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Robotic surgery M. Diana and J. Marescaux Research Institute Against Cancer of the Digestive System (IRCAD), European Institute of TeleSurgery (EITS) and International Institute for Image-Guided Surgery (IHU Strasbourg), Strasbourg, France Correspondence to: Professor J. Marescaux, IRCAD–Hôpitaux Universitaires de Strasbourg, 1 Place de l’Hôpital, F-67091 Strasbourg, France (e-mail: [email protected])

Background: Proficiency in minimally invasive surgery requires intensive and continuous training, as it

is technically challenging for unnatural visual and haptic perceptions. Robotic and computer sciences are producing innovations to augment the surgeon’s skills to achieve accuracy and high precision during complex surgery. This article reviews the current use of robotically assisted surgery, focusing on technology as well as main applications in digestive surgery, and future perspectives. Methods: The PubMed database was interrogated to retrieve evidence-based data on surgical applications. Internal and external consulting with key opinion leaders, renowned robotics laboratories and robotic platform manufacturers was used to produce state-of-the art business intelligence around robotically assisted surgery. Results: Selected digestive procedures (oesophagectomy, gastric bypass, pancreatic and liver resections, rectal resection for cancer) might benefit from robotic assistance, although the current level of evidence is insufficient to support widespread adoption. The surgical robotic market is growing, and a variety of projects have recently been launched at both academic and corporate levels to develop lightweight, miniaturized surgical robotic prototypes. Conclusion: The magnified view, and improved ergonomics and dexterity offered by robotic platforms, might facilitate the uptake of minimally invasive procedures. Image guidance to complement robotically assisted procedures, through the concepts of augmented reality, could well represent a major revolution to increase safety and deal with difficulties associated with the new minimally invasive approaches. Paper accepted 20 October 2014 Published online in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.9711

Robotics and computer sciences applied to surgery

Successful surgical innovations focus on increasing patient safety and quality of life. In an era in which patient outcomes and healthcare budget policies are paramount, postoperative results are increasingly scrutinized and research should focus on the most effective treatments with respect to quality of life and accelerated recovery. The single greatest surgical innovation of the past three decades is the advent of minimally invasive surgery (MIS). This revolution has radically changed surgical practice, by combining multiple technological developments. High-definition cameras and microinstruments, which enter the human body through small incisions, replace the eyes and hands of the surgeon. Reduced surgical trauma and incision-related complications, such as surgical-site infections1,2 , pain and hernias3 , reduced hospital stay, earlier return to daily activities and © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

improved cosmetic outcome, represent the proven advantages of MIS over traditional open surgery. Proficiency in MIS requires intensive and continuous training as it is technically challenging for unnatural visual and haptic perceptions. The two-dimensional (2D) monitor reduces in-depth perception and hand–eye coordination, and microinstruments yield reduced force feedback while manipulating tissues. Difficulties are amplified when dealing with already complex surgical procedures4 . Robotics and computer sciences have produced innovations to augment the surgeon’s skills to achieve accuracy and high precision during complex surgery. Similar to aeronautics and military equipment, surgeons have been provided with tools conferring capacities that can replace the lack of physical palpation to identify target structures, surgical planes and resection margins. Just like aircraft pilots, surgeons can train on virtual reality (VR) simulators, which offer increasingly BJS 2015; 102: e15–e28

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realistic three-dimensional (3D) immersive environments, through the development of patient-specific virtual models which can be used to plan and perform the surgical procedure virtually, before moving on to the actual operation. 3D patient-specific virtual models can be obtained from DICOM (Digital Imaging and Communication in Medicine) format images using VR medical software. A virtual surgical and anatomical exploration can be performed on a 3D virtual model; this improves the mental representation of anatomical details, which could be underestimated with standard medical imaging alone5,6 . The surgical strategy can be planned and simulated using a virtual patient model; the 3D model may eventually be fused with real-time patient images, providing an intraoperative navigation tool that highlights target structures and anatomical variations. Fusion of live images and synthetic computer-generated images is defined as augmented reality7 . The augmented surgical eye can see by transparency, through virtual and augmented reality. It can see the invisible, through infrared technology or laparoendoscopes8 equipped with narrowband filters that provide the ability to detect invisible structures. This technology allows observation of the infinitely small through endomicroscopic systems9 and virtual biopsies with real-time histological examination. The augmented surgical hand has been provided by robotic technologies offering enhanced telemanipulation to facilitate MIS. The surgeon is seated at the master console and observes the surgical field through a stereoscopic camera, which offers high-resolution magnified vision. Surgical instruments are guided by haptic interfaces that replicate and filter hand movements (Fig. 1). Use of surgical robotic platforms

A robot is a mechatronic device (combining mechanics, electronics and informatics) that can be programmed to perform specific tasks or task sequences automatically, or can be controlled manually via computer-based and/or mechanical interfaces. Robotics were applied to surgery in the 1970s as a military project endorsed by the National Aeronautics and Space Administration (NASA) and funded by the Defense Advanced Research Project Administration (DARPA), with the aim of replacing the surgeon’s physical presence and providing care to astronauts in spacecrafts or to soldiers in battlefields. In the event of natural catastrophes, remote-controlled robots could work in protected surgical pods. © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

M. Diana and J. Marescaux

The first generation of robots to enter the operating theatre was designed to perform image-guided precision tasks. In 1985, a modified PUMA 200 industrial robot (Programmable Universal Manipulation Arm; Unimation, Stanford, California, USA) was used for CT-guided brain biopsy10 . Later, the PROBOT (Imperial College, London, UK), an ultrasound-guided system, served to perform prostatic resections11 , and in 1992 the medical robot ROBODOC® (Integrated Surgical Systems, Sacramento, California, USA) was approved for cementless total hip arthroplasty12 . These platforms were limited by basic computer interfaces and required lengthy preoperative planning. The current generation of real-time telemanipulators are set in a master–slave configuration, in which the master unit (the surgeon’s console) controls a separate slave unit formed by robotic arms with multiple degrees of freedom. From initial DARPA-funded research, two main surgical telemanipulators were developed and subsequently approved by the US Food and Drug Administration: the Zeus® system (Computer Motion, Goleta, California, USA) and the da Vinci® Surgical System (Intuitive Surgical, Sunnyvale, California, USA). In 2003, Surgical Intuitive acquired Computer Motion, which created a situation of corporate monopoly in the surgical robotics market, a situation that has not changed to date. The Zeus® telemanipulator was composed of three robotic arms, controlled remotely by the surgeon. One of the robotic arms was a voice-controlled camera navigator, AESOP (Automated Endoscopic System for Optimal Positioning). The other two arms were controlled with a haptic interface, which transferred the surgeon’s hand movements to the instruments in a precise and downscaled fashion. The robotic arms were independent and table-mounted, which provided the advantage of modularity, simplifying the operative set-up. The surgical field was displayed on a 2D screen. This did not, however, solve the problem of depth perception that already existed with standard, non-robotically assisted MIS (Fig. 2). After the merger of Computer Motion and Surgical Intuitive, development of the Zeus® robot was discontinued in favour of the da Vinci® system. Some differences compared with the Zeus® robot can be noted from the patient’s standpoint, including a compact platform moving on wheels, equipped with three (initially) to four (upgraded versions) robotic operating arms, which can be docked around the operating table. The major improvement compared with the Zeus® robot is at the surgeon’s console, equipped with a stereoscopic 3D immersive camera, which gives a tenfold magnified view and is controlled by the surgeon, for stable and precise navigation. www.bjs.co.uk

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Fig. 1 The cyber surgeon. a–f Augmented eye – view by transparency through virtual and augmented reality: a optimal robotic port positioning, projecting anatomical landmarks on to the patient’s skin; b three-dimensional patient-specific virtual model of the liver to plan and simulate the surgical procedure; c,d augmented-reality evaluation of bowel perfusion; e view the invisible through fluorescence-guided sentinel node navigation using near-infrared laser and peritumoral injection of indocyanine green; f view the infinitely small using a confocal endomicroscopic system allowing real-time virtual biopsy. g Augmented hand – the robotic telemanipulator enhances the surgeon’s precision and dexterity

Ergonomic handles reproduce human hand movements more intuitively using Endowrist® (Intuitive Surgical) technology. Improved ergonomics and dexterity are obvious (Fig. 3). The da Vinci® Surgical Robotic System is an amazing concentrate of technology. It has been upgraded over recent years to include additional features, such as near-infrared technology, and to facilitate set-up. The

latest generation, namely the da Vinci Xi™ system, released in 2014, is less bulky and its arms are arranged more ergonomically (Fig. 4). However, it still has major technical drawbacks, such as lack of force feedback. An increasing number of potential competitors are at different stages of development. Some have developed competitive platforms for general surgery based on a similar global architecture. Others are working

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Zeus® telemanipulator. a,b Table-mounted robotic arms. One of the robotic arms is a voice-controlled camera navigator, AESOP (Automated Endoscopic System for Optimal Positioning). c The surgical field is displayed on a two-dimensional screen and a haptic interface controls the instruments, following the surgeon’s hand movements in a precise and downscaled fashion (d) Fig. 2

on miniaturized platforms. What has been revealed concerning the potential of robotic surgical platforms is merely the tip of the iceberg. The real extent of robotic surgical platform development and, more importantly, the major companies involved remain confidential. All-in-one robotic platforms that seemed potential competitors of da Vinci® were being developed by Titan Medical (Toronto, Ontario, Canada). The Amadeus Composer™ (equipped with articulated instruments designed for surgery in restricted spaces in thoracic, pelvic, and ear, nose and throat surgery) and the Amadeus Maestro™ (4 arms) featured a proprietary haptic feedback technology (Titan True Touch Technology™). However, the development of these prototypes, which had

a configuration very similar to that of the Da Vinci®, has been stopped recently, mainly for potential patent infringement, and the company is now producing a special single-access robotic device. A promising platform is the TELELAP Alf-X® system13 , which has been developed by SOFAR (Milan, Italy) and received the CE mark in 2011. This robotic telemanipulator includes proprietary force-feedback technology that allows realistic perception. In addition, a useful eye-tracking solution allows navigation in the surgical field, which is displayed on a glass-based 3D monitor. It also allows zooming in and out. Arm selection is possible and can be activated by the surgeon’s direct vision on specific icons.

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da Vinci® telemanipulator. a Patient site: da Vinci Si® compact platform docked around the operating table; it moves on wheels and is equipped with four robotic operating arms. b Surgeon’s console, equipped with a stereoscopic three-dimensional immersive camera (c) that provides a tenfold magnified view. Ergonomic handles reproduce human hand movements more intuitively using Endowrist® technology. d Global view of the operative setting

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AVRA Surgical Robotics (New York, USA) is developing a modular Surgical Robotic System (ASRS), with a wireless surgeon console controlling up to four arms. The modularity allows greater freedom as well as the possibility of adapting to multiple surgical or image-guided percutaneous procedures. In addition, a variety of projects have been launched recently at both academic and corporate levels to develop lightweight, miniaturized, surgical robotic prototypes, showing the increasing complexity and the interest of several companies in sharing the surgical robotics market. Telesurgery, surgery in space and automatic surgery

A unique feature of surgical robotic platforms is the possibility to be controlled remotely, which enables © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

telesurgery, breaking the tradition of the surgeon’s physical presence. A fundamental component for effective telesurgery is data transmission speed; latency in data transmission limits telemanipulation to a distance of a few hundred kilometres14 . Network latency affects surgical performance exponentially; a short delay in data transmission (250 ms) significantly increases the time required to complete surgical tasks compared with real time15 . However, surgical exercises can still be performed with an acceptable error rate, even with delays up to 1000 ms16 . In September 2001, Operation Lindbergh was the first transatlantic surgical procedure covering the distance between New York (USA) and Strasbourg (France). This was performed in collaboration with France Telecom, using a high-speed fibreoptic connection with an average www.bjs.co.uk

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New-generation da Vinci Xi™; the robotic arms are thinner and arranged in a more ergonomic way, enabling multiquadrant procedures without the need to replace the system

Fig. 4

delay of 155 ms, combined with an advanced asynchronous transfer mode and the Zeus® telemanipulator. Operation Lindbergh is considered a milestone in global telesurgery17,18 . It made it possible to provide surgical care to astronauts, during extreme distance space explorations, in which the space crew would have to be self-sufficient in managing surgical emergencies. The main problems to solve are related to cosmic distance data transmission, reduced gravity conditions and equipment, which must be light and portable. Quality and speed of web-based transmissions, with signal delays of approximately 400 ms, are acceptable for telesurgery to be practised across the Earth. However, more advanced telecommunications are required19 to conduct telesurgery in extremely remote locations, as for space missions. Satellite-based transmissions propagate at light speed (300 000 km/s), which means that there is almost no delay for orbiting space stations and a 1-s delay for the distance between the Earth and the Moon. This means © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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that earth-controlled telesurgery would still be feasible theoretically. For very large distances (average orbiting Earth–Mars distance is approximately 72 million kilometres), the signal delay is around 6 min, which means that no real-time procedures could be telecontrolled effectively. Earth telementoring would also not be effective above a 60-s delay; consequently, a trained surgeon would need to be on board a spacecraft beyond the 1-min delay. The feasibility of zero-gravity surgery was demonstrated in 2006, with an open cyst removal in a human patient aboard the European Space Agency Airbus A-300 Zero-G Aircraft20 . Weightlessness phases were achieved by performing parabolic curves. The feasibility of laparoscopic surgery in weightlessness has been demonstrated in a pig model21 . In 2007, the first test with telesurgery in weightlessness was done using a light and portable robotic device, the M722 , developed by Stanford Research International (Menlo Park, California, USA), in the NASA C-9 aircraft. The same year, the test was repeated with the Raven, a 22-kg robotic device with two arms, integrating long-distance remote controllers23 , developed by the University of Washington. A 3D ultrasound imaging system and a warning system have been integrated into the second-generation Raven II for real-time navigation, and recognition of important anatomical structures. The third generation has been upgraded to allow collaborative surgery with the addition of a second camera and two additional robotic arms. The final solution to surpass any limit of telesurgery and any ground–spacecraft communication lag time would be automation of the surgical procedure via the robotic interface. Well described in many science fiction movies, it is conceivable theoretically because some of the required technology, although not specifically developed for space surgery, is already available or under development. Automation would require integration of a fully automatic and real-time registration between imaging and robotic systems, and a self-controlled robotic platform through algorithms that automatically recognize surgical steps and patient-specific anatomy, and predict organ displacements and deformations. Single complex surgical tasks can be performed semiautomatically through computer-assisted human–machine collaborative surgery using stochastic models of trajectory analysis24 . Semiautonomous telerobotic atrial fibrillation ablation was made possible over a distance between Boston and Milan using real-time electromagnetic navigation and preoperative CT images of the patient. The system created the surgical plane autonomously, using a stochastic model based on an anatomical atlas of 10 000 patients25 . www.bjs.co.uk

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Surgical steps can be recognized automatically and, to some extent, predicted26 . Organ displacements owing to breathing motion and heartbeat can also be predicted effectively, with a relatively small error margin27 . Additionally, ongoing research is bringing exciting results on organ deformation based on biomechanical properties28 – 31 . The process has now begun; however, many improvements are still required to conceive a full multistep complex procedure automatically performed by machine.

interface seems effective in reducing the perforation rate33 . The few studies34 – 36 comparing robotic-assisted with conventional laparoscopic myotomy reported no perforations in the robotic group and a perforation rate of 6–8 per cent in the laparoscopic group. No randomized studies or cost–benefit analysis have yet been performed.

Mini-review of current clinical applications of robotic surgery for the gastrointestinal tract

A meta-analysis37 of six prospective randomized trials comparing laparoscopic versus robotic fundoplication, including a total of 226 patients, showed comparable outcomes but longer operating times and higher costs for robotic procedures.

Robotic assistance should facilitate MIS and should ultimately improve outcomes by reducing complication rates, whenever possible. Although these benefits remain debatable, one thing is obvious: the robotic telemanipulator plays a marketing role and increases the appeal of healthcare centres equipped with cutting-edge technology. Patient recruitment can be influenced positively. Robotic surgery has disadvantages, such as high costs and longer set-up times compared with open and laparoscopic surgery. In the future, set-up time may be reduced by increased experience with robotics. Operative costs may decrease as the monopoly is likely to disappear with a new generation of surgical robots. Radical prostatectomy is the procedure in which robotic assistance has shown concrete advantages over both open and standard MIS, achieving reduced complications, shorter hospital stay and an increased rate of free surgical margins32 . Operating times, however, remain longer. Things are different in other soft tissue operations. The following is a brief overview of the current applications of robotic assistance in some gastrointestinal procedures, with analysis of whether the enhanced dexterity translates into measurable clinical benefits. Generally, the more complex the procedure, the more justified is robotic assistance. To date the evidence is insufficient to support the general use of robotic technology in minimally invasive digestive surgery. Some applications, such as rectal resection and pancreaticoduodenectomy (PD), require further investigation for the potential benefits of the MIS approach, which is facilitated significantly by use of a robot.

Laparoscopic fundoplication

Minimally invasive oesophagectomy The greater dexterity and magnified view of surgical robotic platforms should theoretically facilitate dissection in the narrow working space up to the mediastinum, and improve oncological outcomes in terms of negative resection margins and lymph node retrieval. A systematic review38 of robotically assisted oesophageal resection for cancer, including nine case series and 130 patients, demonstrated the safety of the approach and ability to achieve acceptable oncological dissections.

Minimally invasive gastrectomy Robotics might help to increase the accuracy of lymph node dissections in gastrectomy for cancer39 – 41 . In a large comparative study (827 patients with gastric cancer undergoing 236 robotic and 591 laparoscopic gastrectomies), the mean duration of surgery was 49 min longer, whereas blood loss was less in the robotic group. Morbidity, mortality and number of lymph nodes retrieved per level were comparable42 . Lower estimated blood loss with the robotic approach was reported in a few series, but was not confirmed elsewhere. No robust data support the use of robotically assisted gastrectomy and any real benefits remain elusive43 .

Bariatric surgery Heller myotomy Laparoscopic myotomy is effective for symptomatic patients with achalasia. However, a rate of oesophageal perforation as high as 16 per cent has been reported33 . Improved visualization of muscular layers and microcontrolled movements through the surgical robotic © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

The learning curve for Roux-en-Y gastric bypass (RYGBP) is steep and lasts for approximately 100 procedures44 . Robotic aid can flatten the learning curve45 . Additionally, suturing ability, enhanced by robotics, helps performance of manual gastrointestinal anastomoses within a reasonable operative time frame46 . In one case–control study47 , www.bjs.co.uk

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Robotically assisted image-guided liver resection. a Three-dimensional patient-specific virtual model demonstrating a large tumour in liver segment V. b,c Preoperative planning and automated volumetrics. d Optimal port placement through augmented-reality modular transparency. e Augmented reality seen through the robotic stereoscopic camera. f Augmented-reality navigation during robotically assisted liver resection

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robotic assistance in RYGBP seemed cost-effective when balancing overall robotic costs against the savings generated by avoiding use of mechanical staplers47 . Robotic sleeve gastrectomy48,49 is feasible and safe, but does not seem to be a special application for robotic assistance. Oversewing the long staple line using the robot is easier and could help reduce bleeding, but it has no impact on the staple-line leak rate48,50 .

Laparoscopic cholecystectomy The only available prospective clinical trial comparing robotically assisted and standard laparoscopic cholecystectomy51 found no clinical benefits to substantiate the use of such expensive technology. However, the drop in robotic device costs could modify this scenario, because cholecystectomy is a common procedure and might serve as the testing bench for future robotics developments, and also to maintain team training in surgical robotics. © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

Robotically assisted pancreatic surgery The feasibility of laparoscopic PD dates back to the 1990s52 , but it has been performed only sporadically. Considering the complexity of PD, robotic assistance could be a way to increase the rate of MIS procedures. Robotically assisted PD is feasible and safe53 . Preliminary comparisons with open PD54 favoured robotics in terms of shorter operating times, reduced blood loss and a greater number of harvested nodes. A meta-analysis55 including six studies showed a higher rate of radical (R0) resections in the robotic group. Subjectively, surgeons perceived that technical assets of the robot facilitated very complex steps, such as dissection and reconstruction56 . Recently, the authors performed several robotically assisted PD procedures complemented by augmented reality and near-infrared fluorescence guidance57 , which highlighted the window of opportunity offered by technological advances to deal with complex conditions. Caudal pancreatectomy with spleen preservation also seems to be an indication for robotic assistance, as www.bjs.co.uk

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could be a way of further assessing the role of robotic assistance in pelvic surgery. Facilitating natural-orifice transluminal endoscopic surgery and laparoendoscopic single-site surgery

SPORT™ (Single Port Orifice Robotic Technology) prototype. The effector of the SPORT™ consists of a 2⋅5-cm tubular device including a three-dimensional camera and two multiarticulating operating instruments (6 mm diameter). The camera is deployed after being inserted into the patient’s body to achieve a working position in surgical triangulation with the operative instruments. The device can perform basic and complex surgical tasks. (Courtesy of Titan Medical)

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demonstrated by the superior oncological outcomes obtained in initial experiences58 .

Robotically assisted liver resection Oncological outcomes of laparoscopic liver resection are comparable to those of the open approach, with the benefits of minimally invasive surgery59 . Surgical robots simplify microsurgical dissection of the hepatic pedicle and biliary reconstruction, which are difficult steps in standard laparoscopy. However, the current experience with robot-aided liver resection is limited to several hundred procedures worldwide60 – 64 . The authors currently undertake the majority of minor hepatectomies using robotic assistance, complemented by preoperative simulation and intraoperative augmented-reality navigation (Fig. 5).

Colorectal surgery Initial experiences with robotic colorectal resection were reported more than 10 years ago65 . For colonic resection, a systematic review66 , including mainly case series and comparative studies, suggested no benefit from robotic assistance compared with standard laparoscopy in procedures for both malignant and benign disease. For rectal resection, there is evidence that robotic assistance reduces the rate of conversion to open surgery. No differences were found in duration of surgery, morbidity, length of hospital stay or oncological outcomes67,68 . The 3D magnified view and dexterity could improve nerve-sparing total mesorectal excision, with potentially earlier recovery of urinary and sexual function69 . Focusing on quality-of-life outcomes © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

Natural-orifice transluminal endoscopic surgery (NOTES) and laparoendoscopic single-site surgery (LESS) are relatively new minimally invasive surgical techniques aiming to reduce surgical trauma. In NOTES, the abdominal cavity is reached through a viscerotomy via natural orifices (vagina, rectum, stomach), whereas a single abdominal incision is performed in LESS. These techniques present new and specific challenges that robotics could address to simplify and bring the procedures to reality. The main difficulty in LESS, with instruments entering the same incision, is the lack of surgical triangulation giving no other option but to use a chopstick technique, and causing a continuous internal and external conflict between operating instruments and the optical system. Robotics could effectively overcome this problem with the ability to cross instruments and simultaneously invert the control panel through software manipulation70 . The current armamentarium to perform NOTES safely is missing an appropriate flexible endoscopic platform, which could simultaneously offer stability to provide traction and countertraction to expose tissues, optimal visualization of the operating field, triangulation and microcontrol of endoscopic instruments, advanced suturing, stapling and forceful dissection. Surgical Intuitive has developed a dedicated platform enabling LESS, the VeSPA®, comprising a specifically designed silicone access port in which curved cannulas are introduced to house semirigid instruments. This overcomes problems with surgical triangulation. The system has been used largely in the clinical setting, for robotic cholecystectomy70 . However, the incision required is still around 2⋅5–3 cm. Titan is developing SPORT™ (Single Port Orifice Robotic Technology). The effector of SPORT™ consists of a 2⋅5-cm tubular device including a 3D camera and two multiarticulating operating instruments (6 mm diameter). The camera is deployed after being inserted into the patient’s body to achieve a working position in surgical triangulation with the operative instruments. The relatively large diameter of the multiarticulating instruments enables good torque force without hampering freedom of movement (Fig. 6). However, the design of SPORT™ is still under development and the device has been tested www.bjs.co.uk

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STRAS (Single-access Transluminal Robotic Assistance for Surgeons) flexible endoscopic surgical robotic platform: a tip effector; b motor controllers; c surgeon’s console equipped with intuitive haptic interface; d intraoperative view of STRAS performing a laparoendoscopic single-site cholecystectomy; e same frame from direct view of STRAS

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only in the experimental setting so far. Its dexterity in performing microsutures and the user-friendly surgeon’s console make it an interesting device for promoting LESS, provided that LESS surgery is demonstrated to be superior to multiport surgery. In the framework of a large ongoing European project, ARAKNES (Array of Robots Augmenting the KiNematics of Endoluminal Surgery), two miniaturized robotic platforms, dedicated to LESS and NOTES, have been developed: the SPRINT (Single Port lapaRoscopy bImaNual roboT) and the ARAKNES endoluminal platform. The SPRINT is composed of two remotely controlled robotic arms with six degrees of freedom and a stereoscopic camera, which are inserted into the abdominal cavity through a 3-cm introducer. The full intra-abdominal position of robotic units allows optimal triangulation.

The ARAKNES endoluminal platform includes a set of robotic components performing distinct tasks (imaging, manipulation, organ retraction), and each unit can be introduced separately through natural orifices to reach body cavities. Once in place, the units can be anchored to the abdominal wall by magnetic force and offer a stadium view, and enhanced surgical triangulation. Several snake-like robots71 are currently under development. The flexible architecture and multiple degrees of freedom render this concept the most suitable one for NOTES and LESS. The authors are developing two flexible endoscopic platforms (Anubiscope® for NOTES and Isisscope® for LESS; Karl Storz, Tuttlingen, Germany). These endoscopic platforms are provided with a bivalve tip that opens once in the peritoneal cavity, with flexible instruments passing through working channels and exiting in a

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triangulated fashion72,73 . Two ergonomic handles control the instruments, allowing the endoscopic surgeon to operate with both hands and to perform microsurgical sutures and endoluminal surgery (such as endoscopic submucosal dissection). A telerobotic version of these instruments (STRAS, Single-access Transluminal Robotic Assistance for Surgeons), which integrates a high-resolution scope, an intuitive haptic interface, and a visual tracking system with which to follow target structures and to compensate for physiological movements, is currently under development74 . STRAS has been used successfully to perform delicate procedures such as colonic endoscopic submucosal dissections in a porcine model (Fig. 7). Image-guided robotic surgery

Cybernetic surgery relies on the use of robotics and real-time image guidance. This combination of augmented skills is likely to increase the safety and accuracy of the surgical procedure. VR is a computer-generated realistic 3D environment and medical imaging is a developing area of application for VR. VR medical software can elaborate a 3D virtual clone of the patient from a CT or MRI image, enabling navigation through a patient’s anatomy5,6 . The virtual exploration can help the surgeon to plan and simulate the procedure. During surgery, the 3D VR model can be overlaid on real-time patient images, obtaining augmented reality which provides surgical navigation through modular virtual organ transparency. As with the first robotic applications, augmented reality and image-guided surgery were applied initially to brain75 and maxillofacial76 surgery. In these situations, the presence of fixed and highly contrasted structures allowed a high level of congruency between the virtual model and real patient anatomy. In soft tissue surgery, the situation is made more complex by the presence of respiratory movement and by the deformation of soft tissues during surgical manipulation. The problem is that the virtual model obtained before operation is rigid, representing a snapshot of a given moment. The perfect superimposition of real and computer-generated images, defined as the registration process, is inaccurate when rigid models of mobile structures are used. To deal with registration challenges, the best approach is to acquire a 3D image of the zone of interest in the operating suite, which can be updated at any time during surgery. This can be achieved using four-dimensional ultrasonography with ultrasound–CT image fusion77 or by low-dose CT78 or MRI. Another approach is to provide more flexible virtual modelling to deal with registration challenges, based on organ © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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motion prediction27 and/or on deformation prediction31 , derived by computational models of biomechanical properties of organs29 . In addition, while waiting for real-time MRI systems, work is ongoing to obtain a real-time refresh of the patient model using the Artis Zeego (Siemens Healthcare, Erlangen, Germany) coupled with a custom-made electromagnetic guidance system79 , for both endoluminal and laparoscopic procedures with, or without robotic assistance. Conclusion

The magnified view, improved ergonomics and dexterity offered by robotic platforms might facilitate the uptake of minimally invasive procedures. Selected procedures (oesophagectomy, gastric bypass, pancreatic and liver resections, rectal resection for cancer) may benefit from robotic assistance. Higher costs of robotically assisted procedures are likely to decrease with upcoming competitors’ surgical robotic platforms. Robotics research is providing solutions to push the concepts of NOTES and LESS forward. Telesurgery is still considered a futuristic field given the significant technical challenges. However, the potential benefits of telesurgery have become clearer with telementoring programmes. Research on extreme applications such as space missions and military projects could be the primer for further developments in robotics. Image guidance to complement robotically assisted procedures, through the concepts of augmented reality, represents the major revolution to increase safety and deal with difficulties associated with minimally invasive approaches. Disclosure

The authors declare no conflict of interest. References 1 Mutter D, Callari C, Diana M, Dallemagne B, Leroy J, Marescaux J. Single port laparoscopic cholecystectomy: which technique, which surgeon, for which patient? A study of the implementation in a teaching hospital. J Hepatobiliary Pancreat Sci 2011; 18: 453–457. 2 Hübner M, Diana M, Zanetti G, Eisenring MC, Demartines N, Troillet N. Surgical site infections in colon surgery: the patient, the procedure, the hospital, and the surgeon. Arch Surg 2011; 146: 1240–1245. 3 Diana M, Dhumane P, Cahill RA, Mortensen N, Leroy J, Marescaux J. Minimal invasive single-site surgery in colorectal procedures: current state of the art. J Minim Access Surg 2011; 7: 52–60. 4 Tekkis PP, Senagore AJ, Delaney CP, Fazio VW. Evaluation of the learning curve in laparoscopic colorectal surgery:

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comparison of right-sided and left-sided resections. Ann Surg 2005; 242: 83–91. Nicolau S, Soler L, Mutter D, Marescaux J. Augmented reality in laparoscopic surgical oncology. Surg Oncol 2011; 20: 189–201. D’Agostino J, Diana M, Soler L, Vix M, Marescaux J. Three-dimensional virtual neck exploration prior to parathyroidectomy. N Engl J Med 2012; 367: 1072–1073. Marescaux J, Rubino F, Arenas M, Mutter D, Soler L. Augmented-reality-assisted laparoscopic adrenalectomy. JAMA 2004; 292: 2214–2215. Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V et al. Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 2014; 259: 700–707. Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V et al. Probe-based confocal laser endomicroscopy and fluorescence-based enhanced reality for real-time assessment of intestinal microcirculation in a porcine model of sigmoid ischemia. Surg Endosc 2014; 28: 3224–3233. Kwoh YS, Hou J, Jonckheere EA, Hayati S. A robot with improved absolute positioning accuracy for CT guided stereotactic brain surgery. IEEE Trans Biomed Eng 1988; 35: 153–160. Harris SJ, Arambula-Cosio F, Mei Q, Hibberd RD, Davies BL, Wickham JE et al. The Probot – an active robot for prostate resection. Proc Inst Mech Eng H 1997; 211: 317–325. Paul HA, Bargar WL, Mittlestadt B, Musits B, Taylor RH, Kazanzides P et al. Development of a surgical robot for cementless total hip arthroplasty. Clin Orthop Relat Res 1992; (285): 57–66. Gidaro S, Altobelli E, Falavolti C, Bove AM, Ruiz EM, Stark M et al. Vesicourethral anastomosis using a novel telesurgical system with haptic sensation, the Telelap Alf-X: a pilot study. Surg Technol Int 2014; 24: 35–40. Satava RM. Emerging technologies for surgery in the 21st century. Arch Surg 1999; 134: 1197–1202. Lum MJ, Rosen J, King H, Friedman DC, Lendvay TS, Wright AS et al. Teleoperation in surgical robotics – network latency effects on surgical performance. Conf Proc IEEE Eng Med Biol Soc 2009; 2009: 6860–6863. Rayman R, Croome K, Galbraith N, McClure R, Morady R, Peterson S et al. Long-distance robotic telesurgery: a feasibility study for care in remote environments. Int J Med Robot 2006; 2: 216–224. Marescaux J, Leroy J, Gagner M, Rubino F, Mutter D, Vix M et al. Transatlantic robot-assisted telesurgery. Nature 2001; 413: 379–380. Haidegger T, Sándor J, Benyó Z. Surgery in space: the future of robotic telesurgery. Surg Endosc 2011; 25: 681–690. Rayman R, Croome K, Galbraith N, McClure R, Morady R, Peterson S et al. Robotic telesurgery: a real-world comparison of ground- and satellite-based internet performance. Int J Med Robot 2007; 3: 111–116.

© 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

20 The Independent. ‘Weightless’ Surgery Performed for First Time. http://www.independent.co.uk/news/world/europe/ weightless-surgery-performed-for-first-time-417826.html [accessed 10 May 2012]. 21 Kirkpatrick AW, Keaney M, Kmet L, Ball CG, Campbell MR, Kindratsky C et al. Intraperitoneal gas insufflation will be required for laparoscopic visualization in space: a comparison of laparoscopic techniques in weightlessness. J Am Coll Surg 2009; 209: 233–241. 22 Doarn CR, Anvari M, Low T, Broderick TJ. Evaluation of teleoperated surgical robots in an enclosed undersea environment. Telemed J E Health 2009; 15: 325–335. 23 Lum MJ, Rosen J, King H, Friedman DC, Donlin G, Sankaranarayanan G et al. Telesurgery via Unmanned Aerial Vehicle (UAV) with a field deployable surgical robot. Stud Health Technol Inform 2007; 125: 313–315. 24 Padoy N, Hager GD. Spatio-temporal registration of multiple trajectories. Med Image Comput Comput Assist Interv 2011; 14: 145–152. 25 Pappone C, Vicedomini G, Manguso F, Gugliotta F, Mazzone P, Gulletta S et al. Robotic magnetic navigation for atrial fibrillation ablation. J Am Coll Cardiol 2006; 47: 1390–1400. 26 Padoy N, Blum T, Ahmadi SA, Feussner H, Berger MO, Navab N. Statistical modeling and recognition of surgical workflow. Med Image Anal 2012; 16: 632–641. 27 Hostettler A, Nicolau SA, Rémond Y, Marescaux J, Soler L. A real-time predictive simulation of abdominal viscera positions during quiet free breathing. Prog Biophys Mol Biol 2010; 103: 169–184. 28 Courtecuisse H, Peterlik I, Trivisonne R, Duriez C, Cotin S. Constraint-based simulation for non-rigid real-time registration. Stud Health Technol Inform 2014; 196: 76–82. 29 Umale S, Chatelin S, Bourdet N, Deck C, Diana M, Dhumane P et al. Experimental in vitro mechanical characterization of porcine Glisson’s capsule and hepatic veins. J Biomech 2011; 44: 1678–1683. 30 Oktay O, Zhang L, Mansi T, Mountney P, Mewes P, Nicolau S et al. Biomechanically driven registration of preto intra-operative 3D images for laparoscopic surgery. Med Image Comput Comput Assist Interv 2013; 16: 1–9. 31 Haouchine N, Dequidt J, Berger MO, Cotin S. Deformation-based augmented reality for hepatic surgery. Stud Health Technol Inform 2013; 184: 182–188. 32 Alemozaffar M, Sanda M, Yecies D, Mucci LA, Stampfer MJ, Kenfield SA. Benchmarks for operative outcomes of robotic and open radical prostatectomy: results from the Health Professionals Follow-up Study. Eur Urol 2014; [Epub ahead of print]. 33 Melvin WS, Dundon JM, Talamini M, Horgan S. Computer-enhanced robotic telesurgery minimizes esophageal perforation during Heller myotomy. Surgery 2005; 138: 553–558. 34 Huffmanm LC, Pandalai PK, Boulton BJ, James L, Starnes SL, Reed MF et al. Robotic Heller myotomy: a safe

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35

36

37

38

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40

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operation with higher postoperative quality-of-life indices. Surgery 2007; 142: 613–618. Iqbal A, Haider M, Desai K, Garg N, Kavan J, Mittal S et al. Technique and follow-up of minimally invasive Heller myotomy for achalasia. Surg Endosc 2006; 20: 394–401. Horgan S, Galvani C, Gorodner MV, Omelanczuck P, Elli F, Moser F et al. Robotic-assisted Heller myotomy versus laparoscopic Heller myotomy for the treatment of esophageal achalasia: multicenter study. J Gastrointest Surg 2005; 9: 1020–1029. Markar SR, Karthikesalingam AP, Hagen ME, Talamini M, Horgan S, Wagner OJ. Robotic vs. laparoscopic Nissen fundoplication for gastro-oesophageal reflux disease: systematic review and meta-analysis. Int J Med Robot 2010; 6: 125–131. Clark J, Sodergren MH, Purkayastha S, Mayer EK, James D, Athanasiou T et al. The role of robotic assisted laparoscopy for oesophagogastric oncological resection; an appraisal of the literature. Dis Esophagus 2011; 24: 240–250. Kim MC, Heo GU, Jung GJ. Robotic gastrectomy for gastric cancer: surgical techniques and clinical merits. Surg Endosc 2010; 24: 610–615. Song J, Oh SJ, Kang WH, Hyung WJ, Choi SH, Noh SH. Robot-assisted gastrectomy with lymph node dissection for gastric cancer: lessons learned from an initial 100 consecutive procedures. Ann Surg 2009; 249: 927–932. Uyama I, Kanaya S, Ishida Y, Inaba K, Suda K, Satoh S. Novel integrated robotic approach for suprapancreatic D2 nodal dissection for treating gastric cancer: technique and initial experience. World J Surg 2012; 36: 331–337. Woo Y, Hyung WJ, Pak KH, Inaba K, Obama K, Choi SH et al. Robotic gastrectomy as an oncologically sound alternative to laparoscopic resections for the treatment of early-stage gastric cancers. Arch Surg 2011; 146: 1086–1092. Leroy J, Diana M, Perretta S, Wall J, De Ruijter V, Marescaux J. Original technique to close the transrectal viscerotomy access in a NOTES transrectal and transgastric segmental colectomy. Surg Innov 2011; 18: 193–200. Schauer P, Ikramuddin S, Hamad G, Gourash W. The learning curve for laparoscopic Roux-en-Y gastric bypass is 100 cases. Surg Endosc 2003; 17: 212–215. Buchs NC, Pugin F, Bucher P, Hagen ME, Chassot G, Koutny-Fong P et al. Learning curve for robot-assisted Roux-en-Y gastric bypass. Surg Endosc 2012; 26: 1116–1121. Markar SR, Karthikesalingam AP, Venkat-Ramen V, Kinross J, Ziprin P. Robotic vs. laparoscopic Roux-en-Y gastric bypass in morbidly obese patients: systematic review and pooled analysis. Int J Med Robot 2011; 7: 393–400. Hagen ME, Pugin F, Chassot G, Huber O, Buchs N, Iranmanesh P et al. Reducing cost of surgery by avoiding complications: the model of robotic Roux-en-Y gastric bypass. Obes Surg 2012; 22: 52–61. Ayloo S, Buchs NC, Addeo P, Bianco FM, Giulianotti PC. Robot-assisted sleeve gastrectomy for super-morbidly obese patients. J Laparoendosc Adv Surg Tech A 2011; 21: 295–299.

© 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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49 Diamantis T, Alexandrou A, Nikiteas N, Giannopoulos A, Papalambros E. Initial experience with robotic sleeve gastrectomy for morbid obesity. Obes Surg 2011; 21: 1172–1179. 50 Chen B, Kiriakopoulos A, Tsakayannis D, Wachtel MS, Linos D, Frezza EE. Reinforcement does not necessarily reduce the rate of staple line leaks after sleeve gastrectomy. A review of the literature and clinical experiences. Obes Surg 2009; 19: 166–172. 51 Breitenstein S, Nocito A, Puhan M, Held U, Weber M, Clavien PA. Robotic-assisted versus laparoscopic cholecystectomy: outcome and cost analyses of a case-matched control study. Ann Surg 2008; 247: 987–993. 52 Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 1994; 8: 408–410. 53 Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P et al. Robot-assisted laparoscopic pancreatic surgery: single-surgeon experience. Surg Endosc 2010; 24: 1646–1657. 54 Buchs NC, Addeo P, Bianco FM, Ayloo S, Benedetti E, Giulianotti PC. Robotic versus open pancreaticoduodenectomy: a comparative study at a single institution. World J Surg 2011; 35: 2739–2746. 55 Chen Y, Yan J, Yuan Z, Yu S, Wang Z, Zheng Q. A meta-analysis of robotic-assisted pancreatectomy versus laparoscopic and open pancreatectomy. Saudi Med J 2013; 34: 1229–1236. 56 Nguyen KT, Zureikat AH, Chalikonda S, Bartlett DL, Moser AJ, Zeh HJ. Technical aspects of robotic-assisted pancreaticoduodenectomy (RAPD). J Gastrointest Surg 2011; 15: 870–875. 57 Pessaux P, Diana M, Soler L, Piardi T, Mutter D, Marescaux J. Robotic duodenopancreatectomy assisted with augmented reality and real-time fluorescence guidance. Surg Endosc 2014; 28: 2493–2498. 58 Daouadi M, Zureikat AH, Zenati MS, Choudry H, Tsung A, Bartlett DL et al. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg 2013; 257: 128–132. 59 Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection – 2804 patients. Ann Surg 2009; 250: 831–841. 60 Giulianotti PC, Coratti A, Sbrana F, Addeo P, Bianco FM, Buchs NC et al. Robotic liver surgery: results for 70 resections. Surgery 2011; 149: 29–39. 61 Chan OC, Tang CN, Lai EC, Yang GP, Li MK. Robotic hepatobiliary and pancreatic surgery: a cohort study. J Hepatobiliary Pancreat Sci 2011; 18: 471–480. 62 Choi GH, Choi SH, Kim SH, Hwang HK, Kang CM, Choi JS et al. Robotic liver resection: technique and results of 30 consecutive procedures. Surg Endosc 2012; 26: 2247–2258. 63 Lai EC, Tang CN, Li MK. Robot-assisted laparoscopic hemi-hepatectomy: technique and surgical outcomes. Int J Surg 2012; 10: 11–15. 64 Lai EC, Tang CN, Yang GP, Li MK. Multimodality laparoscopic liver resection for hepatic malignancy – from

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e28

65

66

67

68

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70

71

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M. Diana and J. Marescaux

conventional total laparoscopic approach to robot-assisted laparoscopic approach. Int J Surg 2011; 9: 324–328. Delaney CP, Lynch AC, Senagore AJ, Fazio VW. Comparison of robotically performed and traditional laparoscopic colorectal surgery. Dis Colon Rectum 2003; 46: 1633–1639. Kanji A, Gill RS, Shi X, Birch DW, Karmali S. Robotic-assisted colon and rectal surgery: a systematic review. Int J Med Robot 2011; 7: 401–407. Memon S, Heriot AG, Murphy DG, Bressel M, Lynch AC. Robotic versus laparoscopic proctectomy for rectal cancer: a meta-analysis. Ann Surg Oncol 2012; 19: 2095–2101. Trastulli S, Farinella E, Cirocchi R, Cavaliere D, Avenia N, Sciannameo F et al. Robotic resection compared with laparoscopic rectal resection for cancer: systematic review and meta-analysis of short-term outcome. Colorectal Dis 2012; 14: e134–e156. Kim JY, Kim NK, Lee KY, Hur H, Min BS, Kim JH. A comparative study of voiding and sexual function after total mesorectal excision with autonomic nerve preservation for rectal cancer: laparoscopic versus robotic surgery. Ann Surg Oncol 2012; 19: 2485–2493. Allemann P, Leroy J, Asakuma M, Al Abeidi F, Dallemagne B, Marescaux J. Robotics may overcome technical limitations of single-trocar surgery: an experimental prospective study of Nissen fundoplication. Arch Surg 2010; 145: 267–271. Mahvash M, Zenati M. Toward a hybrid snake robot for single-port surgery. Conf Proc IEEE Eng Med Biol Soc 2011; 2011: 5372–5375. Diana M, Chung H, Liu KH, Dallemagne B, Demartines N, Mutter D et al. Endoluminal surgical triangulation: overcoming challenges of colonic endoscopic submucosal

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74

75

76

77

78

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dissections using a novel flexible endoscopic surgical platform: feasibility study in a porcine model. Surg Endosc 2013; 27: 4130–4135. Leroy J, Diana M, Barry B, Mutter D, Melani AG, Wu HS et al. Perirectal Oncologic Gateway to Retroperitoneal Endoscopic Single-Site Surgery (PROGRESSS): a feasibility study for a new NOTES approach in a swine model. Surg Innov 2012; 19: 345–352. Diana M, Pessaux P, Marescaux J. New technologies for single-site robotic surgery in hepato-biliary-pancreatic surgery. J Hepatobiliary Pancreat Sci 2014; 21: 34–42. Iseki H, Masutani Y, Iwahara M, Tanikawa T, Muragaki Y, Taira T et al. Volumegraph (overlaid three-dimensional image-guided navigation). Clinical application of augmented reality in neurosurgery. Stereotact Funct Neurosurg 1997; 68: 18–24. Wagner A, Ploder O, Enislidis G, Truppe M, Ewers R. Virtual image guided navigation in tumor surgery – technical innovation. J Craniomaxillofac Surg 1995; 23: 217–213. Mauri G, Cova L, De Beni S, Ierace T, Tondolo T, Cerri A et al. Real-time US–CT/MRI image fusion for guidance of thermal ablation of liver tumors undetectable with US: results in 295 cases. Cardiovasc Intervent Radiol 2014; [Epub ahead of print]. Shekhar R, Dandekar O, Bhat V, Philip M, Lei P, Godinez C et al. Live augmented reality: a new visualization method for laparoscopic surgery using continuous volumetric computed tomography. Surg Endosc 2010; 24: 1976–1985. Diana M, Wall J, Perretta S, Dallemagne B, Gonzales KD, Harrison MR et al. Totally endoscopic magnetic enteral bypass by external guided rendez-vous technique. Surg Innov 2011; 18: 317–320.

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