Robotic Surgery of the Liver and Biliary Tract

Robotic surgery of the liver

Minimally invasive liver surgery is gaining momentum, and presently its safety and efficacy have been universally recognized.^3,14–18 Indeed, despite the scarcity of high-level evidence, over the past decade there has been a dramatic increase in the number of scientific reports on laparoscopic hepatectomy.^{2,12,14,17–19}

The available evidence on robotic liver surgery is still limited.^{14,15,17,18,20,21} In fact, the two most recent reviews of the literature, by Ocuin and Tsung ³ and Salloum et al., ¹⁴ report only 14 major case series with <500 patients undergoing robotic hepatectomy.

Salloum et al. ¹⁴ reported data of six studies, which were pooled and meta-analyzed. In all studies, robotic surgery showed lower rates of mortality and morbidity than conventional laparoscopy, although this benefit was never significant in each individual study.

Nota et al. ¹³ recently performed a comprehensive systematic review on robotic hepatectomy pooling the available data of minor and major resections (4 or more segments) of 363 patients from 12 studies. The authors further divided minor hepatectomy into two subgroups: minor resections of anteroinferior segments (2, 3, 4b, 5, and 6) and minor resection of difficult lesions, namely posterosuperior segments (1, 4a, 7, and 8). Overall, the mean conversion rate was 7%, which ranged between 0% (minor resection in the posterosuperior segments) and 8% (major hepatectomy). The mean length of hospital stay was 7 days for the total of patients, 5 days for minor resection, and 11 days for major hepatectomy. The rate of patients with postoperative complication was 17%, with the relative morbidity after major resection being 26%.

In the largest matched analysis to date, Chen et al. compared the robot with conventional celiotomy for the treatment of hepatocellular cancer. ²⁰ Eighty-one robotic resections were compared with 81 open resections using the propensity score matching method, so that the two groups could be analyzed in terms of baseline characteristics, including tumor stage, the rate of major resections, and the percentage of cirrhotic patients. Overall, robotic procedures were significantly associated with shorter hospital stay and diminished use of postoperative analgesics at the price of longer operative times. Interestingly, the analysis of solely major hepatectomies favored robotics also on estimated perioperative blood losses. Patients receiving robotic resection showed better disease-free survival and overall survival than patients who received open surgery, although this difference did not reach statistical significance (P = .06 and P = .4, respectively).

Kingham et al., ²² from Memorial Sloan Kettering Cancer Center, recently published a case-matched analysis comparing 64 cases of robotic liver surgeries with a series of 64 open hepatectomies. Robotic and open procedures included similar rates of major hepatectomies (3 or more segments), while differed on the relative percentage of wedge resections and formal segmentectomy (wedges were more frequent in the robotic group), and on the rate of combined procedures (10% versus 20%). Interestingly, robotic resection showed shorter operative times, diminished blood losses, and decreased length of hospital stay. Overall, there was a rate of positive resection margins of 1.6% and 14% for robotic and open resection, respectively, although this was not statistically significant.

Patriti et al. ²³ reported on a matched comparison between robotic and conventional open approach, focusing on the right-posterior resection. The authors analyzed ∼90 patients who were matched 1:3 between the robotic and open approach on demographics, comorbidity, tumor stage, and location. The results showed that there was no significant difference in outcomes between the two groups. Of note, perioperative blood loss, morbidity, mortality, and the rate of R0 resections were comparable between the two groups. In contrast, robotic surgery had significantly longer operative times and hepatic pedicle clamping times.

Overall, the robot has shown to be oncologically safe and effective for both minor and major hepatectomies. However, the remaining question is whether the robot can offer significant advantages over conventional laparoscopy.^3,8,14,15,24

Tsung et al. ²⁵ published the results of a comparative analysis between robotic and laparoscopic procedures performed at a single institution. They performed a matched analysis including >150 patients. The two groups did not differ on demographics, comorbidity, and extent of hepatectomy, and yielded similar outcomes. However, total complication rates favored the robot, though without statistical significance (19% versus 26%, P = .34). Furthermore, the robotic approach permitted a higher rate of procedures to be accomplished in a minimally invasive manner (93% versus 50%). This was particularly evident when analyzing major hepatectomies (80% versus 7%).

A systematic review and meta-analysis published by Montalti et al. ¹⁵ compared robotic with conventional laparoscopic liver resection on estimated blood loss, operative time, conversion rate, resection margin status, rates of morbidity and mortality, length of hospital stay, and the rate of major resections. They included both comparative and case–control studies for a total of seven articles. Overall, the laparoscopic approach resulted in significantly lower estimated blood loss and operative time than the robotic counterpart. Conversely, the relative rates of conversion, R0 resection, morbidity, and mortality did not differ between the two approaches. More recently, Qiu et al. ¹⁸ published a comprehensive meta-analysis comparing the outcomes of robotic and laparoscopic hepatectomies. They pooled and meta-analyzed the data of 776 patients from nine comparative studies. The percentage of major hepatectomies was significantly higher in the robotic group. Operative times with the robot were significantly longer than those with standard laparoscopy. Neither estimated blood loss nor conversion rate differed between the two groups. The duration of postoperative hospitalization slightly favored robotic surgery, although without statistical significance. Ultimately, no differences were observed with regard to morbidity and mortality.

Resection in the posterosuperior segments

The value of laparoscopic liver surgery has been universally recognized. However, its application to the posterosuperior segment still remains an open debate. This procedure is generally considered as technically demanding due to its complexity and the need to perform fine dissections in a narrow surgical space.^8,9,26–28 Resecting lesions located in the hepatic dome typically requires curved or angulated lines of section, which can be difficult to execute with rigid laparoscopic instruments.^{9,8,26,27,29–31} The robotic approach would theoretically provide technical advantages; however, the available data on its use for resection of the posterosuperior segment are controversial.^32,33 Some authors suggest that, if the principle of parenchymal-sparing surgery is to be followed, this type of resection can be more likely achieved with a robotic approach rather than laparoscopically.^{9,26,31,32,34,35}

Recently, Montalti et al. investigated the outcomes of laparoscopic and robotic resections of posterosuperior segments. They compared the two approaches with a propensity-score-matched method on ∼100 patients. ³⁶ Overall, no significant differences were observed between the two approaches on blood loss, hospital stay, morbidity, mortality, and rate of R0 resection.

Learning curve

At present, scarce data are available on learning curves for minimally invasive liver surgery,^6,32,33,37 with only one study comparing robotic surgery with conventional laparoscopy. ³²

Tsung et al. ²⁵ analyzed their experience with 57 consecutive robotic hepatectomies. They reported significant improvement in terms of blood loss, operative time, and length of hospitalization when comparing initial and late phase of their experience. Other results, such as complication rate and length of intensive care unit stay, also showed a positive trend. Interestingly, the rate of R0 resection was higher in the early (77% versus 66%).

Efanov et al. recently published a study comparing the learning curves of robotic and laparoscopic liver resection. ³² They reported a consecutive series including 131 minimally invasive hepatectomies. Two surgeons, who were well trained in liver surgery but with no experience in MIS, performed all procedures. Overall, the difficulty level of the procedures was comparable between the robotic and laparoscopic groups with respect to the following criteria: number of posterosuperior segment resections, rate of anatomical resection, and presence of cirrhosis. However, the proximity to major vascular structures and tumor size were higher in the robotic group. The number of procedures required to move to more demanding resections was significantly lower for robotic surgery—16 versus 29. In addition, the level of difficulty of robotic resections increased between the early and the late phase of the learning curve, while it did not for laparoscopy.

The presence of a second console has been indicated as a key to success for a dedicated program in robotic surgery. Furthermore, proctoring has been reported as an essential mechanism for robotic surgery institutional credentialing and as a prerequisite for granting unrestricted privileges on the robot. ³⁸

Costs of robotic hepatectomy

Scarce and nonunivocal data are currently available on the economic impact of robotics on liver surgery. ³⁹ Patti et al. recently published an economic assessment of robotic pancreas and liver surgery. ³⁹ In their analysis of the literature, they found five articles that provided relevant data on liver surgery. In brief, robotic surgery was associated with increased costs, with no clear clinical advantages over standard laparoscopy.

There is only one study ² that shows a trend favoring robotics over conventional celiotomy. In this study, Sham et al. ² compared the relative costs of >150 open versus robotic hepatectomies over a 3-year period. They combined the impact of both perioperative and postoperative costs on the overall economic burden of each operation. The operating room-associated higher cost of robotic procedures was mitigated by a significantly decreased cost of postoperative care, mainly due to the reduced length of stay in the intensive care unit and total length of hospitalization. The authors demonstrated that direct cost of robotic procedures was lower than open counterparts. However, while the two groups were well matched for demographics, patients undergoing open surgery had higher physical status classification (ASA) and rate of major resections. In addition, the purchase and maintenance costs of the robotic platform were not included in the final estimate.

Salloum et al., in a recent analysis, ³³ reported on a propensity-score-matched comparison between laparoscopic and robotic left lateral sectionectomy. The two techniques were equal on both perioperative and postoperative outcomes, while robotic surgery resulted to be less expensive than laparoscopy. However, this difference was not supported by the statistical analysis.

Robotic hepatectomy is still in its infancy, and probably a reliable evaluation of its actual economic impact on clinical practice should include some indirect aspects, most of which are not fully predictable. Furthermore, given the exponential evolvement of robotic surgery, it is likely that a wide variety of products will enter the market in the near future, resulting in more competition.^11,39,40

Liver transplantation

A special mention should be given to the application of robotic surgery to liver transplantation. In 2012 Giulianotti and colleagues from the University of Illinois at Chicago (UIC) reported the first case of a robotic living donor right hepatectomy. Only a limited number of cases were subsequently performed worldwide.^41,42 However, robotic hepatectomy has been successfully performed as a bridging procedure on patients awaiting transplantation.^41,43–46 These resections, ranging from caudate lobe resection to the thoracoscopic through-the-diaphragm resection in the hepatic dome, are technically demanding due to the underlying liver disease. ⁴¹ Any condition that may contraindicate a standard approach is considered as an indication to perform robotic surgery.^41,43,44 The relevance in widening the application of MIS for bridging purposes lies in the fact that transplantation is almost invariably easier and safer when previous surgery has been performed with a minimally invasive approach.^41,45,46

Integration of new technologies

Another aspect deserving special attention is the increasing digitalization of the surgical procedure provided by the robotic platforms.^8,21,22 In fact, the robotic platform represents an ideal system for the evolution of image-guided surgery. In 2015, we reported our initial experience with the clinical application of a robot-integrated ultrasound probe to resect liver malignancies. ⁸ During parenchymal transections, this allowed easier margin assessment and better understanding of vascular and biliary anatomy. The surgeon is provided with direct control on section lines. The TilePro function allows the visualization of both surgical and sonographic anatomy during procedures. ⁸ Similarly, near-infrared fluorescence with the use of indocyanine green cholangiography for easier vascular and biliary identification has been recently reported as a promising innovation in robotic surgery.^21,22,47 Easier recognition of possible anatomical variations as well as improved accuracy in lesion detection and characterization are the main features that will promote its application with the potential of reducing perioperative complications.^22,47–49 Liver surgery is a field in continuous evolution, and the integration with CT- or MRI guidance is likely to be available in the near future. This will give the possibility to superimpose preoperative images on the original operative view, and provide the surgeon with 3D information on the exact location of tumors, vasculature, and biliary structures.^{8,21,50,48,49}

Surgery of the biliary tract

Although the past decade has seen a dramatic increase in the adoption of MIS for liver resection, bile duct surgery has been traditionally considered as a relative contraindication to the use of laparoscopy and minimally invasive techniques.^51–54 At present, only a few case series describing a minimally invasive approach to bile duct neoplasms are available in the literature. The application of laparoscopy to the surgical treatment of cholangiocarcinoma (CC) has been very limited due to the need of fine dissections and the technical difficulty of bilioenteric reconstruction.^{16,51–53,55} Levi Sandri et al. ⁵¹ recently published the results of a systematic review on the use of the minimally invasive methods (including conventional and robotic laparoscopy) for the treatment of CC. Excluding staging laparoscopy for perihilar cholangiocarcinoma (PHC), their review reported <100 minimally invasive procedures. Among these, there were a limited number of robotic surgeries, most of which were reported as case reports.^5,51 Nonetheless, they concluded that the robotic system could be a valid approach to the biliary tract, particularly for major resections and procedures requiring bilioenteric reconstruction.

Xu et al. ⁵³ analyzed their initial experience on radical PHC resection with the robot. Ten patients undergoing robotic surgery were matched with 32 open surgeries performed at the same institution. Overall, robotic resection showed significantly higher operative times and higher incidence of postoperative complications. There was no statistical difference in terms of estimated blood losses, mortality, and length of postoperative stay. As such, robotic surgery resulted in significantly poorer disease-free survival. Lai et al. ⁵⁶ reported on their experience with robotic surgery for advanced malignant biliary obstruction. They performed a hepaticojejunostomy with or without Roux-en-Y reconstruction on 9 patients yielding acceptable postoperative morbidity and improved quality of life.

The literature still fails to provide substantial data on the treatment of benign liver conditions, with the exception of cholecystectomy.^21,52,57,58 Robotic cholecystectomy has gained popularity as a gateway procedure during the initial phase of robotic training. As a result, the economic burden of the robot is still considered a main issue.^21,57 Currently, only anecdotal data, mostly in the form of simple case reports, have described successful cases of choledocholithiasis management, resection of choledochal cysts, RE-DO of prior bilioenteric anastomoses, and surgical revision of iatrogenic bile duct injuries.^16,58–60 In this regard, Giulianotti et al. ⁵² reported the first consecutive series of robotic surgeries for the management of iatrogenic bile duct injuries after cholecystectomy. They combined the results of 14 procedures performed over a 9-year period. A Roux-en-Y hepaticojejunostomy was performed in most cases. The results were encouraging. They demonstrated that even for complex cases, the robot could offer a valid option to perform bile duct reconstruction. Recently, Almamar et al. ⁶¹ compared robotic and open choledochotomy and common bile duct exploration for the management of choledocholithiasis, after failed endoscopic management. They performed a matched comparison, including a total of 80 patients (50 robotic versus 30 open) over a 10-year period. Overall, the analysis favored robotic over an open approach based on frequency of external biliary drainage (52% versus 77%), postoperative morbidity (22% versus 56%), and length of hospitalization (6 versus 12 days). It is noteworthy to point out that the cost of robotic surgery was lower than that of open surgery. By combining the costs of the operating room and those of postoperative hospitalization, there was a net saving of nearly U.S. $3000 per procedure. Finally, the robotic platform has also been applied for the resection of congenital choledochal cysts in children.^21,62–64 The few existing reports show encouraging results.^62–64

Despite limited amount of data in the current literature, MIS has become the standard of care for the surgery of the biliary tract in specialized centers, as it is associated with excellent results. ⁶⁵ Accordingly, any potential benefit of robotic surgery has still to be clarified in comparison with conventional laparoscopy.