Oral Oncology 46 (2010) Contents lists available at ScienceDirect. Oral Oncology. journal homepage:

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1 Oral Oncology 46 (2010) Contents lists available at ScienceDirect Oral Oncology journal homepage: Feasiblity of transoral robotic hypopharyngectomy for early-stage hypopharyngeal carcinoma Young Min Park a, Won Shik Kim a, Hyung Kwon Byeon a, Armando De Virgilio a,b, Jin Sei Jung a, Se-Heon Kim a, * a Department of Otorhinolaryngology, Yonsei University College of Medicine, Seoul, Republic of Korea b Department of Otorhinolaryngology G. Ferreri, University La Sapienza, Rome, Italy article info summary Article history: Received 19 April 2010 Received in revised form 14 May 2010 Accepted 14 May 2010 Available online 8 July 2010 Keywords: Robotics Surgical procedures Minimally invasive Hypopharyngeal neoplasms Conventional surgical approaches for hypopharyngeal carcinomas have a great risk for developing treatment-related morbidity. To minimize this morbidity, hypopharyngectomy by transoral robotic surgery (TORS) was performed, and the efficacy and feasibility of this procedure were evaluated. TORS was performed using da Vinci Surgical Robot (Intuitive Surgical Inc., Sunnyvale, CA) in 10 patients with T1 or T2 pyriform sinus cancer and posterior pharyngeal wall cancer. FK retractor (Gyrus Medical Inc., Maple Grove, MN) was used for transoral exposure of the lesion. A face-up 30-degree endoscope was inserted through the oral cavity and two instrument arms were located in both sides of the endoscope. Pyriform sinus was totally resected as a cone-shape from the vallecular to apex region, and ipsilateral arytenoid cartilage was saved for function preservation. The aryepiglottic fold was resected medially. Laterally, the inner perichondrium of the thyroid cartilage was peeled off after perichondrium was incised horizontally to make sure of the safe margin of antero-lateral portion. The posterior margin is an inferior constrictor muscle of the posterior pharyngeal wall. We evaluated the robotic set up time, robotic operation time, blood loss, surgical margins, swallowing time, decannulation time, and surgery related complications. Transoral robotic hypopharyngectomy was performed successfully in all 10 patients. The mean robotic operation time was 62.4 min, and an average of 17.5 min was required for the setting of the robotic system. There was no significant perioperative complication in the cases. Swallowing function returned to all patients within 8.3 days average. Decannulation was carried out within an average of 6.3 days after surgery. Transoral robotic hypopharyngectomy was feasible and ontologically safe technique for the treatment of early hypopharyngeal cancer. Ó 2010 Elsevier Ltd. All rights reserved. Introduction Hypopharyngeal carcinoma has the worst prognosis among the head and neck carcinomas, and its survival has not been significantly improved despite the development of treatment modalities. 1 3 With advancement of chemo-radiation therapy, the recent treatment trend of hypopharyngeal carcinomas is to improve the quality of life in patients through organ preservation. 4 Many studies are under progress to decrease treatment-related morbidities and to increase postoperative quality of life. Previous studies showed that transoral LASER microsurgery (TLM) decreased treatment-related morbidity and helped preserve organs because it proceeds through the oral cavity without an external incision. 5 However, classic transoral surgery has not been widely * Corresponding author. Address: Department of Otorhinolaryngology, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul , Republic of Korea. Tel.: ; fax: address: shkimmd@yuhs.ac (S.-H. Kim). applied because of the limitation of microscope and LASER and difficulties in performing the surgery. Recently, there have been many studies about transoral robotic surgery (TORS) which transorally removed tumors in the upper aerodigestive tract using a robotic surgical system. 6,7 TORS ensures the operation to be done more precisely compared to the classic transoral procedure, thanks to the advanced minimally invasive technique. This study analyzes prospectively the results of our experience in order to evaluate the feasibility of TORS in the organ preservative treatment of hypopharyngeal carcinomas. Materials and methods Patients The Institutional Review Board of Yonsei University approved the protocol to evaluate the feasibility and efficacy of TORS in the treatment of hypopharyngeal carcinomas (approval number: /$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi: /j.oraloncology

2 598 Y.M. Park et al. / Oral Oncology 46 (2010) ). The inclusion criteria were as follows: (1) age of 18 years or older at the time of surgery, (2) diagnosis of hypopharyngeal carcinoma and indication for surgery and (3) intact mobility of more than at least one arytenoid cartilage. The exclusion criteria were as follows: (1) contraindication of surgery and general anesthesia due to medical conditions, (2) since the surgery proceeds with the introduction of one endoscopic arm and two instrument arms through the narrow oral cavity, obtaining sufficient surgical view could be difficult for patients with certain anatomic features such as small retrognathic mandible. Therefore, from preliminary physical examination including endoscopy in the office, patients with anatomic features which were difficult in obtaining sufficient view were excluded from the study, (3) where the primary lesion has advanced so as to cause vocal cord fixation, thyroid cartilage invasion, post-cricoid involvement or pyriform sinus apex involvement, these were considered not suitable for TORS so the cases were excluded, (4) unresectable nodal diseases such as carotid artery invasion were excluded, and (5) previous treatment, including surgery or chemoradiation. A total of 10 patients who met the inclusion and exclusion criteria participated in the prospective study from April 2008 through March Informed consent was collected from all patients. All 10 patients were male. The mean age of patients was 68.4 years (range, years). All patients were histologically diagnosed as squamous cell carcinoma. The primary sites were the pyriform sinus (n = 8) and posterior pharyngeal wall (n = 2). Clinical information of the patients is shown in Table 1. Procedure of study Physical examination including 70 degree rigid endoscope of the pharynx and larynx was performed at the outpatient Table 1 Clinical information of patients. Case Age (yr) Sex Site Pathology Karnofsky scale (%) TNM stage 1 64 M PS SCC 70 T2N2bM M PS SCC 80 T1N2bM M PS SCC 90 T2N0M M PS SCC 90 T1N2bM M PS SCC 90 T3N2bM M PPW SCC 80 T1N0M M PS SCC 90 T2N2bM M PS SCC 90 T1N1M M PPW SCC 90 T2N0M M PS SCC 90 T1N0M0 PS: pyriform sinus, PPW: posterior pharyngeal wall, and SSC: squamous cell carcinoma. department in all patients. TORS was considered, if mobility of the arytenoid cartilage was maintained. Because hypopharyngeal carcinoma often shows wide submucosal spread or deep infiltration, computed tomography (CT) or magnetic resonance imaging (MRI) were taken preoperatively to evaluate the exact extent of the disease. After general anesthesia, a biopsy of the primary lesion was taken for histological diagnosis. At that time, we confirmed whether a sufficient view could be acquired by using the FK retractor and panendoscopy was carried to investigate the presence of the secondary primary tumor. Then, positron emission tomography (PET) scanning was performed in the patients to detect distant metastasis. Configuration of robotic surgical system The da Vinci surgical system (Intuitive Surgical Inc., Sunnyvale, CA) was used to perform the TORS. The robotic surgical system consists of a surgeon s console, a surgical cart and a manipulator cart where three robotic arms are instrumented. The surgeon placed oneself at the surgeon s console, and received three-dimensional magnified vision from an endoscopic arm located at the manipulator cart. Two instrument arms on the manipulator cart were delicately controlled from the surgeon s console which carried out the operation. Operation procedures All operations were performed under general anesthesia. Tracheotomy was performed transiently to prevent airway obstruction due to postoperative swelling and bleeding. A neck dissection was done first, if required. Then, the patient was placed in the Boyce position, and the primary lesion was exposed using the FK retractor. The robotic surgical system was set by the method described in our previous studies. 8,9 The patient s head was put on the foot side of the surgical bed and the manipulator cart was located 30 degrees apart from the surgical bed. A face-up 30-degree endoscope was inserted through the oral cavity and two instrument arms were located in both sides of the endoscope. The operation began after a sufficient view was obtained and the two instrument arms worked well without interrupting each other. We obtained a nice surgical view and working space by using the FK retractor and tongue spade blade (Fig. 1A and B). Total pyriform sinus resection was carried out as follows: pyriform sinus was totally resected as a cone-shape, and ipsilateral arytenoid cartilage was saved for function preservation. First, the dissection started in the direction of the anterior to the posterior along the medial side of the aryepiglottic fold (Fig. 2A and B). After the Figure 1 (A) TORS setting and (B) TORS surgical view and schematic drawing of the surgical boundary of total pyriform sinus resection.

3 Y.M. Park et al. / Oral Oncology 46 (2010) Figure 2 Images show the process of total pyriform sinus resection, left. (A) First, dissection was done along the medial side of the aryepiglottic fold using a 5 mm spatula cautery. (B) After localizing the thyroid cartilage, dissection was carried out in the direction of the medial to the lateral. (C) Inner perichondrium of the thyroid cartilage was peeled off to make a safe margin of the antero-lateral portion and the ipsilateral arytenoid cartilage was preserved for functional preservation. A lateral dissection was done along the medial side of the thyroid cartilage. (D) After pyriform sinus resection, pulsation of the carotid artery was observed in the operative bed. (E) Postoperative 3 months 70 degree endoscopic view of the lesion and pharyngogram. The left pyriform sinus was obliterated and mobility of the vocal cord was maintained. The patient swallowed liquid and solid material without aspiration on pharyngogram. Figure 3 Images show the process of partial pharyngectomy in the posterior pharyngeal wall carcinoma. (A) The first dissection was done along the superior margin. (B) Dissection was followed along the prevertebral fascia. (C) Finally, dissection of the inferior portion was done using the images supported by a face-up 30-degree endoscope. (D) The surgical bed after en-bloc tumor removal. (E) Postoperative 3 months 70 degree endoscopic view of the lesion.

4 600 Y.M. Park et al. / Oral Oncology 46 (2010) thyroid cartilage and thyrohyoid membrane was localized, dissection preceded in the direction of the medial to the lateral along the thyroid cartilage. The inner perichondrium of the thyroid cartilage was peeled off after the perichondrium was incised horizontally to make sure of the safe margin of the antero-lateral portion (Fig. 2C). Then, the dissection followed along the lateral side of the thyroid cartilage and the dissection of the posterior part was completed. The posterior margin is an inferior constrictor muscle of the posterior pharyngeal wall. While the posterior dissection was underway, pulsation of the carotid artery was easily noticed through the three-dimensional magnified view. The risk of injury to the carotid artery decreased to its minimum by locating it on the postero-lateral side of the surgical bed using an articulated robotic arm. Lastly, the apex of the pyriform sinus was dissected, and the specimen was removed en-bloc pattern (Fig. 2D). The lesion on the posterior pharyngeal wall was removed as follows. The tumor including the safety margin was removed in a circular manner after appropriate view was obtained using a face-up 30-degree endoscope. First, an incision was made along the superior margin of the lesion and the superior portion was dissected along the prevertebral fascia (Fig. 3A and B). Next, the dissection of the inferior portion followed (Fig. 3C). In the classic transoral procedure using the microscope and LASER, the inferior surgical view can not be obtained sufficiently. However, the inferior margin was observed easily through the 30-degree angled three-dimensional magnified view in this study. Based on these images and articulation of robotic arms, geometric resection of the posterior wall carcinoma could be performed and the specimen was removed en-bloc pattern (Fig. 3D). Treatment of the neck All patients were evaluated preoperatively physical examination of the neck and imaging studies such as CT or MRI. If a lymph node with a metastatic tumor was not suspected preoperatively, elective ipsilateral selective neck dissection including level II, III, and IV was performed. If a positive neck node was observed, therapeutic ipsilateral modified radical neck dissection was performed. This neck dissection was performed simultaneously with TORS. The rationale for performing simultaneous neck dissection are as follows. First, the compliance of the patient can be improved as it is a one stage surgery. Second, meticulous dissection was done according to the plane using articulated robotic arms under extended view obtained and there was no case where there was through and through defect between the pharynx and the neck. For the TLM, it is difficult to sense the depth through the twodimensional images obtained by the microscope and there is an increased risk of fistula formation if an acute angle forms between the pharyngeal wall and the dissection plane due to the linear property of the LASER. However in TORS, extended three-dimensional view provides more accurate sense of depth and the risk of fistula formation is decreased because surgery can be proceeded maintaining an obtuse angle between the dissection plane and the pharyngeal wall using articulated arms. Third, if an accidental arterial bleeding occurs during surgical excision of the primary lesion, bleeding control can be managed by certain methods such as monopolar cauterization, bipolar cauterization, surgical clipping or suture ligation but in the case of massive bleeding, obtaining sufficient view within the limited space and managing vessels by exchanging robotic arms may be troublesome. In view of this possible situation, exposing the major neck vessels in the surgical field by simultaneous neck dissection could provide easy access when bleeding management is required. Adjuvant therapy Postoperative radiotherapy was prescribed (1) nodal diseases of more than N2 stage; (2) cases with close margins under 5 mm; and (3) evidence of margins positive for tumor at primary site. In comparison to the definitive RT where normally over 70 Gy of radiation is required, adjuvant radiotherapy is sufficient with under 70 Gy radiation so complications following therapy can be minimized. Adjuvant chemotherapy was considered in the following cases: (1) existence of extracapsular spread and (2) tumor with perineural invasion, angioinvasion or poor lymphoid response. Results Ability to perform TORS in hypopharyngeal carcinoma Sufficient view was acquired by using the FK retractor in all cases. Robotic arms were equipped with 5 mm-sized instruments, and geometric resection could be conducted in the narrow pharyngeal lumen, thanks to the advantages of the articulated robotic arms. The mean robotic operative time was 62.4 min and that for setting up the robotic system was 17.5 min. In all patients, TORS was completed successfully. Advantageous surgical technique First, images supported by the endoscopic arm equipped with two integrated cameras made it possible to three-dimensionally analyze the cancerous lesion in the hypopharynx. Also, human-like articulated joints of the robotic arms made it possible to geometrically resect the lesion in the hypopharynx with a complex anatomic structure. Based on these advantages, the robotic surgical system can remove the lesion en-bloc in contrast with the piecemeal removal by the LASER surgery. Second, the LASER surgery was performed only by cutting through the tissue. On the other hand, the robotic surgical system supports a similar surgical technique for an open surgery; for example, retraction of tissue by using Maryland forceps and suture technique. Moreover, the operator can bimanually palpate the tissue by controlling the two instrument arms. Using the above surgical techniques, thyroid inner perichondrium was peeled off to obtain a safe margin of antero-lateral portion. Third, a multi-angled sufficient view can not be acquired in the conventional transoral surgery because of the limited sight of the microscope. However, TORS supports multi-angled view using an endoscope with variable angles and allows deciding a definite inferior margin of the lesion. Surgical margins A frozen biopsy was taken to confirm the clear margin. If positive or suspicious margin was reported, further resection was conducted. In all cases, negative for malignancy was reported on the final pathology (Table 2 and Fig. 4). Complication and blood loss No significant complication was observed in the patients. In spite of concurrent neck dissection, pharyngocutaneous fistula did not occur. The average blood loss during the operation was 15.5 ml. Functional outcome Tracheotomy was performed to prevent an airway compromise due to excessive swelling and severe bleeding. Decannulation was

5 Y.M. Park et al. / Oral Oncology 46 (2010) Table 2 Treatment outcome of the patients. Case ND Resection margin RTx Return to swallowing (d) Decannulation (d) Robotic setup time (min) Robotic operative time (min) EBL (ml) 1 MRND Negative Yes MRND Negative Yes LND Negative Yes MRND Negative Yes MRND Negative Yes Negative No MRND Negative Yes MRND Negative Yes LND Negative No LND Negative No ND: neck dissection, MRND: modified radical neck dissection, SND: selective neck dissection, RTx: adjuvant radiotherapy, and EBL: estimated blood loss. Figure 4 Graph shows three-dimensional analysis on resection safety margin of specimens that removed as en-bloc. (Medial: side along aryepiglottic fold and lateral: side along thyroid cartilage.) completed within 6.3 days on average, and no specific problem with voice was reported. Normal swallowing was possible within an average of 8.3 days, and the feeding tube was removed from all patients before they were discharged. Patients that received open approaches such as pharyngotomy usually complained of postoperative dysphagia because of damage to the constrictor muscles and pharyngeal nerve plexus. However, patients undergoing TORS showed rapid recovery of swallowing because of preservation of these structures (Figs. 2E and 3E). Follow up of patients The average period of follow up for the patients is 12.2 months (2 25 months). All patients are disease free status. Seven patients have completed adjuvant radiotherapy according to NCCN guideline and three patients considered as complete response state are under close follow up without further adjuvant therapy. All patients have managed to return to their everyday lives without any problems concerning swallowing and phonation. Discussion Treatment modalities of hypopharyngeal carcinoma include radiation, concurrent chemoradiation, and surgery with or without adjuvant radiation. Despite these various modalities, the survival of hypopharyngeal carcinoma was not significantly improved. Thus, the current trend of treatment is to preserve the organ and improve the quality of life of the patients. Many studies showed the possibility of TLM as method of organ preservation. 5,10 TLM has many advantages, including rapid recovery of swallowing, no requirement of tracheotomy, short indwelling of the feeding tube, and low treatment-related morbidity. 11 However, to be good at TLM requires detailed knowledge of endoscopic anatomy, plenty of microsurgery experience, and skillful use of LASER. It is hard to resect the lesion in hypopharynx which presents complex anatomy due to the limited sight. Because the LASER procedure starts from outside the oral cavity, it could be interrupted by a surrounding structure such as the tongue base or pharyngeal fold. In the field of head and neck surgery, Hockstein et al. had first reported the feasibility of transoral use of the robotic surgical system in mannequin and cadaver models. 12,13 Later, Weinstein et al. performed transoral supraglottic laryngectomy in a canine model using the robotic system and developed a procedure known as TORS. 14 TORS is currently defined as a surgical procedure using a bimanual technique, with at least three robotic arms entered transorally. TORS do not require an external incision and preserve more healthy tissue that permits rapid recovery, and function preservation is possible. Moreover, this can overcome the limitation of TLM through the advanced minimally invasive technique which still has the TLM advantages described above. 15,16 Optimal surgical view could be obtained by transorally locating the multi-angled endoscopic arm, and moving it actively along with the process of operation. Instrument arms rotating 360 degrees freely like human

6 602 Y.M. Park et al. / Oral Oncology 46 (2010) arms allow the operation to be carried out more precisely in a narrow space. Using such as advantages, it was possible to peel off the inner perichondrium of the thyroid cartilage to obtain a safe margin of antero-lateral portion and to maximally preserve the surrounding structure for maintaining the function. In particular, multi-angled three-dimensional magnified images helped the operator observe the inferior margin that was blocked by surrounding anatomic structures. In the case of TLM, if the tumor was not dissected directly, this area was not easily viewed by microscope. The advantages of TORS as primary treatment of hypopharyngeal carcinoma over definitive radiotherapy are as follows. Possible existence of radio-resistant portion within the tumor can be eliminated by complete resection of the primary tumor which can maximize the effect of adjuvant radiotherapy. Also, adjuvant radiotherapy or chemotherapy can be performed in selected cases with adverse features according to postoperative histopathological reports such as extracapsular spread, perineural invasion or angioinvasion and so unnecessary treatment can be avoided. When performing adjuvant radiotherapy, exact extent of the lesion can be evaluated and treatment can be proceeded under precise knowledge of the surgical margins. In comparison to the definitive RT where normally over 70 Gy of radiation is required, adjuvant radiotherapy is sufficient with under 70 Gy radiation so complications following therapy can be minimized. Previous studies showed that the learning curve of TORS was shorter than the conventional laparoscopic procedure. 17,18 A surgeon with little experience in maneuvering the robotic surgical system can easily perform TORS. Basically, bimanual palpation of tissue by using two instrument arms and their articulated joints help the operator rapidly adapt to TORS. In this study, the mean total therapeutic time, including the time for setting the robotic surgical system was 1 h or less and the fastest case took only 27 min. Also, the ergonomic design of the surgeon s console minimizes the surgeon s fatigue during the long operation hours. Another study reported complications of TORS such as airway obstruction, edema, aspiration, bleeding, and salivary fistula. 19 However, no perioperative complication was reported in our study. Tracheotomy was done transiently to prevent airway obstruction. The patient s burden can be further decreased if tracheotomy is not performed in the next study. Normal swallowing returned in the mean of 8.3 days, and the feeding tube was removed before the patients were discharged. Rapid recovery of swallowing was possible because the constrictor muscles and pharyngeal nerve plexus were preserved during the procedure. Also, the risk of salivary fistula decreased to a minimum because communication between the primary site and the neck did not occur in patients treated with TORS. Considering that the delay of postoperative radiotherapy deteriorates the local control rate, rapid recovery of TORS without complication favors the oncologic results. 20 Currently, unipolar cautery is usually used to cut or coagulate the tissues in the TORS process. A wound made by unipolar cautery is wider and deeper than one done by LASER, and more thermal damage to the surrounding tissue occured as well. 21 These characteristics are disadvantages of TORS to be applied for surgery of hypopharyngeal carcinoma which requires more precise operation. However, LASER has some advantages, including more precise cutting of tissue, effective control over the bleeding of vessels less than 5 mm, and lymphatic sealing effect that prevents tumor cell spread Moreover, postoperative tissue swelling is less in the LASER cases. Recently, Zeitels et al. reported the use of thulium LA- SER through a fiber-based delivery system. 25 If this new technology combines with the robotic arms of the da Vinci surgical system, it would produce better merits than the current TORS procedure using unipolar cautery in the treatment of hypopharyngeal carcinoma. Conclusions Transoral robotic hypopharyngectomy was feasible and ontologically safe technique for the treatment of early hypopharyngeal cancer. It can be an option for minimally invasive organ preservation surgery and increase the patients quality of life. Conflict of Interest Statement None declared. References 1. Johansen LV, Grau C, Overgaard J. Hypopharyngeal squamous cell carcinomatreatment results in 138 consecutively admitted patients. Acta Oncol 2000;39: Carpenter RJ, DeSanto LW, Devine KD, Taylor WF. Cancer of the hypopharynx analysis of treatment and results in 162 patients. Arch Otolaryngol 1976;102: Wang T, Li X, Lu Y, Yu Z. 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