Laparoscopic major and complex liver resection

Terminology and definitions

In 2008 the first expert consensus meeting on laparoscopic liver surgery was held to discuss the international position on LLR. In the resulting Louisville Statement, they agreed on three procedural definitions: pure laparoscopy, hand-assisted laparoscopy, and hybrid technique. Pure laparoscopy applies to complete mobilization and resection through laparoscopic ports, with an incision for specimen extraction only. Hand-assisted laparoscopy applies to the elective placement of a hand port to assist the operation, with transection performed under video laparoscopic view and extraction of tumor through the hand port incision. Hybrid technique refers to a procedure in which laparoscopy, with or without hand assistance, is used for liver mobilization, whereas resection is performed under direct vision through a small incision. According to a comprehensive international review performed by Nguyen and colleagues, 75% of reported laparoscopic resections were pure laparoscopic, 17% were hand-assisted procedures, and 2% used the hybrid technique. In addition, 4% were conversions to laparotomy or hand-assisted procedures, with the remaining 2% using less common techniques, such as a thoracoscopic approach.

Considerable debate arose at the Second International Laparoscopic Liver Consensus Conference, regarding the terminology and definitions of laparoscopic major hepatectomy versus “degree of difficulty.” For example, isolated laparoscopic resection of segment VII or VIII as a single segment might be defined as a minor hepatectomy using the classical definition of Couinaud, but the degree of difficulty for these operations minimally invasively is very high. A novel difficulty scoring system for laparoscopic liver resections has been proposed.

Laparoscopic resections should be categorized no differently than open resections. Based on Couinaud and Brisbane 2000 terminology of liver anatomy and resections, segments II, III, IVb, V, and VI are most amenable to laparoscopic resection (see Chapter 2 ). Isolated resection of tumors located in posterior-superior liver (segments I, IVa, VII, and VIII) and major hepatectomy have been reported ^{, , ,} (see Chapter 127D ). However, these operations are technically more challenging and should be reserved for expert surgeons who are able to extend the limits after safe mastery of segments II to VI laparoscopic resections. In the comprehensive review by Ciria and colleagues, the majority (70%) were minor resections (two segments or less), including nonanatomic wedge resections and left lateral sectionectomies (20% each). Anatomic segmentectomies and sectionectomies, classified as minor by the amount of resected liver, are complex resections reported mainly by Asian surgeons and accounted for 13% and 5% of the cases, respectively. Major resections, consisting of three or more segments, accounted for 24% of the cases, with right and left hepatectomies representing 13% and 11%, respectively. Anecdotal extended hepatectomies were reported, and 6% were unspecified.

Indications

Indications for LLR should be categorized no differently than open resections (see Chapters 101 , 118 , and 127A ). It must be emphasized that the potential benefits of a minimally invasive resection must not lead to an increase in the indications outside the guidelines or to resection of 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 patient history, imaging, and tumor markers to be benign and without harmful potential, including cysts, hemangiomas, and focal nodular hyperplasia. Also, laparoscopic resection should not be performed for the purpose of diagnosis when lesions are safely amenable to percutaneous biopsy.

Indications for LLR rely on the same guidelines as open liver surgery. Cases should be discussed at multidisciplinary tumor boards. Once the indication for resection has been established, the feasibility of the laparoscopic approach should be evaluated. The extent of resection; the size, location, and number of lesions; and proximity to the major vessels are important factors in determining when laparoscopic resection is appropriate ( Table 127E.1 ). The selection criteria of patients are crucial for successfully performing right or left hepatectomy ( Box 127E.1 ). Liver function is a determinant regardless of the technique and surgical skills (see Chapter 4 ). Patients with decompensated liver function are often associated with a vulnerable body condition, which may lead to intraoperative bleeding and anesthetic accident. Thus a Child A score must be achieved preoperatively. No major vascular invasion is essential for radical operation. It is challenging to perform laparoscopic operation in patients with a large subcapsular tumor. The limited space and mobilization of the liver may cause the tumor to break up and spread. The status of the underlying liver should also be considered. Although patients with benign disease have an underlying normal liver (see Chapter 88 ), patients with malignant disease usually have some degree of liver injury (see Chapters 68 , 69 , and 74 ). About 90% of patients with hepatocellular carcinoma (HCC) have a background of chronic liver injury, with chronic hepatitis B or C infection (see Chapter 68 ), alcohol, and nonalcoholic steatohepatitis (see Chapter 69 ) being the most common causes. In addition, a significant proportion of patients with colorectal liver metastases increasingly have some degree of liver disease from chemotherapy-induced injury (see Chapter 69 ). This should be taken into consideration for the laparoscopic approach. The surgical difficulty is highly subjective and influenced by not only tumor and patient factors but also the surgeon’s experience. It is important to increase skills gradually according to experience level before performing more complex procedures.

Tumor size and location

The most favorable lesions for laparoscopic resection are solitary tumors less than 5 cm and located in peripheral liver segments II to VI ( Fig. 127E.1 ). Such cases are recommended as initial procedures when initiating an LLR program. Pedunculated tumors located at inferior or left lateral liver even greater than 5 cm are also favorable to laparoscopic resection. The laparoscopic approach should be considered the standard approach for left lateral sectionectomy ^{, ,} (see Chapter 127D ). Peripheral wedge resections are also considered easy procedures. Tumor size itself is no longer an absolute contraindication for LLR.

The complexity of each major hepatectomy procedure differs widely and the number of segments alone does not convey the complexity of a resection. To this end, Lee et al. recently reported that the complexity of open liver resections should not be classified based on whether the resection is “major or minor” but instead based on the extent of the liver resection. The classification divides open liver resection procedures into three complexity groups: low, medium, and high. In this system, a left lateral sectionectomy is classified as low complexity. Left hepatectomy, right hepatectomy, and right posterior sectionectomy are considered medium complexity, and right anterior sectionectomy and central bisectionectomy are considered high complexity. Kawaguchi et al. proposed another classification system of laparoscopic liver resection according to their surgical difficulty. This classification provides levels of difficulty: grade I (the beginning and least complex level, which includes wedge resection and left lateral sectionectomy), grade II (the intermediate level, which includes anterolateral segmentectomy and left hepatectomy), and grade III (the advanced level, which includes posterosuperior segmentectomy, right posterior sectionectomy, right hepatectomy, central hepatectomy, and extended left/right hepatectomy). The rates of overall morbidity and major complications increased significantly with a stepwise increase from grade I to III. Laparoscopic major resections are now well-standardized procedures. ^, As they gain wider acceptance, these resections will require a higher level of training and experience.

More difficult cases include lesions located at the posterosuperior liver (segments I, IVa, VII, and VIII) and lesions in proximity to major vessels or the hepatic hilum. The laparoscopic field for posterosuperior liver resection lies in the deep area of the subphrenic rib cage and may be overlaid by the side of the diaphragm and abdominal wall. These cases should be restricted to experienced centers, but such resections are increasingly reported ^{, ,} and may involve a more extensive resection by laparoscopic approach than would otherwise be necessary to avoid an open approach. An example would be a laparoscopic right hepatectomy for a posterior lesion that could be resected by a more limited, open segmentectomy or posterior sectionectomy (see Chapter 118B ). For each patient, the surgeon must weigh the risks and benefits of the laparoscopic and open techniques with the benefits of parenchymal preservation.

Tumor pathology

As previously emphasized, the availability of minimally invasive techniques should not lead to extending the indications for resection of benign lesions (see Chapter 88 ) with no harmful potential. The observed trend has been toward a higher proportion of benign disease being treated laparoscopically because these pathologies are more amenable to a minimally invasive approach because of a higher incentive in young patients, and no margins are required.

The main indications for LLR are, as in open surgery, primary liver and biliary cancer (see Chapters 49 , 50 , 51 , and 89 ), selected patients with metastatic liver cancer (see Chapters 90 , 91 , and 92 ) and highly selected patients with symptomatic benign liver lesions (see Chapter 88 ). Principles of oncologic resection are essential. Surgical margins should 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 open approach should be indicated. In this respect, bilobar disease, especially in the case of colorectal liver metastases, is considered a contraindication to the laparoscopic approach by most teams because of the risk of missing some lesions or performing an inadequate oncologic procedure (see Chapter 90 ). Recently, Okumura et al. reported that laparoscopic two-stage hepatectomy for bilobar colorectal liver metastases is safe and feasible with favorable surgical and oncologic outcomes compared with open two-stage hepatectomy. Perihilar cholangiocarcinoma or gallbladder cancer are also considered contraindications to the laparoscopic approach because of the complexity of biliary and possible vascular resections/reconstructions, as well as the necessary radical dissection of hilar lymph nodes (see Chapters 49 , 51A , and 51B ).

Interestingly, HCC occurs mainly in patients with cirrhosis, which is the most common single reported indication for LLR, representing more than 50% of those for malignancy ^, (see Chapters 74 , 89 , and 120 ), whereas in most open liver resection series, colorectal liver metastases form the majority of cases (see Chapter 90 ). The main reason that HCC appears more amenable to a laparoscopic approach is that screening programs allow a diagnosis of early HCC in patients with known liver disease (i.e., small solitary nodules). A major issue with liver resection in cirrhotic patients, even minor procedures, is postoperative decompensation, including liver failure and ascites (see Chapters 74 and 120 ). Our group observed that LLR was very well tolerated by cirrhotic patients. In particular, we observed less postoperative ascites than previously experienced after open surgery, probably because the abdominal wall and its collateral venous drainage are better preserved.

This was confirmed by several authors and in meta-analyses. It seems that laparoscopy itself may offer some protection from postoperative decompensation. Reasons may include less fluid requirement, avoidance of long abdominal incisions with muscle division, better collateral preservation, less manipulation, and less respiratory impairment. Recognition of the efficacy and safety of LLR for HCC has led to increased numbers of cases performed, especially in patients with peripheral tumors less than 5 cm. ^,

Almost 50% of our laparoscopic experience has been with patients who have chronic liver disease. These patients typically require longer operations and more pedicle clamping, but globally they have a better recovery than their open counterparts. In our experience, however, colorectal liver metastases (see Chapter 90 ) have been less amenable to a laparoscopic approach. This is the result of our referral base consisting mainly of bilobar or difficult-to-resect liver metastases.

Safety and benefits

Laparoscopic liver resection appears to provide the benefits that laparoscopy has offered to patients undergoing many other abdominal operations. Case-control studies have demonstrated lower morbidity, ^{, ,} shorter length of hospitalization, less operative blood loss, ^{, , , , ,} reduced transfusion requirements, ^{, ,} a reduced need for analgesia and quicker return to oral consumption, ^, and fewer postoperative adhesions. ^, Studies have demonstrated decreased costs when accounting for shorter operative time and LOS. ^{, ,} The mortality rates in these studies are at least equivalent to those of large case series of open liver resections. In their review of 463 published articles on LLR, Ciria and colleagues concluded a cumulative mortality rate of 0.4%. This compares favorably to the 0% to 5.4% reported in the open-resection literature from high-volume centers. Of 37 deaths, the cause of death was attributed to bleeding, sepsis, or liver failure. There were no reported intraoperative deaths. A 10.5% morbidity rate was reported, with a range of 0% to 50% across studies. Liver-specific complications accounted for 4% and included bile leaks, transient liver failure and ascites, and abdominal collections. The remaining 6% were complications common to all operations, including but not limited to hemorrhage, wound infection, hernia, bowel injury, intra-abdominal fluid accumulation, and urinary or respiratory tract infections. Fretland et al. reported the first single-center RCT (OSLO-COMET study) in patients with colorectal liver metastases who underwent minor parenchyma sparing liver resection and successfully demonstrated the safety of laparoscopic liver surgery and its superiority compared with the open approach regarding postoperative morbidity. Another RCT, the ORANGE II PLUS trial (NCT01441856) comparing the early outcomes of right and left hepatectomy either by laparoscopy or open route, is still active and its results are not yet known.

Tozzi et al. compared laparoscopic versus open approach for right and left hepatectomy using a propensity score matching analysis and concluded that laparoscopic major hepatectomies are safe and feasible procedures allowing a similar complication rate with a shorter LOS and diminished postoperative pain with respect to the standard approach. Laparoscopic right hepatectomy is associated with a longer operative time but less blood loss and shorter LOS than open right hepatectomy. Bleeding control was superior possibly because of improved intraoperative magnification for surgical manipulations, use of new coagulation devices, and the pressure associated with the pneumoperitoneum that may have helped decrease bleeding during liver parenchymal transection. Yoh et al. compared the short-term outcomes between laparoscopic right hepatectomy using the caudal approach and open right hepatectomy with the anterior approach and liver hanging maneuver. Perioperative blood loss and transfusion rates, overall and symptomatic pulmonary complication rates, and hospital LOS were significantly lower in the laparoscopic group, but operation time was significantly longer. In their meta-analysis comparing clinical outcomes of laparoscopic versus open right hepatectomy for liver tumors, Hong et al. showed that no significant difference was observed between the two groups in portal occlusion, rate of R0 resection, transfusion rate, mild complications, and postoperative mortality. Intraoperative blood loss was significantly lower and LOS was shorter in the laparoscopic group compared with the open group. The disadvantage of laparoscopy was the longer operating time.

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 operation time than after an initial open hepatectomy. ^{, , ,} Another potential advantage of quicker recovery after the laparoscopic approach is the possibility of increased and earlier access to chemotherapy.

Barriers to the wide acceptance of laparoscopic hepatic surgery—such as threat of gas embolism, violation of oncologic principles, and significant risk of bleeding—have not been apparent in the literature. In addition, studies have consistently demonstrated that operative safety and postoperative morbidity improve with experience. When comparing our early and late groups, we found statistically significant reductions in operative time (from 210 to 150 minutes), blood loss (from 300 to 200 mL), conversion (from 16.9% to 2.4%), and morbidity (from 17.2% to 3.4%). We used the technique of cumulative sum analysis (CUSUM) to determine when the learning curve reached a statistical plateau, based on conversion rate in minor hepatectomies, and this was found to be at 60 cases. Cai et al. showed a learning curve for four different well-defined laparoscopic hepatectomy procedures in a single-center experience. On average, 15 to 30 cases for left hepatectomy, 43 cases for left lateral sectionectomy, 35 cases for nonanatomic liver resection, and 28 cases for segmentectomies were necessary. Hasegawa et al. demonstrated that a major laparoscopic liver resection could be safely introduced for a surgeon with an experience level of at least 60 minor laparoscopic liver resection. Nomi et al. reported that 45 major laparoscopic liver resections were required before operating times were reduced. For Chan et al., by overcoming the learning curve at the 25th laparoscopic major hepatectomy, more pure laparoscopic hepatectomies could be performed. Using this as the cutoff, operative time, need for Pringle, blood loss, and transfusion requirement were brought down with more proficient resection. In a literature review, a steep learning curve of 45 to 60 cases is necessary for laparoscopic major hepatectomy. Nitta et al. compared outcomes between the first 21 and second 21 cases of laparoscopic-assisted major liver resections using the hanging technique and found a decrease in estimated blood loss, shorter LOS, and no difference in complications. The report from the national clinical database in Japan concluded that among the major laparoscopic liver resection procedures, a left hepatectomy could be a good option for a standard practice. This concept was also reported by other studies. ^, Laparoscopic left hepatectomy has a lower potential risk of bleeding from the inferior vena cava than laparoscopic right hepatectomy because dissection between the inferior vena cava and the liver is not needed. The parenchymal transection area of left hepatectomy is smaller compared with right hepatectomy or posterior sectionectomy. The parenchymal transection along the Cantlie’s line is easier than that of the right intersectional plane because of both the lower risk of disorientation and the lower bleeding risk because of the lower hepatic venous pressure.

Additional benefits of laparoscopy include better cosmesis and improved maintenance of the sensorimotor integrity of the abdominal wall. Despite these favorable results, it is important to acknowledge that these findings are mostly 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.