Overview

Over the latter portion of the twentieth century, liver surgery has rapidly progressed from a risky procedure to a safe therapy for benign and malignant liver disease. As with many surgery disciplines, minimally invasive approaches were pursued in the 1990s. Gagner is credited for the first laparoscopic partial hepatectomy in 1992 (Gagner et al, 1992), and in a prospective series of 30 patients published in 2000, we demonstrated the safety and reproducibility of laparoscopic partial hepatectomy (Cherqui et al, 2000), which was followed by the safe application of these techniques to living donor left lateral sectionectomy in 2002 (Cherqui et al, 2002). Despite close to 20 years of development and nearly 3000 reported cases internationally, minimally invasive liver surgery remains an emerging field that should be approached with caution by surgeons experienced in the perioperative care and planning of both liver and laparoscopic surgery (Nguyen et al, 2009). Six centers have reported series of more than 100 patients, and most perform fewer than half of their total cases laparoscopically (Bryant et al, 2009; Buell et al, 2008; Chen et al, 2008; Cho et al, 2008; Koffron et al, 2006, 2007; Topal et al, 2008;). We have performed more than 200 laparoscopic partial hepatectomies since 1996, which represents 23% of our hepatectomy volume.

Whereas the percentage of resections for benign lesions has remained relatively stable over our experience, the percentage of resections for malignant lesions continues to increase year after year. The objective of this chapter is twofold: to present a balanced view of the current understanding of these techniques and to elucidate the technical details of the most commonly performed resections.

Terminology

In 2008, leaders in the field met to discuss the current status of laparoscopic liver surgery (Buell et al, 2009). In the so-called Louisville Statement that resulted, those in attendance agreed on three procedural definitions: 1) pure, 2) hand-assisted, and 3) hybrid laparoscopy. Pure laparoscopy involves complete mobilization and resection via laparoscopic ports, with an incision for specimen extraction only. Hand-assisted laparoscopy involves the elective placement of a hand port for mobilization or resection, which is then used for specimen extraction. Hybrid laparoscopy refers to a procedure in which the resection and extraction are performed through a minilaparotomy, but laparoscopy, with or without hand assistance, is utilized for mobilization.

According to a comprehensive international review performed by Nguyen and colleagues (2009), 75% of reported laparoscopic resections were pure laparoscopy, 17% were hand-assisted procedures, and 2% used the hybrid technique. In addition, 4.8% were conversions to laparotomy or hand-assisted procedures, with the remaining 2% using less common techniques, such as a thoracoscopic approach.

Laparoscopic resections should be categorized no differently than open resections, based on the Brisbane 2000 terminology of liver anatomy and resections (Pang, 2002). Anterior and lateral segments II, III, IVb, V, and VI are most amenable to laparoscopic resection. Isolated resections of segments I, IVa, VII, and VIII have been reported, as surgeons extend the limits after safe mastery of anterior resections. Of the nearly 3000 internationally reported laparoscopic liver resections, the majority (44.9%) were wedge resections or segmentectomies, followed by left lateral sectionectomies (20.3%). Major resections, consisting of three or more Couinaud segments, included right hemihepatectomy (9%) and left hemihepatectomy (6.8%). Extended right hepatectomy, caudate lobectomy, central hepatectomy, and extended left hepatectomy each made up less than 1% of the total reported cases (Nguyen et al 2009).

We performed 96% of our resections using pure laparoscopy, with hand assistance (4%) selectively used for right hepatectomies or posterior segmentectomies. Major resections comprise 19% of our experience, and limited resections comprise 81% (Bryant et al 2009).

Indications

Liver pathology under consideration for open partial hepatectomy should be evaluated for the feasibility of a laparoscopic resection (see Chapter 90A); however, the potential benefits of a minimally invasive resection do not confer a prescription to resect all hepatic lesions for the purpose of providing a definitive diagnosis. Specifically, the laparoscopic approach should not be used to resect incidental, asymptomatic lesions convincingly recognized by imaging and markers to be benign and without harmful potential (cysts, hemangiomas, focal nodular hyperplasia), nor should laparoscopic resection be performed for the purpose of diagnosis, when lesions are safely amenable to percutaneous biopsy.

The indications for laparoscopic resection do not vary from those for open resection (Box 90E.1); however, lesion size and location are the most important determinants of when laparoscopic resection is appropriate. Resection of benign and malignant solid lesions and cystic and parasitic lesions are possible laparoscopically. The most favorable lesions for laparoscopic resection are solitary, 5 cm or less, and located in peripheral liver segments II to VI (Fig. 90E.1; Buell et al, 2009). Pedunculated tumors greater than 5 cm are often easily resectable laparoscopically. In experienced hands, laparoscopic left lateral sectionectomy should be the standard approach for pathology in segments II and III (Buell et al, 2009; Chang et al, 2007).

FIGURE 90E.1 The anterolateral liver—composed of segments II, III, IVb, V, and VI—is most amenable to the laparoscopic approach.

Relative contraindications include lesions isolated to segments VII and VIII, multiple or bilateral lesions, and lesions located in proximity to the major hepatic veins, the inferior vena cava, or the hepatic hilum. These contraindications are considered relative, because in experienced centers, these lesions are increasingly managed laparoscopically (Buell et al, 2008; Koffron et al, 2007; Vigano et al, 2009a). A more extensive laparoscopic resection than would otherwise be necessary through an open approach may be contraindicated. An example would be a laparoscopic right hemihepatectomy for a posterior lesion that could be resected by a more limited open posterior segmentectomy. For each patient, the surgeon must weigh the risks and benefits of the laparoscopic and open techniques with the benefits of parenchymal preservation.

Surgical margins for benign lesions do not vary between open and laparoscopic resections. If there is concern that an adequate margin cannot be obtained laparoscopically, but it is technically feasible by an open approach, the former is contraindicated. Other contraindications include gallbladder cancer and hilar cholangiocarcinoma, because of the risk of peritoneal and port-site seeding and the necessary complex hilar dissection and extensive resection, respectively (see Chapters 49, 50B, 90B, and 90C).

Safety and Benefits

Laparoscopic partial hepatectomy provides the benefits that laparoscopy has offered to patients undergoing many other abdominal operations. Case-control studies have demonstrated shorter operative times (Bryant et al, 2009; Buell et al, 2008; Koffron et al, 2007), shorter lengths of hospitalization (Buell et al, 2009; Cai et al, 2008; Koffron et al, 2007; Topal et al, 2008), less operative blood loss (Bryant et al, 2009; Buell et al, 2008; Koffron et al, 2007; Lesurtel et al, 2003), reduced transfusion requirements (Buell et al, 2008; Koffron et al, 2007; Topal et al, 2008), a reduced need for analgesia (Cai et al, 2008), quicker return to oral consumption (Cai et al, 2008), lower morbidity (Buell et al, 2008; Koffron et al, 2007; Topal et al, 2008), and fewer postoperative adhesions (Belli et al, 2009; Laurent et al, 2009). Studies have demonstrated decreased costs when accounting for shorter operative times and hospitalizations (Buell et al, 2008; Koffron et al, 2007; Polignano et al, 2008).

The mortality and morbidity rates in these studies are at least equivalent to, if not better than, those of large case series of open liver resections. In their review of 127 published articles on laparoscopic hepatic resection, Nguyen and colleagues (2009) found a cumulative mortality rate of 0.3%. This compares favorably to the 0% to 5.4% reported in the open-resection literature from high-volume centers. All deaths were postoperative, and most often caused by liver and multiorgan system failure. Of 2804 patients, 295 morbid complications were reported (10.5%), with a range of 0% to 50% across the 127 studies (Nguyen et al 2009). Liver-specific complications included bile leaks (1.5%), transient liver failure and ascites (1%), and abscess (2%). The remaining 6% were complications common to all operations, including but not limited to hemorrhage, wound infection, hernia, bowel injury, arrhythmia, and urinary or respiratory tract infections.

Laparoscopy has been utilized with success in cirrhotic patients (see Chapter 90F), with multiple small case-control studies and series demonstrating lower morbidity and improved recovery. The laparoscopic approach also decreases the rate of postoperative ascites in this subgroup. Possible explanations include the preservation of venous and lymphatic collateral pathways in the abdominal wall, less intraoperative mobilization of the liver, and reduced intraoperative volume loading (Belli et al, 2007; Buell et al, 2009; Cherqui, 2006; Gigot et al, 2002; Kaneko et al, 2009; Laurent et al, 2003; Santambrogio et al, 2009; Vigano et al, 2009a). Nearly 40% of our laparoscopic experience has been with those patients who have chronic liver disease. These patients typically require longer operations and more pedicle clamping but globally have a better recovery than their open counterparts (Bryant et al, 2009).

As a consequence of decreased adhesions formed after an initial laparoscopic resection, reoperations, such as repeat hepatectomy and liver transplantation can often be performed more easily, with less blood loss, reduced transfusion requirements, and reduced operative time than following an initial, open partial hepatectomy (Belli et al, 2009; Bryant et al, 2009; Laurent et al, 2003). In our study comparing patients who had undergone a previous open or laparoscopic liver resection, the absence of adhesions at the time of liver transplantation in the laparoscopic group allowed for hepatectomy in a mean of 150 ± 52 minutes versus 247 ± 71 minutes in the open group. Additionally, a median of 2 U blood was transfused during hepatectomy in the open group versus zero in the laparoscopic group (Laurent et al, 2009). These are significant benefits, given that patients who require repeat operations often have diseased parenchyma because of cirrhosis or chemotherapy effects and the negative immune and oncologic impact of blood transfusion.

Barriers to the wide acceptance of laparoscopic surgery—such as threat of gas embolism, violation of oncologic principles, and significant risk of bleeding—have not been apparent in the literature (Vigano et al, 2009a). In addition, studies have consistently demonstrated that operative safety and postoperative morbidity improve with experience (Nguyen et al, 2009). When comparing our early and late groups, we found statistically significant reductions in operative time (210 to 150 minutes), blood loss (300 to 200 mL), conversion (16.9% to 2.4%), and morbidity (17.2% to 3.4%) (Vigano et al, 2009b).

Additional benefits include better cosmesis, improved maintenance of the sensorimotor integrity of the abdominal wall, and earlier access to adjuvant therapy because of quicker recovery. Despite these favorable results, it is important to acknowledge that these findings are from nonrandomized studies, and that laparoscopic cases remain highly selected for their potential for success. It can be inferred from the colorectal and bariatric literature that these benefits are real, especially for indicated cases (see Box 90E.1); however, the benefits may not be as robust for cases with relative contraindications (Castaing et al, 2009; Cho et al, 2008).

Oncologic Outcomes

Perhaps more important than demonstrating perioperative benefit is confirmation that oncologic principles are not dismissed. With regard to margins, recurrence, and survival, comparable results between open and laparoscopic resections have been well demonstrated in the literature (Nguyen et al, 2009; Vigano et al, 2009). In a meta-analysis of 165 laparoscopic liver resections and 244 open liver resections, Simillis and colleagues (2007) found no difference in tumor-free margin status, overall survival, and disease-free survival between laparoscopic and open liver resection for cancer. This has been demonstrated for both hepatocellular carcinoma (HCC) and colorectal metastatic disease (Castaing et al, 2009; Cherqui et al, 2009; Nguyen et al, 2009; Sarpel et al, 2009). Laparoscopic resection of other metastatic tumors has been reported in small numbers, mainly breast cancers and melanomas. Further, port-site metastases and peritoneal dissemination have not occurred with the use of closed-bag methods for specimen extraction.

As chemotherapeutic, biologic, and radiation options expand, patients with primary and metastatic liver cancer may anticipate longer survival despite the high possibility of recurrence. Resection of HCC as a bridge to future transplantation should also be a consideration (Cherqui et al, 2009; Laurent et al, 2009). As such, parenchyma-sparing procedures should be promoted in anticipation of repeat operative needs. Rather than performing a laparoscopic right or left hepatectomy because of relative ease technically, segmental resections along anatomic lines must be performed when possible.

General Principles

Incisions, Exploration, and Exposure

The open technique is used to gain access to the abdomen supraumbilically. The remaining four ports are placed under direct vision, with incisions sized to accommodate the necessary cannulas as pictured in Figure 90E.2. The median trocar is the camera port, the paramedian ones are the working ports, and the most lateral right and left ports are for retraction. For segment VI and VII resections, four ports are used: a 10-mm port in the left upper quadrant, a supraumbilical 12-mm port, a 12-mm paraumbilical port in the midclavicular line, and a 10-mm trocar in the anterior-axillary line (Fig. 90E.3).

FIGURE 90E.2 Common port sites, trocar sizes (in millimeters), and positioning for laparoscopic partial hepatectomy. The patient is supine, and the surgeon is positioned between the patient’s legs. Specimen extraction may be through a suprapubic or right lower quadrant incision (dotted lines).

(From Cherqui D, et al, 2000: Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg 232:753-762.)

FIGURE 90E.3 Port sites and trocar sizes (in millimeters) for laparoscopic resection of segments VI and VII. The patient is in the left lateral decubitus position with the surgeon and assistant ventral to the patient.

(From Cherqui D, et al, 2000: Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg 232:753-762.)

After a thorough inspection of the peritoneal cavity for ascites, carcinomatosis, and signs of portal hypertension, attention is turned to the liver for signs of superficial lesions, steatosis, cholestasis, cirrhosis, or other gross pathology. Next, laparoscopic ultrasound is performed. A thorough knowledge of both B-mode and Doppler laparoscopic ultrasonography is mandatory for safe and accurate laparoscopic resections. A high-frequency laparoscopic probe is used to look for lesions less than 1 cm, which may be difficult to assess by extracorporeal imaging, and to confirm adequate margins (Foroutani et al, 2000; Milsom et al, 2000; Montorsi et al, 2001).

The round ligament is divided close to the abdominal wall. This prevents a dangling remnant that might obstruct the view or soil the tip of the scope. Then the falciform ligament is divided along its length to the insertion of the hepatic veins into the vena cava. The round ligament along with the gallbladder or remnant cystic duct can be used as “handles” for manipulation of the liver.

If pedicle occlusion is anticipated, the pars flaccida is opened, and an instrument is passed behind the portal triad to encircle it with a tape. The tape is then extracorporeally inserted through a 16-Fr rubber tube to serve as a tourniquet, and it is returned to the abdomen. If pedicle clamping is to be used, we favor 15 minutes of clamping interrupted by 5 minutes of pedicle flow. If parenchymal bleeding occurs during the 5 minute period, the transected parenchyma can be opposed or packed with some gentle lateral pressure. Although we do not routinely clamp the pedicle, this should be another safety tool in the arsenal of the new laparoscopic liver surgeon, or it may be used as an emergent maneuver, if parenchymal bleeding obscures visualization. Liberal use of on-demand, intermittent inflow occlusion, meticulous technique, and low central venous pressure (CVP) anesthesia are very effective at limiting blood loss during these cases. Complete vascular occlusion is difficult laparoscopically, and any resection requiring this should be performed as an open procedure.

Specific Partial Hepatectomy Procedures

Left Lateral Sectionectomy

The left lateral sectionectomy is the most straightforward laparoscopic liver procedure, and it represents the standard of care for our division. The left lateral section is mobilized by dividing the round, falciform, left triangular, and coronary ligaments with the Harmonic or LigaSure. The entire length of the lesser omentum is opened close to the liver, and a replaced left hepatic artery is divided if present. If a parenchymal bridge covers the inferior surface of the round ligament, it is divided with the harmonic shears.

The parenchymal transection is performed to the left of the patient’s falciform ligament with the Harmonic or LigaSure. The plane of transection is better visualized by retracting the round ligament superiorly and to the right and the left lateral segment superiorly and to the left. The ultrasonic dissector can then be used to open the deeper parenchyma, progressing cranially from anterior to posterior, with small vessels and ducts controlled as previously discussed; however, transection can be completed with the Harmonic Scalpel or LigaSure device, because there are few bridging structures in this procedure. Transection is continued until the portal pedicles of segments II and III are visualized. These pedicles can then be divided with two to three firings of the linear stapler (Fig. 90E.4). Parenchymal transection continues cranially, until the left hepatic vein is visualized, at which point it is divided with the linear stapler (Fig. 90E.5).

FIGURE 90E.4 Left lateral sectionectomy. Atraumatic graspers retract the round ligament to the right and the specimen to the left. The ultrasonic dissector is used to dissect the parenchyma, exposing the segment II and III pedicles for subsequent ligation and division.

FIGURE 90E.5 After the left hepatic vein is dissected free of parenchyma, a tape is passed around it for better control and exposure. A linear stapler is passed around the hepatic vein and fired, thereby ligating and dividing the vessel. The left and right hepatic veins are divided in a similar manner for the left and right hemihepatectomy, respectively.

Right Hemihepatectomy

Right hemihepatectomy is the most difficult of the common laparoscopic liver resections, and previous mastery of more limited laparoscopic resections is a prerequisite. As previously detailed, the falciform and round ligaments are dissected, and a tourniquet around the main portal triad is assembled. The cystic duct and artery are ligated and divided, and the gallbladder remains in situ as a retraction point for elevating the liver to the right. The remnant cystic duct is retracted to the left, exposing the short course of the extrahepatic right glissonian pedicle. A replaced right hepatic artery is ligated and divided if present, and the right branches of the hepatic artery and portal vein are gently dissected and individually encircled with tapes to retract them for easier division. The right branch of the artery is divided between plastic locking clips, and the right branch of the portal vein is divided with a linear stapler or between locking clips. Identification of the origin of the left branch of the portal vein should be assured before occluding the right portal branch. When possible, intraparenchymal dissection to the branches of the hepatic artery and portal vein limits risk to the portal triad bifurcation. The line of demarcation along the midplane of the liver is identified and marked. The procedure can be done without or with initial mobilization of the right lobe; the former is referred to as the anterior approach, which is our preferred method.

For the anterior approach, the right hepatic vein is not controlled prior to parenchymal transection. After ligation of the right hepatic artery and portal vein, parenchymal transection is started at the inferior edge of the liver in the anterior-posterior direction along the line of demarcation. The previously described techniques are utilized. As progress is made cranially, the proximal hepatic veins draining segments V and VIII toward the middle hepatic vein are exposed, clipped, and divided (Fig. 90E.6). At the level of the hilar plate, the right bile duct’s anterior and posterior branches are divided between clips or staples. Division of the intraparenchymal bile ducts and hilar plate allows the plane to be opened widely for easier parenchymal transection, and the junction between the right lobe and segment I is divided to allow exposure of the retrohepatic vena cava. The posterior Glisson capsule is now divided along the anterior surface of the vena cava, while systematically clipping and dividing the small bridging veins. The right hepatic vein is identified at its insertion into the vena cava and is transected with a linear stapler. The specimen is now retracted to the right, as the hepatocaval ligament and the attachments of the right hemiliver are freed from the diaphragm.

FIGURE 90E.6 Right hemihepatectomy. Atraumatic graspers retract the gallbladder to the right and the round ligament to the left, opening the dissection plane (white dashed line). The right hepatic artery and right portal vein are ligated extraparenchymally, and the right bile duct is ligated intraparenchymally. The hepatic veins draining segments V and VIII into the middle hepatic vein are encountered intraparenchymally, ligated, and divided. A laparoscopically assembled tourniquet around the portal pedicle is pictured and can be used for the Pringle maneuver if necessary.

(From Cherqui D, et al, 2010: Hepatectomies par abord laparoscopique, Encyclopedie Medico Chirurgicale. Masson, France, Elsevier.)

When parenchymal transection is to be performed after mobilization of the right hemiliver, the right glissonian pedicle is dissected and divided as discussed for the anterior approach. This mobilization approach may require the use of a hand port (Fig. 90E.7). Next, the right triangular and coronary ligaments are divided. The liver is retracted to the left and anteriorly, and the accessory veins between the right hemiliver and vena cava are clipped and divided. As progress is made cranially, the hepatocaval ligament is divided between clips, and the right hepatic vein is subsequently divided with a linear stapler. The liver is now both completely mobilized and devascularized, and parenchymal transection is performed along the line of demarcation according to previously discussed principles.

FIGURE 90E.7 The use of a hand port in the right iliac fossa allows for manual manipulation and palpation of the liver; it is only used for difficult right-sided resections. Fewer laparoscopic ports are necessary, and the specimen is removed through the hand-port incision. Hand ports can be used from the outset of the operation or as an adjunct during a difficult resection.

(From Cherqui D, Chouillard E, 2007: Laparoscopic liver resections. In Clavien PA, et al [eds]: Atlas of Upper Gastrointestinal and Hepato-Pancreato-Biliary Surgery, Berlin, Springer.)

Peripheral Partial Hepatectomies: Segmentectomy, Metastasectomy, or Tumorectomy

Peripheral partial hepatectomies are performed for lesions in the anterior or lateral segments. They can be anatomic, such as segmentectomies along theoretic segmental borders, or they can be nonanatomic, as with metastasectomy or tumorectomy (Fig. 90E.8). They usually do not require liver mobilization, especially for anterior lesions. For malignant lesions, 10- to 20-mm margins are determined using ultrasonography and are marked using diathermy. For benign lesions, a wide margin is unnecessary. Parenchymal transection can be performed with the Harmonic Scalpel or LigaSure, and it follows the margins marked on the liver surface. Hemostasis is achieved with bipolar diathermy and clips. If significant veins or pedicles are within the resection margins, these are clipped and divided; the use of a linear stapler is rarely necessary.

FIGURE 90E.8 Metastasectomy. The lesion is circumscribed with a 1- to 2-cm margin, and either a Harmonic Scalpel or LigaSure device can be used to resect the lesion.

(From Cherqui D, Chouillard E, 2007: Laparoscopic liver resections. In Clavien PA, et al [eds], 2007: Atlas of Upper Gastrointestinal and Hepato-Pancreato-Biliary Surgery. Berlin, Springer.)

Conclusion

Laparoscopic partial hepatectomy is a safe procedure for selected patients, when performed by appropriately trained surgeons, and it offers considerable perioperative benefits compared with laparotomy. In addition, oncologic outcomes and survival for HCC and colorectal metastases have been demonstrated to be equivalent in nonrandomized trials. Although the indications for laparoscopic surgery are somewhat rigid when it comes to lesion size and location, greater experience and newer technology are continually expanding the possibilities of this procedure. Surgical resection of benign, asymptomatic lesions remains contraindicated despite the safety and benefits of laparoscopic surgery. The most common laparoscopic procedures are detailed above, based on safe practices developed over our 14 years of experience. Left lateral sectionectomies and limited resections of the anterior and lateral segments of the liver are safe and well-accepted procedures. Major hepatectomies and limited segmentectomies involving segments I, IVa, VII, and VIII are increasingly reported, but by no means are they approaching the standard of care. This remains an expanding and exciting field in liver surgery, especially considering its role in the multidisciplinary approach to primary and secondary liver cancers and transplantation.