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INTRODUCTION
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.
MATERIALS AND METHODS
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).
RESULTS
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.
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).
2. Direct compression to occlude the inflow structures using a vascular clamp (Fig. 3).
3. Constriction of hilar structures using Foley catheter—Huang Loop technique (Fig. 4).
CONCLUSIONS
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.
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