Techniques for lung surgery: a review of robotic lobectomy

Transcription

1 Expert Review of Respiratory Medicine ISSN: (Print) (Online) Journal homepage: Techniques for lung surgery: a review of robotic lobectomy Sophia Chen, Travis C Geraci & Robert James Cerfolio To cite this article: Sophia Chen, Travis C Geraci & Robert James Cerfolio (2018): Techniques for lung surgery: a review of robotic lobectomy, Expert Review of Respiratory Medicine, DOI: / To link to this article: Accepted author version posted online: 05 Mar Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at

2 Publisher: Taylor & Francis Journal: Expert Review of Respiratory Medicine DOI: / Review Techniques for lung surgery: a review of robotic lobectomy Sophia Chen 1, Travis C Geraci 1, Robert James Cerfolio* 1 1 New York University School of Medicine, 550 First Ave, New York, NY *Corresponding author: Robert James Cerfolio New York University School of Medicine, 550 First Ave, New York, NY, Robert.Cerfolio@nyumc.org

3 ABSTRACT Introduction: Robotic lobectomy is an increasingly common surgical approach for anatomic lung resection. Over the last decade, robotic lobectomy has shown to be safe, with oncologic efficacy similar to lobectomy via thoracotomy or video-assisted thoracoscopic surgery (VATS). Comparative analysis between these modalities is an active area of investigation. While initially expensive, the costs of a robotic platform decrease as the number of operations performed increases, length of stay is shortened, and postoperative morbidity is reduced. Moreover, the added cost has value which is defined over long periods of time. Areas covered: The clinical technique and optimal conduct of lobectomy is explained in granular detail for all five types of lobectomies. The advantages and disadvantages of a robotic platform are analyzed, including a review of the recent literature. Expert Commentary: The number of robotic pulmonary resections performed has tripled in the past two years. Anticipated developments in robotic surgery include improvements in robotic training, continued refinement of robotic instrumentation, and additional adjunctive technologies. The overall costs of robotic surgery will decrease, in part, due to increasing competition as additional companies enter the market. KEYWORDS: lung cancer surgery, minimally invasive surgery, robotic lobectomy, thoracic surgery, video-assisted thoracoscopic surgery. 1. INTRODUCTION

4 Robotic surgery developed in the 1990s, as a number of surgical disciplines adopted the technology in an effort to improve upon established minimally invasive techniques [1]. However, less than 1% of anatomic resections in the United States were performed robotically until about Robotic thoracic surgery was designed to enhance the rigid instrumentation and suboptimal operative view provided by video-assisted thoracoscopic surgery (VATS). Robotic thoracic surgery provides the surgeon with greater control of the operation: wide instrument angulation and precision, a three-dimensional and magnified operative view, integrated access to adjunctive technologies, and more control over instrument exchange. Other advantages include the ability of the surgeon to sit, which may reduce injuries, provide better ergonomics, prolong careers, have improved education value, and allow a greater number of surgeons to perform a complete thoracic lymphadenectomy in a minimally invasive platform. Robotic surgery has its limitations, however, including added cost, absence of tactile feedback, and a learning curve for the surgeon and operating room team. To allow accurate communication among surgeons and to ensure proper outcome comparison, the American Association of Thoracic Surgeons Writing Committee has proposed a definition and nomenclature for robotic thoracic surgery [2]. A robotic thoracic operation is defined as a minimally invasive procedure that does not remove, spread, or lift any part of the chest or abdominal wall. A robotic portal (RP) operation is defined as an operation that uses ports only, and the port incision(s) is/are not generally enlarged at any time during the operation to be larger than the trocars in them, except for the removal of a specimen. Robotic operations that include a utility incision are defined as robotic-assisted (RA) procedures. After it was first reported in 2002, the number of robotic lobectomies has increased

5 dramatically [3]. Over 6,000 are now done in the US and 8,600 worldwide [4-6]. In 2009, only 1% of lobectomies performed in non-academic U.S. hospital utilized robots. By 2013, this percentage increased to 11% [7]. The adoption rate is more than doubled that seen with VATS. With increasing experience, a number of institutional studies have reported their short-term results with robotic lobectomy, establishing the approach as safe, feasible, and with oncologic outcome similar to open surgery, but with the perioperative morbidity of a minimally-invasive platform [7,8,9,10]. 2. INDICATIONS, CONTRAINDICATIONS, AND PREOPERATIVE ASSESSMENT Robotic pulmonary lobectomy may be considered in almost all patients who are evaluated for pulmonary resection. In the past, surgeons have favored thoracotomy for chest wall resections, believing the benefit of a minimally invasive approach is lost with rib resection [11]. These patients, it has been argued, should not be considered for robotic pulmonary lobectomy [12,13]. However, we have previously described successful lobectomy with chest wall resection, and therefore, chest wall involvement is not a strict contraindication [14]. A minimally invasive method of chest wall resection, which spares the chest wall musculature is safe and may decrease pain and morbidity compared to resection by rib-spreading thoracotomy [14,15]. Other previously reported contraindications for robotic lobectomy that are no longer prohibitive, include Pancoast tumors, vascular invasion, locally invasive T4 lesions, and tumors greater than >10 cm [7, 16]. We and others have operated on all of these pathologies using a robotic platform, with successful oncologic resection, and without conversion to thoracotomy or major complications. In addition, we have reported robotic sleeve lobectomy with a 0% 90-day

6 mortality and limited major morbidity [17]. Factors such as chemotherapy and/or radiation, prior thoracic surgery, and hilar nodal disease are not contraindications for experienced surgeons [17,18]. The preoperative evaluation of patients undergoing robotic lung resection is similar to patients undergoing planned VATS or open thoracotomy, including pulmonary function testing, cardiac stress testing in patients at risk of cardiovascular disease, and complete patient-specific staging [7,19]. Oncologic staging also involves a PET-CT scan in most patients and in select patients, either brain MRI or CT (for symptomatic patients or for patients with large central adenocarcinomas). Mediastinal assessment is completed by endobronchial and esophageal ultrasound-guided fine needle aspiration and/or cervical mediastinoscopy, depending on the tumor size and experience of the institution [7]. From a respiratory point of view, the same criteria used for VATS apply for robotic lobectomy. Predicted postoperative forced expiratory volume (FEV1) and/or diffusing capacity of the lungs for carbon monoxide (DLCO) greater than 40% of predicted is considered safe with acceptable morbidity and mortality [10]. Additional considerations for robotic proficiency are necessary when employing robotic techniques [20,21]. These include training the operating room personnel, consistent access to the robot to increase familiarity with the robot console and instruments, certification in cockpit awareness, robotic safety training, and simulator exercises. Surgical residents and thoracic fellows can be taught robotic techniques without compromising patient safety and outcomes [21]. The robot is uniquely apt in training with a console as it allows a matching visual field (same exact view as the operating surgeon), smooth transition of instruments, and the ability to review operative film. A series of virtual modules allow residents to gain proficiency with basic and

7 advanced robotic skills before operating on patients. Equally, the training console allows surgeons learning robotic surgery to be proctored by a robotic surgeon before they operate independently, thereby helping to reduce the learning curve. Despite the outstanding quality of visualization when a robotic system is used, it is important to mention the difference in viewing angle between open, VATS and robotic lobectomy. During an open lobectomy, the surgeon has two views of the hilum: the anterior or posterior direction. In VATS and robotic lobectomy, the camera approaches the hilum from an inferior direction. The relationships between the various anatomic structures do not change, however the perception and visibility need to be adjusted. As a consequence, the different viewing angle could affect the interpretation of the anatomy, especially at the beginning of the surgeon s learning curve. The learning curve for robotic surgery is steep and has been suggested by some surgeons to be at least 20 cases for a surgeon who has mastered VATS [4]. 3. SURGERY SETUP AND EQUIPMENT Robots can be anxiety-inducing for inexperienced robotic surgeons and anesthesiologists. Therefore, the set-up of the operating room is important. Some concepts specific to robotic operations include: Clear communication between members of the surgical team is important, as are carefully orchestrated moves. It is helpful for the team to develop a communication system to prevent iatrogenic injuries. Certain movements require particular attention to detail, such as when inserting robotic instruments, or when passing vascular staplers around fragile structures such as the pulmonary artery and pulmonary veins.

8 When initially placing the robotic instruments during thoracic surgery they should be inserted under direct vision. After the instruments are safely positioned, the surgeon can then use the memory feature of the robot to insert or change other instruments. This feature of the robot automatically inserts new instruments 1 cm proximal to the latest position. When using this feature, however, the surgeon must ensure that no vital structures, most commonly the lung, have moved into the path of the newly placed instrument. The only currently FDA-approved robotic system for lung surgery is the Da Vinci Surgical System (Sunnyvale, CA, USA), which offers both Xi and Si systems. All generations share the same general concept: the operating surgeon sits at a console some distance from the patient, who is positioned on an operating table in close proximity to the robotic unit with its four operating arms. Fine proprietary endowrist instruments are attached to the arms allowing a wide range of high-precision motions. Those motions are initiated and controlled by the surgeon s hand movements, via master instruments located at the console. The master instruments sense the surgeon s hand movements and translate them electronically into scaleddown micromovements to manipulate the small surgical instruments. Computer-assisted translation is able to filter out surgeon tremors. The newer Xi system lets the surgeon autonomously staple and use infrared technology. It features an overhead beam that lets the instrument arms rotate, allowing the robot greater directional flexibility in its approach to the patient. Compared to Si, Xi technology can allow for camera hopping which allows the camera to move ports and also has thinner instrument arms and longer instruments. Nonetheless, older models such as the Si are safe and effective for pulmonary resection. We have performed over 600 robotic lobectomies using an Si generation robot with only a single 90-day mortality [22].

9 3.1 Patient Positioning and Port Placement The patient is positioned in the lateral decubitus position. Before draping the patient, ensure that the patient can tolerate single lung ventilation and establish the exact placement of the double lumen endotracheal tube. Axillary rolls and arm boards are not necessary [23]. In the right chest, the robotic ports are inserted over the ninth rib and in the left chest, we have moved to the eighth rib. For the Si robot, the ports are placed as follows: robotic arm 3 (5- mm port) is 1 to 2 cm lateral to the spinous process of the vertebral body, robotic arm 2 (8 mm) is 10 cm medial to robotic arm 3, the camera port (we prefer the 12-mm camera) is 9 cm medial to robotic arm 2, and robotic arm 1 (12 mm) is right anteriorly above the diaphragm. The assistant port is triangulated behind the most anterior robotic port and the camera port, as inferiorly as possible without disrupting the diaphragm. For this operation we use a zero-degree camera. The camera or assistant port is insufflated with carbon dioxide to depress the diaphragm, compress the lung, and reduce bleeding. For a left-sided lobectomy, the port placement is a mirror image. The difference is that instead of robotic arm 2, robotic arm 3 is next to robotic arm 1. The ports are in the same locations, but are simply numbered differently. Once the ports are placed, the robotic system is brought in from the side of the operating table. There is important difference in room set-ups for the Si system compared to the Xi robotic system. Since the Xi robot is able to fully rotate on its boom, it is able to be brought in over the patient s side and not in over the head as has to be done with the Si. This allows the room to be set-up in a more consistent way, saves time, and ultimately leads to greater operating room

10 efficiency. In the Xi system, a laser guide helps to center the robot precisely on the patient s chest for efficient docking. 4. GENERAL CONCEPTS For a right-handed surgeon, robotic arm 2 is always the left hand and a blunt instrument, such as a Cadiere forceps, is placed in this arm. Robotic arm 1 is always the right hand and we prefer a bipolar thoracic dissector. It is helpful to place a vessel loop under the vessel to be stapled to elevate it while the stapler is passed under it. There are three ports that a stapler may be placed through the access port, robotic arm 1, or robotic arm 2. Based on the current commercially available design, gray or white vascular staplers require a 12 mm port while the green loaded stapler, often used for the bronchus, requires a 15 mm port. Our preference is to remove the trocar, leaving it docked to the robotic arm, and then place the stapler through the skin incision. A pre-rolled sponge can be used to absorb blood from the operative field or to help blunt dissection to improve visibility. Significant adhesions may be initially dealt with via the assistant port using VATS techniques until the surgeon is able to safely place all the robotic instruments. The camera used in robotic surgeries gives the surgeon the key advantage of changing the view for greater than that achieved in either open surgery or VATS [7]. We prefer a zero-degree camera because we believe it has less intercostal nerve neuralgia as well as more room for the bedside assistant. Five types of lobectomy can be performed, one for each of the lung lobes. As in any surgical procedure, there are several described techniques to robotic lobectomy. Louie et al. and Anderson et al. described a three-arm robotic lobectomy with a utility port [24, 25]. Park et al.

11 reported a three arms technique with two thoracoscopic ports and a 4 cm utility incision [26]. Gharagozloo et al. reported a hybrid technique with three robotic arms, (positioned at the 8th, camera, 6th and 5th intercostal space); in this case the surgeon used a robotic approach for hilar structures dissection, then the platform was removed and he returned to the operating table to complete the operation [27]. Jang et al. used a utility incision at the fifth intercostal space [28]. Ninan and Dylewski reported a three arms technique using the same intercostal space for all ports (the 5th or 6th) and a utility port over the 11th rib [29]. Veronesi et al. reported the safety of a 4-arm robotic assisted (not completely portal) lobectomy, using a 3- to 4-cm access incision as used by VATS surgeons [30]. 5. MEDIASTINAL LYMPH NODE DISSECTION Robotic surgery is feasible and safe for mediastinal and hilar lymph node dissection [27]. It is helpful to dissect mediastinal and hilar lymph nodes before lobectomy to both evaluate the lymph nodes and to access the bronchus and arterial and venous branches [7]. Right side: The inferior pulmonary ligament is divided and the lymph nodes at stations 8 and 9 are removed. The most posterior arm, robotic arm 3, is used to retract the lower lobe anteriorly and medially to remove lymph nodes at station 7. It is also used to retract the upper lobe inferiorly during dissection of stations 2R and 4R, which clears the space between the superior vena cava anteriorly, the esophagus posteriorly, and the azygos vein inferiorly. Left side: The inferior pulmonary ligament is divided to remove the station 9 lymph node, and then the station 8 nodes are removed. Station 7 is accessed lateral to the esophagus, between the lower lobe bronchus and the inferior pulmonary vein. During this process, robotic arm 3 is used to retract the lower lobe medially and anteriorly. Absence of the lower

12 lobe helps with dissecting level 7 from the left. Finally, robotic arm 3 is wrapped around the left upper lobe and presses it inferiorly so the surgeon can dissect lymph nodes at stations 5 and 6. While working in the aorto-pulmonary window, the surgeon should take care to avoid injuring the left recurrent laryngeal nerve. The presence of the aortic arch typically prevents Station 2L from being accessed during left sided mediastinal lymph node dissection, but the 4L lymph node is frequently removed. 6. THE FIVE LOBECTOMIES 6.1 Right upper lobectomy A posterior approach to right upper lobectomy is recommended. The lung is not flipped or turned, and all structures are taken from the back. The order of ligation or removal is: 1. Station 9 and 8 lymph nodes, then station 7 2. Station 11 lymph nodes between the right upper lobe and bronchus intermedius are removed 3. The post fissure is then stapled 4. Small posterior ascending right upper lobe pulmonary artery branch 5. Right upper lobe bronchus 6. Anterior apical pulmonary artery trunk 7. Right upper lobe vein 8. Anterior fissure 6.2 Right middle lobectomy To expose the hilum, robot arm 1 is used to retract the right middle lobe laterally and posteriorly.

13 The bifurcation between the right upper and middle lobar veins is developed by dissecting it off the pulmonary artery lying beneath, and the right middle lobe vein is encircled and divided. If not complete, the fissure between the right middle and lower lobes is divided anteriorly to posteriorly. The surgeon should avoid transecting the right lower lobe s segmental arteries. The right middle lobe bronchus which runs from left to right in the fissure, is isolated and the level 11 lymph nodes from around it dissected. The surgeon should take care to avoid the right middle lobar artery directly behind the right middle lobe while encircling and dividing it. The surgeon should continue to divide the fissure posteriorly until the branches to the superior segment are identified, and then should isolate and divide the one or two right middle lobar segmental arteries. The stapler is passed posteriorly to anteriorly to allow for greater working distance and facilitate stapling of the middle lobar structures. The fissure between the right upper and middle lobes is divided. 6.3 Right lower lobectomy The inferior pulmonary ligament is divided to the level of the inferior pulmonary vein, and the bifurcation of the right superior and inferior pulmonary veins is dissected out. The right middle lobar vein should be identified to avoid accidental transection. A subadventitial plane is established on the ongoing pulmonary artery. If the major fissure is incomplete, it is divided. The superior segmental artery is identified, isolated, and divided. The right middle lobe arterial branch is also identified. The common trunk to right lower lobe basilar segments can be removed, so long as this does not compromise any middle lobar segmental arteries. If it does, the dissection may have to extend further distally for a safe division. The inferior pulmonary vein is

14 then divided. While taking care to visualize the right middle lobar bronchus crossing from left to right, the surgeon should isolate the right lower lobe bronchus. As usual, dissect the surrounding lymph nodes and divide the bronchus. If the right middle lobe bronchus is in danger of getting compromised, the surgeon can ask the anesthesiologist to hand-ventilate the right lung to confirm middle lobe expansion. 6.4 Left upper lobectomy A posterior approach is also favored in a left upper lobectomy. The order of takes is: 1. Station 9, 8, and 7 lymph nodes are dissected. 2. Station 10 and 11 nodes off the pulmonary artery in the back. The posterior segmental artery to the left upper lobe and superior segment artery to the left lower lobe are identified posteriorly. 3. The post-fissure is exposed during this process and stapled. 4. Posterior segmental artery 5. Lingular artery 6. Left upper lobe vein 7. Left upper lobe bronchus if the anterior apical trunk is not seen 8. Anterior apical pulmonary trunk 6.5 Left lower lobectomy The inferior pulmonary ligament is divided to the level of the inferior pulmonary vein, and robotic arm 3 used to posteriorly reflect the lower lobe. The bifurcation of the left superior and

15 inferior pulmonary veins is dissected. Robotic arm 3 is used to anteriorly reflect the lung. From this view, the posterior ascending arteries to the left upper lobe are frequently visible. The superior segmental artery should be identified, isolated, and divided. If no middle lobar segmental arteries are not compromised, the common trunk to left lower lobe basilar segments can be taken; otherwise, the dissection is extended further distally for safe division. The fissure is divided if it is not complete, in order to expose the ongoing pulmonary artery to the lower lobe. After dividing the arterial branches, the lung is again reflected posteriorly, and the inferior pulmonary vein divided. The left lower lobe bronchus is isolated, the surrounding lymph nodes dissected as usual, and the bronchus divided. In a left lower lobectomy, it may be easier to wait until after resection before targeting the subcarinal space to remove level 7 lymph nodes. 6.6 Specimen removal / Conclusion of operation The pulmonary artery should be far away from the drop zone for the specimen, as it can be injured in this process. Robotic arm 3 holds the specimen before the bag is inserted via the assistant port. Robotic arms 1 and/or 2 are used to ensure the bag is deployed under the trocar and opened in the right direction. Robotic arm 3 drops the resected specimen into the bag and next grasps the far lip of the bag so that the bag does not spin. Meanwhile, robotic arms 1 and 2 place the specimen in the bag. The robotic arms should not be inside the bag. Normal saline is used to irrigate the chest only if needed and insufflation to check the presence of air leaks. Hemostasis is confirmed, and via the anterior-most port (robotic arm 1 in the right chest or robotic arm 2 in the left chest), a 20 Fr chest tube is placed. Under direct vision with insufflation discontinued, the robotic arms are removed to confirm that there is no bleeding.

16 The camera port is removed, the robot undocked and pushed away from the patient s bed, and the bag removed from the body, typically after posteriorly enlarging the assistant non-robotic port to avoid injuring the diagram. These techniques avoid all diaphragmatic fibers. A #5 ethibond suture is used to secure the chest tube. After the break is removed from the table, the fascial layer in the 12 mm ports is closed with 0 vicryl suture, and the skin closed in a knotless subcuticular fashion with 3-0 vicryl suture. 7 POSTOPERATIVE MANAGEMENT Management of patients who undergo robotic lobectomy is similar to that of patients who undergo VATS lobectomy. The key to post-operative pain is to prevent it pre-emptively using multi-modality agents prior to injury. Our current protocol is to employ gabapentin 900 mg and 1000 mg of Tylenol by mouth with a sip of water just prior to surgery. After placement of the first port and scope, we then use a paravertebral block with lidocaine or Experal from ribs 5 to 12, created a 2-3 ml subpleural pocket under direct vision, and then a field block around each port after port placement. Robotic lobectomy patients do not go to the intensive care unit, but directly to the floor, and they generally fare well with analgesia by mouth. If an air leak is present, when it resolves, chest tubes are removed at outputs of up to 450 ml/day (patient-dependent). Patients are discharged on the second or third postoperative day. The same complications of open or VATS lobectomy can also occur with robotic lobectomy. When comparing VATS lobectomy to robotic lobectomy, Louie et al found that both types of procedures have similar blood loss, operative time, and length of stay, but robotic

17 lobectomy has the additional advantage of reduced time of narcotic use and faster return to activities [24]. Robotic lobectomy performed in high-volume centers has been associated with significantly shorter length of stay [31]. This could be attributed to the ability of high volume centers to standardize patient preparation, robot docking, and surgical procedures, all of which may play a role in reducing operating times and complications. Novelli et al. reported that in their Italian hospital, robotic lobectomy was associated with reduced length of stay both in their hospital and intensive care unit, as well as fewer postoperative examinations, and reduced use of painkillers and other drugs [32]. 8 ESTABLISHING VALVE FOR ROBOTIC LOBECTOMY Despite its ascendance in surgical practice, robotic surgery has its challenges. The foremost, is the significant capital outlay for purchasing and maintaining robot systems. The various costs associated with robotic surgeries include the cost of the robot, limited-use instruments, costs of depreciation, and costs of training the surgical team. The annual maintenance costs are approximately 10% of the initial capital investment. Each new robot system costs about $2 million, with a range of $1 million to $2.5 million [33]. The robots also come with consumables, which include instruments attached to the robotic arms that according to da Vinci protocol, can only be sterilized and reused a certain number of times before being discarded, regardless of how much time they were used in the operation. The cost of training the surgeon and surgical team also makes robotic lobectomy expensive. Simulators to help the surgeon gain familiarity with the robots cost between $35,000 and $158,000 [34]. The surgeon-in-training progresses from the simulator to a dual console to

18 become proficient in switching the robotic arms. A second console may also be purchased, so that an expert robotic surgeon can teach a trainee in real-time, but these further increases the total cost to around $3 million [35]. All this leads to a robotic lobectomy costing $3,000 to $5,000 more than a VATS operation, mostly as a result of robot-specific supplies and depreciation [36,37]. The greatest opportunity for reducing the cost of robotic lobectomy is to decrease the length of the operation and supply costs. In order to establish overall value for robotic lobectomy, clinical outcomes must balance financial cost. Robotic lobectomy is equivocal to VATS in regards to perioperative morbidity, including blood loss, blood transfusion, air leak, chest tube duration, length of stay, and mortality when compared to traditional open technique [38]. Cerfolio et al. reported median blood loss of 50cc per lobectomy [22]. Vascular injury is rare event, and when it does occur, it can occasionally be repaired without converting to a thoracotomy. In a propensity-matched analysis, Oh et al. demonstrated comparative analysis of perioperative clinical outcomes from elective RL, VATS, and open lobectomy [39]. When comparing a total of 2775 patients in each group, the operative time required to perform robotic lobectomy (275 minutes) was slightly longer, but statistically significant when compared to open (235 minutes) or VATS lobectomy respectively (247 minutes). Considering the data of this study spans over 4 years (from ) one could assume that the prolonged OR time is based on evolving technology (transition from one generation console to another) and the learning curve of the surgeons. In a multicenter retrospective study including 325 patients, Park et al. reported that both conversion rates (11% vs 5.7%) and median operative times (210 minutes vs 195 minutes) were lower after the first 50 cases at each center [12]. We have been able to reduce our operating times to a median of 136

19 minutes (range, ), nearly twice as fast than the data provided in the propensity matched analysis [40]. Hospital length of stay is another important metric when assessing the value of an operation. Oh et al. reported median hospital length of stay of 5 days for robotic lobectomy, 6 days for VATS, and 7 days after an open operation [39]. In their multi-institutional cohort of robotic lobectomy, Park et al. reported median length of stay of 5 days and Cerfolio et al. reported a median length of stay of 3 days [12,40]. Lymph nodes are well known predictors of oncologic outcome and survival. Appropriate lymph node dissection is important not only for accurate staging, but also for the potential oncologic benefit. From a technical point of view, a robotic lymph node dissection is facilitated by the precision of the wristed instruments. In a retrospective review by Cerfolio et al., 10.9% of all patients were upstaged after robotic lobectomy: 6.6% were upstaged owing to hilar (pn1) disease and 4.3% were upstaged owing to mediastinal (pn2) disease [40]. Compared with prior series, this rate of overall nodal upstaging was similar to VATS (8% 12%), but lower than thoracotomy (20% 25%) [29]. In a multicenter review of 325 patients, Park et al. reported comparable perioperative morbidity similar to a VATS lobectomy, with a low rate of major morbidity (3.7%) and inhospital mortality (0.3%) [12]. In total, 76% of the patients had pathologic stage I disease (IA, 176; IB, 72), and in 68 (21%) patients the severity of disease was upstaged. It is theorized that robotic lobectomy facilitates a thorough dissection of mediastinal lymph nodes, which increases the accuracy of staging, ultimately leading to more optimal adjuvant therapy. The authors reported a median tumor size of 2.2 cm (range, cm), and the median number of lymph node stations dissected was 5 (range, 2-8). From the entire cohort, 19% patients had metastatic

20 nodal disease, and 67 patients received adjuvant cytotoxic chemotherapy. Conversion to thoracotomy was required in 8%, the majority of which was to control minor bleeding. Regarding long term outcomes, after a median follow-up of 27 months, 32 (10%) patients had had recurrence, and 25 died of their disease. The majority (72%) of detected recurrences were distant, and 28% were locoregional. The overall 5-year survival for the group was 80% and stage specific survival at 5 years was as follow: 91% for stage IA, 88% of stage IB, 49% for stage II. According to the authors, the excellent 5-year survival in pathologic stage I (IA, 91%; IB, 88%) was likely related to the fact that the median tumor size was small (2.2 cm). Perhaps the best example of long-term value was an updated follow-up to this series was reported by Cerfolio et al. in 2017, representing the largest series with the longest follow-up after robotic lobectomy for NSCLC [40]. In review of 1330 patients after robotic lobectomy, shortterm outcomes confirmed the safety of the procedure: conversion to thoracotomy was required in 9%, median length of stay was 3 days, and major morbidity occurred in 8%, with a low 30-day (0.2%) and 90-day (0.5%) mortality rate. The authors reported a stage-specific 5-year survival of 83% for patients with stage IA NSCLC and 77% for patients with stage IB NSCLC. The cumulative incidence of metastasis was 15%. The stage-specific survival was higher then in any other reported series either open or minimal invasive series. The question is why: is this because the series is only a surrogate of other co-founders of excellence such as tumor conference, more experienced surgeons and surgical teams, or just better staging? If a platform provides better staging by identification of N1 or N2 disease, and therefore, more patients receive adjuvant therapy, this may improve survival. In addition, a minimally invasive approach may be less immuno-compromising, which may help protect against the development of metastases. These

21 concepts are theoretically until they are proven in a prospective randomized trial. Promising long-term survival post robotic lobectomy has been observed in a number of institutional series. Onaitis et al. reported 2-year overall survival of 80% and stage-specific survivals of 85% for stage I and 77% for stages II and higher in a cohort of 500 patients undergoing VATS lobectomy for clinical early-stage disease (41). Goldstraw et al. reported 5- year overall survivals of 73% and 58% for stages IA and IB, respectively, and 46% and 36% for stages IIA and IIB (42). A number of database reviews have reported comparisons of the surgical approach to lobectomy. Addressing robotic, VATS, and open lobectomy, DeCamp et al. compared an impressive 62,206 patients in 1,215 hospitals from the National Cancer Database [43]. Their propensity-match cohort study revealed similar outcomes between the two minimally invasive modalities, both of which were superior to an open procedure in terms of perioperative morbidity, but not in re-admission rate or mortality at 30 or 90-days. The review, however, did not have a method for adjusting for surgeon expertise and experience and was limited by the metrics reported to the database. Another database review of the Society of Thoracic Surgeons General Thoracic Surgery (STS-GTS) database comparing outcomes of VATS and robotic lobectomy for early-stage NSCLC was completed by Block et al., involving over 1,200 robotic and 12,000 VATS lobectomies from 2009 to 2013 [44]. The robotic cohort represented a relatively older population with a greater number of comorbidities. Despite longer operating times in a robotic operation (median of 186 minutes versus 173 minutes), there were no differences in all quality metrics, including complications, nodal upstaging, and 30-day mortality. A higher portion of robotic operations had a length of stay less than four days compared to the VATS group. In the

22 discussion, the authors conclude that robotic and VATS lobectomy are equivalent, and that if thoracic surgeons currently performing thoracotomy are uncomfortable with their skill in VATS, a robotic platform may allow a more accessible minimally invasive approach. In addition, a yet quantified value of the robot lies in the ability to have surgeons seated and not standing for hours a day. Surgery is a physically demanding event and a number of studies have confirmed the substantial risk of stress injury [45]. Another advantage of robotic surgery is its educational value. An interactive screen allows the experienced surgeon to draw on the screen and display optimal hand movements. In addition, a duel console system allows the attending to easily switch the controls to a junior attending, fellow, or resident and to insert interactive arrows on the three dimensional console that teach. Finally, the simulators for robotics are fair advances to other systems. 9 CONCLUSION Robotic lobectomy for lung cancer provides favorable short-term and long-term outcomes. Robotic lobectomy can achieve an appropriate oncologic resection via a minimally invasive platform that reduces perioperative morbidity and mortality. Robotic lobectomy also offers certain special benefits beyond VATS, which we believe translates to improved patient outcomes. We have previously reported our experience in transitioning to a robot program [46]. The initial enthusiasm of surgeons needs to be matched with institutional support, as building a robotic surgery practice is a team effort. Some of the key sequences in a becoming a robotic surgeon includes training a trustworthy bed-side assistant, mentorship and proctorship by a trained robotic surgeon, and establishing a dedicated robotic operating room team. Challenges of robotic lobectomy include its expenses, but the cost is expected to decrease

23 with market competition. The significant investment required in training is also a challenge. The need for well-trained team members who are familiar with each other and with the operation is not to be taken lightly for robotic lobectomy. Systematic learning and executing of the procedure is recommended. The relative value of robotic lobectomy versus VATS remains an area of active investigation. We believe robotics will be the future of thoracic surgery. 10 EXPERT COMMENTARY Robotic surgery is the clear minimally invasive platform of the future. It provides advanced novel views of the operative field such as the on-laying of three-dimensional anatomy over the actual operative field, the ability to immuno-fluoresce and/or image nerves, vessels and even muscle cells. This visualization is accomplished by placing a robotic camera into the operative field and giving various intra-venous materials that allows the surgeon to view tissue by fluorescence. Indigotine (indigo carmine, ICG) is the fluorescent agent of choice we currently use to identify vascular anatomy. With ICG the surgeon sees vascularized tissue and it lights up with a vivid green. In the future, robotics will be able to light up or immuno-fluoresce various types of tissues. It may be able to be used for specific antigens, like thymic antigens, so that by using the da Vinci monitor with a specialized robotic camera, the thoracic surgeon can differentiate between thymus gland and surrounding fat. Fluorescence can also help visualize any small pulmonary nodules embedded in pulmonary parenchyma as we have using for the past several years, by injecting ICG via the bronchoscope into nodules. A computerized system will enable the surgeon to view smaller and more subtle defects or even early cancers in the operative

24 field. It may also be able to identify sentinel lymph nodes. In the future, computerized systems and robotic technology will be able to differentiate cancer from benign tissue. The major obstacle to robotic technology is cost. The capital of robotic lobectomy is high. Its costs include the robots themselves, maintenance, and other software and tools used for the procedure that need to be continuously replaced. It is important to show value for any added cost, and the value has to be for the patient or surgeon. In addition, research that continues to show long-term oncologic effectiveness is needed to justify the initial investment of robots and training and the ongoing costs of maintenance. Another obstacle besides cost is the training required to ensure that these new technologic advancements are implemented in a safe fashion for patients. Robotic lobectomy lacks a systematic approach in its teaching and training. The need for highly-trained team that works well with each other is critical, because the success of robotic lobectomy depends upon thorough training and preparation of the surgeon and the team. A standardized approach to learning is needed. Currently, the lack of such a nationwide systematic training program, coupled with a long learning curve for robotic surgery, is a challenge in the field. This is an area that needs research and future direction, because so far, no method has been established as the optimal way to train surgeons in robotic lobectomy. We are now four years into the American Association of Thoracic Surgery Training program and using surgical specialties to mandate set and formalized training of residents and attending surgeons in robotic surgery. It will be helpful to track the short-term and long-term results of established pulmonary robotic surgery programs at highvolume centers. Thoracic surgeons newly trained in robotic procedures are also encouraged to make note of the results of their robotic lobectomy procedures and report them to not only learn

25 more about the techniques and outcomes of robotic lobectomy, but also to add to the literature on the robotic lobectomy teaching and training. 11 FIVE-YEAR VIEW Robotic lobectomy is an evolving technology. Multiple studies have established its safety and efficacy, so we anticipate continued adoption of this technology by thoracic surgeons. The robot is an enticing technology for surgeons performing thoracotomy for lobectomy and as robotic technology improves and costs decrease, we believe robotic lobectomy will provide surgical and clinical benefit beyond VATS. Robotic lobectomy has the potential to become the standard of care intervention for non-small cell lung cancer. Part of the excitement of robotic surgery is the continued development of the technology it is not a stagnant tool, but will continue to adapt and adjust to operative demands. Over the next five years we anticipate the introduction of new models of robotic surgical systems, including those with new and different instruments, robotics tailored to specific surgeries, and systems with single-port technology. Equally, we expect the continued development of new adjunctive technologies that will augment the capabilities of the robotic platform. Robotic technology is an evolving field, one that will continue to translate to greater clinical benefit for our patients. KEY ISSUES Robotic lobectomy is increasingly used in the treatment of non-small cell lung cancer. It is an alternative to open thoracotomy and video-assisted thoracoscopic surgery (VATS). It has similar short and long-term outcomes to VATS, but is more expensive because the

26 price of robotic lobectomy must include the cost of the robot, additional instruments used in robotic lobectomy, maintenance fees, depreciation, and costs for training. Systematic training and teaching is necessary for surgeon expertise and for developing a robotic operative team. Further studies that show the value of robotic lobectomy are needed to balance the Funding significant financial cost. This manuscript has not been funded. Declaration of interest R Cerfolio serves as a consultant for Intuitive, C-SATS, Bovie, Ethicon, Covidien/Medtronic, Community Health Services, Davol/Bard, Myriad Genetics, KCI, and Verb Medical. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed. Peer reviewers on this manuscript have no relevant financial or other relationships to disclose.

27 References Papers of special note have been highlighted as either of interest ( ) or of considerable interest ( ) to readers. 1. Veronesi G. Robotic lobectomy and segmentectomy for lung cancer: results and operating technique. J Thorac Dis, 7, S (2015) 2. Cerfolio R, Louie BE, Farivar AS, et al. Consensus statement on definitions and nomenclature for robotic thoracic surgery. J Thorac Cardiovasc Surg, 154, (2017) *Nomenclature and definitions for robotic thoracic surgery 3. Melfi FM, Menconi GF, Mariani AM et al. Early experience with robotic technology for thoracoscopic surgery. Eur J Cardiothorac Surg, 21, (2002) 4. Suda T. Transition from video-assisted thoracic surgery to robotic pulmonary surgery. J Vis Surg, 3, 55 (2017) 5. Morgan JA, Ginsburg ME, Sonett JR et al. Advanced thoracoscopic procedures are facilitated by computer-aided robotic technology. Eur J Cardiothorac Surg, 23, 883-7; discussion 887 (2003) 6. Ashton RC, Jr., Connery CP, Swistel DG, et al. Robot-assisted lobectomy. J Thorac Cardiovasc Surg, 126, (2003) 7. Linsky P, Wei B. Robotic lobectomy. J Vis Surg, 3, 132 (2017) 8. Louie BE, Wilson JL, Kim S et al. Comparison of Video-Assisted Thoracoscopic Surgery and Robotic Approaches for Clinical Stage I and Stage II Non-Small Cell Lung Cancer Using The Society of Thoracic Surgeons Database. Ann Thorac Surg, 102, (2016)

28 9. Flores RM, Alam N. Video-assisted thoracic surgery lobectomy (VATS), open thoracotomy, and the robot for lung cancer. Ann Thorac Surg, 85, S (2008) 10. Adams RD, Bolton WD, Stephenson JE, et al. Initial multicenter community robotic lobectomy experience: comparisons to a national database. Ann Thorac Surg, 97, ; discussion (2014) 11. Yendamuri S, Nwogu CE, Demmy TL. Thoracoscopic lobectomy with chest wall resection after neoadjuvant therapy. Innovations (Phila), 4, 36-8 (2009) 12. Park BJ, Melfi F, Mussi A et al. Robotic lobectomy for non-small cell lung cancer (NSCLC): Multi-center resistry study of long-term oncologic results. J Thorac Cardiovasc Surg, 143, (2012) 13. Ambrogi MC, Fanucchi O, Melfi F, Mussi A. Robotic surgery for lung cancer. Korean J Thorac Cardiovasc Surg, 47, (2014) 14. Cerfolio RJ, Bryant AS, Minnich DJ. Minimally invasive chest wall resection: sparing the overlying, uninvolved extrathoracic musculature of the chest. Ann Thorac Surg, 94, (2012) 15. Wei B. CR, Gillaspie E.A., et al. Minimally Invasive Approaches to Chest Wall and Superior Sulcus Tumors. In: Atlas of Minimally Invasive Surgery for Lung and Esophageal Cancer. Wang J., KFM (Ed. (Springer, Dordrecht, 2017) 16. Wei B. CR. Robotic Lobectomy. In: The SAGES Manual of Robotic Surgery. Patel A., OD (Ed. (Springer, Cham, 2017) **Additional details for techniques on robotic lobectomy

29 17. Cerfolio RJ. Robotic sleeve lobectomy: technical details and early results. J Thorac Dis, 8, S223-6 (2016) 18. Wei B, Eldaif SM, Cerfolio RJ. Robotic Lung Resection for Non-Small Cell Lung Cancer. Surg Oncol Clin N Am, 25, (2016) 19. Kaiser LR, Jamieson GG, Thompson SK. Operative thoracic surgery (CRC Press, Boca Raton, 2016) 20. Ramadan OI, Cerfolio RJ, Wei B. Tips and tricks to decrease the duration of operation in robotic surgery for lung cancer. J Vis Surg, 3, 11 (2017) 21. Cerfolio RJ, Cichos KH, Wei B, et al. Robotic lobectomy can be taught while maintaining quality patient outcomes. J Thorac Cardiovasc Surg, 152, (2016) 22. Cerfolio RJ, Bryant AS, Skylizard L, et al. Initial consecutive experience of completely portal robotic pulmonary resection with 4 arms. J Thorac Cardiovasc Surg, 142, (2011) 23. Cerfolio RJ, Steenwyk BL, Watson C et al. Decreasing the Preincision Time for Pulmonary Lobectomy: The Process of Lean and Value Stream Mapping. Ann Thorac Surg, 101, (2016) 24. Louie BE, Farivar AS, Aye RW, Vallieres E. Early experience with robotic lung resection results in similar operative outcomes and morbidity when compared with matched video-assisted thoracoscopic surgery cases. Ann Thorac Surg, 93, ; discussion (2012) 25. Anderson CA, Hellan M, Falebella A, Lau CS, Grannis FW, Kernstine KH. Roboticassisted lung resection for malignant disease. Innovations (Phila). 5, (2007)

30 26. Park BJ, Flores RM, Rusch VW. Robotic assistance for video-assisted thoracic surgical lobectomy: technique and initial results. J Thorac Cardiovasc Surg, 131, 54-9 (2006) 27. Gharagozloo F, Margolis M, Tempesta B, et al. Robot-assisted lobectomy for early-stage lung cancer: report of 100 consecutive cases. Ann Thorac Surg, 88, (2009) 28. Jang HJ, Lee HS, Park SY, et al. Comparison of the early robot-assisted lobectomy experience to video-assisted thoracic surgery lobectomy for lung cancer: a singleinstitution case series matching study. Innovations (Phila), 6, (2011) 29. Ninan M, Dylewski MR. Total port-access robot-assisted pulmonary lobectomy without utility thoracotomy. Eur J Cardio-Thorac Surg, 38, (2010) 30. Veronesi G, Galetta D, Maisonneuve P et al. Four-arm robotic lobectomy for the treatment of early-stage lung cancer. J Thorac Cardiovasc Surg, 140, (2010) 31. Tchouta LN, Park HS, Boffa DJ, et al. Hospital Volume and Outcomes of Robot-Assisted Lobectomies. Chest, 151(2), (2017) 32. Novellis P, Alloisio M, Vanni E, et al. Robotic lung cancer surgery: review of experience and costs. J Vis Surg, 3, 39 (2017) *Review of costs associated with robotic lobectomies 33. Turchetti G, Palla I, Pierotti F, et al. Economic evaluation of da Vinci-assisted robotic surgery: a systematic review. Surg Endosc, 26, (2012) 34. Abboudi H, Khan MS, Aboumarzouk O et al. Current status of validation for robotic surgery simulators - a systematic review. BJU Int, 111, (2013)

31 35. Hernandez JD, Bann SD, Munz Y et al. Qualitative and quantitative analysis of the learning curve of a simulated surgical task on the da Vinci system. Surg Endosc, 18, (2004) 36. Deen SA, Wilson JL, Wilshire CL et al. Defining the cost of care for lobectomy and segmentectomy: a comparison of open, video-assisted thoracoscopic, and robotic approaches. Ann Thorac Surg, 97, (2014) 37. Swanson SJ, Miller DL, McKenna RJ, Jr. et al. Comparing robot-assisted thoracic surgical lobectomy with conventional video-assisted thoracic surgical lobectomy and wedge resection: results from a multihospital database (Premier). J Thorac Cardiovasc Surg, 147, (2014) 38. Adams RD, Bolton WD, Stephenson JE, Henry G, Robbins ET, Sommers E. Initial multicenter community robotic lobectomy experience: comparisons to a national database. Ann Thorac Surg, 97, ; discussion (2014) 39. Oh DS, Reddy RM, Gorrepati ML, et al. Robotic-Assisted, Video-Assisted Thoracoscopic and Open Lobectomy: Propensity-Matched Analysis of Recent Premier Data. Ann Thorac Surg, 104, (2017) 40. Cerfolio RJ, Ghanim AF, Dylewski M, et al. The long-term survival of robotic lobectomy for non-small cell lung cancer: A multi-institutional study. J Thorac Cardiovasc Surg, 155, (2018) **The largest series with the longest follow-up of robotic lobectomy for non small cell lung cancer