Anatomically unfavorable segments: laparoscopic and robotic liver resection in posterosuperior segments and the caudate lobe, a narrative review
Introduction
Laparoscopic liver resection (LLR) has spread since the First International Consensus Conference on Laparoscopic Liver Surgery held in Louisville in 2008. It is nowadays adopted for the surgical treatment of liver malignancies (1). Hepatocellular carcinoma (HCC) is the most common liver cancer in cirrhotic patients. In selected cases requiring a downstaging, surgical resection can be considered both a curative therapy and a “bridge-to-transplantation”. The minimally invasive approach techniques potentially bring benefits to patients who need liver resection for HCC (2), bearing in mind that surgery option for HCC, especially in cirrhotic patients, should aim to obtain a radical resection preserving as much liver parenchyma as possible and allowing a lower rate of post-hepatectomy liver failure, less impact on the abdominal wall with the respect of venous shunts, reduced surgical trauma and delicate tissues manipulation.
LLR is worldwide accepted for the treatment of tumors located in the anterior lateral segments, according to Couinaud’s classification (segments II, III, V, VI, and IVb) (3). They were considered for years as the classical “laparoscopic liver segments” because of their easy access to a minimally invasive approach, and in the second consensus meeting held in Morioka in 2014, anterolateral segment laparoscopic resections were recognized as a standard treatment; in contrast, it has been stated that posterosuperior segment resections could be applied experimentally by experienced surgeons in advanced centers where innovative procedures are carried out (4).
Different minimally invasive liver surgery (MILS) reports were published in the last years for tumors located in the unfavorable segments (I, IVa, VI, VII, and VIII) (5-7).
This review aims to analyze the role of MILS for HCC located in unfavorable segments, considering laparoscopic and robotic resection. We present the following article in accordance with the Narrative Review reporting checklist (available at https://ls.amegroups.com/article/view/10.21037/ls-21-20/rc).
Materials and methods
Literature review of published robotic and LLR for HCC focused specifically on posterosuperior segments
A literature search was performed using the PubMed database with the search phrases “robotic liver resection”, “laparoscopic liver resection”, “posterosuperior liver segments”, “caudate lobe laparoscopic resection”, “caudate lobe robotic resection”, “unfavorable liver segments”, “laparoscopic liver resection for hepatocellular carcinoma” or “robotic liver resection for hepatocellular carcinoma”. All titles, abstracts, and articles were screened for review, carefully examining the data to remove double counting of patients between series. Series focused on biliary reconstruction (choledochal cyst or biliary atresia), colorectal liver metastases, cholangiocarcinoma, and resection for benign pathology of the liver were excluded. Perioperative characteristics (tumor size, operating maneuvers, and technique, patient installation) and outcomes (operation time, blood loss, need for hepatic pedicle clamping and mean clamping time, conversion, and hospital stay) were analyzed.
Results
Search results and baseline characteristics of patients in the included studies
Thirty-eight publications, including 371 patients, were relevant to laparoscopic or robotic resection for HCC in unfavorable liver segments. All the articles with no clear indications about the histology of the tumor or the precise posterosuperior localization were excluded. A check for the doubly counted cases was performed. All the cases concerning resection for other pathologies such as colorectal liver metastases, cholangiocarcinoma, choledochal cyst or biliary atresia, and other benign pathologies of the liver were excluded (Table 1).
Table 1
Authors | Year | Journal | Type of study | Patients | Technique | HCC | Other pathologies |
---|---|---|---|---|---|---|---|
Ishizawa et al. (8) | 2012 | Annals of Surgery | Surgical technique | 62 (30 with posterosuperior malignancy localization) | Laparoscopic resection | 11 | 19 |
Chen et al. (9) | 2017 | Chinese Journal of Cancer | Article | 10 | Laparoscopic resection | 10 | 0 |
Xiao et al. (10) | 2015 | Journal of Surgical Oncology | How I do it | 10 | Laparoscopic resection | 10 | 0 |
D’Hondt et al. (11) | 2019 | Langenbeck’s Archives of Surgery | Original article | 18 | Laparoscopic resection | 6 | 12 |
Jang et al. (12) | 2017 | Annals of Surgical Oncology | Original article | 1 | Laparoscopic resection | 1 | 0 |
Tarantino et al. (13) | 2017 | Journal of Laparoendoscopic & Advanced Surgical Techniques | Full report | 13 | Laparoscopic resection | 13 | 0 |
Magistri et al. (14) | 2017 | Journal of Surgical Research | – | 46 | Laparoscopic and robotic resection | 11 (LLR, posterolateral segments); 7 (RLR, posterolateral segments) | 0 |
Ikeda et al. (15) | 2014 | Surgical Endoscopy | Video | 76 | Laparoscopic resection | 44 | 32 |
Lee et al. (16) | 2014 | J Hepatobiliary Pancreat Sci | Case series | 5 | Laparoscopic resection | 1 | 4 |
Berardi et al. (17) | 2019 | Annals of Surgical Oncology | Original article | 1 | Laparoscopic resection | 1 | 0 |
Cheng et al. (18) | 2011 | Surgical Endoscopy | Multimedia manuscript | 1 | Laparoscopic resection | 1 | 0 |
Cho et al. (19) | 2008 | Surgery | Article | 82 | Laparoscopic resection | 52 (20 in posterosuperior segments) | 30 |
Yoon et al. (20) | 2006 | Journal of Laparoendoscopic & Advanced Surgical Techniques | Case report | 1 | Laparoscopic resection | 1 | 0 |
Kim et al. (21) | 2019 | Surgical Oncology | Video | 1 | Laparoscopic resection | 1 | 0 |
Lim et al. (22) | 2021 | Surgical Endoscopy | Article | 93 (6 laparoscopic resection of posterosuperior segments, 5 robotic resection of posterosuperior segments) | Laparoscopic and robotic resection | 11 | 0 |
Teramoto et al. (23) | 2003 | World Journal of Surgery | Original article | 11 | Laparoscopic resection | 11 | 0 |
Parikh et al. (24) | 2021 | Scientific Reports | Article | 21 (12 laparoscopic resection, 9 open resection) | Laparoscopic resection | 11 | 1 |
Oh et al. (25) | 2016 | – | – | 6 | Laparoscopic resection | 6 | |
Ho et al. (26) | 2017 | Journal of Laparoendoscopic & Advanced Surgical Techniques | Article | 1 | Laparoscopic resection | 1 | 0 |
Liu et al. (27) | 2019 | Annals of Surgical Oncology | Original article | 1 | Laparoscopic resection | 1 | 0 |
Jin et al. (28) | 2018 | Biomed Research International | Research article | 12 | Laparoscopic resection | 7 | 5 |
Xu et al. (29) | 2021 | Surgical Endoscopy | – | 131 (19 laparoscopic resection, 112 open surgery resection) | Laparoscopic resection | 7 | 12 |
Chai et al. (30) | 2018 | Journal of Laparoscopic and Advanced Surgical Technique | Article | 4 | Laparoscopic resection | 4 | |
Patriti et al. (31) | 2014 | Journal of the Society of Laparoscopic & Robotic Surgeons | Article | 88 (19 robotic resection, 69 open surgery resection) | Robotic resection | 1 | |
Casciola et al. (32) | 2011 | Surgical Endoscopy | Article | 23 | Robotic resection | 3 | 20 |
Montalti et al. (33) | 2015 | Surgical Endoscopy | Article | 108 (36 robotic resection, 72 laparoscopic resection) | Laparoscopic resection and robotic resection | 9 | 99 |
Magistri et al. (34) | 2020 | Cancer | Article | 24 | Robotic resection | 24 | 0 |
Ong et al. (35) | 2016 | Journal of Endourology Case Reports | Case report | 1 | Robotic resection | 1 | 0 |
Khan et al. (36) | 2018 | Annals of Surgical Oncology | Original article | 61 | Robotic resection | 34 (4 posterolateral segments) | 27 |
Nota et al. (37) | 2019 | Annals of Surgical Oncology | Original article | 51 | Robotic resection | 12 | 39 |
Boggi et al. (38) | 2015 | Updates in Surgery | Original article | 12 | Robotic resection | 7 | 5 |
Chen et al. (39) | 2017 | Annals of Surgical Oncology | Original article | 81 (10 posterosuperior resections) | Robotic resection | 10 | 0 |
Lai et al. (40) | 2016 | Surg Laparosc Endosc Percutan Tech | Original article | 100 (29 posterosuperior resection) | Robotic resection | 29 | 0 |
Zhao et al. (41) | 2020 | Hepatobiliary and Pancreatic Diseases International | Original article | 32 | Robotic resection | 17 | 15 |
Cañada Trofo Surjan and do Prado Silveira (42) | 2020 | The International Journal of Medical Robotics and Computer Assisted Surgery | Original article | 1 | Robotic resection | 1 | 0 |
Marino et al. (43) | 2018 | Cirugia Espanola | Original article | 10 | Robotic resection | 5 | 5 |
Lai et al. (44) | 2014 | Surgical Laparoscopy, Endoscopy and Percutaneous Techniques | Technical reports | 2 | Robotic resection | 2 | 0 |
Chen et al. (45) | 2017 | Medicine (Baltimore) | Article | 526 (225 laparoscopic resection, 291 open surgery resection) | Laparoscopic resection | 225 (19 in posterosuperior segments) | 0 |
HCC, hepatocellular carcinoma; LLR, laparoscopic liver resection; RLR, robotic liver resection.
All the studies concerning robotic surgery used the Da Vinci robot system (Intuitive, Sunnyvale, CA, USA).
Laparoscopic resection of posterosuperior segments
Seventeen articles were selected (8-23,33,45) (Table 2). The mean tumor size was 33.1±15.9 mm. The techniques used were heterogeneous, varying from the anterior approach in the supine position to the left lateral decubitus or semi-prone position. The number of trocars placed is strictly dependent on the operator so that in three cases, five ports were placed [Ishizawa et al. (8), Chen et al. (9), Xiao et al. (10)], D’Hondt et al. (11) placed five or six ports, Jang et al. (12) placed five abdominal ports, and one intercostal port, Tarantino et al. five or five ports (13), Magistri et al. (14) placed only four ports. In contrast, Ikeda et al. (15) and Lee et al. (16) placed four abdominal ports, adding 1 or 2 intercostal ports. Teramoto et al. (23) described the total transthoracic technique for segment 8 laparoscopic resections, with the patient in left decubitus position and 5 transthoracic trocars. The mean operating time (OT) was 258.9±123.3 minutes (ranging from 66 to 599 minutes), the intraoperative estimated blood loss (EBL) was on average 363.9±293.1 mL (ranging from 0 to 1,200 mL). The hepatic pedicle clamping was not performed according to three authors [Tarantino et al. (13), D’Hondt et al. (11), Magistri et al. (14)]. In contrast, an intermittent Pringle’s Maneuver consisting of a 15-minute clamping and 5-minute release was performed by Jang et al. (12). All the other authors reported nothing about hepatic pedicle clamping time (HPCT). The length of stay (LOS) was on average 6.8±2.9 days, ranging from 2 to 23 days, and the mean percentage of conversion to open resection was equal to 4.6±7.9 [5.6% reported from D’Hondt et al. (11) to 23% reported from Tarantino et al. (13)].
Table 2
Authors | Patients | Tumor size | Technique | Trocars | OT | EBL | HPCT | LOS | Conversion rate |
---|---|---|---|---|---|---|---|---|---|
Ishizawa et al. (8), 2012 | 22 patients | N/A | Anterior approach (segmentectomy VI) and lateral approach (segmentectomy VII); *anatomical resection (segmentectomy) | 5 ports | 90–240 min | 50–1,200 mL | N/A | N/A | 0 (0%) |
Chen et al. (9), 2017 | 10 patients | 31 mm [23–41] | Jack-knife position; *anatomical resection | 5 ports | 166±28 min | 220±135 mL | N/A | 2.5 days [2–3] | 0 (0%) |
Xiao et al. (10), 2015 | 10 patients | 38 mm [20–60] | Supine position + anatomical segmentectomy with the hepatic veins exposed from the head side; *non anatomical and anatomical resection | 5 ports | 326.20±51.13 min | 375.0±166.42 mL | N/A | 6.70±0.82 days | 0 (0%) |
D’Hondt et al. (11), 2019 | 6 patients | N/A | Semiprone position; *anatomical resection | 5 or 6 ports | 162.5 min [140–190] | 325 mL [150–450] | 0 | 6 days [5–8] | 1 (5.6%) |
Jang et al. (12), 2017 | 1 patient | 66 mm | Lithotomy and left semi-decubitus position; *anatomical resection | 5 ports + 1 intercostal port | 420 min | 600 mL | Intermittent 15 + 5 min release period (for 8 times) | 6 days | 0 (0%) |
Tarantino et al. (13), 2017 | 13 patients | 26.5±9 mm | 45° right hemi-lateral supine position | 4 or 5 ports | 234±57 min | 125±80 mL | 0 | 5.7±3 days | 3 (23%) |
Magistri et al. (14), 2017 | 11 patients | 22.61±11.33 mm | Left decubitus position; *non anatomical and anatomical resection | 4 ports | 211±78.13 min | 328 mL [100–1,100] | 0 | 6.2±2.57 days | 4 (16.7%) |
Ikeda et al. (15), 2014 | 44 (15 Group-S, 29 Group-SP) | 2.9±1.3 (3.0±1.3 Group-S; 2.5±1.0 Group-SP) | Supine position and Semiprone position; *non-anatomical and anatomical resection | Group-SP: 4 ports + additional intercostal port in case of S8 or S7 resection; Group-S: 4 ports | Group-S 344 min [99–685]; Group-SP 296 min [66–599] | Group-S 899 mL [120–3,200]; Group-SP 158 mL [0–1070] | N/A | Group-S 35 days [7–71]; Group-SP 11 days [5–23] | 0 (0%) |
Lee et al. (16), 2014 | 1 patient | 2.2±1.1 | Anterior approach + transthoracic; *non anatomical resection | 4 ports + 2 intercostal ports | 197±68 min [110–300] | 161±138 mL | N/A | 7±3.5 days | 0 (0%) |
Berardi et al. (17), 2019 | 1 patient | 30 mm | Glissonian approach + ICG dye; *anatomical resection | – | 420 min | 261 mL | N/A | 8 days | 0 (0%) |
Cheng et al. (18), 2011 | 1 patient | 26 mm | Posterior approach; *anatomical resection | – | 510 min | 800 mL | N/A | 6 days | – |
Cho et al. (19), 2008 | 20 patients of Group-PS (20/28) | 33±15 mm | Supine or 15° right semilateral position; *anatomical and non-anatomical resection | – | 320 min [160–540] | 500 mL [200–900] | N/A | 10 days [4–19] | 3 (11%) |
Yoon et al. (20), 2006 | 1 patient | 50 mm | *Anatomical resection | – | – | – | N/A | 13 days | 0 (0%) |
Lim et al. (22), 2021 | 6 patients | 40±25 mm | Supine position + 15° reverse Trendelenburg; *non anatomical and anatomical resection | 5 or 6 ports | 269±100 min | N/A | N/A | 7±5 days | N/A |
Teramoto et al. (23), 2003 | 11 patients (3 tumors in posterosuperior segments) | 15–55 mm | Thoracoscopic hepatectomy—left decubitus position and transthoracic ports | 5 ports | 198–310 min | 50–650 mL | N/A | 8–15 days | 0 (0%) |
Montalti et al. (33), 2015 | 6 patients (total of 72 patients who underwent LLR) | 49.5±35 mm | Supine position + 30° reverse Trendelenburg, turned two-thirds on the left side; *non anatomical and anatomical resection | 4 or 6 ports | 295±107 min | 437±523 mL | 24.6±16.5 min | 4.9±2.95 days | 7 patients on the total (9.7%) |
Chen et al. (45), 2017 | 29 patients | 64 mm [14–130] | Left decubitus position; *anatomical resection | 5 ports | 240 min [75–590] | 200 mL [20–2,500] | N/A | 6 days [3–21] | N/A |
*, when anatomical resection is described. Group-S: group supine; Group-SP: group semiprone; Group-PS: posterosuperior. LLR, laparoscopic liver resection; OT, operating time; EBL, estimated blood loss; HPCT, hepatic pedicle clamping time; LOS, length of stay; ICG, indocyanine green.
Laparoscopic resection of the caudate lobe
Seven articles were selected (24-30) (Table 3). The tumor means size was equal to 36.6±20.4 mm (ranging from 9 to 65 mm). Four authors approached the caudate lobe from the left side [Parikh et al. (24), Oh et al. (25), Ho et al. (26)], while Liu et al. (27) and Jin et al. (28) chose respectively a combined and an anterior approach; Xu et al. (29) used a left side or a right side or a combined approach depending on the tumor localization. An innovative approach is reported by Chai et al. (30), who proposed the Arantius ligament suspension. The number of ports placed was 5 in all cases, except in the cases reported by Jin et al. (28), in which six ports were used. The mean OT in laparoscopic caudate resection was 229.8±86.4 minutes (ranging from 128.5 to 615 minutes), the reported EBL was 164.7±72.8 mL (ranging from 0 to 650 mL), and the hepatic pedicle clamping was performed only by three authors, with a mean time of 25.22±16.7 minutes [Xu et al. (29), Liu et al. (27), Jin et al. (28)]. The conversion rate was equal to 0%; the mean LOS was 5.7±2.2 days.
Table 3
Authors | Patients | Tumor size | Technique | Trocars | OT | EBL | HPCT | LOS | Conversion rate |
---|---|---|---|---|---|---|---|---|---|
Parikh et al. (24) | 11 | 20 mm [9–41] | Left to right approach; *anatomical resection | Five-port technique | 204.5 min [75–450] | 250 mL [0–650] | Not available | 4 days [2–10] | 0% |
Oh et al. (25) | 6 | 9–51 mm | Left to right approach; *non-anatomical and anatomical resection | Five-port technique | 382 min [168–615] | 242.5 mL [120–360] | Not available | 7 days [6–13] | 0% |
Ho et al. (26) | 1 | 10 mm | Left to right approach; *anatomical resection | Five-port technique | 270 min | 200 mL | Not available | 4 days | 0% |
Liu et al. (27) | 1 | 25 mm | Combined left/right approach; *anatomical resection | N/A | 300 min | N/A | 50 min | N/A | 0% |
Jin et al. (28) | 7 | 49–65mm | Anterior approach; *anatomical resection | Six-port technique | 140.8±95.34min | 97.92±90.54mL | 15–21 min | 9.17±2.88 days | 0% |
Xu et al. (29) | 7 | 38.7 mm | Left side, right side or combined approach; *anatomical resection | Five-port technique | 186.5 min [128.5–219] | 75 mL [48.75–200] | 14.88 min | 6 days [4.75–8] | N/A |
Chai et al. (30) | 4 | 44.5 mm [27–65] | Arantius ligament suspension; *anatomical resection | Five-port technique | 235 min [173–320] | 187.5 mL [50–280] | Not available | 6.75 days [5–9] | 0% |
*, when anatomical resection is described. OT, operating time; EBL, estimated blood loss; HPCT, hepatic pedicle clamping time; LOS, length of stay.
Robotic resection of posterosuperior segments
Twelve articles about posterosuperior segments robotic resection for HCC were selected (14,22,31-40) (Table 4). The tumor means size was 36.91±6.34 mm (ranging from 2 to 160 mm). The technique has undergone slight variations according to the preferences of the authors, but generally, the patient was in the supine position (tilted 20° in reverse Trendelenburg) or in left lateral position; the number of ports ranged from 4 to 5 abdominal ports, which disposition is highly depending on patient conformation and tumor localization. In the case series by Patriti et al. (31), Casciola et al. (32) and Montalti et al. (33) is also reported the placement of an intercostal port between the 10th and the 11th rib along the scapular line. The mean OT was 281.06±63.14 minutes (ranging from 53 to 825 minutes), the reported EBL was 288.22±94.76 mL (ranging from 10 to 3,500 mL), and eight authors performed the hepatic pedicle clamping with a mean clamping time equal to 50.70±23.39 minutes (ranging from 13.3 to 166 minutes). In these series, the mean conversion to open surgery rate was 4.47% (ranging from 0% to 13.9%), and the mean LOS was 6.23±1.92 days.
Table 4
Authors | Patients | Tumor size | Technique | Trocars | OT | EBL | HPCT | LOS | Conversion rate |
---|---|---|---|---|---|---|---|---|---|
Magistri et al. (14) | 22 patients | 34.06±13.50 mm | Da Vinci—supine position + 20° reverse Trendelenburg; *non anatomical and anatomical resection | 4 ports (disposition of the trocars highly depending on patients conformation and lesion localization) | 318±113.5 min | 400 mL [50–1,500] | 1 case (13.3 min) | 5.1±2.4 days | 0 (0%) |
Lim et al. (22) | 44 patients (5 posterior segments) | 42±28 mm | Da Vinci—supine + reverse Trendelenburg; *non anatomical and anatomical resection | 4 or 5 ports | 252±137 min | N/A | 9 cases (34±29 min) | 9±14 days | 2 (5%) |
Patriti et al. (31) | 1 patient | 41±26 mm | Da Vinci—left decubitus position; *non anatomical and anatomical resection | 4 abdominal trocars and 1 intercostal trocar | 303±132.3 min | 376.3±410 mL | 75.4±43.2 min | 6.7 ± 3 days | 0 (0%) |
Casciola et al. (32) | 3 patients | 34±18 mm [5–60] | Da Vinci—segment VI-VII-VIII left lateral position; *anatomical resection | 5 ports—camera port and left robotic trocars placed at the level of right costal margin + right robotic trocar inserted in the intercostal space between the 10th and the 11th rib along the scapular line | 280±101 min [150–420] | 245 ± 254 mL [0–1,000] | 68.9±31.7 min [40–120] | 8.9±9.4 days [3–46] | 2/23 (8.6%) |
Montalti et al. (33) | 3 patients (36 RLR) | 44.4±30.6 mm [2–110] | Da Vinci—left lateral position; *non anatomical and anatomical | 5 ports—camera port and left robotic trocars placed at the level of right costal margin + right robotic trocar inserted in the intercostal space between the 10th and the 11th rib along the scapular line | 306±182 min [53–790] | 415±414 mL [0–1,500] | 76.7±41.3 min [24–166] | 6±2.9 days [2–91] | 5/36 (13.9%) |
Magistri et al. (34) | 24 patients | <30 mm | Da Vinci—supine position + 20° reverse Trendelenburg; *non anatomical and anatomical resection [16 wedge resections and 8 segmentectomies] | 4 ports [disposition of the trocars highly depending on patients conformation and lesion localization] | 200 min [70–380] | 230 mL [10–800] | 3 cases [total clamping time 32/50/72 min] | 4 days [1–18] | 0 (0%) |
Ong et al. (35) | 1 patient | 30 mm | Da Vinci—left decubitus with flank banding; retroperitoneal approach | 5 ports | 312 min [115–458] | 251 mL [10–650] | N/A | 6 days [3–10] | 0 (0%) |
Khan et al. (36) | 34 patients (4 posterior segments) | 41 mm [7–160] | Da Vinci—supine position; *non anatomical and anatomical resection | 4 ports | 246 min [114–790] | 125 mL [10–2,200] | N/A | 4 days [2–91] | 3 (8.8%) |
Nota et al. (37) | 12 patients | 25 mm [16–31] | Da Vinci; *anatomical and non anatomical | – | 198 min [141–381] | 180 mL [100–400] | N/A | 4 days [3–6] | 4 (8%) |
Boggi et al. (38) | 7 patients | 42.4 mm [12–50] | Da Vinci—segments VIII or IVa supine position + reverse Trendelenburg; segment VII left flank position + reverse Trendelemburg; *anatomical resection | 5 ports—segments VIII or IVa optic port placed along midclavicular line; segment VII optic port placed along anterior axillary line | 260.4 min [115–430] | 252.7 mL [50–600] | – | 8.5 days [7–96] | 1 (8.3%) |
Chen et al. (39) | 112 patients (21 posterior segments) | N/A | Da Vinci—supine position + 30° reverse Trendelenburg | 5 ports | 361 min [102–805] | 249 mL [50–2,250] | N/A | 7.5 days [2–41] | N/A |
Lai et al. (40) | 100 patients (29 posterior segments) | 33±19 mm | Da Vinci—supine position + 20° reverse Trendelenburg; *non anatomical and anatomical resection | 5 ports | 207.4±77.1 min | 334.6 mL [5–3,500] | 34.0±15.4 min | 7.3±5.3 days | 4/100 (4%) conversion to open approach; 1/100 (1%) conversion to hand-assisted approach |
*, when anatomical resection is described. OT, operating time; EBL, estimated blood loss; HPCT, hepatic pedicle clamping time; LOS, length of stay; RLR, robotic liver resection.
Robotic resection of the caudate lobe
Only four articles about caudate lobe robotic resection for HCC were selected (41-44) (Table 5), with a mean tumor size equal to 28.12±13.16 mm, all performed in supine position with a variable tilted position angle in reverse Trendelenburg and five ports placement. The mean OT was 186.64±54.29 minutes (ranging from 70 to 522 minutes), the EBL 76.71±38.67 mL (ranging from 10 to 1,500 mL), conversion to open surgery rate 0% and a LOS on average equal to 4.95±1.74 days (ranging from 2 to 19 days).
Table 5
Authors | Patients | Tumor size | Technique | Trocars | OT | EBL | HPCT | LOS | Conversion rate |
---|---|---|---|---|---|---|---|---|---|
Zhao et al. (41) | 17 patients | 49.29±4.95 mm | Da Vinci—supine position; *anatomical resection | 5 ports—in Spiegel lobectomy and in total caudate lobectomy the left-side approach was preferred; in caudate process or paracaval portion resection the right-side approach was preferred | Group-S: 114 min [70–165]; Group-P: 210 min [85–230]; Group-C: 197.5 min [120–330] | Group-S: 50 mL [10–100]; Group-P: 100 mL [50–1,000]; Group-C: 100 mL [20–1,500] | N/A | Group-S: 4 days [2–6]; Group-P: 4 days [3–12]; Group-C: 7.5 days [4–19] | 0% |
Cañada Trofo Surjan and do Prado Silveira (42) | 1 patient | 30 mm | Da Vinci—supine position + 18° reverse Trendelenburg; *anatomical resection | 5 ports—left-side approach | 240 min | 40 mL | N/A | 3 days | 0% |
Marino et al. (43) | 5 patients | 26.3 mm [9–30] | Da Vinci—supine position + 25° reverse Trendelenburg; *anatomical partial resection | 5 ports—left-side approach | 258 min [150–522] | 137 mL [50–359] | N/A | 7.2 days [4–13] | 0% |
Lai et al. (44) | 2 patients | P1: 20 mm; P2: 15 mm | Da Vinci—supine position + reverse Trendelenburg; *anatomical partial resection | 5 ports—left-side approach | P1: 137 min; P2: 150 min | P1: 80 mL; P2: 30 mL | N/A | P1: 4 days; P2: 5 days | 0% |
*, when anatomical resection is described. Group-S: group supine; Group-SP: group semiprone; Group-C: caudate group; P1: first port; P2: second port. OT, operating time; EBL, estimated blood loss; HPCT, hepatic pedicle clamping time; LOS, length of stay.
Discussion
Laparoscopic resection of posterosuperior segments (segments VIII-VII-IVa)
Laparoscopic posterior segments resection is considered a challenging procedure. First, because of anatomical reasons: this is an area located in the dome of the liver, in the small sub-phrenic space; it could be technically demanding since it requires the handling of the liver. Moreover, hepatic segments VII and VIII are located deeply and adjacent to the hepatic vein, inferior vena cava (IVC), and hepatic hilum.
Also, patients with lesions located in segment IVa are considered poor candidates for laparoscopic resection; it could be technically challenging mainly for the limited visualization and the difficult bleeding control, taking care not to injure the hepatic vein running between segments III and IV.
The introduction of efficient and useful equipment allows the surgeon to minimize bleeding during liver dissection. The ultrasound (US) liver map technique enables planning and real-time guidance during LLRs (8); moreover, the US can detect safe margins confirming sufficient tumor-free resections and demonstrate the adjacent hepatic vasculature, justifying LLR.
From the technical point of view, handling the right liver may be performed by a hand-assisted approach, robotic liver resection (RLR), or spacers, such as a sterile glove pouch.
According to Kawaguchi et al. (46), LLR can be stratified based on their difficulty in three categories: the first level, including wedge resections and left lateral sectionectomy; an intermediate level with anterolateral segmentectomy and left hepatectomy; a highly advanced level which includes posterosuperior segmentectomy, right posterior sectionectomy, right hepatectomy, extended right hepatectomy, central hepatectomy, and extended left hepatectomy. First-level procedures are classified as less technically demanding. Furthermore, this classification is closely related to the postoperative outcome. First and intermediate-level procedures are less likely to be associated with severe postoperative complications and are less complicated than advanced-level LLRs.
Many techniques have been described, focusing on the trocar introduction and the patient’s position.
Their anatomical disposition and technical issues hinder nodules in segments VII and VIII; the insertion of a port through an intercostal space can provide a better operative field, facilitating the direct lateral approach into the target area (9). The additional intercostal ports can be placed at the 7th and 9th intercostal space, paying attention to the trocars’ insertion at the center of the intercostal space, to avoid intercostal vessels bleeding or parenchymal lung injury when the lung is unexpanded. According to Ishizawa et al. (8), deflation of the right lung is not necessary. After removing the intercostal trocars, the diaphragm’s incisions should be sutured, and any remaining gas should be aspired both from the abdominal cavity and the thoracic cavity. The trans-thoracic approach to the posterosuperior segments is not common, and in literature, only a few reports are available. A lateral approach was used in seven of the ten patients who underwent segmentectomy VII or VIII. A prophylactic chest tube was not required in any patients, and lung injury or postoperative pneumothorax did not occur (10).
The intercostal port can be placed in three different ways based on their relation to the diaphragm: between the ribs below the diaphragm; between the ribs, and through the diaphragm with instrument pressure on the diaphragm imposed from below to push it against the chest wall to ensure that the lung is pushed away and not injured, and finally, ports can be optically inserted between the ribs into the thoracic cavity and then through the diaphragm. The latter technique will require an additional laparoscopic stack but offers a better view.
Postural changes during the LLR procedure have also been reported to have a crucial role in facilitating the resection. Ikeda et al. (15) in 2014 evaluated the outcomes of patients undergoing LLR in a semi-prone position compared to the classic supine position, showing less blood loss in the semi-prone group and a shorter hospital stay. The semi-prone position has proved to have some advantages over the supine one, such as an immediate visualization of Rouviere’s sulcus after the laparoscope’s insertion and, consequently, a good exposition of the right liver and hepatic hilum. After the transection of coronary and triangular ligaments, the liver is naturally mobilized by its weight falling to the left and leaving a space under the right side of the diaphragm. According to the position, all the fluids and blood decline in the abdominal cavity’s left side without interferences in the operative field. Moreover, blood loss in the semi-prone position seems to be reduced because the right liver position is higher than the IVC.
Chen et al. (9) employed the left jackknife position in LLR of segments VII and VIII: patients were placed on their left side. Then, the lumbar region was elevated by adjusting the operating table to adjust a 120° angle. Ten patients underwent LLR using this position for lesions located in segments VI, VII, or VIII. These postural changes seem to be necessary to perform a posterosuperior resection of liver lesions because of a better view of the operative field obtained not only thanks to the position but also through a correct mobilization of the right liver: the section of triangular and coronary ligaments associated to the patient position allowed the gravity to rotate the liver to the left. An adequate liver exposure can reduce blood loss. On the contrary, compared with the supine position, the semi-prone position or the lateral decubitus may cause an insufficient exposure of the hepatic hilum, making hilar dissection difficult when hepatic inflow blocking is required.
Among the technically demanding resections, the caudate lobe one has still considered a challenge for its tricky exposure. It is adjacent to the IVC, portal vein, and hepatic vein, inducing significant blood loss or high complications after open surgery (28). Tumors originating in the caudate lobe have been managed by combining a hemi-liver with the caudate lobe to simplify the procedure. However, the frequent association of HCC with cirrhosis restricts the extent of major hepatic resections (47).
Laparoscopic resection of the caudate lobe
The caudate lobe generally includes three parts, the Spiegel’s lobe on the left corresponding to Couinaud’s segment I, the paracaval portion on the right (Couinaud’s segment IX), and the caudate process. A fibrous ligament surrounding the IVC to join segment VII usually occurs along the caudate lobe’s posterior wall. Sometimes, this ligament could be replaced by hepatic parenchyma embracing the IVC completely and adding further difficulty to the caudate resection (48,49). Generally, the arterial supply to the caudate lobe derives from the left hepatic artery and, portal vascularization derives from the left portal branch. Venous drainage occurs directly into the IVC through multiple small branches of variable size, number, and location. Biliary drainage includes small tributaries to both sides, mainly directed to the left hepatic duct (50). Considering all these intricate anatomical landmarks, intra-operative ultrasound (IOUS) should be used during the procedure to enable a radical laparoscopic resection, providing a precise evaluation of tumor location and the adjacent vascular structures.
Three approaches have been described in the caudate resection: the left-sided approach, the right-sided approach, and the anterior trans-hepatic approach. In the first technique, the left lobe is mobilized, turned to the right, and progressively, all the short hepatic veins (SHVs) from the caudate lobe to the IVC are divided caudate lobe could be lifted off the IVC and become more mobile. Parenchymal dissection separates the caudate lobe from the liver’s right lobe. This part of the procedure could be the most difficult since there is no definite distinction between the two parts. A right-sided approach could be appropriate and undertaken in all cases. The mobilization from the left side is difficult, for example, in tumors located in the paracaval portion of the caudate lobe or bulky tumors. In the right-sided approach, the right liver is mobilized from the diaphragm until it reaches the IVC’s lateral surface in the right-sided approach. Dissection should be continued in the plane between the IVC’s anterior and posterior surface of the caudate lobe, dividing all the retro hepatic veins originating from the caudate lobe from the paracaval portion and extending superiorly until the hepatic vein. Finally, in the anterior trans-hepatic approach, the caudate lobe is reached through the split of liver parenchyma anteriorly along the median fissure. This approach’s main advantage is that it allows a good view and the access to perform a complete caudate lobe resection, but it could take a long OT and increase blood loss. One of the critical points in the caudate lobe resection is dividing all the small branches from the caudate lobe to the IVC; a good exposure of the retro-hepatic tunnel is therefore mandatory. Laparoscopy allows the view of the surgical field from the caudal to the cranial side, providing excellent access to the retro-hepatic tunnel along the IVC and improving precise dissection and efficient hemostasis (51).
The left-sided laparoscopic approach is suitable in the case of lesions of the Spiegel lobe or lesions with a diameter of <3 cm; the right-sided laparoscopic approach is mainly suitable for the paracaval lesions and the caudate process; the anterior approach or the combination between the left- and right-sided laparoscopic approaches are suggested in lesions involving the whole caudate lobe (28). Some authors prefer the anterior approach for a lesion with a diameter >4 cm since this technique not providing the hepatic rotation can prevent hepatic veins rupture (52,53).
In addition to the difficulties related to the exposure, hemostasis control is fundamental in caudate lobe resection. This procedure is made harsh by caudate vascularization, which doesn’t consist of a single pedicle. Moreover, the venous branches of the caudate lobe are usually conformed into the IVC in the form of the SHV, in number variable from 2 to 4, featured by a thin vascular wall, short trunk, and a deep location (54). This anatomical conformation shows how important it is a good exposure of the operating field to establish a safe passage between all the SHVs, the superior hepatic veins, and the IVC (55,56).
Robotic resection
Robotic surgery was introduced in medicine nearly two decades ago. The main innovation was overpassing the laparoscopic instruments (such as image amplification, two-dimensional view, essential tremor, fulcrum effect, limited freedom of movement and ergonomics) and providing a better view of the surgical field. The popularity of RLR has increased since Giulianotti (57) published the first report of robotic liver surgery in 2003. According to the Italian Group of Minimally Invasive Liver Surgery (IgoMILS), HCC represents 56% of indications to minimally invasive liver resection for liver malignancies (58).
The Da Vinci® station is the most used equipment for this kind of surgery. Its three-dimensional view camera allows a better sense of depth; the most important feature of the robot is that it is capable of more movements than the human hand is naturally capable of (59). Despite all these advantages, robotic-assisted hepatectomy and liver resection have evolved slowly over the years, mainly because of the robot’s costs and the learning-curve.
Melstrom et al. (60) divided the liver resections into three categories: (I) major hepatectomy, (II) minor hepatectomy for segments 3, 4b, 5, 6, and (III) minor hepatectomy for segments 1, 2, 4a, 7 and 8. For resections belonging to categories II and III, the minimally invasive approach can hasten and improve postoperative recovery. The robotic approach might benefit from the laparoscopic approach in treating lesions of category III due to higher instrument dexterity. Melstrom mainly focused on selecting patients to be submitted to RLR, analyzing the cost-effectiveness of this approach and the real postoperative benefits. For instance, the robotic instruments and the 3D optics are handy to approach anatomically “remote” areas of the liver (segments VII, VIII, IVa, and I).
Consequently, the robotic minimally invasive surgery (MIS) approach is ideal for tumors in these regions, achieving fewer complication rates and very short hospital stays than open surgery. Moreover, this article highlighted the indication of minimally invasive liver resection: small tumors under challenging locations that would otherwise require a large incision for removal in an open approach. As the surgical trauma is the least, the access trauma rather than liver regeneration’s physiology dominates the postoperative recovery (61).
Many authors discussed the advantages of robotic-assisted liver resection for HCC. In a study by Magistri et al. (14), a comparison between robotic and LLR demonstrated a robotic approach’s superiority with minor postoperative complications rates, balancing the high costs derived from the investment on robot purchase and the learning curve with a shorter postoperative hospital stay. Operative time was longer than in conventional LLR because of the docking time and the initial robotic surgery experience. The non-systematic review published by Rodrigues et al. (62) showed that robotic assistance could overcome many limitations that laparoscopic surgery presents. However, robotic hepatectomy still hasn’t spread worldwide due to the high cost and different learning levels required. Moreover, hospital stay, morbidity, and EBL are similar between laparoscopic and robotic resection. Patriti et al. (31) investigated the robotic approach’s role for right posterior resection compared with open surgery, observing that both techniques are equally safe and feasible, without differences in overall postoperative morbidity contributing to short patient hospitalizations.
Compared to conventional laparoscopy, the robotic platform’s significant advantage is the technology itself, which adds value when precise vessel dissection or major suturing is needed (63,64). Robotic systems provide the surgeon with a full range of motion, with a global range of movements within the abdomen similar to open surgery and the ergonomic advantage, especially when angulated or curved lines of the section are needed parenchyma-sparing principle could be performed (65).
All liver segments can be resected with a minimally invasive approach and, the first size limitation described in the Consensus Conference and the Guidelines (1,4) has been overpassed (66). According to these results, size and locations are no more a contraindication for HCC resection. Moreover, the minimally invasive approach is a protective factor for salvage liver transplantation, allowing better survival than an open approach (67). Besides all the considerations regarding the surgical technique, Aldrighetti et al. (58) highlight that the three main causes of conversion to open technique is intraoperative bleeding (34.4%), concerns for oncological radicality (26.1%), and technical difficulties (23.8%). Still, the purpose of reaching oncological radicality is the only statistically significant reason (P value =0.02) for conversion in surgeons who fully completed their learning curve.
This study’s main limitation is the access to new techniques and only retrospective data available in the literature; however, publication bias and selection bias could be present in this analysis. Because the articles selected are all retrospective analyses of prospective data, this review is not designed to prove the superiority of laparoscopic or robotic approach, but we intend to demonstrate that both robotic and laparoscopic approaches are a feasible and valid option also in technically demanding liver segments resections, including extremely fragile patients such as the cirrhotic ones. Thus, a prospective randomized trial is ideally needed to investigate which technique may be the best.
Conclusions
LLR and RLR for HCC can be safely achieved in all segments with the outcomes of open surgery. Each technique has specific advantages, besides those familiar to minimally invasive surgeries and rapid recovery patients. In the case of a minimally invasive resection of a lesion located in an unfavorable segment, the surgeon’s experience is fundamental. It is necessary to gradually increase the skills of laparoscopic or robotic surgery according to the experience level before performing technically demanding procedures. When the oncological radicality is not achieved, a conversion to an open approach is still essential.
Acknowledgments
Funding: None.
Footnote
Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://ls.amegroups.com/article/view/10.21037/ls-21-20/rc
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ls.amegroups.com/article/view/10.21037/ls-21-20/coif). GBLS serves as the Editor-in-Chief of Laparoscopic Surgery. The other authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
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References
- Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009;250:825-30. [Crossref] [PubMed]
- Sposito C, Monteleone M, Aldrighetti L, et al. Preoperative predictors of liver decompensation after mini-invasive liver resection. Surg Endosc 2021;35:718-27. [Crossref] [PubMed]
- Levi Sandri GB, de Werra E, Mascianà G, et al. Laparoscopic and robotic approach for hepatocellular carcinoma-state of the art. Hepatobiliary Surg Nutr 2016;5:478-84. [Crossref] [PubMed]
- Abu Hilal M, Aldrighetti L, Dagher I, et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann Surg 2018;268:11-8. [Crossref] [PubMed]
- Ettorre GM, Levi Sandri GB, Santoro R, et al. Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: single center experience of 90 cases. Hepatobiliary Surg Nutr 2015;4:320-4. [PubMed]
- Levi Sandri GB, Ettorre GM, Aldrighetti L, et al. Laparoscopic liver resection of hepatocellular carcinoma located in unfavorable segments: a propensity score-matched analysis from the I Go MILS (Italian Group of Minimally Invasive Liver Surgery) Registry. Surg Endosc 2019;33:1451-8. [Crossref] [PubMed]
- Ome Y, Honda G, Kawamoto Y, et al. Minimally invasive liver resections for malignancies: where is the limit? Laparosc Surg 2021;5:37. [Crossref]
- Ishizawa T, Gumbs AA, Kokudo N, et al. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012;256:959-64. [Crossref] [PubMed]
- Chen JC, Zhang RX, Chen MS, et al. Left jackknife position: a novel position for laparoscopic hepatectomy. Chin J Cancer 2017;36:31. [Crossref] [PubMed]
- Xiao L, Xiang LJ, Li JW, et al. Laparoscopic versus open liver resection for hepatocellular carcinoma in posterosuperior segments. Surg Endosc 2015;29:2994-3001. [Crossref] [PubMed]
- D’Hondt M, Ovaere S, Knol J, et al. Laparoscopic right posterior sectionectomy: single-center experience and technical aspects. Langenbecks Arch Surg 2019;404:21-9. [Crossref] [PubMed]
- Jang JY, Han HS, Yoon YS, et al. Three-Dimensional Laparoscopic Anatomical Segment 8 Liver Resection with Glissonian Approach. Ann Surg Oncol 2017;24:1606-9. [Crossref] [PubMed]
- Tarantino G, Magistri P, Serra V, et al. Laparoscopic Liver Resection of Right Posterior Segments for Hepatocellular Carcinoma on Cirrhosis. J Laparoendosc Adv Surg Tech A 2017;27:559-63. [Crossref] [PubMed]
- Magistri P, Tarantino G, Guidetti C, et al. Laparoscopic versus robotic surgery for hepatocellular carcinoma: the first 46 consecutive cases. J Surg Res 2017;217:92-9. [Crossref] [PubMed]
- Ikeda T, Toshima T, Harimoto N, et al. Laparoscopic liver resection in the semiprone position for tumors in the anterosuperior and posterior segments, using a novel dual-handling technique and bipolar irrigation system. Surg Endosc 2014;28:2484-92. [Crossref] [PubMed]
- Lee W, Han HS, Yoon YS, et al. Role of intercostal trocars on laparoscopic liver resection for tumors in segments 7 and 8. J Hepatobiliary Pancreat Sci 2014;21:E65-8. [Crossref] [PubMed]
- Berardi G, Wakabayashi G, Igarashi K, et al. Full Laparoscopic Anatomical Segment 8 Resection for Hepatocellular Carcinoma Using the Glissonian Approach with Indocyanine Green Dye Fluorescence. Ann Surg Oncol 2019;26:2577-8. [Crossref] [PubMed]
- Cheng KC, Yeung YP, Hui J, et al. Multimedia manuscript: laparoscopic resection of hepatocellular carcinoma at segment 7: the posterior approach to anatomic resection. Surg Endosc 2011;25:3437. [Crossref] [PubMed]
- Cho JY, Han HS, Yoon YS, et al. Feasibility of laparoscopic liver resection for tumors located in the posterosuperior segments of the liver, with a special reference to overcoming current limitations on tumor location. Surgery 2008;144:32-8. [Crossref] [PubMed]
- Yoon YS, Han HS, Choi YS, et al. Total laparoscopic right posterior sectionectomy for hepatocellular carcinoma. J Laparoendosc Adv Surg Tech A 2006;16:274-7. [Crossref] [PubMed]
- Kim S, Han HS, Sham JG, et al. Laparoscopic anatomical S7 segmentectomy by the intrahepatic glissonian approach. Surg Oncol 2019;28:158. [Crossref] [PubMed]
- Lim C, Goumard C, Salloum C, et al. Outcomes after 3D laparoscopic and robotic liver resection for hepatocellular carcinoma: a multicenter comparative study. Surg Endosc 2021;35:3258-66. [Crossref] [PubMed]
- Teramoto K, Kawamura T, Takamatsu S, et al. Laparoscopic and thoracoscopic partial hepatectomy for hepatocellular carcinoma. World J Surg 2003;27:1131-6. [Crossref] [PubMed]
- Parikh M, Han HS, Cho JY, et al. Laparoscopic isolated caudate lobe resection. Sci Rep 2021;11:4328. [Crossref] [PubMed]
- Oh D, Kwon CH, Na BG, et al. Surgical Techniques for Totally Laparoscopic Caudate Lobectomy. J Laparoendosc Adv Surg Tech A 2016;26:689-92. [Crossref] [PubMed]
- Ho KM, Han HS, Yoon YS, et al. Laparoscopic Total Caudate Lobectomy for Hepatocellular Carcinoma. J Laparoendosc Adv Surg Tech A 2017;27:1074-8. [Crossref] [PubMed]
- Liu F, Wei Y, Li B. Laparoscopic Isolated Total Caudate Lobectomy for Hepatocellular Carcinoma Located in the Paracaval Portion of the Cirrhotic Liver. Ann Surg Oncol 2019;26:2980. [Crossref] [PubMed]
- Jin B, Jiang Z, Hu S, et al. Surgical Technique and Clinical Analysis of Twelve Cases of Isolated Laparoscopic Resection of the Hepatic Caudate Lobe. Biomed Res Int 2018;2018:5848309. [Crossref] [PubMed]
- Xu G, Tong J, Ji J, et al. Laparoscopic caudate lobectomy: a multicenter, propensity score-matched report of safety, feasibility, and early outcomes. Surg Endosc 2021;35:1138-47. [Crossref] [PubMed]
- Chai S, Zhao J, Zhang Y, et al. Arantius Ligament Suspension: A Novel Technique for Retraction of the Left Lateral Lobe Liver During Laparoscopic Isolated Caudate Lobectomy. J Laparoendosc Adv Surg Tech A 2018;28:740-4. [Crossref] [PubMed]
- Patriti A, Cipriani F, Ratti F, et al. Robot-assisted versus open liver resection in the right posterior section. JSLS 2014;18:e2014. [Crossref] [PubMed]
- Casciola L, Patriti A, Ceccarelli G, et al. Robot-assisted parenchymal-sparing liver surgery including lesions located in the posterosuperior segments. Surg Endosc 2011;25:3815-24. [Crossref] [PubMed]
- Montalti R, Scuderi V, Patriti A, et al. Robotic versus laparoscopic resections of posterosuperior segments of the liver: a propensity score-matched comparison. Surg Endosc 2016;30:1004-13. [Crossref] [PubMed]
- Magistri P, Catellani B, Frassoni S, et al. Robotic Liver Resection Versus Percutaneous Ablation for Early HCC: Short- and Long-Term Results. Cancers (Basel) 2020;12:3578. [Crossref] [PubMed]
- Ong KH, Huang SK, Yen CS, et al. Simultaneous Retroperitoneal Robotic Partial Nephrectomy and Hepatectomy for Synchronous Renal-Cell Carcinoma and Hepatocellular Carcinoma in a Cirrhotic Patient. J Endourol Case Rep 2016;2:215-7. [Crossref] [PubMed]
- Khan S, Beard RE, Kingham PT, et al. Long-Term Oncologic Outcomes Following Robotic Liver Resections for Primary Hepatobiliary Malignancies: A Multicenter Study. Ann Surg Oncol 2018;25:2652-60. [Crossref] [PubMed]
- Nota CL, Woo Y, Raoof M, et al. Robotic Versus Open Minor Liver Resections of the Posterosuperior Segments: A Multinational, Propensity Score-Matched Study. Ann Surg Oncol 2019;26:583-90. [Crossref] [PubMed]
- Boggi U, Caniglia F, Vistoli F, et al. Laparoscopic robot-assisted resection of tumors located in posterosuperior liver segments. Updates Surg 2015;67:177-83. [Crossref] [PubMed]
- Chen PD, Wu CY, Hu RH, et al. Robotic Versus Open Hepatectomy for Hepatocellular Carcinoma: A Matched Comparison. Ann Surg Oncol 2017;24:1021-8. [Crossref] [PubMed]
- Lai EC, Tang CN. Long-term Survival Analysis of Robotic Versus Conventional Laparoscopic Hepatectomy for Hepatocellular Carcinoma: A Comparative Study. Surg Laparosc Endosc Percutan Tech 2016;26:162-6. [Crossref] [PubMed]
- Zhao ZM, Yin ZZ, Pan LC, et al. Robotic isolated partial and complete hepatic caudate lobectomy: A single institution experience. Hepatobiliary Pancreat Dis Int 2020;19:435-9. [Crossref] [PubMed]
- Cañada Trofo Surjan R, do Prado Silveira S. Totally robotic caudate lobe liver resection: Bridge over troubled water. Int J Med Robot 2020;16:1-6. [Crossref] [PubMed]
- Marino MV, Glagolieva A, Guarrasi D. Robotic resection of the liver caudate lobe: technical description and initial consideration. Cir Esp 2018;96:162-8. (Engl Ed). [Crossref] [PubMed]
- Lai EC, Tang CN. Robot-assisted laparoscopic partial caudate lobe resection for hepatocellular carcinoma in cirrhotic liver. Surg Laparosc Endosc Percutan Tech 2014;24:e88-91. [Crossref] [PubMed]
- Chen J, Li H, Liu F, et al. Surgical outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma for various resection extent. Medicine (Baltimore) 2017;96:e6460. [Crossref] [PubMed]
- Kawaguchi Y, Fuks D, Kokudo N, et al. Difficulty of Laparoscopic Liver Resection: Proposal for a New Classification. Ann Surg 2018;267:13-7. [Crossref] [PubMed]
- Ahanatha Pillai S, Sathyanesan J, Perumal S, et al. Isolated caudate lobe resection: technical challenges. Ann Gastroenterol 2013;26:150-5. [PubMed]
- Gringeri E, Boetto R, Bassi D, et al. Totally laparoscopic caudate lobe resection: technical aspects and literature review. Surg Laparosc Endosc Percutan Tech 2014;24:e233-6. [Crossref] [PubMed]
- Nitta H, Sasaki A, Fujita T, et al. Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 2010;251:450-3. [Crossref] [PubMed]
- Siming Z, Jie Z, Hong L, et al. Laparoscopic caudate lobe resection for the treatment of hepatolithiasis. J Minim Access Surg 2019;16:106-10. [Crossref] [PubMed]
- Li Y, Zeng KN, Ruan DY, et al. Feasibility of laparoscopic isolated caudate lobe resection for rare hepatic mesenchymal neoplasms. World J Clin Cases 2019;7:3194-201. [Crossref] [PubMed]
- Asahara T, Dohi K, Hino H, et al. Isolated caudate lobectomy by anterior approach for hepatocellular carcinoma originating in the paracaval portion of the caudate lobe. J Hepatobiliary Pancreat Surg 1998;5:416-21. [Crossref] [PubMed]
- Peng SY, Li JT, Mou YP, et al. Different approaches to caudate lobectomy with "curettage and aspiration" technique using a special instrument PMOD: a report of 76 cases. World J Gastroenterol 2003;9:2169-73. [Crossref] [PubMed]
- Afaneh C, Kluger MD. Laparoscopic liver resection: lessons at the end of the second decade. Semin Liver Dis 2013;33:226-35. [Crossref] [PubMed]
- Kyriakides C, Panagiotopoulos N, Jiao LR. Isolated laparoscopic caudate lobe resection. Surg Laparosc Endosc Percutan Tech 2012;22:e209. [Crossref] [PubMed]
- Inamori H, Ido K, Isoda N, et al. Laparoscopic radiofrequency ablation of hepatocellular carcinoma in the caudate lobe by using a new laparoscopic US probe with a forward-viewing convex-array transducer. Gastrointest Endosc 2004;60:628-31. [Crossref] [PubMed]
- Giulianotti PC, Coratti A, Angelini M, et al. Robotics in general surgery: personal experience in a large community hospital. Arch Surg 2003;138:777-84. [Crossref] [PubMed]
- Aldrighetti L, Belli G, Boni L, et al. Italian experience in minimally invasive liver surgery: a national survey. Updates Surg 2015;67:129-40. [Crossref] [PubMed]
- Montalti R, Berardi G, Patriti A, et al. Outcomes of robotic vs laparoscopic hepatectomy: A systematic review and meta-analysis. World J Gastroenterol 2015;21:8441-51. [Crossref] [PubMed]
- Melstrom LG, Warner SG, Woo Y, et al. Selecting incision-dominant cases for robotic liver resection: towards outpatient hepatectomy with rapid recovery. Hepatobiliary Surg Nutr 2018;7:77-84. [Crossref] [PubMed]
- Fung AKY, Lee KF. Robotic resection for posterosuperior liver lesions: is it really superior to laparoscopic resection? Hepatobiliary Surg Nutr 2019;8:264-6. [Crossref] [PubMed]
- Rodrigues TFDC, Silveira B, Tavares FP, et al. Open, laparoscopic, and robotic-assisted hepatectomy in resection of liver tumors: a non-systematic review. Arq Bras Cir Dig 2017;30:155-60. [Crossref] [PubMed]
- Magistri P, Carrano FM, Guidetti C, et al. Challenges of a minimally invasive approach to posterior liver segments. Laparosc Surg 2018;2:26. [Crossref]
- Guerra F, Bonapasta SA, Annecchiarico M, et al. Liver Malignancies in Segment VII: The Role of Robot-assisted Surgery. Ann Surg 2017;265:E80. [Crossref] [PubMed]
- Pesi B, Guerra F, Coratti A. Robotic versus laparoscopic surgery of the liver. Laparosc Surg 2017;1:2. [Crossref]
- Levi Sandri GB, Spoletini G, Vennarecci G, et al. Laparoscopic liver resection for large HCC: short- and long-term outcomes in relation to tumor size. Surg Endosc 2018;32:4772-9. [Crossref] [PubMed]
- Levi Sandri GB, Lai Q, Ravaioli M, et al. The Role of Salvage Transplantation in Patients Initially Treated With Open Versus Minimally Invasive Liver Surgery: An Intention-to-Treat Analysis. Liver Transpl 2020;26:878-87. [Crossref] [PubMed]
Cite this article as: Usai S, Del Basso C, Levi Sandri GB. Anatomically unfavorable segments: laparoscopic and robotic liver resection in posterosuperior segments and the caudate lobe, a narrative review. Laparosc Surg 2022;6:3.