Demonstration of transoral robotic supraglottic laryngectomy and total laryngectomy in cadaveric specimens using the Medrobotics Flex System

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1 ORIGINAL ARTICLE Demonstration of transoral robotic supraglottic laryngectomy and total laryngectomy in cadaveric specimens using the Medrobotics Flex System Emily Funk, BA, 1 David Goldenberg, MD, 2 Neerav Goyal, MD, MPH 2 * 1 The Pennsylvania State University, College of Medicine, Hershey, Pennsylvania, 2 Department of Surgery, Division of Otolaryngology Head and Neck Surgery, The Pennsylvania State University, College of Medicine, Hershey, Pennsylvania. Accepted 11 January 2017 Published online 16 March 2017 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. Current management of laryngeal malignancies is associated with significant morbidity. Application of minimally invasive transoral techniques may reduce the morbidity associated with traditional procedures. The purpose of this study was to present our investigation of the utility of a novel flexible robotic system for transoral supraglottic laryngectomy and total laryngectomy. Methods. Transoral total laryngectomy and transoral supraglottic laryngectomy were performed in cadaveric specimens using the Flex Robotic System (Medrobotics, Raynham, MA). Results. All procedures were completed successfully in the cadaveric models. The articulated endoscope allowed for access to the desired surgical site. Flexible instruments enabled an atraumatic approach and allowed for precise surgical technique. Conclusion. Access to deep anatomic structures remains problematic using current minimally invasive robotic approaches. Improvements in visualization and access to the laryngopharyngeal complex offered by this system may improve surgical applications to the larynx. This study demonstrates the technical feasibility using the Flex Robotic System for transoral robotic supraglottic laryngectomy and total laryngectomy. VC 2017 Wiley Periodicals, Inc. Head Neck 39: , 2017 KEY WORDS: flexible endoscope, transoral robotic surgery, laryngectomy, minimally invasive surgery, head and neck cancer INTRODUCTION Malignancy of the larynx poses a unique challenge in management related to anatomic limitations to surgical approaches and involvement of crucial functional structures controlling speech, swallowing, and breathing. Advanced laryngeal cancer is historically associated with the morbidities and communication handicaps related to primary treatment with an open total laryngectomy. Organ preservation with chemoradiotherapy offers comparable survival rates, but is associated with high toxicity and poor functional outcomes. 1 5 Endoscopic approaches using transoral laser microsurgery (TLM) utilize natural body openings for direct access to laryngeal structures while avoiding damage to surrounding external anatomy, but can be technically difficult and are limited in their indications. 6 8 Advances in the field of robotics have expanded the applications of transoral approaches to head and neck cancers. Over the past decade, the use of the da Vinci robotic system (Intuitive, Sunnyvale, CA) in otolaryngologic procedures has *Corresponding author: N. Goyal, Division of Otolaryngology Head and Neck Surgery, The Pennsylvania State University College of Medicine, 500 University Drive, H091, P. O. Box 850, Hershey, PA ngoyal1@hmc. psu.edu Declaration of Conflicting Interests: The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. been widely studied, gaining acceptance and rapid popularity as a minimally invasive technique for procedures that have previously been limited to open approaches The use of the robotic system provides tremor filtration, scaled movements, and wristed instruments that facilitate precise manipulation of delicate tissues. 18,19 The safety and feasibility of transoral robotic surgery (TORS) has been well demonstrated, with numerous studies showing excellent oncologic and functional outcomes, including limited need for tracheotomy, more rapid postoperative recovery of swallowing and phonation, and decreased hospital stays. 12,13,20 23 Inadequate exposure and access is a major hurdle using the da Vinci system, and can be attributed to multiple factors: (1) the introduction of robotic arms into the narrow funnel created by the oral cavity, pharynx, and larynx can lead to collisions of the arms with one another or with surrounding anatomy; (2) advancing the rigid endoscope and instruments is prohibited in patients with limited transoral access; and (3) instrument size in the restricted space of the surgical field may limit adequate manipulation of instrumentation. 19,24 26 Access can be further limited by individual patient anatomy; thus, patient selection and preoperative evaluation is essential. 26 A newly developed device, the Medrobotics Flex Robotic System (Medrobotics, Raynham, MA), received Food and Drug Administration approval for head and neck surgery in The Flex system utilizes a joystick navigation system to advance a chip-on-tip flexible endoscope in a nonlinear, snake-like approach. The size and 1218 HEAD & NECK DOI /HED JUNE 2017

2 FLEX ROBOTIC LARYNGECTOMY flexibility of this robotic platform provides access to and maneuverability within narrow, restrictive areas via the transoral approach. Small, flexible instruments follow the path of the endoscope, in contrast to the rigid instruments of other systems. These improvements address many of the limitations of current robotic technology used in TORS. Presently, this robotic platform has been successful in cadaveric applications to base of tongue resection, 27,28 tonsillectomy, 27 epiglotectomy, 28,29 posterior cordectomy, 29 vocal cord resection, 28 and complete nasopharyngectomy. 30 The present study is a cadaveric trial that demonstrates the feasibility of the Medrobotics Flex System for its use in transoral supraglottic laryngectomy and total laryngectomy. We describe the visualization, access, and performance offered by this robotic technology in the limited confines of the laryngopharyngeal complex. MATERIALS AND METHODS We performed a feasibility study of the transoral robotic application of the Flex Robotic System in a fresh, frozen cadaver model. This study was deemed exempt by our institution s institutional review board. Seven adult cadavers were used in a simulated surgical setting in accordance with institutional protocols. Three specimens consisted of a head, neck, and torso region with all structures intact from head to diaphragm; the lungs were removed in each specimen. Four specimens consisted of a head and neck transected several tracheal rings below the cricoid cartilage. One cadaver was male and 6 cadavers were female. Cadaver ages ranged from 47 to 79 years with a mean age of 68.4 years. Two cadavers were edentulous, whereas 5 cadavers showed partial or full dentition. All cadavers were inspected and demonstrated intact relevant anatomy superior to the upper tracheal rings without obvious anomalies. Cadavers were placed in the supine position on the operating table. Standard mouth retraction was provided by the use of the Flex Retractor (Medrobotics) to achieve proper visualization and angle of entry. Anterior manual displacement of the tongue was used to facilitate entry of the robot using a 2-0 silk suture to retract the tongue. The robot was mounted to the surgical table side rails and arranged to approach the oral cavity from the caudal direction. A description of the design of the Flex System has been previously published. 28,29 In brief, the system consists of a surgeon-controlled console with a touchscreen monitor and 3-axis joystick that controls the flexible endoscope (Figure 1). The endoscope is fixed to a base console that can be placed on either side of the operating table. The endoscope unit is placed over the patient in the midline to allow for a caudal approach to the oral cavity. The flexible endoscope is equipped with a 2D-HD digital camera and 6 LED lights, and consists of 50 cylindrical links that advance in a follow-the-leader mechanism controlled by the joystick of the surgeon s console. The camera is able to move superiorly, inferiorly, left, and right, and can rotate on its axis to provide optimum visualization. Two accessory working channels located on either side of the endoscope allow for introduction of flexible instruments that are guided into place in the same configuration as the endoscope. FIGURE 1. Flex Robotic System flexible endoscope demonstrating flexible positioning within oral cavity. [Color figure can be viewed at wileyonlinelibrary.com] The robot was driven via the joystick controller through the oral cavity to the laryngopharyngeal complex. Relevant anatomic landmarks were identified before performing each procedure (Figure 2). Instruments were inserted through the 2 external accessory channels to perform the procedure. A 3.5 mm grasper (Flex Fenestrated Grasper) and 3.5 mm cauterizing instrument (Flex Monopolar Needle Knife) were used for tissue retraction, manipulation, and cutting. Instruments were switched for work on opposing sides of the surgical field. The surgical procedure was performed in each cadaver, by previously described methods, in a superior to inferior direction. 26,31 33 The procedure was successfully completed once the specimen was fully mobilized and removed transorally. All procedures were recorded with continuous video and still photography. RESULTS Transoral supraglottic laryngectomy was performed in 4 transected head specimens and total laryngectomy was performed in 3 bell torso specimens. Time for setup, including robot start-up, placement, draping, and retractor placement in the cadaver, was approximately 10 minutes. In our experience, the learning curve for the optimal positioning of the robot was short and improved quickly. The average time for driving of the robotic endoscope from the oral aperture to the obtainment of adequate view of the larynx with insertion of the instrument arms was 58 seconds. The robot was docked in place once the desired surgical site was reached. Advancement and repositioning of the endoscope was performed as the procedure proceeded inferiorly. The surgical techniques used for supraglottic laryngectomy and total laryngectomy have been previously described. 26,31 33 As noted in these articles, the supraglottic laryngectomy included resection of the epiglottis, aryepiglottic folds, and false vocal cords (Figure 3). With our dissection, the hyoid was left intact but the preepiglottic fat was resected with the specimen. For the total laryngectomy, an annular stoma was created by first excising a ring of skin and transecting the trachea with a beveled HEAD & NECK DOI /HED JUNE

3 FUNK ET AL. FIGURE 2. Endoscopic view of (A) the larynx, (B) proximity to the vocal folds, (C) placement of the suction tubing through the instrument port across the glottis, and (D) access to the laryngeal complex using the flexible instruments. [Color figure can be viewed at wileyonlinelibrary.com] cut just below the first tracheal ring. The sternohyoid and sternothyroid muscles were reflected away freeing the inferior portion of the larynx (Figure 4). The remainder of the surgery was performed endolaryngeally, as described with the da Vinci system. Using the Flex system, visualization of the laryngopharyngeal complex and identification of relevant structures was obtained (Figure 2). The base of tongue, epiglottis, vallecula, arytenoid cartilages, aryepiglottic folds, piriform fossae, false and true vocal cords, anterior commissure, and most cephalic tracheal rings were visualized in each cadaver (Figures 5 and 6). A moderate degree of haptic feedback was noted using the flexible instruments, allowing the surgeon to assess the firmness of tissues. The use of a tongue retraction stitch allowed for placement of the retractor while avoiding obstruction by excess bulk from the base of tongue distally. The built-in evacuation ports of the Flex retractor aided in smoke evacuation from the surgical field. If needed, a 14-French FIGURE 3. Incision of (A) the lateral glossoepiglottic fold, (B) the aryepiglottic fold, (C) the ventricle with preservation of the true vocal folds during supraglottic laryngectomy, and (D) the defect after the supraglottic laryngectomy. [Color figure can be viewed at wileyonlinelibrary.com] 1220 HEAD & NECK DOI /HED JUNE 2017

4 FLEX ROBOTIC LARYNGECTOMY FIGURE 4. (A) Outline of key structures identified by palpation and (B) formation of an annular stoma before the total laryngectomy. [Color figure can be viewed at wileyonlinelibrary.com] flexible suction was able to fit into the instrument port to reach the more distal field and evacuate smoke. Gross and fine motor control of the robotic endoscope using the joystick facilitated driving of the endoscope to the desired site. The 4-handed approach was crucial, especially in performing total laryngectomy. Robotic docking on a slight angle to the left or right at the oral aperture allowed additional space for the straight-line access of the assistant in the 4-handed technique. Increased exposure and counter-traction of tissue for optimal exposure was aided by digital manipulation of the thyroid cartilage through the stoma during total laryngectomy. In each procedure, flexible instruments were introduced into the accessory channels without difficulty. There were no collisions or crossover of instruments during the procedure or with instrument exchange. All procedures resulted in the complete resection using the described instruments (Figure 7). The flexible instruments allowed for coordinated and adequate range of motion. However, the lack of memory and rigidity at times resulted in an unpredictable rebound movement after incision through a tissue plane. Tension against the instrument was released, causing the instrument to bounce in the direction of applied pressure. Although incisions using the needle knife were clean and precise, there was a learning curve associated with its use as judging the depth of cuts could be difficult given the 2D nature of the image. The grip strength of both the Flex Fenestrated Grasper and Flex Monopolar Maryland Grasper was adequate for retraction of tissue but was occasionally suboptimal for strong retraction when grasping dense, thick tissues, and especially cartilage and bone. Instrument durability was limited to a few hours of use, particularly when using the Flex Fenestrated Grasper, after which the instrument seemed to wear down resulting in weaker grip strength. FIGURE 5. Lateral extension of total laryngectomy with mucosal incisions exposing the hyoid bone. [Color figure can be viewed at wileyonlinelibrary.com] HEAD & NECK DOI /HED JUNE

5 FUNK ET AL. FIGURE 6. Posterior view of the piriform sinuses and the posterior incision in the total laryngectomy. [Color figure can be viewed at wileyonlinelibrary.com] During the procedure, we attempted to use the Flex instruments to place sutures to close the neopharynx with difficulty. Instead, the camera was used to provide visualization for closure by hand. DISCUSSION Despite recent advances in minimally invasive approaches to head and neck cancers, management of laryngeal malignancy continues to be riddled with challenges and poor outcomes. The ultimate goal in the treatment of laryngeal malignancies is cure, but also includes preservation of organ function, which improves quality of life and decreases treatment-related morbidities, including loss of phonation and swallowing. Open surgery and conventional laryngoscopic approaches remain the standard of treatment, with or without adjuvant chemoradiation therapies. Extending the application of the transoral robotic approach using novel technologies is a promising possibility in the future treatment of laryngeal cancer. The advantages of transoral robotic approaches are numerous. TORS allows for access to deep sites in a minimally invasive fashion, offers high-definition visualization, and provides exemplary instrumentation for precise and delicate handling of tissue. The transoral approach reduces involvement of surrounding structures and healthy tissues that can be damaged in open approaches. 23,34 The chief advantage of transoral approaches to the laryngopharyngeal complex is preservation of organ structure and function; however, this is predominantly a postulated benefit as few studies have described the use of TORS for supraglottic and total laryngectomy in the patient setting. 9,26,35 The use of the da Vinci system for cancers of the oral cavity, oropharynx, hypopharynx, and larynx have shown improved postoperative recovery demonstrated by fewer requirements for tracheotomy, quicker rehabilitation of swallowing and vocal function, shorter requirements for feeding tube placement, and low rates of aspiration pneumonia. In addition, hospital stays are reported to be shorter than for open procedures. 12,13,20 23 This decrease in morbidity and the concomitant reports of excellent cure rates justifies the efforts for implementation of TORS in an increasing number of applications. Successful application of TORS for supraglottic laryngectomy and total laryngectomy requires adequate exposure of the lesion and key structures. Visualization of the vallecula, aryepiglottic folds, and anterior commissure are FIGURE 7. (A) Specimen after the removal, (B) the hypopharyngeal defect after the resection, and (C) the closure after the resection. [Color figure can be viewed at wileyonlinelibrary.com] 1222 HEAD & NECK DOI /HED JUNE 2017

6 FLEX ROBOTIC LARYNGECTOMY considered prerequisite for surgery. 26 The surgeon must ensure that there is sufficient space for manipulation of instrumentation. Incomplete visualization places undue risk of inadequate tumor resection and damage to vital structures and necessitates that the procedure be aborted. Preoperative evaluation with panendoscopy using the retractor planned for the surgery to ensure adequate visualization on an individual basis is recommended to avoid the excess cost of aborting a robotic procedure. 10,35,36 Cadaveric studies in the hypopharynx and larynx describe excellent visualization. 18,37 However, in clinical studies, adequate exposure of the tumor and surgical field has been a limiting factor in the application of TORS, particularly in the larynx. 12,13,16,17,25,26,35 In a multi-institutional prospective cohort study of supraglottic laryngeal and hypopharyngeal transoral robotic resections by Vergez et al, 16 6 of the 130 patients required conversion to open surgery because of a lack of exposure. Thirty-three patients were considered to have suboptimal exposure related to anatomic causes (small oral opening, dentition, or base of tongue volume) or oncologic causes (large tumor volume). Glottic tumors were linked to notably poor exposure related to a narrow channel and difficulty accessing the anterior commissure. Weinstein et al 17 reported preoperative endoscopic evaluation of 192 patients undergoing oropharyngeal or laryngeal resections and identified 13 patients in which they were unable to expose the affected area, with 2 additional patients who required conversion to an open procedure. Additional studies describe inadequate exposure or inadequate access to tumors as the cause for unsuccessful completion of TORS. 12,13,25 Thus, exposure and access remain the principal hurdles in the application of TORS to the laryngopharyngeal complex. The underlying causes for inadequate access up to this point may be accounted for by the discrepancy between current robotic design and intended function. In the same manner that a rigid key would be impossible to introduce into a curved lock, the linear approaches are incompatible with the nonlinear confines of the anatomy of the upper aerodigestive tract. The da Vinci robotic system was designed for work within the larger spaces of the abdomen and thorax, which allow the introduction of effector arms at wide angles. In the transoral approach, the acute angles of the bulky effector arms can lead to conflict outside the mouth while collisions of the rigid arms can occur with surrounding anatomy during manipulation. 19,25,34 These characteristics reduce the applicability of the da Vinci, especially in deep anatomic structures distal to the base of the tongue. The design of the Flex Robotic System expands the functionality of current technologies by incorporating unique features to optimize exposure and access to the upper aerodigestive tract. In addition to the benefits of a nonlinear endoscope, this robotic platform incorporates the endoscope and instrument channels into a single arm, replacing the bulk of the multiple arms of the da Vinci system. This design also eliminates the need for a larger entry space to insert instrument arms at angles wide enough for maneuverability in the distal working site. Considering these features, it is reasonable to suggest that the design of this robot may allow for application in patients with restrictive anatomy, including small mouth opening, prominent dentition, limited neck flexion, micrognathia, bulky tumors, and irradiated tissues. 29 This could be particularly beneficial in patients after prior failed TLM or those undergoing salvage total laryngectomy in recurrence after primary chemoradiotherapy, a somewhat common occurrence. 38 However, because of its recent approval, there are limited data evaluating the use of the Flex robot in patients with difficult anatomy. This study shows the feasibility of the Flex Robotic System in visualizing the laryngopharyngeal complex and demonstrates technical feasibility of transoral robotic supraglottic laryngectomy and total laryngectomy in the cadaveric model. To the best of our knowledge, this is the first report to describe the use of the Flex Robotic System for these procedures, whereas previous studies using the da Vinci system have been described. TORS supraglottic laryngectomy has been reported in small cohorts, with few attempts proving unsuccessful. 9,15,33,39,40 Limited experience demonstrates that TORS total laryngectomy is a more daunting endeavor. Dowthwaite et al 35 report conversion to open total laryngectomy in 1 of their 3 patients, after access was achieved but visualization was suboptimal, which was attributed to the patient s poor mouth opening, retrognathic jaw, and significant soft tissue edema from a prior transcervical neck dissection. In a total laryngectomy case series reported by Smith et al, 26 2 of their 7 patients required conversion to open total laryngectomy for the inferior portion of the procedure owing to inadequate exposure of the surgical field. The procedure was not attempted in 2 additional patients because of identified deficits in robotic access related to anterior positioning of the larynx preventing exposure of the vallecula, a narrow mandibular arch preventing placement of the endoscope and robotic arms, and poor visualization because of inadequate retractor application. In the present study, adequate visualization and access using the Flex Robotic System was obtained in each cadaver. The flexible endoscope allowed for visualization of the lateral, inferior, or superior portions within the surgical field without the need to use angled endoscopes. The size of the endoscope permitted entry into the oral cavity in specimens with dentition and restricted mouth opening. The coaxial nature of the robotic arms in relation to the camera ensured that the instrumentation remained within view of the field provided by the camera. Familiarity with use of the robot was quickly achieved, as setup and time to exposure improved significantly after initial procedures. The controlled flexibility of the robot allowed the operator to maneuver the endoscope to provide direct views and adequate working space in all areas during the resections. There were no collisions of the endoscope or instruments with surrounding tissues. The 4- handed approach was particularly useful throughout both the supraglottic laryngectomy and total laryngectomy procedures. The main disadvantage using this robot was the difficulty of endolaryngeal suturing after the removal of the specimen. Specifically, we noted some limitation with the graspers with a lack of a specific needle-holding platform. The needle would spin when trying to pierce the HEAD & NECK DOI /HED JUNE

7 FUNK ET AL. cadaveric tissue because of inconsistent grasping of the needle. Additionally, needle exchange was difficult between instruments and often required placing the needle on the wound bed. We also noted a learning curve associated with the 2D view, especially when judging the depth of incisions made using the needle knife. As we evaluate the applications of TORS in the larynx, it is important to build upon prior experiences. A fundamental difference in the transoral approach is the change in the anatomic perspective and success is dependent upon an understanding of the anatomy from the endolaryngeal vantage point. 41,42 Proficiency in surgical technique is required, as the experience of a surgeon may be reflected in the number of complications that occur. 9 As with any new technology, there is a learning curve inherent to successful application in patients. In the case of TORS, this seems to be rapid, as evidenced by decreasing operative times and fewer conversions to open total laryngectomy after several cases. 13,16,27,43 Additional experience highlights the importance of performing neck dissection after TORS to prevent complications from subsequent edema. 35 Additionally, with future iterations of the equipment of the Flex System, improvements in durability and grip strength are expected, which when combined with increased experience may help overcome some of the current limitations noted. A major consideration in the application of TORS continues to be the cost. Current studies evaluating cost efficacy in TORS are limited, but Dombree et al 44 demonstrated that robotic partial and total laryngectomies are significantly more expensive than open approaches and TLM. Additional studies are required that include evaluation of additional parameters, such as costs of postoperative hospital stay, complications, and rehabilitation. CONCLUSION The purpose of this study was to demonstrate the feasibility of using the Flex Robotic System for transoral supraglottic laryngectomy and total laryngectomy. In our experience, both supraglottic laryngectomy and total laryngectomy were performed successfully in the cadaveric model. Applications of this robotic system to transoral surgery have been described, and we demonstrate feasibility in exposure and access for performance of surgery in a more distal location than previously reported. Enhancing surgical access to the larynx using the Flex Robotic System has great potential for management of laryngeal malignancies, but requires subsequent studies to further investigate its applicability. Further studies are needed to evaluate patient safety and oncologic outcomes in the setting of TORS supraglottic laryngectomy and total laryngectomy. Acknowledgment The cadaveric specimens were generously provided by Medrobotics (Raynham, MA). REFERENCES 1. 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