Our study demonstrates that the implementation and adaption of laparoscopic liver surgery does not adversely impact morbidity and mortality in a surgical high-volume liver centre. The introduction of laparoscopic liver resections, which accounted for a fraction of more than 30% of all procedures, was accompanied by a first series of feasible and save surgical interventions. This included 66% major and technically major liver resections affecting benign and malign lesions also in the posterolateral segments (VII, VIII and IVa) of the liver (12). Smaller parenchyma sparing resections were intuitively performed applying the Diamond resection technique as described by Cipriani et al. (17). Our data are in line with the literature that laparoscopic liver resections allows for shorter operation times, reduced intraoperative blood loss, less wound infections, faster recovery and hence shorter hospital stay (18). Until recently, liver resections In Germany were predominantly performed by open surgery. In contrast, specialized groups in Asia (19), the United States (20), Italy (18) France (21) and the United Kingdom (22) can draw on more than twenty years of experience in this still maturing field of minimally invasive surgery. Since the first international position statement on laparoscopic liver surgery (23) major scientific effort has propelled the application of minimally invasive surgical techniques in Europe. Major concerns regarding morbidity and mortality (24), especially after complex laparoscopic liver surgery with high death rates have been reported (25). However, oncological inferiority and technical inapplicability have been scientifically disproved by a solid amount of research data (26).
Our findings support the position that laparoscopic surgery is well suited for resectable HCCs in cirrhotic livers (27) (21), and resections for HCC also accounted for the major part of our oncologic LLRs in this study. International data also demonstrate that in selected patients with HCC, liver resection does not increase the morbidity or impair long-term survival following liver transplantation (28). Therefore, laparoscopic liver resection prior to transplantation has been integrated into our treatment strategy for HCC as well.
Biliary leakage remains a serious complication after liver resection with an incidence of up to 12% (29). Intraperitoneal septic complications resulting from biliary leakages may lead to secondary organ failure and even death (30) (31). Leakages can derive from previously ligated bile ducts at the resection surface of the liver, either based on a separated biliary system or based on an elevated intrabiliary pressure due to downstream stenosis of the biliary system or papillary dysfunction. Moreover, leakage from a bilioenteric anastomosis if performed, is another source of BL (32). Risk factors include prolonged operation time, age, preoperative chemotherapy and special types of liver resections such as left hemihepatectomy (33). In our study bile leaks were detected after five major (6.7%) and three minor open liver resections (8.8%). An increased incidence for biliary leakages after left hemihepatectomie has also been recently highlighted in a meta-analysis on laparoscopic liver resections (9). Fortunately, we did not detect any biliary leakages in our series of LLR which also included ten laparoscopic left hemihepatectomies.
Despite a very low morbidity and especially BL rate in OLR without bilioenteric anastomosis the introduction of a minimally invasive liver resection program did not increase the BL-rate, despite modifications in the technique of parenchymal transection. It could be shown by others, that BL is a persisting problem in modern liver surgery. Whereas, despite an increasing number of complex liver resections the overall morbidity remains stable, but the rate of bile leaks is increasing with an increasing complexity of liver resection (34) leading to an incidence of BL of more than 7% even in high volume centres (35)
Prevention of bile leaks may include several measures as: (1) omitting of abdominal drains, (2) meticulous anatomy orientated liver surgery, (3) pre- or intraoperative recognition of variants of the biliary system, (4) application of bile leak tests and (5) eventually biliary decompression e.g. by means of T-tubes in case of complex liver surgery. However, the latter is not supported by enough evidence, so far. All these measures were considered in the present series.
The lower rate of bile leaks in patients without abdominal drains has been confirmed in other analysis with an OR of 2.04 (36) to 5.6 (37) . During the study period the use of abdominal drains was successively reduced, leading to about 50% of patients without abdominal drains, however those included predominantly patients with a low risk of bile leak (e.g. without bilioenteric anastomosis). The ‘white test’ was also adopted liberally in OLR, since it could be shown in a meta-analysis, that its use leads to a significant reduction of postoperative BL (OR 0.3, p=0.002) (15) , however it was not used in LLR. Other measures, which did not prove effective in the prevention of BL like routine application of fibrin sealant was not used at all in the present series. However, surveys e.g. from the Netherlands have shown that more than around 25% of surgeons use fibrin sealants on a frequent/routine basis (38), among others to reduce resection surface-related complications like BL. However, the use of fibrin sealants disproved to reduce the incidence of BL in a meta-analysis (39). However, insertion of a T-tube was afflicted with a (slightly) higher incidence of BL in the present series. Since a T-tube was used mainly in complex cases or in case of long central exposure of the bile duct, this phenomenon is supposed to be based on a consecutive selection of a high risk population for BL based on our previous experience (7) rather than an increased rate of bile leaks caused by T-tube insertion itself. However, this hypothesis cannot be finally proven, but no patient developed BL caused by the T-tube itself, e.g. at the site of insertion into the common bile duct. Influencing factors and the distribution of T-tubes within open liver resected patients (without a BDA) are demonstrated in Table 4.
However, the incidence of BL in our series compared well with other analyses, e.g. of the National Clinical Database (NCD) of Japan including 14,970 patients with a revealed a BL-rate of 8.0% (40). In this analysis gallbladder cancer and extrahepatic bile duct carcinoma were also unravelled as risk factors for BL, moreover peripheral vascular disease and open wounds were pointed out as further risk factors
The rate of other complications was low in the present analysis for LLR as well as OLR, including blood loss and blood transfusions, e.g. compared to NSQIP data (41), where transfusions were required in 33% of patients. Also, the overall morbidity was very low after LLR and significantly reduced compared to OLR. Even the morbidity of the OLR group compares well with other reports from other European centres (35) and clinics from North America (42). However, since patient characteristics differed between both groups, a direct comparison of both groups is debatable. Especially the mortality seems to be rather dependant on patient characteristics than on surgical technique. Likewise, in an analysis using data on 7621 hepatectomies form the US- NSQIP-database (42) it has been shown that mortality after liver resection is predominantly seen in elderly patients in combination with major liver resection.
A recent randomized controlled trial which compared laparoscopic and open liver resection for CRLM indicated superiority of laparoscopic surgery in terms of postoperative complications and cost effectiveness (43). Almost 15% of our minimally invasive operated patients were treated for CRLM and laparoscopic parenchyma sparing liver surgery was furthermore included into our multimodal treatment strategy for this disease (44). Recent short-term data also indicate that repeat laparoscopic liver resection after open liver resection might be associated with favourable outcomes in selected groups of patients including those with CRLM (45).
Reports on laparoscopic liver resection for patients with cholangiocarcinoma are still scarce. In our cohort, only two patients with intrahepatic Cholangiocarcinoma were treated by laparoscopic liver resection. All other CCA patients, and especially those with perihilar cholangiocarcinoma received an open liver resection, as described by our group earlier (13). To date, due to oncological superiority, portal vein embolization for preoperative future liver remnant augmentation and “hilar on block resection” remains our treatment strategy for central bile duct carcinomas (14). However, this type of resection which also requires vascular reconstruction of the portal vein, to date was not performed laparoscopically by our group. Furthermore, postoperative hepatic insufficiency and bile leakage after demanding biliary reconstruction, often with several small orifices, contribute to the postoperative complication rate of this complex surgical disease pattern (46). In our study presented here postoperative biliary leakages were predominantly detected in patients with Cholangiocarcinoma or gallbladder carcinoma, which in five cases required extrahepatic bile duct resection. All patients were operated by means of open surgery and received a bilioenteric anastomoses with external biliary drainage, if applicable. A recent study revealed that external biliary drainage following major liver resection did not necessarily decrease the risk of biliary anastomotic leakage and was furthermore associated with an increased incidence of post hepatectomy liver failure (47). Our incidence in post hepatectomy liver failure however was comparatively low, probably due to extensive perioperative liver function testing including the LiMAx test for this selected group of patients.
Our study has several limitations. A direct comparison of the minimally invasive and open liver resections is invalid, since we did not perform a propensity score matching. Patients in the LLR group hence displayed a better ASA performance status and comprised fewer complex resections including extrahepatic bile duct resections. Furthermore, laparoscopic resections included a significant smaller number of radical lymphadenectomies. The extrahepatic bile duct obtains its blood supply mainly from small branches of the hepatic artery. Hence, extensive lymphadenectomy and long segment bile duct exposure can cause blood deprivation and segmental ischemia induced necrosis which ultimately results in bile leakage. Our overall biliary leakage rate was low when compared to the international literature (48) (49).
Increased experience is commonly paralleled by increased confidence to perform more complex resections. Our overall morbidity and mortality rates are satisfying, especially when compared to the overall German average (50).
We were able to safely develop a minimally invasive liver resection program at our institution which so far resulted in an excellent patient outcome. It could be shown, that technical modifications of the surgical approach, like introduction of ultrasonic shears for parenchymal transection are safe and especially not afflicted with an increased rate of biliary leakage or bleeding complications.