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ABSTRACT

Minimally invasive liver surgery has continued to evolve over the past few decades since its introduction in the 1990s. Although laparoscopic liver surgery is becoming the standard of care, particularly for favorable minor liver resection, its feasibility in advanced and complexed cases is still limited and it is mostly performed in a few high volume liver centers. The advent of robotic surgery, albeit still in the early phases, has enhanced the capability of surgeons to operate on more complex cases in a minimally invasive manner. Equipped with advantageous instruments (a stable camera offering a 3-dimensional view, wristed instruments, no tremors, and improved ergonomics), robotic surgery allows surgeons to perform major hepatectomies, operate on posteriorly-located tumors (segments 7 and 8), perform liver surgery requiring complex biliary reconstructions, and even perform donor hepatectomies. More importantly, the surgical outcomes of robotic surgery do not compromise the patient's safety, with comparable outcomes or even better outcomes than a laparoscopic approach. Several studies have reported better performance of robotic surgery in terms of perioperative outcomes such as less blood loss, fewer complications, and decreased length of hospital stay compared to laparoscopic surgery. Emergence of new robotic systems in the market will likely decrease the high costs of robotic surgery, which will further expand the population who will benefit from minimally invasive surgery. However, further randomized and multicenter trials need to be undertaken to clearly delineate the advantages of robotic surgery over laparoscopy.

Keywords: Robotic surgery; Liver resection; Surgical outcomes

INTRODUCTION

Since Mouret performed the first laparoscopic cholecystectomy in 1987, there has been a dramatic revolution in the surgical arena [1]. With continued technological advances, laparoscopy is now being utilized for various surgical procedures [2]. Although laparoscopic liver resection has been performed since the 1990s, it is still not yet widely used, unlike laparoscopic gastrointestinal procedures. Nevertheless, continued refinement of surgical techniques and the evolution of surgical instruments has resulted in improvement in the clinical outcomes of minimally invasive surgery, and less complex laparoscopic liver resection was standardized in 2008 in Louisville [3]. This procedure was subsequently updated in 2015

Ann Robot Innov Surg. 2020 Feb;1(1):15-32https://doi.org/10.37007/aris.2020.1.1.15pISSN 2635-6678·eISSN 2635-666X

Review Article

Received: Oct 10, 2019Accepted: Jan 7, 2020

Correspondence toGi Hong ChoiDepartment of Surgery, Yonsei University College of Medicine, Alffred I. Ludlow Faculty Building, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea.E-mail: CHOIGH@yuhs.ac

Copyright © 2020 The Korean Association of Robotic SurgeonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

ORCID iDsJonathan Geograpo Navarro https://orcid.org/0000-0001-5435-2333Seoung Yoon Rho https://orcid.org/0000-0002-1265-826XGi Hong Choi https://orcid.org/0000-0002-1593-3773

Conflict of InterestThe authors have no conflict of interest to declare

Author ContributionsConceptualization: Navarro JG, Choi GH; Data curation: Rho SY; Investigation: Navarro JG; Methodology: Navarro JG, Rho SY, Choi GH; Supervision: Choi GH; Validation: Choi GH; Visualization: Navarro JG, Choi GH; Writing - original draft: Navarro JG; Writing - review & editing: Navarro JG, Choi GH.

Jonathan Geograpo Navarro ,1 Seoung Yoon Rho ,2 Gi Hong Choi 2

1Department of Surgery, Vicente Sotto Memorial Medical Center, Cebu City, Philippines2Department of Surgery, Yonsei University College of Medicine, Seoul, Korea

Robotic Liver Resection

by Marioka [4] to include more complex and difficult procedures. The advantages of this procedure, such as fewer complications, less blood loss, and decreased length of hospital stay relative to laparoscopic surgery are well documented [5]. However, certain caveats are associated with the propagation of laparoscopic liver surgery. One of these is the innate complexity of the procedure itself in terms of hilar dissection and parenchymal transection, which requires more advanced laparoscopic skills [6]. This sophisticated procedure has a steep learning curve and therefore requires a long surgical experience [7,8]. As such, until recently, laparoscopic liver resection was generally performed only in high volume centers by expert surgeons.

The inherent limitations of the surgeon's dexterity in laparoscopic surgery and the resulting technical complexity might potentially be overcome by use of robotic surgical systems. Since the first robotic cholecystectomy was successfully performed in 1997 [9] using the da Vinci® Surgical System, this new technology has gradually gained popularity. Its key advantages compared to laparoscopic surgery include an augmented three-dimensional view, stable camera, greater freedom of motion of surgical instruments, no tremors, and improved ergonomics for the operator [10]. These advantages have been demonstrated in subspecialties such as urologic, gynecologic, and rectal procedures where the application of robotic surgery is widely implemented and standardized [11]. Despite these advantages, however, the high costs of robotic surgery remain one of the reasons for the slow penetration of robotic liver surgery in the surgical arena. In terms of cost-effectiveness, its superiority compared to laparoscopic surgery remains unjustified. Although some reports argue that the cost-effectiveness of the robotic system should be evaluated taking into consideration improved perioperative outcomes, including fewer complications and early discharge of patients [12,13], more data is required. Moreover, some scenarios require complex manipulation that are beyond the capabilities of currently available laparoscopic instruments; in this context, robotic endowrist movement is greatly advantageous.

Evidence to support the superiority of robotic liver resection relative to laparoscopic liver resection is lacking. Therefore, the present review focuses on the feasibility and safety of robotic liver resection and presents some unique advantages of robotic surgery over laparoscopic surgery.

APPLICATION OF THE DA ROBOTIC SURGICAL SYSTEM FOR PRECISE LIVER RESECTIONMinimally invasive liver surgery remains one of the most challenging procedures to perform because of the complex anatomy of the liver, which is a highly vascular organ. However, advancements in preoperative imaging modalities have facilitated better delineation of vascular anatomy, and this together with refinement of surgical laparoscopic instruments and energy devices and continued improvements in perioperative management have made liver surgery safe to perform [3,14]. Since the International Consensus Conference (ICC) held in Louisville in 2008, the growth of laparoscopic liver resection has increased exponentially worldwide, especially among high volume centers in Europe and the United States [15-17]. In line with the second ICC in Marioka, laparoscopic liver resection is continually expanding to encompass a higher degree of complexity, such as superior-posterior segment surgery [18]. Despite this, only 32% of liver resections were performed laparoscopically according to an international survey in which 27 centers worldwide participated; of these liver resections,

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Robotic Liver Surgery

74% were minor operations [19]. Thus, from a technical point of view, laparoscopic liver resection, particularly major resection, remains a challenging procedure that requires a highly trained and experienced surgeon.

Robotic surgical systems may theoretically be superior to a laparoscopic approach because of the following unique features of robotic systems: 1) a 3-dimensional (3D) view with a stable camera, 2) wristed instruments with no tremors, and 3) improved ergonomics. These key features can potentially allow the surgeon to perform more precise and complex operations [20,21]. Giulianotti et al. [22] demonstrated the key advantages of the da Vinci® Surgical System during hilar and hepatocaval dissection for liver resection. Hilar dissection is facilitated by a stable, magnified, high-quality 3D camera view and fine endowrist movement of the instruments. As such, a robotic surgical system can clearly identify, isolate, and safely handle hilar vascular structures, which require fine and delicate dissection. Choi et al. [23] emphasized that caudate branches from the portal vein can be meticulously isolated and suture ligated using a robotic surgical system; these procedures are difficult to perform laparoscopically. Tsung et al. [24] also demonstrated excellent and safe inflow control with a robotic surgical system. They noted that the greater degrees of freedom and magnified 3D view greatly facilitated safe portal vein dissection and allow for portal vein control with suture ligation. Importantly, the robotic surgical system has shown outstanding performance during hilar dissection in living donor right hepatectomy. Aside from individual isolation and identification of the portal vein and artery, closure of the hepatic duct stump with a running suture can be easily and safely performed with a robotic surgical system [25,26].

At Severance Hospital, Yonsei University College of Medicine, we have performed 55 cases of robotic living donor right hepatectomy since 2016. Individual isolation of the hilar structures (right portal vein, right hepatic artery, and hepatic duct) can be safely performed using a robotic surgical system. Most importantly, safe transection and closure with a running suture of the bile duct stump is facilitated by the 3D camera view and wristed instruments.

Likewise, the robotic surgical system enhances hepatocaval dissections during right hemihepatectomy. The robotic third arm provides strong and stable traction, creating a steady working space in the hepatocaval area. As a result, short hepatic veins can be safely suture ligated even within this limited space [22,23,26].

In terms of parenchymal transection, the robotic surgical system we use has hand tremor filtration and motion scaling capacity that allows for optimal energy delivery from the robotic instruments to the tissue and fine dissection of liver parenchyma. An unarticulated harmonic device is usually used to transect the liver parenchyma [27-33]. Some centers utilize an endowrist robotic vessel sealer during parenchymal transection [33,34]. They activate the instrument while the jaws are in the open position and gradually close the jaws as parenchymal coagulation advances [34].

CURRENT STATUS OF ROBOTIC LIVER RESECTION

The number of published articles about robotic liver resection has been increasingly since 2009 as shown in Fig. 1. Published articles, excluding case series of fewer than three patients that have been published since 2009, are listed in Table 1 [13,20,21,24,26,27,29,32,33,35-62]. This trend suggests increasing application of robotic systems for liver surgery. Currently,

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Robotic Liver Surgery

robotic liver resection is commonly performed in Asia (44.2%), followed by the United States (31.3%) and Europe (24.5%) (Fig. 2).

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Robotic Liver Surgery

0

300

400

250

350

50

100

150

200

1 7

2009

1 9

2010

3

101

2011

1 13

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4

147

2013

3

49

2014

5

127

2015

5

185

2016

6

363

2017

4

275

2018

4

174

2019

No. of studiesNo. of patients

Fig. 1. Number of published robotic liver resection studies.

Table 1. Clinical studies of robotic liver resection since 2009Reference Year Robotic surgery center No. of patientsChen et al. [35] 2017 Taipei, Taiwan 183Zhu et al. [36] 2019 Tonji, China 140Sucandy et al. [37] 2019 Tampa, USA 80Sham et al. [13] 2016 Seattle, USA 71Giulianotti et al. [38] 2011 Chicago, USA 70Lee et al. [33] 2015 Hong Kong, China 70Choi et al. [39] 2017 Seoul, Korea 69Kingham et al. [32] 2016 New York, USA 64Lim et al. [40] 2019 Cretel/Pisa, France/Italy 61Tsung et al. [24] 2014 Pittsburgh, USA 57Fruscione et al. [41] 2018 Charlotte, USA 57Lai et al. [42] 2013 Hong Kong, China 42Goh et al. [20] 2019 Singapore, Singapore 43Troisi et al. [21] 2013 Spoleto, Italy 40Efanov et al. [43] 2017 Moscow, Russia 40O'Connor et al. [44] 2017 Los Angeles, USA 39Marino et al. [45] 2018 Palermo, Italy 35Chan et al. [46] 2011 Hong Kong, China 27Spampinato et al. [47] 2014 Four Italian centers 25Magistri et al. [48] 2017 Modena, Italy 22Quijano et al. [29] 2016 Madrid, Spain 21Felli et al. [49] 2015 Rome, Italy 20Guadagni et al. [50] 2019 Pisa, Italy 20Morel et al. [27] 2015 Geneva, Switzerland 16Nota et al. [51] 2016 Utrecht, Netherlands 16Ji et al. [52] 2012 Beijing, China 13Yu et al. [53] 2014 Seoul, Korea 13Chen et al. [26] 2016 Taipei, Taiwan 13Lee et al. [54] 2019 Seoul, Korea 13Boggi et al. [55] 2015 Pisa, Italy 12Buchs et al. [56] 2014 Geneva, Switzerland 11Goja et al. [57] 2017 Delhi, India 10Berber et al. [58] 2010 Cleveland, USA 9Croner et al. [59] 2015 Erlangen, Germany 9Kandil et al. [60] 2013 New Orleans, USA 7Vasile et al. [61] 2009 Bucharest, Rumania 7Wakabayashi et al. [62] 2011 Morioka, Japan 4Total studies (n=37) Centers (n=41) 1,450

Table 2 [13,20,21,24,26,27,29,32,33,35-62] presents the demographic profile of the 1,450 (range, 4–183) patients from the combined population of included studies. Age range was from 4 to 91 years old with an almost equal ratio of males and females (1.4: 1). Majority of the cases were malignant tumors (74.9%), comprising hepatocellular carcinoma (n=591, 40.1%) and colorectal metastases (n=292, 20.1%). With regard to the extent of liver resection, major resections were performed in 33% of cases (Table 3), followed by wedge resection (18.3%) and segmentectomy (18.0%). Interestingly, there was an almost equal number cases of left hepatectomies (15.6%) and left lateral sectionectomies (15.3%). Right hepatectomy and bisegmentectomy comprised 11.7% and 10.9% of cases, respectively. This result is incongruent with the report by Nguyen et al. [14] of 2,804 cases of laparoscopic liver resection, where major hepatectomy comprised only 17% of the whole population. As such, although robotic liver resection is still in the early stages, more extensive and complex procedures are already being performed.

PERIOPERATIVE OUTCOMES OF ROBOTIC LIVER RESECTIONRobotic liver resection had acceptable perioperative outcomes (Table 4) [13,20,21,24,26,27,29,32,33,35-62]. Although it is difficult to determine the exact operative time and blood loss among the studies due to heterogeneity in the type and extent of resections, the overall average operative time and average blood loss of the combined 37 studies was 280 minutes (range, 56–1,186 minutes) and 244 mL (range, 0–4,500 mL), respectively. Blood transfusion was required in 92 patients (6.2%). Average length of hospital stay was 6.45 days (1–48 days). However, it should be emphasized that operative time and blood loss improve as surgeon accumulate more experience [43]. Chen et al. [63] based on their experience with 92 cases of major robotic hepatectomy reported that operative time,

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Robotic Liver Surgery

USASucandy et al. [37]

Kingham et al. [32]Tsung et al. [24]Fruscione et al. [41]O'Connor et al. [44]Berber et al. [58]Kandil et al. [60]

Sham et al. [13]Giulianotti et al. [38]

80

6457573997

7170

EuropeLim et al. [40]

Marino et al. [45]Spampinato et al. [47]Magistri et al. [48]Quijano et al. [29]Felli et al. [49]Guadagni et al. [50]Nota et al. [51]Morel et al. [27]Boggi et al. [55]Buchs et al. [56]Croner et al. [59]Vasile et al. [61]

Troisi et al. [21]Efanov et al. [43]

61

35252221

20201616121197

4040

AsiaChen et al. [35]

Choi et al. [39]Goh et al. [20]Lai et al. [42]Chan et al. [46]Chen et al. [26]Yu et al. [53]Lee et al. [54]Ji et al. [52]Goja et al. [57]Wakabayashi et al. [62]

Zhu et al. [36]Lee et al. [33]

183

6943432713131313104

14070Europe

15 studies, 355 patients

Asia13 studies, 641 patients

USA9 studies, 454 patients

Fig. 2. Geographical distribution of robotic liver resection.

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Table 2. Demographic profile of the 1,450 patientsReference Year No. Age (yr) Male/Female Malignant Major resectionChen et al. [35] 2017 183 60.8 (22–89) 118/65 123 (67.2) 92 (50.3)Zhu et al. [36] 2018 140 49 (4–74) 91/49 104 (74.3) 17 (12.1)Sucandy et al. [37] 2019 80 63 (62.4±14.1) 32/48 59 (73.7) 37 (46.3)Sham et al. [13] 2016 71 54.8±14.7 35/36 60 (84.5) 17 (23.9)Lee et al. [33] 2015 70 58 (20–82) 46/24 52 (74.3) 14 (20.0)Giulianotti et al. [38] 2011 70 57 (21–84) 30/40 42 (60.0) 27 (38.6)Choi et al. [39] 2017 69 53 (18–89) 44/25 53 (76.8) 54 (78.3)Kingham et al. [32] 2016 64 64 (40–91) 32/32 57 (89.1) 10 (15.6)Lim et al. [40] 2019 61 66±10 41/20 61 (100.0) 9 (14.8)Tsung et al. [24] 2013 57 58.4±14.6 24/33 38 (66.7) 21 (36.8)Fruscione et al. [41] 2018 57 58.1±15.7 20/37 42 (73.7) 40 (70.2)Lai et al. [42] 2013 43 61.4±10.9 31/10 43 (100.0) 10 (23.3)Goh et al. [20] 2018 43 66 (38–78) 27/16 32 (74.4) 7 (16.3)Troisi et al. [21] 2013 40 64.6±12.1 27/13 28 (70.0) 0Efanov et al. [43] 2017 40 45 (18–76) 31/9 11 (27.5) 7 (17.5)O'Connor et al. [44] 2017 39 63 (31–83) 26/13 31 (79.5) 0Marino et al. [45] 2018 35 63.8 (42–77) 22/13 35 (100.0) 35 (100.0)Chan et al. [46] 2011 27 61 (37–85) 16/11 21 (77.8) 1 (3.7)Spampinato et al. [47] 2014 25 63 (32–80) 13/12 17 (68.0) 25 (100.0)Magistri et al. [48] 2017 22 60.88±9.85 18/4 22 (100.0) 2 (9.1)Quijano et al. [29] 2016 21 59.3 (41–69) 9/12 13 (61.9) 10 (47.6)Guadagni et al. [50] 2019 20 66.1±11.8 13/7 20 (100.0) 0Felli et al. [49] 2015 20 64.6 (47–81) 8/12 17 (85.0) 6 (30.0)Morel et al. [27] 2015 16 60.37±15.6 7/9 11 (68.7) 0Nota et al. [51] 2016 16 69 (34–75) 9/7 14 (87.5) 0Yu et al. [53] 2014 13 50±12.2 7/6 10 (76.9) 3 (23.1)Lee et al. [54] 2019 13 62.2±9.8 7/6 11 (84.6) 8 (61.8)Ji et al. [52] 2012 13 53 (39–79) 9/4 8 (61.5) 9 (69.2)Chen et al. [26] 2016 13 NA 4/9 0 13 (100.0)Boggi et al. [55] 2015 12 61.1 (30–70) 4/8 NA 0Buchs et al. [56] 2014 11 61.3±15.2 6/5 7 (63.6) 0Goja et al. [57] 2017 10 47.1 (15–72) 6/4 3 (30.0) 3 (30.0)Croner et al. [59] 2015 9 64 (45–75) NA 9 (100.0) 0Berber et al. [58] 2010 9 66.6±6.4 7/2 9 (100.0) 0Vasile et al. [61] 2009 7 NA NA NA 0Kandil et al. [60] 2013 7 44.6 (21–68) 5/2 4 (57.1) 1 (14.3)Wakabayashi et al. [62] 2011 4 NA NA 3 (75.0) 0Overall 1,450 4–91 825/603 1,070/1,428 (74.9) 478/1,450 (33.0)Values are presented as median (range or mean±standard deviation), mean±standard deviation, or number of patients (%).NA, not available.

Table 3. Types of robotic liver resection (n=1,434)Type of resection ValuesMinor hepatectomy 964 (67.2)

Wedge resection/sub-segmentectomy 263 (18.3)Segmentectomy 258 (18.0)Left lateral sectionectomy 219 (15.3)Bisegmentectomy 156 (10.9)Mixed segments 10 (0.7)Pericystectomy 6 (0.4)

Major hepatectomy 470 (32.8)Left hepatectomy 223 (15.6)Right hepatectomy 168 (11.7)Left trisectionectomy 9 (0.6)Right trisectionectomy 12 (0.8)Three segmentectomy 49 (3.4)

Values are presented as number of patients (%).

blood loss, and length of hospital stay improved significantly improved after 15, 25, and 15 cases, respectively. Choi et al. [39] reported that among 19 cases of robotic left hepatectomy, operative time and blood loss decreased significantly after 10 cases. Although operative time was longer, perioperative outcomes of robotic liver resection including blood loss, complication rates, and length of hospital stay were comparable or even significantly better than those of open liver resection [13,32,64]. As a result, this approach is a reasonable alternative option as long as the surgeon has sufficient experience and expertise.

Overall surgical morbidity was 17.8% (range, 0%–68%). Table 5 presents the associated complications of the 1,450 patients. Bile leakage was the most common liver resection-related complication (2.1%), followed by intraabdominal fluid collection (0.76%) and postoperative bleeding (0.50%). These results are comparable to those reported for 2,804 cases of laparoscopic liver resection by Nguyen and colleagues [14].

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Table 4. Perioperative outcomes of 1,450 patients who underwent robotic liver resectionReference Year No. Operative time (min) Blood loss (mL) Transfusion Conversion Morbidity LOS (days)Chen et al. [35] 2017 183 361 (102–805) 249 (50–2,250) 10 (5.5) 3 (1.6) 8 (4.4) 7.5 (2–41)Zhu et al. [36] 2018 140 193 (60–560) 300 (10–2,000) 10 (7.1) 25 (17.9) 37 (26.4) 6 (3–48)Sucandy et al. [37] 2019 80 233 (267.2±109.6) 150 (265.7±319.9) 5 (6.3) 1 (1.3) 11 (13.8) 3 (5.0±4.6)Sham et al. [13] 2016 71 284±122 495±600 7 (10.0) 4 (5.7) 11 (15.7) 3.9±2.3Lee et al. [33] 2015 70 251.5 (97–620) 100 (2–2,500) 3 (4.3) 4 (5.7) 8 (11.4) 5Giulianotti et al. [38] 2011 70 270 (90–660) 262 (20–2,000) 15 (21.4) 4 (5.7) 15 (21.4) 7 (2–26)Choi et al. [39] 2017 69 491 (135–1,186) 170 (20–1,610) 6 (8.7) 6 (9.1) 7 (10.6) 8 (5–46)Kingham et al. [32] 2016 64 163 (56–480) 100 (10–1,700) 1 (1.6) 4 (6.3) 28 (43.7) NALim et al. [40] 2019 61 277±156 NA 6 (9.8) 0 15 (24.6) 9±12Tsung et al. [24] 2013 57 253 (180–355) 200 (50–338) 2 (3.8) 4 (7.0) 11 (19.3) 4 (3–6)Fruscione et al. [41] 2018 57 194 (152–255) 250 (125–600) NA NA 16 (28.1) 4 (3–5)Lai et al. [42] 2013 43 229.4±82.8 412.6 (10–3,500) 3 (7.0) 3 (7.0) 3 (7.0) 6.2±3.6Goh et al. [20] 2018 43 360 (75–825) 300 (25–4,500) 2 (4.6) 1 (2.3) 8 (18.6) 4 (2–33)Troisi et al. [21] 2013 40 271±100 330±303 NA 8 (20.0) 5 (12.5) 6.1±2.6Efanov et al. [43] 2017 40 407 (85–980) 465 (0–2,000) 3 (7.5) 2 (5.0) 8 (20.0) 11 (6–30)O'Connor et al. [44] 2017 39 216 (80–300) 298 (5–1,650) NA 3 (7.7) 7 (17.9) 3 (1–9)Marino et al. [45] 2018 35 315 (200–445) 245 (125–628) 3 (8.5) 2 (5.7) 6 (17.2) 6.5 (5–14)Chan et al. [46] 2011 27 200 (90–307) 50 (5–1,000) NA 1 (3.7) 2 (7.0) 5.5 (3–11)Spampinato et al. [47] 2014 25 430 250 11 (44.0) 1 (4.0) 5 (20.0) 8 (4–22)Magistri et al. [48] 2017 22 318±113.5 400 (50–1,500) NA 0 15 (68.2) 5.1±2.4Quijano et al. [29] 2016 21 262 NA NA 1 (4.8) 4 (19.0) 12Guadagni et al. [50] 2019 20 198.5±98 250 (200–300) 2 (10.0) 0 5 (25.0) 4.7±1.8Felli et al. [49] 2015 20 141.5 (99–197) 50 (0–200) 1 (5.0) 0 0 5.7Morel et al. [27] 2015 16 352±163 NA 1 (6.3) 0 5 (31.2) 7.9±4.8Nota et al. [51] 2016 16 146 (60–265) 150 (5–600) NA 1 (6.3) 7 (43.8) 4 (1–8)Yu et al. [53] 2014 13 292±85 389 0 0 0 8Lee et al. [54] 2019 13 204±33 320±331 0 0 1 (7.7) 7±2.4Ji et al. [52] 2012 13 338 (150–720) 280 0 0 1 (7.8) 6.7Chen et al. [26] 2016 13 596 (353–753) 169 (50–500) 0 0 1 (7.6) 7 (6–8)Boggi et al. [55] 2015 12 260.4 (115–430) 252.7 (50–600) 3 (25.0) 1 (8.3) 4 (33.3) 8.5Buchs et al. [56] 2014 11 329±136.3 200 (50–1,500) 1 (9.1) 0 3 (27.3) 9.3±4.9Goja et al. [57] 2017 10 510 (370–660) NA 1 (10.0) 0 NA 8 (4–28)Croner et al. [59] 2015 9 312 (115–458) 251 NA 0 1 (11.1) 6Berber et al. [58] 2010 9 258.5±27.9 136±61 NA 1 (11.1) 1 (11.1) NAVasile et al. [61] 2009 7 137 (120–180) NA NA 0 0 11 (4–19)Kandil et al. [60] 2013 7 61.4±26.7 100 (10–200) NA 0 0 2 (1–5)Wakabayashi et al. [62] 2011 4 272 (160–370) NA 0 0 0 NAOverall 1,450 280.7 (56–1,186) 244.3 (0–4,500) 92/1,450 (6.2) 80/1,450 (5.8) 259/1,450 (17.8) 6.49 (1–48)Values are presented as median (range or mean±standard deviation), mean±standard deviation, or number of patients (%).LOS, length of hospital stay; NA, not available.

The overall conversion rate was 5.8% (range, 0%–17.9%). The most common cause for conversion was bleeding during parenchymal transection (2.4%), followed by oncologic problems such as inadequate margin or tumor rupture (1.17%) and difficulty in liver mobilization (0.06%) (Table 6). Compared to open resection, Nguyen et al. [14] reported that the conversion rate for laparoscopic liver resection among 2,804 patients was only 4.1% with bleeding the most common reason for conversion. Although the result is comparable to that for robotic resection, 33% of cases in our review underwent major liver resection compared to only 16% of cases that underwent major laparoscopic resection in Nguyen et al.'s study [14]. Although this is not solid evidence, it does suggest that robotic surgical systems have

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Table 5. Complications after robotic liver resection among the 1,450 patientsVariables ValuesGeneral complications 191

Pleural effusion/pneumonia/atelectasis 10/19/1Wound infection/incisional hernia 8/4Diarrhea/ileus/colon anastomotic leak 3/3/2Bowel injury 1Deep venous/pulmonary thrombosis 4/3Recurrent pyogenic cholangitis 8Abdominal wall hematoma 1Transient ischemic cerebral attack 2Fever 1Hepatitis B virus reactivation 1Postoperative anemia 2Volume overload 1Bladder injury/retention/UTI 2/3/1Ileus 2Cardiac problem 4Sepsis 1Skin rash 1Enterocutaneous fistula 1Not available 102

Liver resection-related 68Transient liver failure 3Postoperative bleeding 7Bile leakage or biloma 30Bile stricture 1Ascites 10Intra-abdominal fluid/collection/abscess 11/5Parenchymal congestion/ischemia 1

UTI, urinary tract infection.

Table 6. Reasons for conversion (n=84)Variables ValuesTo open laparotomy 82/84 (97.6)

Oncologic problems (margin or rupture) 17 (20.7)Bleeding during parenchymal transection 36 (43.9)Difficulty in approaching the hilum 5 (6.1)Difficulty in mobilization 9 (11.0)Malignant hyperthermia 1 (1.2)Bile duct injury 1 (1.2)Poor exposure 2 (2.4)Intolerance of pneumoperitoneum 1 (1.2)Not available 10 (12.2)

To hand-port laparoscopic surgery 2/84 (2.4)Bleeding during parenchymal transection 2 (100.0)

Total 84/1,450 (5.8)Values are presented as number of patients (%).

inherent advantages (articulated instruments and a 3D view) that facilitate more complex resections. Nonetheless, it should be emphasized that conversion should never be equated with failure, rather wise intraoperative judgment to prioritize a patient's safety.

ONCOLOGIC OUTCOMES

Among 1,450 patients, malignant lesions were noted in 883 patients (60.1%), including 591 cases of hepatocellular carcinoma and 292 cases of colorectal metastasis. R0 resection was achieved in 84%–100% of cases (Table 7) [13,20,21,24,26,27,29,32,33,35-60,62]. In terms of long-term survival, Chen et al. [26] reported that overall survival (OS) and disease-free survival (DFS) rates for robotic surgery were comparable to those obtained using an open liver open approach. In their study, 81 patients with hepatocellular carcinoma who underwent robotic resection were compared with 81 open hepatectomy cases after propensity score-matching. The 1-, 2-, and 3-year DFS rates for robotic surgery were 91.5%, 84.3%, and 72.2%,

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Table 7. Clinical diagnosis and pathologic outcomes of the 1,405 patientsReference Year Type of tumor (No.) R0 resection (%)

HCC CRM OtherChen et al. [35] 2017 112 4 67 100Zhu et al. [36] 2018 79 8 17 78 (98.7)Lim et al. [40] 2019 42 15 4 54 (89)Lai et al. [42] 2013 41 0 0 93Lee et al. [33] 2015 40 8 22 NAChoi et al. [39] 2017 36 12 5 NAO'Connor et al. [44] 2017 27 4 0 35 (90)Sham et al. [13] 2016 22 24 24 NASucandy et al. [37] 2019 22 21 16 NAMagistri et al. [48] 2017 22 0 0 21 (95.5)Goh et al. [20] 2018 19 11 2 NAMarino et al. [45] 2018 14 18 3 33 (94.3)Giulianotti et al. [38] 2011 13 16 13 100Chan et al. [46] 2011 13 7 1 NAKingham et al. [32] 2016 12 NA NA 98.4Yu et al. [53] 2014 10 0 0 NAMorel et al. [27] 2016 8 3 0 16 (100)Tsung et al. [24] 2013 7 21 10 95Boggi et al. [55] 2015 7 2 3 100Felli et al. [49] 2015 6 7 7 84Ji et al. [52] 2012 6 0 2 100Buchs et al. [56] 2014 6 1 0 100Lee et al. [54] 2019 5 3 3 NACroner et al. [59] 2015 4 4 1 100Fruscione [41] 2018 4 24 14 34 (91.9)Troisi et al. [21] 2013 3 24 3 92.5Berber et al. [58] 2010 3 4 2 100Wakabayashi et al. [62] 2011 3 0 0 NASpampinato et al. [47] 2014 2 11 4 100Nota et al. [51] 2016 1 12 3 87.5Goja et al. [57] 2017 1 0 9 100Kandil et al. [60] 2013 1 1 2 NAQuijano et al. [29] 2016 0 7 14 100Chen et al. [26] 2016 0 0 13 NAGuadagni et al. [50] 2019 0 20 0 NAEfanov et al. [43] 2017 NA NA NA NAOverall 591 292 264 84.0–100HCC, hepatocellular carcinoma; CRM, colorectal metastasis; NA, not available.

respectively, compared to 79.2%, 73.0%, and 58.0%, respectively, for the open approach. The 1-, 2-, and 3-year OS rates for robotic surgery were 100%, 97.8%, and 92.6%, respectively, compared to 98.4%, 93.7%, and 93.7%, respectively, for the open approach. Similarly, Wang et al. [65] compared the OS and DFS of 63 patients with hepatocellular carcinoma (HCC) who underwent robotic surgery compared to 177 patients who underwent open surgery. There was no significant difference in the overall 3-year survival rates of the robotic and open approaches (92.65 vs. 93.7%, P=0.431). Likewise, the 3-year DFS of the robotic group was similar to that of the open group (72.2% vs. 58.0%; P=0.062). As such, although no randomized trial has yet compared robotic and open surgery in terms of long-term oncologic outcomes, the comparable oncologic outcomes relative to standard open surgery affirm the feasibility and safety of a robotic approach for treating hepatocellular carcinoma.

POTENTIAL ADVANTAGES OF ROBOTIC SURGERY

The inherent technological advantages of robotic surgery such as the 3D camera, articulated instruments with 7 degrees of freedom, no fulcrum effect, elimination of tremors, the ability to scale motion, and improved dexterity due to the surgeon's ergonomic position can potentially translate to improved perioperative outcomes, increase the feasibility of performing complex procedures, and decrease the learning curve for minimally invasive surgery. A study by Stiles and colleagues [66], which utilized data from the American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP), including 1,062 minimally invasive liver resection cases (989 laparoscopic and 73 robotic), identified the robotic approach as a negative predictive factor for unplanned conversion to open surgery. Wang et al. [30] compared 92 patients who underwent robotic liver resection and 48 patients who underwent a laparoscopic approach. They found that the robotic approach was associated with less blood loss and a lower conversion rate than the laparoscopic approach (1.09% vs. 10.42%, respectively; P=0.034). Fruscione et al. [41] also demonstrated in a comparative study of 57 robotic and 116 laparoscopic surgery cases that patients who underwent robot-assisted hepatectomy had fewer intensive care unit admissions (43.9% vs. 61.2%, P=0.043) and readmissions within 90 days (7.0% vs. 28.5%, P=0.001). Lim et al. [40], however, found that robotic resection had no advantages in terms of blood transfusion, major morbidity, hospital stay, or R1 resection compared to laparoscopy when they compared 55 patients in the robotic group and 55 patients in the laparoscopic group after propensity score-matching. Recently, however, a meta-analysis by Guan et al. [67] comparing robotic and laparoscopic surgery, which included 13 studies involving 938 patients, reported that transfusion rate, complication rate, conversion rate, and length of hospital stay did not differ significantly between the 2 groups. Subgroup analysis of patients who underwent right hepatectomy in fact revealed more blood loss in the robotic surgery group. This finding is not consistent with the expected outcomes of the previously mentioned advantages of robotic surgical systems. However, robotic surgery performance is strongly influenced by the learning curve, hence it may improve over time. In fact, it was interesting to note that during a subgroup analysis of surgeries performed after 2010 in the Guan study, robotic surgery was associated with a lower incidence of conversion (odds ratio, 0.34; 95% confidence interval, 0.13–0.87; P=0.02). A similar scenario was observed in learning effects analysis in the ROLARR trial [68]. The authors of that study compared robotic and laparoscopic rectal surgery and concluded that the risk of conversion to open surgery was less in the robotic group than in the laparoscopic group when the robotic surgery was performed by a surgeon with extensive experience in robotic surgery. O'Connor et al. [44] compared the outcome of 39 cases of robotic to 50 cases of laparoscopic minor liver resection. After 25 cases were performed, the robotic approach was associated with

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fewer complications, a shorter hospital stay, and less blood loss than the laparoscopic approach. Therefore, the benefits of robotic surgery may depend on accumulated experienced, albeit less than that required for laparoscopic surgery.

Unlike other gastrointestinal surgeries, liver surgery involves various types of resection because of the liver's complex anatomy. As a result, a difficulty scoring system has been established to guide surgeons in performing simple and complex laparoscopic resections [69]. This difficulty index model includes the extent of liver resection, tumor location, tumor size, liver function, and proximity to major vessels; major liver resection and posteriorly located tumors (segments 7 and 8) have a high index score. Chong et al. [70] analyzed 91 patients in the robotic group and 92 patients in the laparoscopic group. Although a difficulty score of >6 (advance/expert difficulty scoring system) was associated with a longer operative time, greater blood loss, and more overall complications, a significantly higher proportion of hepatectomies with an advanced/expert difficulty level were successfully performed in the robotic group than the laparoscopic group. Consistent with this, the technical advantages of the robotic approach for superior-posterior segments (segment 7 and 8) has been documented in numerous studies [21,48,49,51,55,71]. Troisi et al. [21] reported that robot-assisted surgery can facilitate resections of more types of liver lesions, particularly those lesions located in posterosuperior segments. However, when Montalti et al. [72] compared 36 robotic liver resections and 72 laparoscopic live resections in the posterior-superior segment after propensity score matching, they found that a robotic approach offered no advantages compared to a laparoscopic approach in terms of the perioperative outcomes.

In terms of the extent of live resection, Lee at al. [33] compared 70 robotic surgeries to 66 laparoscopic surgeries. Although perioperative outcomes were similar between the two groups, there were more major hepatectomies performed in the robotic group than the laparoscopic group (20.0% vs. 3.0%, P=0.002). Tsung et al. [24] and Wu et al. [73] both reported that use of a robotic system increased the percentage of major liver resections compared to a laparoscopic approach. Although more data is needed, especially from randomized trials, the results to date suggest that the improved dexterity afforded by robotic instruments could allow more complex procedures, such as major hepatic resections, to be performed.

In line with the progress in minimally invasive surgery, the indications for robotic liver resection have expanded to more advanced cases. Giulianotti et al. [74] first reported successful robotic-assisted extended right hepatectomy with biliary-enteric reconstruction in a patient with hilar cholangiocarcinoma. Since then, more case studies of robotic major liver resection and biliary reconstruction have been reported [75-78]. In particular, Xu et al. [79] reported the feasibility of robotic major liver resection and biliary reconstruction in a case series of 10 patients with hilar cholangiocarcinoma. However, long-term outcomes were inferior to those of the open approach in their study. The application of robotic surgical system to living donor right hepatectomy is reportedly safe and feasible [22,26]. As mentioned previously, robotic surgery facilitates the dissection of hilar structures, liver mobilization, and hepatocaval dissection.

A major drawback of robotic surgery is its high cost [57,80-82]. In Korea, the National Health Insurance does not cover robotic liver surgery. Kim et al. [83] showed that the total inpatient hospitalization (from admission to discharge) cost for patients who underwent robotic left lateral sectionectomy was significantly higher than that of a laparoscopic approach ($8,183 vs. $5,190, p = 0.009). This finding is consistent with the study of Croner et al. [59] in Germany

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where robotic procedures had a perioperative cost of 8,765 Euros compared to 2,672 and 3,437 Euros for open and laparoscopic surgeries, respectively. In Taiwan, Wu et al. [84] reported that although the in-patient cost of robotic liver resection was lower than that of open surgery ($1,546.2 vs. $2,185.2), the perioperative cost (operating room and anesthesia used) of robotic surgery was significantly higher than that of open surgery ($10,951.8 vs. $2,735.4). Cortolillo et al. [85] reported the costs of laparoscopic, robotic, and open approaches for hepatectomy using the Nationwide Readmission Database of the United States for 2013 to 2014. A total of 10,870 patients underwent hepatectomy (open=10,146, laparoscopic=520, and robot=204). The robotic group had a lower mean initial admission cost (robotic=$24,983±$18,329, open=$32,391±$31,983, and laparoscopic=$30,194±$26,977; P=0.001). Moreover, robotic surgery was associated with a shorter length of stay than laparoscopic and open surgery (robotic=4.5±3.8 days, laparoscopic=6.8±6.0 days, and open=7.6±7.7 days, P<0.01) and lower readmission rates within 45 days (robotic=7.9%, laparoscopic=13.0%, and open=13.8%, P=0.05). The cost, however, varies among countries, with presumably higher costs in western countries [59,83-85]. The longer operative time and anesthesia used in robotic surgery may contribute to the higher intraoperative costs of robotic surgery than open and laparoscopic approaches, while the overall cost of hospitalization may be lowered by the lower postoperative cost of robotic surgery [13]. As surgeons accumulate more experience and are able to overcome the learning curve, perioperative outcomes will improve, thereby decreasing the cost of robotic surgery [39,63,86].

NEW ROBOTIC SYSTEMS

Currently, the da Vinci® Surgical System is the only surgical robotic system used for liver resections. The increased use of robotic surgical systems in clinical practice [11] suggests that new robotic platforms will soon be introduced in the market. To date, there are 2 robotic system products that have received regulatory approval. The REVO-I Robot Platform in South Korea has recently received Korean Food and Drug Administration (FDA) approval for use in Korea [87]. With close similarities to the da Vinci surgical system, its safety for use in humans was first reported in 17 consecutive patients with prostatic cancer [88]. The Senhance Surgical Robotic System (formerly named ALF-X) manufactured by US-based Transenterix Company has also received FDA approval. This robotic platform consists of a remote-control unit called the “cockpit,” with haptic handles, a three-dimensional high-definition monitor, an infrared eye-tracking system, a keyboard and touchpad, one foot pedal, and up to 4 detached and independent robotic arms, which is different from the 4-arm cart of the da Vinci system, in addition to a connection node, and reusable endoscopic instruments [89]. Its feasibility and safety have been already evaluated in gastrointestinal surgeries [90-92].

Additional robotic systems that will soon enter the market are the Versius robotic surgical system manufactured by Cambridge Medical Robot Surgical, which was recently approved for use in Europe, the Verb Surgical system by Verily and Ethicon, and the robotic surgical system manufactured by the Medtronic Company. More competition in the market is likely to decrease the cost of robotic surgery.

CONCLUSIONS

Application of minimally invasive liver surgery has been increasing in recent decades. Accumulated experience, refinement of surgical techniques, and improved surgical

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instruments have expanded the indications for minimally invasive liver surgery. The technical complexity and inherent limitations of laparoscopic instruments have paved the way for robotic surgical systems. Although the true advantages of robotic surgery over conventional laparoscopy still need to be confirmed based on more data, especially from randomized clinical trials, a robotic surgical system enables surgeons to perform more complex and advanced procedures in a minimally invasive way. In this review, we highlighted the increasing penetration of robotic liver resection in the surgical arena. With proper training, implementation, and standardization of procedures, more patients with contraindications for a laparoscopic approach will benefit from robotically-achieved minimally invasive surgery.

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