Liver resection performed by a minimally invasive technique (laparoscopic, robotic or hybrid approaches) is an increasingly used treatment strategy for patients requiring hepatectomy for various benign and malignant diseases [1,2]. Minimally invasive liver resection (MILR) has demonstrated oncological safety and is associated with low mortality and morbidity rates [3]. However, the procedure requires experienced surgical teams because the operative aspects are complex. One of the significant challenges is maintaining haemostasis at the transection plane.

The Pringle maneuver has been successfully used in open hepatectomy to address this challenge and facilitate safe hepatectomy [4]. The concept of inflow occlusion to control hepatic bleeding is named after James Pringle, a 19th century surgeon from Glasgow. It is a valuable procedure to reduce hemorrhage in the setting of hepatic trauma [5]. When applied to MILR, the Pringle maneuver may provide several advantages. Primarily the Pringle maneuver helps reduce blood loss and reduces need for perioperative blood transfusions. Additional advantages include providing a more apparent operative field and an enhanced ability for the surgeon to visualize intrahepatic vascular and biliary structures during the transaction. This could theoretically reduce bleeding or damage to major vascular/biliary radicles.

Several techniques describe performance of the Pringle maneuver in minimally invasive surgery. However, an optimal method has yet to be identified. This review article aims to set out the various techniques described in the literature with their respective advantages and disadvantages.

A systematic literature search on MEDLINE/PubMed was performed from its earliest records to June 2022. The following medical search headings and keywords were used: "liver resection" OR "hepatectomy" AND "Pringle maneuver" OR "Pringle maneuver" OR "inflow occlusion" OR "hepatic inflow occlusion" AND "minimally invasive" OR "laparoscopic" OR "robotic" in non-MeSH terms.

The primary outcome was identifying techniques for performing hepatic inflow occlusion during laparoscopic/robotic hepatectomy. Inclusion criteria consisted of publications describing technical steps to obtain hepatic inflow occlusion during minimally invasive hepatectomy. Includes only articles reporting studies using human subjects written in English. The full-text articles were acquired and screened for eligibility. Publications which did not include laparoscopic or robotic surgical approaches to hepatectomy were excluded.

Descriptive technical reports were requested rather than statistical analyses of outcomes and therefore no validated scale was used. Author assessment (OAM and SA) of the quality of individual articles was performed. Report of the literature search results according to PRISMA guidelines (Fig. 1).

Fig 1. PRISMA diagram of study inclusion.

After the initial search, 38 records were found. Seven studies were excluded because of inability to retrieve the full-text article. Five of the 31 full-text articles screened were excluded because they did not comply with the study topic. Furthermore, two were excluded because no description of the technique for using the Pringle maneuver was provided or the technique did not pertain to minimally invasive surgery. One article was subsequently withdrawn by the authors and was therefore excluded. Finally, 23 publications were identified and the full texts were examined. Table 1 presents the records [6-28]. Table 2 presents the reported advantages and disadvantages of the techniques.

Table 1 . Summary of published articles describing the Pringle technique in minimally invasive liver resection

	Authors	Year of publication	Publication type	Intra/extra-corporeal	Laparoscopic/robotic/both	Technical details
1	Onda et al. [7]	2021	Case series (n = 14)	Extracorporeal	Laparoscopic	A laparoscopic Satinksy vascular clamp was used to occlude portal structures.
2	Zhang et al. [11]	2021	Technical report	Intracorporeal	Laparoscopic	This technique described a modification of the Huang Loop technique. Encirclement of the hepatoduodenal ligament was achieved using a Foley catheter with a suture attached to the distal end. The Goldfinger dissector was utilised from the patient's right side to grasp the suture and guide the Foley behind the portal structures.
3	SteinbrÜck et al. [12]	2021	Case series (n = 35)	Extracorporeal	Laparoscopic	This technique used a cotton tape as a tourniquet threaded through a 24-French chest tube. The chest tube was controlled extracorporeally to apply Pringle.
4	Gao et al. [13]	2021	Technical report	Intracorporeal	Laparoscopic	This technique described a modification of the Huang Loop technique. A custom-made tourniquet (silica gel-based) was used with a Hem-o-Lok used to prevent slippage when not in occlusive mode.
5	Choi et al. [14]	2020	Case series (n = 25)	Intracorporeal	Laparoscopic	This technique described use of a Penrose drain to perform occlusion. The Goldfinger dissector was used to facilitate encirclement of the hepatoduodenal ligament.
6	Cai et al. [9]	2020	Case series (n = 34)	Intracorporeal	Laparoscopic	This intracorporeal technique used the elasticated cuff from surgical gloves. The elasticated cuff was passed behind the hepatoduodenal ligament with Desjardins forceps. The cuff was secured with a Hem-o-Lok at the time of occlusion and removed using loose clip forceps.
7	Huang et al. [8]	2018	Technical report	Intracorporeal	Laparoscopic	This technique used a 14-French Foley catheter to encircle portal structures.
8	Peng et al. [15]	2019	Propensity case-matched analysis (n = 92)	Extracorporeal	Laparoscopic	Encirclement of the portal structures was performed with intravenous infusion tubing (cut to 70 cm). The infusion tubing was passed through a size 7.5 endotracheal tube (cut to 30 cm). Pringle was applied extracorporeally.
9	Lim et al. [16]	2018	Case series (n = 48)	Intracorporeal and extra­corporeal	Both (Laparo­scopic and Robotic)	This technique used a cotton tape passed around the portal structures and through a catheter.
10	Laurenzi et al. [17]	2018	Case series (n = 400)	Intracorporeal	Laparoscopic	In this technique a Teflon tape and drain tubing was used (when applying occlusion a heavy duty clip was applied to maintain compression).
11	Piardi et al. [18]	2016	Technical report	Both intra­corporeal and extra­corporeal	Laparoscopic	This publication describes an intracorporeal and extracorporeal technique, which were similar in using a cotton tape passed through a tube.
12	Mizuguchi et al. [19]	2015	Case series (n = 11)	Extracorporeal	Laparoscopic	In this technique clamping took place outside the abdominal wall. The authors demonstrated feasibility in 11 patients.
13	Nomi et al. [20]	2015	Case series (n = 6)	Intracorporeal	Laparoscopic	This publication reported 6 cases using "modified laparoscopic Pringle" in which only the hepatic artery was clamped—as an alternative to total inflow occlusion which is postulated may result in greater ischaemia-reperfusion injury.
14	Dua et al. [21]	2015	Case series (n = 88)	Extracorporeal	Laparoscopic	In this technique encirclement of the hepatoduodenal ligament is performed with umbilical tape which is threaded through a flexible Rummel tourniquet (7 inch, 10 French). One end is intracorporeal and in contact with the hepatoduodenal ligament and the other end is passed extracorporeally alongside a working port. A Mayo clamp is extracorporeally used to maintain constriction of the hepatoduodenal ligament.
15	Okuda et al. [6]	2013	Case series (n = 23)	Extracorporeal	Laparoscopic	In this technique cotton tape is threaded through a tube which is partly intracorporeal and partly extracorporeal (passes through an abdominal wall defect created by 5 mm trocar/port).
16	Chao et al. [22]	2012	Case series (n = 20)	Intracorporeal	Laparoscopic	This technique described the use of a T-tube and 10-French urethral catheter to fashion a "6-loop" with a stitch inserted to maintain occlusion.
17	Rotellar et al. [23]	2012	Case series (n = 39)	Extracorporeal	Laparoscopic	Tourniquet technique: this technique uses a cotton tape (with ink to mark the midpoint) to encircle hepatoduodenal ligament, which is threaded through a Tiemanns catheter (22 Fr) with the internal tip at the hepatoduodenal ligament and the other end passed externally.
18	Patriti et al. [24]	2011	Case series (n = 10)	Extracorporeal	Robotic	This technique is used in robotic hepatectomy. Exteriorisation takes place at the epigastrium allowing the assistant to apply Pringle whilst the operating surgeon remains at the console.
19	Herman et al. [25]	2010	Case series (n = 9)	Extracorporeal	Laparoscopic	This technique describes use of a laparoscopic vascular clamp to occlude the pedicle to the hemi-liver only—as the authors cited concerns about the possibility of ischaemia-reperfusion injury with total pedicle clamping. Hence this technique was described by the authors as a "half-Pringle" manoeuvre.
20	Cho et al. [26]	2009	Case series (n = 32)	Extracorporeal	Laparoscopic	Use of the Endo Retract Maxi to pass behind the hepatoduodenal ligament and encircle with vascular tape with use of a Nelaton catheter for a Rummel tourniquet-type technique.
21	Belli et al. [10]	2008	Case report	Extracorporeal	Laparoscopic	Use of the Endo Retract Maxi to pass behind the hepatoduodenal ligament and encircle with vascular tape with use of a Nelaton catheter for a Rummel tourniquet-type technique.
22	Belli et al. [27]	2005	Case report	Not stated	Laparoscopic	The porta hepatis was surrounded by a tape that was passed through a 16-French rubber catheter for use as a tourniquet to enable rapid and nontraumatic clamping of the pedicle. This precaution was only preventive; the Pringle manoeuvre was never performed.
23	Kurokawa et al. [28]	2002	Case report	Intracorporeal	Laparoscopic	Short report where the technique not described but mentions that it is the Glisson's left hemi-liver pedicle which is selectively clamped.

Table 2 . Reported results from each publication with stated advantages and disadvantages

	Author	Technique detail	Time to prepare Pringle (sec)	Failure to achieve vascular occlusion (rate %)	Complication rate from placement and application of Pringle (rate %)	Advantages and disadvantages of the described technique
1	Onda et al. [7]	Laparoscopic Extracorporeal Satinksy clamp n = 14	Not stated	0% (reported)	0% (reported)	This technique is particularly advantageous in cases of repeat laparoscopic hepatectomy where adhesions may be present at the hepatoduodenal ligament. The Satinksy clamp is applied effectively without need for adhesiolysis which may be challenging, time-consuming and risk inadvertent vascular/biliary injury at the hepatoduodenal ligament. No disadvantages were stated.
2	Zhang et al. [11]	Laparoscopic Intracorporeal Modified Huang Loop technique	Not stated	Not stated	Not stated	No advantages or disadvantages to this technique are stated in the report.
3	SteinbrÜck et al. [12]	Laparoscopic Extracorporeal Rummel tourniquet technique n = 35	Not stated	0% (reported)	0% (reported)	Key advantage reported is safety and effectiveness. The authors also cite cost-effectiveness, reporting that the cost for each case is < US.
4	Gao et al. [13]	Laparoscopic Intracorporeal Modified Huang Loop technique n = 18	41 (versus 60 seconds when using a tourniquet technique)	Not stated	Not stated	The key advantage of their technique is the speed of preparing, applying and releasing Pringle. The time to complete these steps was faster compared with tourniquet technique.
5	Choi et al. [14]	Laparoscopic Intracorporeal Tourniquet technique using Penrose drain n = 25	Not stated	Not stated	Not stated	Advantages stated are that the technique is simple, reliable, cost-effective and reproducible. Furthermore, it does not require an additional working port to be inserted. Due to the flexibility of the Penrose drain it does not obscure the surgeon’s view. A limitation may occur in repeat hepatectomy cases where adhesions hinder encirclement of the hepatoduodenal ligament.
6	Cai et al. [9]	Laparoscopic Intracorporeal Tourniquet technique using elasticated cuff from surgical glove n = 34	Not stated	Not stated	Not stated	Advantages stated for this technique are cost-effectiveness and safety. The elasticated cuff is postulated by the authors to be less traumatic to structures of the hepatoduodenal ligament compared with rape/ribbon. Furthermore, the technique does not require an additional working port. No disadvantages specific to the technique are stated.
7	Huang et al. [8]	Laparoscopic Intracorporeal Original description of the Huang Loop	Not stated	Not stated	Not stated	Advantages stated are ease of use and no requirement for additional port. In addition, the soft nature of the Foley catheter is deemed less likely to injury portal structures during passage behind the hepatoduodenal ligament and during inflow occlusion.
8	Peng et al. [15]	Laparoscopic Extracorporeal Tourniquet technique using intravenous infusion tubing n = 92	408	Not stated	Not stated	The advantage of this technique is the ease of application and ready availability of the apparatus. The disadvantage is the need for an extra working port due to the extracorporeal nature of the described technique.
9	Lim et al. [16]	Laparoscopic and robotic Intracorporeal and extracorporeal Tourniquet technique using cotton tape n = 48	Not stated	0% (reported)	Not stated	The authors postulate that the ability of the surgeon to obtain tactile feedback when applying Pringle is greater with the extracorporeal technique, hence a less theoretical risk of causing injury. Furthermore the intracorporeal technique may have a higher rate of incomplete occlusion. Although specific time duration is not stated the authors state that locking/unlocking of Pringle is slower with the intracorporeal method.
10	Laurenzi et al. [17]	Laparoscopic Intracorporeal Tourniquet technique using Teflon tape and clip n = 400	Not stated	3% (failure occurred in cases where adhesions at the hepatoduodenal ligament were present)	0% (reported)	A key advantage reported is disengaging of the Pringle using this technique is fast (by releasing the clip). A disadvantage is the difficulty of an effective Pringle in cases of adhesions at the hepatoduodenal ligament.
11	Piardi et al. [18]	Laparoscopic Intracorporeal and extracorporeal Tourniquet technique using cotton tape	Not stated	Not stated	Not stated	The advantage of the intracorporeal technique is not requiring an additional port but it may be challenging to apply in “critical moments”. The advantage of the extracorporeal technique is cost-effectiveness and ease of application. It allows quick clamping and unclamping. However it requires an extra port and may be difficult to manoeuvre in the left side/lateral decubitus positions.
12	Mizuguchi et al. [19]	Laparoscopic Extracorporeal Tourniquet technique using Teflon tape and clip n = 11	Not stated	Not stated	0% (reported)	A cheap, reproducible method for laparoscopic Pringle without specific limitations described.
13	Nomi et al. [20]	Laparoscopic Intracorporeal Hepatic artery occlusion only n = 6	Not stated	Not stated	Not stated	The authors postulate that their method of selective arterial clamping may be preferable in cases of major liver resection to avoid ischaemia-reperfusion effects in small liver remnants.
14	Dua et al. [21]	Laparoscopic Extracorporeal Tourniquet technique using umbilical tape and Mayo clamp n = 88	Not stated	Not stated	Not stated	Advantages stated are ease of placement, effectiveness and reproducibility. The tourniquet is placed pre-emptively and thus Pringle can be applied quickly in cases of bleeding. This is in contrary to vascular clamps which may cause injury during placement if the view of the hepatoduodenal ligament is obscured by bleeding.
15	Okuda et al. [6]	Laparoscopic Extracorporeal Tourniquet technique using cotton tape n = 23	354	Not stated	0% (reported)	Advantages stated are ease and speed of application. There were no complications associated with use of Pringle using this technique. No limitations are stated.
16	Chao et al. [22]	Laparoscopic Intracorporeal Tourniquet technique using T-tube and catheter n = 20	Not stated	Not stated	0% (reported)	Advantages are safety of the technique, ease of assembly with materials readily available in operating room. No specific disadvantages stated.
17	Rotellar et al. [23]	Laparoscopic Extracorporeal Tourniquet technique using cotton tape n = 39	Not stated	Not stated	0% (reported)	Advantages include that the technique is fast, simple and safe. No injuries were identified related to setup and application of Pringle.No specific disadvantages stated.
18	Patriti et al. [24]	Robotic Extracorporeal Tourniquet technique n = 10	Not stated	0% (reported)	0% (reported)	A safe, fast and reproducible technique described for use in robotic hepatectomy. No complications or failure to achieve inflow occlusion were reported.
19	Herman et al. [25]	Laparoscopic Extracorporeal Use of vascular clamp n = 9	Not stated	0% (reported)	0% (reported)	The authors describe a technique for hemi-liver Pringle which they state is advantageous to reduce ischaemia/reperfusion injury without excessive splanchnic venous congestion. The other advantages are safety and ease of application.
20	Cho et al. [26]	Laparoscopic Extracorporeal Tourniquet technique using vascular tape n = 32	Not stated	0% (reported)	0% (reported)	The main advantages are safety and effectiveness of the Pringle technique. The disadvantage is in the requirement for additional equipment (Endo Retract Maxi).
21	Belli et al. [10]	Laparoscopic Extracorporeal Tourniquet technique using Nelaton catheter	Not stated	n/a	n/a	The advantage of this technique is in ability to apply whilst patient is in left lateral decubitus position. Application of inflow occlusion was not required in the cases and therefore safety and effectiveness of Pringle technique cannot be assessed.
22	Belli et al. [27]	Laparoscopic Tourniquet technique using rubber catheter	Not stated	n/a	n/a	The advantages were that placement was rapid and nontraumatic. However placement was precautionary only with the Pringle manoeuvre never performed.
23	Kurokawa et al. [28]	Laparoscopic Intracorporeal Details of the technique not fully described	Not stated	Not stated	Not stated	In this short report the technique involved selective clamping of the hemi-liver pedicle. No specific disadvantages were stated.

n/a, non-applicable.

The techniques described in the 23 articles included in the review can be classified as intracorporeal or extracorporeal. Extracorporeal usually requires an additional laparoscopic port. The techniques can be placed into 3 groups as similar principles were followed, albeit using slight modifications in technique. The three types of technique which emerged were:

1. The Rummel tourniquet: wrapping around the hilar structures using tape (cotton, nylon, or umbilical), which is then passed through a rigid tube (Fig. 2).

Fig 2. Rummel tourniquet technique.

2. Direct compression to occlude the inflow structures using a vascular clamp (Fig. 3).

Fig 3. The Bulldog technique.

3. Constriction of hilar structures using Foley catheter—Huang Loop technique (Fig. 4).

Fig 4. The Huang Loop technique.

Laparoscopic liver resection is a complex procedure that requires extensive training and experience [29]. Intra-operative hemorrhage is a primary challenge facing the surgeon, with ramifications including the requirement for a blood transfusion associated with increased postoperative complications, mortality, and reduced disease-free survival [30,31]. Theoretically, bleeding during the transection may increase operative times and impair the operative field, resulting in difficulty identifying intrahepatic biliary and vascular structures. The Pringle maneuver is an established strategy to facilitate hepatectomy whilst maintaining haemostasis in the transection plane.

The early descriptions of the laparoscopic Pringle maneuver tended to describe the Rummel tourniquet technique, widely used by liver surgeons in open hepatectomy. The clear advantage is that the surgeon is familiar with the technique and uses the same apparatus in their open practice. The Rummel tourniquet method is safe and can be used efficiently. Okuda et al. [6] reported that preparing this technique would take 354 seconds. A significant advantage offered by this technique during right hepatectomy is that extracorporeal retraction can be used to retract the hilum to the left, which improves the view of the inflow structures during hilar dissection.

The option of using a vascular clamp to achieve inflow occlusion can be undertaken using an extracorporeal vascular clamp [7]. However, this can be problematic depending on the type of hepatectomy which is being performed, as the long handle of the instrument may obstruct the surgeon’s view or clash with other instruments. The intracorporeal vascular clamps (bulldog clamps) are particularly useful in a recent study demonstrating comparable short-term outcomes to laparoscopic hepatectomy versus cotton tourniquet technique [32]. The bulldog technique is particularly applicable in instances where there is concern that the umbilical tape may damage hilar structures, for example, after hilar lymphadenectomy, where the structures are devoid of protective lymphatics and connective tissue.

The Huang Loop is a relatively recent innovation and is our institution’s current method of choice [8]. It has the benefit of being intracorporeal and relatively cost-effective. The silastic properties of the Foley catheter provide uniform constriction of the inflow structures whilst exerting minimal trauma. A particularly useful property of the 16- or 18-French Foley catheter is its relative rigidity which allows a passage through the Foramen of Winslow to be safely negotiated as it passes posterior from the pars flaccida to the hepatoduodenal ligament. This passage is performed without direct visualization of Winslow’s Foramen, but the Foley catheter’s atraumatic structure is unlikely to cause caval or other injury. The hepatoduodenal ligament may be closed following previous upper abdominal surgery due to adhesions. In such cases, a small amount of adhesiolysis is required before passing the Foley catheter through a window in the pars flaccida. The Foley then enters the safe window and emerges to the right of the ligament. Pringle may be released inadvertently under certain circumstances. This has been noted in our experience when the surface of the Foley is very wet/lubricated, and we advise keeping the Foley as dry as possible.

Intracorporeal techniques have the benefit of not requiring an additional port. Cai et al. [9] report that a straightforward technique successfully uses an inexpensive instrument to apply laparoscopic Pringle in 34 patients. The authors used the elastic rim of a size seven surgical glove to encircle the inflow structures and maintained tension using Hem-o-Lok. Although they reported that Pringle release using loose clip forceps is straightforward, this instrument may be have limited availability in laparoscopic centers, and removal of Hem-o-Loks once applied is associated with difficulty.

The patient’s left lateral decubitus positioning during laparoscopic liver surgery facilitates proper liver mobilization and provides access to the right superior segments (VII and VIII) but increases the technical difficulty of achieving hepatoduodenal ligament encirclement. In particular, the pars flaccida is challenging to access in this position. A preferred option is to use curved retractors, such as the Endo Retract Maxi (Medtronic) to pass the nylon tape around the hilar structures [10]. Using a vascular clamp (intra- or extracorporeal) is another option, and in recent cases, our center has had success using the Huang Loop technique.

Recent years have seen much progress in the robotic approach to MILR. Only two publications identified in this review reported the use of their technique for robotic hepatectomy [6,14]. It is appropriate to appreciate that Pringle technique used an extracorporeal method for both publications. Therefore, the assistant uses Pringle extracorporeally whilst the lead surgeon operates from the robotic console.

In conclusion, the optimal method of performing the Pringle maneuver should be based on simplicity, safety, reproducibility and cost-effectiveness. There are several techniques for using Pringle in both laparoscopic and robotic approaches without evidence of superiority. The surgeon or institutional preference dictates the technique chosen. It is recommended that surgical teams become familiar with more than one technique because of many factors, including adhesions from previous surgery or patient positioning. However, we recommend the Huang loop technique using a Foley catheter because it is inexpensive, straightforward, rapid and a safe way of applying Pringle in both open and laparoscopic cases.

None.

No potential conflict of interest relevant to this article was reported.

Conceptualization: All authors. Data curation: All authors. Methodology: All authors. Visualization: All authors. Writing - original draft: All authors. Writing - review & editing: All authors.