**5. Minimally invasive hepatectomy**

### **5.1. Laparoscopic-assisted partial hepatectomy**

their unique vascular inflow and outflow, each segment can be safely excised without damage to surrounding hepatic segments. Intraoperative ultrasonography is used routinely for identification of the vascular structures, evaluation of tumor location, extent and relationship

**Figure 2.** Schematic illustrations of the standard hepatic resections as labeled. Source: Cho, Fong. Hepatic Resection. In:

After initial laparoscopic inspection excludes unresectable disease (in selected cases), the incision is made. In an open conventional approach, appropriate incision and exposure is critical to safe hepatectomy. There are several incisions used including the bilateral subcostal

Once the liver is mobilized by dividing ligamentous attachments, careful inspection, palpation and ultrasound examination are performed to evaluate for any missed tumors. Arterial aberrancies are identified and portal triad inflow is controlled with sutures and clips or staple ligation. The corresponding hepatic vein is isolated and ligated. Parenchymal transection is performed along the line of devascularization. Different techniques for parenchymal transection exist, varying from clamp-crushing, waterjet, monopolar/bipolar cautery, radiofrequency ablative devices, bipolar vessel sealing devices, ultrasonic dissection devices to staplers. The clamp-crush technique is rapid and has been associated with lower rates of blood loss compared to other methods [24]. Once the resected segment is removed, hemostasis is obtained

(Chevron), right/left subcostal, J-type or the inverted Y (Mercedes) incision.

Ashley SW, editor. Scientific American Surgery. Hamilton: Decker. 7th ed; 2014. pp. 1094–1114.

to the surrounding vasculature.

64 Liver Cancer

Although established as a safe and beneficial approach for numerous intra-abdominal operations, laparoscopic techniques were slow to be adopted for liver surgery for several reasons [26]. Concerns over technical feasibility of vascular dissection and control, organ mobilization, parenchymal dissection and management of intraoperative complications were prohibitive. Furthermore, it was unknown if port-site seeding, inadequate margins and poor oncologic outcomes would be more common in the minimally invasive approach.

The benefits of laparoscopic liver surgery are numerous. In addition to the generalized benefits of laparoscopic surgery including a more rapid functional recovery, smaller incisions which reduce the incidence of surgical site infections and postoperative pulmonary complications, there are additional advantages specific to laparoscopic liver surgery. Steep Trendelenburg positioning reduces intrahepatic venous pressure and the pneumoperitoneum exerts tamponade effect on vasculature leading to reduced intraoperative blood loss. Laparoscopy creates a caudal-cranial surgical view which affords improved visualization of major vascular structures compared to the ventral-dorsal angle of visualization of an open hepatectomy. For cirrhotic patients, small laparoscopic incisions avoid disruption of abdominal wall collaterals and the constraint on fluid shifts in a laparoscopic partial hepatectomy can decrease the incidence of liver-related complications. Minimally invasive hepatectomy also results in less adhesion formation which facilitates additional surgery in the future.

There have been numerous studies to date demonstrating the safety and efficacy of laparoscopic liver surgery. In 2009, a worldwide experience of 127 series including 2804 cases of laparoscopic partial hepatectomy demonstrated comparable 5-year overall survival and disease free survival compared to open hepatectomy [27]. Half of these cases were done for malignant disease with greater than 80% of resections boasting negative surgical margins. In 2015, a randomized control trial was published demonstrating safety and feasibility of laparoscopic liver resection with reduction in length of stay and intraoperative blood loss compared to open hepatectomy [28]. Numerous systematic analyses have substantiated these data, demonstrating that the laparoscopic partial hepatectomy is associated with decreased intraoperative blood loss, shorter length of hospital stay, and decreased number of positive resection margins. Overall, there were consistently fewer complications found in the laparoscopic group in these reviews [29]. A case–control propensity matched studies also found no difference in 1-, 3-, and 5-year overall survival and disease-free survival [30]. The National Surgical Quality Improvement Program database was evaluated to compare short-term outcomes among patients undergoing minimally invasive partial hepatectomy. Over 3000 patients were include in the study and it demonstrated lower postoperative morbidity and shorter length of stay compared with patients undergoing open liver resection [31].

Specific to the treatment of HCC, the safety and efficacy of the laparoscopic approach has been evaluated in several meta-analyses and propensity score analyses. These studies demonstrated the equivalent or superior perioperative outcomes of laparoscopic compared to open resection [32, 33]. In a propensity score analysis, the overall and disease-free survival were similar and for the secondary outcomes, the laparoscopic group had shorter hospital stay, lower morbidity, with fewer transient liver failure and wound complications, and a larger tumor margin [34].

Multiple meta-analyses and case control series were reviewed and analyzed at the second international conference for laparoscopic liver resection in Morioka in 2014. Minor resections were validated as standard practice in the assessment stage, while major or complex resections were considered to be in the exploration stage, with incompletely defined risks. The Jury at Morioka made strong recommendations for higher quality studies including registries to define the role and benefits of laparoscopic major hepatectomy.

Patient selection is critical to ensuring safe laparoscopic partial hepatectomy. Although is technically feasible, resection of lesions in right posterior sections or the hepatic dome can be challenging and should be approached with caution. The patient is placed in the supine position and securely fastened to the table to allow for safe intraoperative repositioning. Generally, five ports are required for laparoscopic resection including two 12 mm and three 5 mm ports. Port placement is dependent upon laterality of the lesion as shown in **Figure 3**. Some surgeons advocate using a hand access port to assist with intraoperative manipulation, intra-corporeal suturing as well as serve as the specimen removal site.

Several large case series have been published demonstrating the success of robotic liver resection [36, 37]. The first large case series of 70 patients included 38.5% major liver resections without any mortalities [36]. An early systematic review of the literature demonstrated safety and feasibility of the robotic technique, with conversion to open rate of 4.6% and complication rate of 20.3% [38]. In 2018, an international, multicenter retrospective review of robotic liver surgery was published specifically evaluating long-term oncologic outcomes in patients with primary hepatobiliary malignancies after a median follow up of 75 months [39]. This study demonstrated comparable outcomes between robotic, open and laparoscopic liver surgery with 3-year overall survival of 90% for HCC. The majority of the cases were non-anatomic resections with an R0 resection achieved in 95% of HCC resections, 68% in cholangiocarci-

**Figure 3.** Suggested port placements for laparoscopic left lateral sectionectomy (a) and hand-assisted laparoscopic right hepatectomy (b). Source: Cho, Fong. Hepatic Resection. In: Ashley SW, editor. Scientific American Surgery. Hamilton:

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Minimally invasive approach to liver surgery, both laparoscopic and robotic-assisted, have their share of limitations. An important potential complication associated with the establishment of pneumoperitoneum and laparoscopic liver surgery is carbon dioxide gas embolism. Reports have demonstrated that this event rate is low, particularly if the pneumoperitoneal pressure is maintained below 12 mmHg [40]. Studies have published and event rate of as low as at 0.5~1.5% [41]. There is a learning curve with gaining proficiency in the laparoscopic technique of liver resection with expert centers estimating the learning curve for laparoscopic liver resection at approximately 45~70 cases with senior partner proctoring [42]. Other limitations include the need for a skilled bedside assistant, and the diminished tactile sense when dealing with friable tissue such as steatotic liver parenchyma or thin venules within a cirrhotic liver can make the case challenging. And in the rare event when massive venous bleeding ensues, it can be difficult to control. Cost is one major barrier to the wide adoption of the robotic approach. There is a significant initial capital investment in addition to maintenance fees and costs of staff training. However, one

noma and 82% in gallbladder cancer.

Decker. 7th ed; 2014. pp. 1094–1114.

#### **5.2. Robotic-assisted partial hepatectomy**

Further advances in surgical technology has created new opportunities in minimally invasive liver surgery. Robotic surgical systems offer unique advantages to the liver surgeon that enhances the minimally invasive approach. There are several key improvements on the robotic surgical system including a camera with optics providing a 3-dimensional stereotactic visual field. In addition, the instruments allow for seven degrees of freedom in their motion, providing easier suturing for hemorrhage control. There is no fulcrum effect on the body wall of the patient as in laparoscopic surgery, and it has been associated with reduction in surgeon fatigue compared to the laparoscopic approach.

Similar to laparoscopic partial hepatectomy, the patient is placed in the supine position and in steep reverse Trendelenburg position. The table is tilted with right side up approximately 25 degrees for right-sided resections. Five ports are placed including four robot-controlled ports and one assistant port (**Figure 4**). The ports are placed based on the laterality of the resection. In general, for a right-sided hepatectomy, the camera port is placed to the right-side of midline. Once the ports have been placed, the robot is docked from the cephalad position (**Figure 5**). Intraoperative ultrasound is critical to establishing vascular anatomy and defining oncologic planes of resection. After vascular control and establishing the line of transection, parenchymal transection is performed using one of many published techniques [35].

and it demonstrated lower postoperative morbidity and shorter length of stay compared

Specific to the treatment of HCC, the safety and efficacy of the laparoscopic approach has been evaluated in several meta-analyses and propensity score analyses. These studies demonstrated the equivalent or superior perioperative outcomes of laparoscopic compared to open resection [32, 33]. In a propensity score analysis, the overall and disease-free survival were similar and for the secondary outcomes, the laparoscopic group had shorter hospital stay, lower morbidity, with fewer transient liver failure and wound complications, and a larger

Multiple meta-analyses and case control series were reviewed and analyzed at the second international conference for laparoscopic liver resection in Morioka in 2014. Minor resections were validated as standard practice in the assessment stage, while major or complex resections were considered to be in the exploration stage, with incompletely defined risks. The Jury at Morioka made strong recommendations for higher quality studies including registries to

Patient selection is critical to ensuring safe laparoscopic partial hepatectomy. Although is technically feasible, resection of lesions in right posterior sections or the hepatic dome can be challenging and should be approached with caution. The patient is placed in the supine position and securely fastened to the table to allow for safe intraoperative repositioning. Generally, five ports are required for laparoscopic resection including two 12 mm and three 5 mm ports. Port placement is dependent upon laterality of the lesion as shown in **Figure 3**. Some surgeons advocate using a hand access port to assist with intraoperative manipulation,

Further advances in surgical technology has created new opportunities in minimally invasive liver surgery. Robotic surgical systems offer unique advantages to the liver surgeon that enhances the minimally invasive approach. There are several key improvements on the robotic surgical system including a camera with optics providing a 3-dimensional stereotactic visual field. In addition, the instruments allow for seven degrees of freedom in their motion, providing easier suturing for hemorrhage control. There is no fulcrum effect on the body wall of the patient as in laparoscopic surgery, and it has been associated with reduction in surgeon

Similar to laparoscopic partial hepatectomy, the patient is placed in the supine position and in steep reverse Trendelenburg position. The table is tilted with right side up approximately 25 degrees for right-sided resections. Five ports are placed including four robot-controlled ports and one assistant port (**Figure 4**). The ports are placed based on the laterality of the resection. In general, for a right-sided hepatectomy, the camera port is placed to the right-side of midline. Once the ports have been placed, the robot is docked from the cephalad position (**Figure 5**). Intraoperative ultrasound is critical to establishing vascular anatomy and defining oncologic planes of resection. After vascular control and establishing the line of transection,

parenchymal transection is performed using one of many published techniques [35].

with patients undergoing open liver resection [31].

define the role and benefits of laparoscopic major hepatectomy.

intra-corporeal suturing as well as serve as the specimen removal site.

**5.2. Robotic-assisted partial hepatectomy**

fatigue compared to the laparoscopic approach.

tumor margin [34].

66 Liver Cancer

**Figure 3.** Suggested port placements for laparoscopic left lateral sectionectomy (a) and hand-assisted laparoscopic right hepatectomy (b). Source: Cho, Fong. Hepatic Resection. In: Ashley SW, editor. Scientific American Surgery. Hamilton: Decker. 7th ed; 2014. pp. 1094–1114.

Several large case series have been published demonstrating the success of robotic liver resection [36, 37]. The first large case series of 70 patients included 38.5% major liver resections without any mortalities [36]. An early systematic review of the literature demonstrated safety and feasibility of the robotic technique, with conversion to open rate of 4.6% and complication rate of 20.3% [38]. In 2018, an international, multicenter retrospective review of robotic liver surgery was published specifically evaluating long-term oncologic outcomes in patients with primary hepatobiliary malignancies after a median follow up of 75 months [39]. This study demonstrated comparable outcomes between robotic, open and laparoscopic liver surgery with 3-year overall survival of 90% for HCC. The majority of the cases were non-anatomic resections with an R0 resection achieved in 95% of HCC resections, 68% in cholangiocarcinoma and 82% in gallbladder cancer.

Minimally invasive approach to liver surgery, both laparoscopic and robotic-assisted, have their share of limitations. An important potential complication associated with the establishment of pneumoperitoneum and laparoscopic liver surgery is carbon dioxide gas embolism. Reports have demonstrated that this event rate is low, particularly if the pneumoperitoneal pressure is maintained below 12 mmHg [40]. Studies have published and event rate of as low as at 0.5~1.5% [41]. There is a learning curve with gaining proficiency in the laparoscopic technique of liver resection with expert centers estimating the learning curve for laparoscopic liver resection at approximately 45~70 cases with senior partner proctoring [42]. Other limitations include the need for a skilled bedside assistant, and the diminished tactile sense when dealing with friable tissue such as steatotic liver parenchyma or thin venules within a cirrhotic liver can make the case challenging. And in the rare event when massive venous bleeding ensues, it can be difficult to control.

Cost is one major barrier to the wide adoption of the robotic approach. There is a significant initial capital investment in addition to maintenance fees and costs of staff training. However, one

**6. Postoperative complications**

supplementation is also advocated.

**7. Emerging technologies**

applications are utilized to reduce liver surface related bleeding.

liver can occur in up to 8% of patients after liver resection [45].

**7.1. Near-infrared fluorescent imaging in hepatic surgery**

The main postoperative complications include postoperative hemorrhage, liver dysfunction, biliary leak and fluid collections. Postoperative hemorrhage is uncommon after liver resection if meticulous attention is given to confirmation of hemostasis at the conclusion of the case. Bleeding may occasionally occur from retroperitoneal structures, such as the adrenal gland, or diaphragmatic musculature. Argon beam coagulator and a variety of topical hemostatic

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Post hepatectomy liver failure (PHLF) is a major postoperative complication with mortality of approximately 30%. The definition of post-hepatectomy liver is the impaired ability of the liver to maintain its synthetic, excretory and detoxifying functions, characterized by an increase in international normalized ratio and bilirubin on or after postoperative day 5 [44]. The most effective treatment of PHLF is liver transplantation but that is reserved for the most severe cases. Initial care is supportive and often includes mechanical ventilation, hemodynamic support and hemodialysis. Administration of colloid products and nutritional

The best way to treat post-hepatectomy liver failure is to prevent it. Preoperative weight loss, nutritional supplementation, careful preoperative selection and risk stratification are important to minimize the risk of PHLF [10]. Intra-operatively, minimizing blood loss and blood transfusion, close attention to hemostasis and minimizing skeletonization of the hepatoduodenal ligament will lower risk of PHLF. In the postoperative period, recognizing and aggressively treating postoperative hemorrhage, biliary obstructions or leaks and intra-abdominal

Postoperative fluid collections collect in the resected liver bed. These collections are varied in etiology but can include hematoma, seroma or biloma. They often to not result in symptoms, but occasionally they can cause pain or fullness requiring drainage. These collections also are at risk for infection and abscess formation. Biliary leakage from the raw surface of the resected

New technologies continue to be developed to enhance minimally invasive liver surgery. One example is intra-operative near-infrared fluorescence (NIF) imaging. NIF imaging has become commonplace in many laparoscopic and robotic camera systems enabling the identification of various dyes, such as indocyanine green, injected preoperatively. Indocyanine green is a green dye that is preferentially metabolized by hepatocytes and excreted in the biliary tree. It lights up the biliary tree and has been utilized for robotic and laparoscopic assisted cholecystectomy. It has been more recently utilized to guide parenchymal dissection after vascular

control by identifying perfused from poorly perfused hepatic parenchyma.

infections will reduce the hepatic stress and likelihood of developing hepatic failure.

**Figure 4.** Image of port placement for a robot-assisted surgeries left lateral sectionectomy. Blue dots denote da Vinci 8-mm reusable cannulas (3). Green dot denotes 12-mm camera port. Purple dot denotes AirSeal® assistant port. Costal margin and midline marked in dotted pen.

**Figure 5.** Standard operating room set up for robotic-assisted liver surgery. Head of bed is on left side of image, anesthesia equipment and personnel on right side of image.

study demonstrated that while perioperative costs are higher with the robot, the overall total direct hospital costs are lower at least in part due to the decrease length of stay with robotic minimally invasive resection [43]. There are several generations of the robot with older generation units best suited for an operation in a single work field, with cumbersome redocking steps to perform multi-quadrant operations. The majority of studies indicate a longer operating time secondary to robot set up and draping. Technically speaking, the robot does not provide haptic feedback challenging the surgeon to "feel with their eyes" and occasionally resulting in excessive tissue damage in inexperienced hands. Further studies are needed to examine the comparative effectiveness of robotic versus laparoscopic minimally invasive hepatectomy.
