokawa, MD, PhD, Department of Gastroenterological Surgery, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-Ku, Tokyo 113-8603, Japan. takahiro-murokawa@nms.ac.jp
Received: August 29, 2025
Revised: October 23, 2025
Accepted: December 2, 2025
Published online: January 7, 2026
Processing time: 129 Days and 16.3 Hours

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.

Key Words: Laparoscopic liver resection; Repeat liver resection; Pringle maneuver; Postoperative adhesion; Minimally invasive liver resection; Hepatocellular carcinoma; Cancer of colon and rectum; Liver metastasis; Guidelines; Second and third hepatectomies

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.


  • Citation: Kawano Y, Murokawa T, Aoki Y, Hamaguchi A, Ono T, Haruna T, Yoshimori D, Irie T, Ueda J, Shimizu T, Matsushita A, Kawashima M, Ga R, Furuki H, Kanda T, Oshiro Y, Minamimura K, Yoshioka M, Taniai N, Nakamura Y, Yoshida H. Utility of liver surface-guided encirclement of hepatoduodenal ligament for the Pringle maneuver in minimally invasive repeat liver resection. World J Gastroenterol 2026; 32(1): 113470
  • URL: https://www.wjgnet.com/1007-9327/full/v32/i1/113470.htm
  • DOI: https://dx.doi.org/10.3748/wjg.v32.i1.113470

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
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 sex55 (76.4)13 (86.7)42 (73.7)0.495
Diagnosis
HCC35 (48.6)8 (53.3)27 (47.4)1.000
CRLM35 (48.6)7 (46.7)28 (49.1)
ICC1 (1.3)0 (0)1 (1.7)
HCC with hepatolithiasis1 (1.3)0 (0)1 (1.7)
Number of histories of liver resection
155 (76.4)12 (80.0)43 (75.4)0.604
≥ 217 (23.6)3 (20.0)14 (24.6)
History of open liver resection20 (28.2)9 (60.0)11 (19.6)0.004
History of anatomical resection18 (25.0)1 (6.7)17 (29.8)0.095
History of multiple liver resection22 (30.5)3 (20.0)19 (33.3)0.529
Previous liver resection involving S1/4/5/650 (69.4)9 (60.0)41 (71.8)0.368
Anti-adhesion barrier use in prior liver resection54 (75.0)9 (60.0)45 (78.9)0.180
Types of surgical approach of MISRLR
Laparoscopic63 (87.5)15 (100)48 (84.2)0.189
Robotic9 (12.5)0 (0)9 (15.8)
Number of recurrent tumors at MISRLR
Single56 (77.8)14 (93.3)44 (77.2)
Multiple15 (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 resection57 (79.2)13 (86.7)44 (77.2)0.368
Sectionectomy2 (2.8)0 (0)2 (3.5)
Left lateral sectionectomy3 (4.2)0 (0)3 (5.3)
Segmentectomy10 (13.9)2 (13.3)8 (14.0)
Pringle maneuver57 (79.2)5 (33.3)52 (91.2)< 0.001
Open conversion2 (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 III4 (5.6)1 (6.7)3 (5.3)1.000
30-day mortality0 (0)0 (0)0 (0)1.000
In-hospital mortality0 (0)0 (0)0 (0)1.000
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
Initial65MCRLMLap-PH (S3)01O-multiple PH (S4, 5, 7, 8)10None102150None6
Initial68MHCCLap-PH (S2)01O-PH (S7)00None81700None9
Initial68MHCCLap-PH (S6)11O-PH (S7), Lap-PH (S2)10None2022040None8
Initial71MCRLMLap-PH (S4)01O-PH (S6/7)00LAC-S20236100None8
Initial83FHCCLap-PH (S4)11O-PH (S1), O-PH (S8)10None1124330None21
Initial86MHCCLap-PH (S5)01O-left hemi hepatectomy01None20254200None16
Initial67MCRLMLap-PH (S6)01Op-LLS + multiple PH (S6, 7, 8)11None15532865None8
Initial57MCRLMLap-PH (S2)01O-PH (S6, 8)10LAR352400None7
Initial63MCRLMLap-PH (S2)01O-multiple PH (S2, 3, 4, 5, 6, 7)10None153300None8
LSEH70FCRLMLap-PH (S3)10Lap-Segmentectomy (S7), Lap-PH (6, 8)11None502680None11
LSEH74MHepatolithiasisLap-PH (S3)00Lap-PH (S5)00O-total gastrectomy with splenectomy; O-choledocoduodenostomy20234100None6
LSEH78MHCCLap-PH (S3)10Lap-right anterior sectionectomy, Lap-segmentectomy (S8)11None1025780None7
LSEH79MHCCLap-PH (S5)10Lap-LLS, Lap-multiple PH (S4, 5, 7, 8)11Lap-cholecystectomy103991680None12
LSEH68MHCCRobot-PH (S3)00Lap-PH (S3, 5)10None53280None8
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, years68 (57-86)70 (58-80)0.939
Male sex8 (88.9)9 (81.8)1.000
HCC
History of anatomical resection1 (11.1)6 (54.5)0.070
History of multiple liver resection3 (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 ≥ 22 (22.2)4 (36.4)0.642
Anti-adhesion barrier use in prior liver resection6 (66.7)9 (81.8)0.617
Recurrent tumor diameter, mm15 (8-35)20 (6-40)0.219
Approaches of MISRLR
Laparoscopic9 (100)10 (90.9)1.000
Robotic0 (0)1 (9.1)0.219
Types of MISRLR
Partial hepatectomy9 (100)6 (54.5)0.068
Sectionectomy0 (0)0 (0)
Left lateral sectionectomy0 (0)2 (18.2)
Segmentectomy0 (0)3 (27.3)
Pringle maneuver0 (0)11 (100)< 0.001
Open conversion00NA
Blood loss, mL30 (0-865)90 (2-1005)0.195
Operative time in minutes240 (170-532)379 (213-644)0.026
Morbidity: ≥ Clavien-Dindo III00NA
Postoperative hospital stay, days8 (6-21))8 (6-13)0.531
30-day mortality00NA
In-hospital mortality00NA
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 sex4 (80.0)38 (73.1)1.000
HCC3 (60.0)24 (46.2)0.660
History of anatomical resection2 (40.0)15 (28.8)0.629
Previous liver resection number
11 (20.0)32 (61.5)0.151
≥ 24 (80.0)20 (38.4)
Three or more liver resections3 (60.0)11 (21.2)0.089
History of open liver resection0 (0)11 (21.6)0.571
Previously S1/4/5/6 resected5 (100)36 (69.2)0.308
Anti-adhesion barrier use in previous liver resection4 (80.0)41 (78.8)1.000
Approach
Laparoscopic4 (80.0)44 (84.6)1.000
Robotic1 (20.0)8 (15.4)
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]Italy20092004-200812LapHCC only433.3433.30018.3
Goh et al[24]Singapore20192015-201720Lap (18)/Robo (2)HCC only65.01155.000420.0
Ogawa et al[34]Japan20202014-201828LapHCC onlyNRNA828.6517.900
Mohan et al[48]Singapore20202012-201933Lap (31)/Robo (2)HCC includedNRNANRNA515.226.1
Chen et al[32]China20212017-201857LapHCC only5291.24884.2610.5610.5
Takase et al[28]Japan20212010-201958LapHCC only1424.15086.23356.900
Shen et al[35]China20222010-202048LapHCC included1939.61837.51429.236.3
Mori et al[36]Japan20222016-202162LapHCC included711.33556.53556.534.8
Inoue et al[29]Japan20222010-201863LapHCC included3047.65993.71930.269.5
Onda et al[37]Japan20232020-202243LapHCC included2967.43683.73581.437.0
Our (LSEH/total)Japan20252017-202472Lap (63)/Robo (9)HCC included11/2018.8/28.244/5777.2/77.852/5791.7/79.21/21.8/2.8

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.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Corresponding Author's Membership in Professional Societies: International Hepato- Pancreato Biliary Association; Japanese Society of Hepato-Biliary-Pancreatic Surgery; Japanese Surgical Society; Japanese Society of Gastroenterological Surgery; Japan Society for Endoscopic surgery.

Specialty type: Gastroenterology and hepatology

Country of origin: Japan

Peer-review report’s classification

Scientific Quality: Grade A, Grade B, Grade B, Grade B

Novelty: Grade B, Grade B, Grade C, Grade C

Creativity or Innovation: Grade A, Grade B, Grade C, Grade C

Scientific Significance: Grade A, Grade B, Grade C, Grade C

P-Reviewer: Li F, MD, Assistant Professor, Associate Chief Physician, China; Takemura N, MD, PhD, Professor, Japan; Zou BJ, MD, Associate Chief Physician, Associate Professor, China S-Editor: Wu S L-Editor: A P-Editor: Yu HG

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