Robotic liver surgery: literature review and current evidence

Type of liver resection

Referring to the type of resections, 1328 (69.5%) were minor, and 584 (30.5%) were major resections. The number of “technically major resections”^[8] (segments 1, 4a, 7, 8) collected was 214 (11.7%). The studies including resections of these segments reported a longer operative time and greater estimated blood loss (EBL). Nota et al.^[11] published a multi-institutional propensity score study (31 matchings), demonstrating that minor robotic resections of postero-superior segments were safe and feasible, improving outcomes in comparison with open surgery [median EBL 180 mL vs. 300 mL, operative time 198 min vs. 255 min, length of stay (LOS) 4 days vs. 10 days].

Surgery related factors

Among the 29 studies collected, the median value of EBL was 200 mL (range 25-495) and the median operative time was 260.65 min (range 107-491). Chong et al.^[1] reported results of resections differentiated by difficulty scoring system (DSS). The authors confirmed a correlation between DSS and EBL and operative time. The mean EBL was 274.6 mL (146.4 mL for low difficulty resections and 646.7 mL for high difficulty resections), while the mean operative time was 259.3 min (205.9 min for low difficulty resections and 433.1 min for high difficulty resections)^[35]. Daskalaki et al.^[12] indicated the specific results of major and minor resections, showing higher EBL and conversion rate, longer operative time and LOS for major resections: mean EBL 354.7 mL vs. 570 mL, mean operative time 223.2 min vs. 404 min, conversion rate 2.5% vs. 17.2%, mean LOS 5.2 days vs. 8.8 days.

Only 10 articles reported data about the use of the Pringle maneuver and the median rate of its application was 23.6% (range 0-55.6). The agreement in the literature on this topic is limited and some authors considered pedicle clamping unnecessary in most cases during RS^[13-15,36]. Otherwise, other authors preferred a routine use of pedicle clamping during major hepatectomies or for difficult resections^[2,16-18].

Conversion to open surgery occurred with a median of 5.45% (range 0-14.8). Four authors reported that higher conversions rates (greater than 10%) were related to bleeding, adhesions, technical difficulty, advanced oncological diseases and the requirement of adequate oncologic margins^[2,18-20].

Histopathology

Among the indications for RS of the 29 articles reviewed, malignancies were the 84% of the cases, in particular the most frequent indication was HCC (40%), followed by CRLM (21%), other metastases (14%), cholangiocarcinoma (CCC) (9%), GBC (3%) and other malignancies (13%). The median tumor size was 33 mm (range 17.8-73). Efanov et al.^[21] emphasized that resections of greater tumors (up to 73 mm) should be performed by RS at the end of the surgeon’s learning process. The median rate of R0 margin status was 95.5% (range 72.9-100).

Interestingly, Khan et al.^[20] published an international multicenter study, in which they stratified their results for RS by tumor type (3-years overall survival was 90% for HCC, 65% for GBC and 49% for CCC) and reached comparable long-term outcomes, such as overall survival (OS) and disease free survival (DFS), to those of open and laparoscopic liver resections available in literature.

In conclusion, despite the lack of long-term results available in literature, RS is considered feasible and effective in the treatment of malignant diseases.

Short-term postoperative outcomes

ICU admission rate was described in 6 studies reporting a median frequency of 27.9% of patients requiring ICU postoperative care (range 0-83.8). Daskalaki et al.^[12], even if reporting the 83.8% of ICU admission after RS, described a reduction in the length of the ICU stay in comparison with open surgery (2.1 days vs. 3.3 days, respectively).

The median rate of overall complications of the 29 reports reviewed was 18.5% (range 1.7-68.2), with a median rate of major complications (Clavien-Dindo grade 3 or greater) of 4.7% (range 0-25). Choi et al.^[22] reported a greater frequency of overall and major complications in minor resections compared to major hepatectomies (46.7% vs. 42.6% and 13.3% vs. 9.3%, respectively), otherwise Daskalaki et al.^[12] described a major rate of overall and major complications in major resections (31% vs. 15.3% and 6.8% vs. 2.5%, respectively).

The median LOS was 5.05 days (range 3-12). In particular, 16 studies reporting an operative time longer than 250 min revealed greater LOS, overall and major complications. Among these 16 articles, the median operative time was 294.2 min (range 251.5-491) and the corresponding median LOS was 6.4 days (range 3.9-12), overall complications rate was 9% (range 1-36) and major complications rate was 3.5 % (range 1-12).

Hospital costs for RS

Many studies documented the costs of robotic liver resections, which were higher than laparoscopy, but lower than open surgery. Daskalaki et al.^[12] published a retrospective single center comparative study between robotic and open liver surgery, describing higher average costs for open surgery ($37,518 vs. $41,948) including readmissions costs, mainly because of the significant impact of ICU stay, inpatient nursing, and pharmacy costs. Similarly, Sham et al.^[23] revealed higher perioperative costs, but significantly lower postoperative and total hospital direct costs for RS ($14,754 vs. $18,998), encouraging the development of RS.

Left lateral sectionectomy

Left lateral sectionectomy (LLS) is currently performed with laparoscopy as a standard of care. Five studies focused on robotic and laparoscopic LLS, including 106 (range 9-58) and 206 (range 18-80) cases, respectively. Most of the articles reported similar perioperative outcomes between laparoscopy and RS. Many authors concluded that laparoscopic LLS remains the gold standard, since RS did not add any significant benefit, but increased the costs^[13,37-39]. However, Hu et al.^[13] established that RS could be the best choice to treat complex cases of LLS (tumor size > 10 cm in diameter, proximity of the tumor to major vessels, BMI > 30 kg/m², combined lymphadenectomy or choledochoscopy, huge left lateral section embedded in splenic fossa), reporting significantly lower EBL than in laparoscopy for these cases (131.9 mL vs. 320.8 mL, respectively).

Other types of resection

Among the 25 articles reviewed, the numbers of major and minor robotic resections included were 395 and 694 (63.7% and 36.3%) respectively, while laparoscopic cases were 460 and 1,002 (68.5% and 31.5%), respectively.

Three papers focused on only major hepatectomies (174 robotic vs. 189 laparoscopic cases). Among these, Fruscione et al.^[24] revealed that robotic technical advantages could improve surgical outcomes in comparison with laparoscopy, reducing postoperative ICU admissions (43.9% vs. 61.2%) and 90-day readmissions (7% vs. 28.5%), with a similar median complications rate (28.1% vs. 35.3%) and median LOS (4 days vs. 5 days).

Many authors focused on the ability of RS to overcome laparoscopic drawbacks, particularly simplifying hilar and hepatocaval dissection, suturing and anastomosis, precise vessel dissection or advanced sewing. However, the numbers of complex parenchymal sparing resections involving postero-superior segments or caudate lobe were similar for RS and laparoscopy, 112 (10.7%) vs. 235 (16.9%), respectively.

In complex cases many comparative studies demonstrated similar safety, feasibility and postoperative outcomes, but RS was preferred over laparoscopy, especially when several and multiplanar transection lines were necessary, resulting in safe surgical margins and increasing the rate of MIS resections^[2,21,26]. In the future these advantages could encourage the choice of RS in challenging cases, otherwise not feasible by laparoscopy^[40,41].

Surgery related factors

Considering the 25 articles reviewed, the median EBL for RS and laparoscopy were 261 mL vs. 290 mL (range 30-465 vs. 30-457, respectively). Only three studies reported statistically significant differences of this parameter. Wu et al.^[42] and Troisi et al.^[43] reported greater EBL for RS (325 mL vs. 173 mL and 330 mL vs. 174 mL, respectively), in contrast with Wang et al.^[31] (243 mL vs. 346 mL).

Referring to the use of the Pringle maneuver, Montalti et al.^[2] reported its significant use during RS compared to in laparoscopy (55.6% vs. 22.2%, respectively) because of the crush technique, leading to a longer inflow occlusion time and greater severity of complications, evaluated by comprehensive complication index (CCI: 34.6% vs. 18.4%). Conversely, Spampinato et al.^[36] published a retrospective comparative multi-institutional study, demonstrating that RS allowed for easier management of bleeding during the transection, making the application of the Pringle maneuver less necessary and reporting a significantly higher EBL for laparoscopy compared to RS (400 mL vs. 250 mL, respectively).

The median operative time for RS and laparoscopy was 271 min (range 107-430) and 227 min (range 96-360), respectively. Ten studies reported statistically significant longer duration with RS compared to laparoscopy, with a mean additional time of 68 min (range 34-153)^{[1,6,14,16,21,37,39,42,44,45]}. Spampinato et al.^[36] specified that longer robotic operative time could be related to instrument replacement and docking time, which could be reduced by improving the training of the surgical team.

In 18 articles the median operative time was longer than 250 min for RS and/or laparoscopy. In these studies, although the frequency of minor resections (69.6% vs. 74.3%, respectively), EBL (293 mL vs. 292.5 mL, respectively), LOS (6.7 days vs. 6.2 days, respectively) and overall complications rates (16% vs. 15.7%, respectively) were similar between RS and laparoscopy, the conversion rate (5% vs. 9.25%, respectively) was lower for RS. These results suggest that RS could increase MIS approach also in complex cases requiring longer operative time.

The reported use of hand-port in RS is lower than in laparoscopy. The reason for this observation could be the distance of the first surgeon from the patient and from the operative field that is mainly occupied by the robotic arms. Moreover, the second surgeon at the operative table could not have enough surgical skills to manage unexpected events. This statement could explain also the lower rate of conversion to hybrid robotic procedures in case of unexpected events. However, many studies reported an easier robotic management of adhesions and major intraoperative complications as bleeding than in laparoscopy, that could explain the lower rate of conversion to open surgery for RS.

The median rates of conversion for RS and laparoscopy were 4% vs. 7.35% (both ranges 0-20). Among the 25 comparative articles reviewed, 4 papers reported a statistically significant higher conversion rate for laparoscopy in comparison with RS^[6,26,31], while the other authors did not reach statistically significant results for this variable. Only Troisi et al.^[43] found a higher conversion rate for RS compared to laparoscopic surgery (20% vs. 7.6%, P = 0.034) but, considering only resections of postero-superior segments, they showed that RS provided a lower conversion rate (20% vs. 35.3%, P = 0.38).

Postoperative outcomes

The median rates of overall robotic and laparoscopic complications were 17.7% vs. 37.6% (ranges 5.7-68.1 vs. 27.2-48), respectively. The median rates of major complications were 2.5% vs. 8.9% (ranges 0-16.6 vs. 0-21.4), respectively.

The median LOS for RS and laparoscopy were 6 days vs. 5.95 days (ranges 3-11 vs. 3-9.5). Only Efanov et al.^[21] and Packiam et al.^[38] reported a statistically significant longer hospital stay for RS, mainly caused by postoperative complications and ICU stay.

Comparison of costs

Many authors confirmed the major costs of robotic resections, although the annual service fees could be cushioned by the utilization of the robot in other surgical specialties at the same institution. Kim et al.^[37] observed that robotic LLS showed higher costs ($8,183 vs. $5,190) and longer operative time. Salloum et al.^[39] suggested that robotic LLS did not add additional advantages in comparison with laparoscopic outcomes. Furthermore, while perioperative costs were higher in the robotic group, total costs were similar in comparison with laparoscopy (€5,522 vs. €6,035). Berber et al.^[46] calculated a general addition of $500 per case for the robotic equipment. Ji et al.^[41] considered RS not routinely applicable, since its higher costs in comparison with laparoscopy ($12,046 vs. $7,618). Packiam et al.^[38] performed a cost analysis differentiating direct and indirect costs of RS. Only robotic indirect costs were significantly higher, adding $1,423 per case ($6,553 vs. $4,408). However, Yu et al.^[47] concluded that RS could really increase in near future, overcoming the drawbacks represented by the major costs ($11,475 vs. $6,762) and the absence of transection tools equivalent to those available in laparoscopy.

Hepatocellular carcinoma

Robotic resections for HCC are feasible, safe, and demonstrated adequate oncologic outcomes. Six retrospective papers, including 294 patients, analyzed the results of RS for HCC [Table 3].

In this field the superiority of robotic MIS over open surgery was confirmed by Chen et al.^[28] by a PSM study. Even in challenging major resections, robotic approach showed longer operative time, but shorter LOS, improved patients’ pain control, not compromising oncologic outcomes and reaching comparable 3-years DFS (72.2% vs. 58.0%) and 3-years OS (92.6% vs. 93.7%). Magistri et al.^[6] and Lai et al.^[16] reported less minor robotic postoperative complications, such as pleural effusion, thanks to gentler manipulation of the diaphragm, especially in the case of lesions located in postero-superior segments. In addition, RS allowed lower rates of conversion, a greater number of resections involving the postero-superior segments, and resections of slightly larger tumors, that could explain the higher rate of major hepatectomies. Lai et al.^[16] did not find significant differences between robotic and laparoscopic oncologic outcomes (5-years OS: 65% vs. 48%, respectively), morbidity and mortality. The authors concluded that robotic MIS was a valid alternative treatment for HCC in selected patients and in the hands of surgeons expert in laparoscopic and robotic liver surgery, following the principles of open liver surgery.

Likewise, Han et al.^[50] revealed the safety and feasibility of the robotic approach to complex procedures and anatomical liver resections, and thus the superiority of minimally invasive liver surgery in terms of EBL, complication rate, LOS and risk of ascites, maintaining DFS and OS similar to open surgery.

Gallbladder cancer

RS seems particularly advantageous in the treatment of GBC, overcoming the difficulties related to the laparoscopic approach. Focusing on this field, 4 articles including 51 patients were reviewed [Table 4]. Zeng et al.^[48] demonstrated safety and feasibility of both robotic and laparoscopic surgery. Otherwise, Goel et al.^[19] and Byun et al.^[51] compared results of robotic and open radical cholecystectomy. They achieved similar results between the two approaches, reaching no significant differences in operative time, EBL and number of retrieved lymph nodes, with a reduction of LOS. Likewise, Shen et al.^[52] confirmed the feasibility of a complete robotic lymphadenectomy of the hepatic artery, the celiac axis, the hepatoduodenal ligament and retropancreatic nodes, in contrast with laparoscopy. In addition, robotic approach could reduce the risk of major iatrogenic injuries and major bleeding could be more easily managed^[51,52].

In conclusion, in selected cases RS for GBC is considered safe, feasible and effective, even during the initial learning curve, allowing sufficient lymph node dissection and enhancing recovery^[19,51,52].

Hilar cholangiocarcinoma

Even if the advantages of the robotic technique for procedures that require extreme precision and microanastomosis are clear, the scientific literature is lacking in reports about robotic treatment of this disease. Probably further implementation in surgeon expertise and robotic tools are necessary to reach encouraging results that could increase its use. Two articles were selected and their data tabulated [Table 5].

Li et al.^[17] highlighted the feasibility of 48 robotic resections for Bismuth-Corlette type I, II or III hilar cholangiocarcinoma. The authors considered RS a valid alternative to open surgery in selected cases, allowing lymphadenectomy of groups 7, 8, 9, 12 and 13. However, they did not report details about the extension of hepatectomies for each tumor stage and the rates of conversion to open surgery. Conversely, Xu et al.^[53] evaluated their results for 10 patients of fully robotic-assisted radical resection for hCCC. The authors demonstrated that this procedure is technically achievable in selected patients by expert surgeons, but without superior results to open surgery. In fact, they observed technical limitations in robotic liver mobilization and exposure, longer operative time and massive EBL, consequently increased morbidity, higher costs and poor long-term outcomes with greater rate of peritoneum implantation and multisite metastases.

Colorectal liver metastases

Many hepatobiliary surgeons encouraged the robotic approach to CRLM, achieving good surgical and oncological outcomes. Seven articles were reviewed, including 242 patients [Table 6]. Beard et al.^[26] focused their PSM on RS for CRLM and considered it feasible and safe, being perioperative and long-term oncologic outcomes largely comparable to laparoscopy.

Araujo et al.^[54] and Troisi et al.^[43] demonstrated feasibility of non-anatomical robotic resections of lesions located in postero-superior segments, simplifying parenchymal sparing resections, not affecting the oncologic outcomes, reducing the necessity of major hepatectomies and overcoming laparoscopic drawbacks.

Fifty-four simultaneous resections of the primary tumor and liver metastases were included. In these cases, RS added additional safety and effectiveness in the management of multiple metastases, improving short-term outcomes such as EBL, bowel function return time and LOS, with the exception of operative time, reaching excellent R0 resection rates^[34,55]. Even in selected cases requiring major liver resections, robotic surgery gained acceptable morbidity^[56]. In addition, it is worth considering that robotic total mesorectal excision demonstrated better preservation of urinary and sexual functions, low conversion rates and favorable morbidity^[49].

In conclusion, these outcomes could support the use of RS, despite the high operative time and costs.