Transoral robotic surgery of the parapharyngeal space: A case series and systematic review
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1 CLINICAL REVIEW Transoral robotic surgery of the parapharyngeal space: A case series and systematic review Jason Y. K. Chan, MBBS, 1 Raymond K. Tsang, FRCSEd (ORL), 2 David W. Eisele, MD, 1 Jeremy D. Richmon, MD 1* 1 Department of Otolaryngology Head and Neck Surgery, Johns Hopkins Medical Institutions, Baltimore, Maryland, 2 Division of Otolaryngology Head and Neck Surgery, Department of Surgery, University of Hong Kong, Queen Mary Hospital, Hong Kong, SAR, China. Accepted 26 November 2013 Published online 13 March 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. The purpose of this study was to evaluate the current use of transoral robotic surgery (TORS) in the treatment of parapharyngeal space (PPS) neoplasms through a case series and systematic analysis. Methods. A case series review of 4 patients was combined with a PubMed, Web of Science, and Scopus search that identified 82 reports. Fifty-three articles remained after screening for duplicates, finally, 8 reports with adequate patient data were included. Statistical analyses and graphical representations were performed with Microsoft Excel (Redmond, WA) and GraphPad Prism software (La Jolla, CA). Results. Forty-four patients had TORS resection of PPS neoplasms. Overall, mean length of stay was 3.0 days with mean time to oral diet of 1.0 day. There were no recurrences but there was a mean follow-up time of only 18.5 months. Twenty-nine of these neoplasms (65.9%) were pleomorphic adenomas of which 7 (24%) had unintended capsule violation or tumor fragmentation during surgery and 2 patients had pharyngeal dehiscence that was managed conservatively. There were no neurovascular complications. Conclusion. TORS is a viable approach to resection of neoplasms of the PPS with minimal surgical morbidity. However, further long-term evaluation, especially for pleomorphic adenomas, is needed to define patient selection and the role of TORS for PPS salivary gland neoplasms. VC 2013 Wiley Periodicals, Inc. Head Neck 37: , 2015 KEY WORDS: Transoral robotic surgery (TORS), parapharyngeal space, pleomorphic adenoma, transoral INTRODUCTION The parapharyngeal space (PPS) is located lateral to the oropharynx, anatomically shaped like an inverted pyramid with the base at the skull base and the apex at the greater cornu of the hyoid bone, bound medially by the superior pharyngeal constrictors and laterally by the medial pterygoid muscle, mandibular ramus, and deep lobe of the parotid gland. 1 The PPS is further divided in the prestyloid and poststyloid region by a fascial band from the styloid process to the tensor veli palatini. The prestyloid space contains primarily the deep lobe of the parotid gland and the poststyloid compartment contains vital neurovascular structures. Tumors in the PPS account for only 0.5% of head and neck neoplasms, 2 most of these being of benign salivary gland or neurogenic origin. Tumors of the PPS are most commonly managed by surgical resection. Because of the relative inaccessibility to the PPS and the close proximity of the neoplasms to vital neurovascular structures, such as the carotid artery, glossopharyngeal nerve, and vagus nerve, transcervical surgical *Corresponding author: J. D. Richmon, Department of Otolaryngology Head and Neck Surgery, 601 N. Caroline St., JHOC 6th Floor, Baltimore, MD Jrichmo7@jhmi.edu David Eisele, MD, clinical reviews editor, was recused from consideration of this manuscript. approaches have been advocated. These approaches have also been advocated because of concerns for tumor rupture and spillage. 3,4 Currently, there has been increased interest in the use of the da Vinci Surgical Robotic System (Intuitive Surgical, Sunnyvale, CA) to resect tumors of the PPS via a transoral approach. Transoral robotic surgery (TORS) has garnered tremendous enthusiasm for the treatment of benign and malignant tumors of the oropharynx and its role has expanded to lesions in the larynx, hypopharynx, nasopharynx, skull base, 5 and, recently, the PPS. In this article, we sought to evaluate the role of TORS for PPS tumors through a systematic analysis of the medical literature with inclusion of our experience. METHODS The purpose of this study was to review the literature regarding the use of TORS for tumors in the PPS and attempt to critically evaluate patient selection, operative factors, and clinical outcomes. Patients treated at The Johns Hopkins Hospital and the Hong Kong University Queen Mary Hospital was included in the analysis. A systematic review of the literature of TORS of the PPS was performed using the PubMed (National Library of Medicine, NCBI), Web of Science, and Scopus databases with the primary search terms robotic surgery or robot or robotics combined with the secondary search terms parapharynx or parapharyngeal. PubMed identified 14 HEAD & NECK DOI /HED FEBRUARY
2 CHAN ET AL. RESULTS In addition to the 4 patients treated at our institutions, there were 40 patients from the 8 reports. Patient data are listed in Table 1. Mean age (n 5 43) was 45.6 years, median age was 43.0 years with an interquartile range of 33.0 to 57.0 years. Of the 29 patients who had their tumor size recorded, the mean tumor size was 4.7 cm and median size of 4.7 cm with an interquartile range of 3.1 to 5.8 cm. Outcomes of patients that were available included robot time, total operating time, estimated blood loss, follow-up duration, time to oral diet, and length of stay (Table 2). Figure 2 further shows the characteristics of the robot time, total operating time, estimated blood loss, and length of stay by study and combined with the average value for each outcome. A complete surgical resection was reported in all patients. The most common diagnosis was pleomorphic adenoma (29 patients; 65.9%). A summary of the subset of patients with pleomorphic adenomas is demonstrated in Table 3. Techniques used in removing the PPS tumors with the robot included direct transoral (n 5 36), combined transoral with the robot and transcervical (n 5 1), transoral and transparotid (n 5 5), and transoral with tumor decompression using the coblator (n 5 2). Complications included pharyngeal dehiscence in 2 patients, conversion to an open approach in 1 patient, and a combined open/tors approach in 5 patients. There was no correlation between tumor size and occurrence of complications. All except 1 patient with data regarding an oral diet were started on a diet by postoperative day 1. Capsule disruption and tumor fragmentation occurred in 9 cases (31%), 2 of which were intended and all of which occurred in patients with pleomorphic adenomas. Figures 3 and 4 demonstrate a CT scan of a pleomorphic adenoma in the PPS and an intraoperative photograph of tumor spillage. With an average follow-up of 18.5 months in the cohort, there were no recorded recurrences of the primary neoplasms. FIGURE 1. Illustration of article identification, screening, eligibility, and final selection for the systematic analysis of transoral robotic surgery for parapharyngeal space lesions. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] publications, Web of Science identified 17, and Scopus identified 51. A total of 82 articles were found accounting for the overlap among the 3 bibliographic databases. After exclusion of review articles and articles without patient listings or adequate data, there were 8 articles left for analysis. Figure 1 demonstrates the selection process of the articles that were considered for the systematic analysis. Four additional patients treated at our institutions were included in this analysis. Statistical analyses and graphical representations were performed with Microsoft Excel (Redmond, WA), and GraphPad Prism software (La Jolla, CA). DISCUSSION Surgical approaches to the PPS include the transoral, transcervical, orbitozygomatic, transcervical with mandibulotomy, and combined transoral and transcervical approaches. 14 The transcervical approach is used to access and remove isolated tumors of the PPS, and the transcervical-parotid approach is used if the neoplasm arises from the deep lobe of the parotid. The orbitozygomatic approach, as described by Fisch, 15 is reserved for extensive lesions involving the PPS and middle cranial fossa skull base. The transcervical with mandibulotomy approach is reserved for neoplasms for which wide exposure is needed to facilitate safe resection of large or malignant neoplasms. 16,17 Despite a direct route to the PPS, the transoral approach has received cautious criticism given the limited access and visualization that this approach affords Concerns include the risk of neurovascular injury, tumor spillage, incomplete tumor excision, and infection. For these reasons, the transoral approach has been limited to small neoplasms that project into the oropharynx, are in close proximity to the constrictor muscles and oral mucosa, and lack poststyloid extension. 6 Recently, there has been growing enthusiasm for the transoral approach with the introduction of the da Vinci robot for TORS. TORS provides an excellent 3D view with either a 30- or 0-degree scope, offering a magnified high resolution view superior to the endoscope and overcoming line-of-site limitations of the microscope. Motion scaling and tremor filtration further allow for delicate dissection around the tumor capsule. 6,10 The majority of the neoplasms in this review were benign pleomorphic adenomas (65.9%), consistent with reports in the literature utilizing approaches other than TORS. 14,16,18,19 Violation of the capsule of a pleomorphic adenoma is most severe when the capsule is ruptured and tumor spillage occurs. This has been found to be significantly associated with recurrence of pleomorphic adenoma. 21 Recurrences of pleomorphic adenoma are particularly problematic as they often manifest as multifocal disease requiring wide surgical access with increased morbidity and the need for adjuvant postoperative radiation therapy. 22,23 After an initial transcervical approach, recurrences are most commonly accessible through a transcervical approach again. In contrast, recurrences of pleomorphic adenoma that are initially approached transorally may result in subsequent increased morbidity as definitive surgical resection often requires resection of the pharyngeal mucosa, mandibulotomy, and possibly free-flap reconstruction. 14,23 Furthermore, recurrences in the PPS are frequently multifocal and likely to re-recur. 22 In our analysis, there were 5 patients with tumor fragmentation, 2 with unintended capsule ruptures, and 2 with 294 HEAD & NECK DOI /HED FEBRUARY 2015
3 TRANSORAL ROBOTIC SURGERY OF THE PARAPHARYNGEAL SPACE TABLE 1. Summary of all patients treated with a transoral robotic surgery approach to the parapharyngeal space. Cases/articles Age, y Sex Maximal tumor size, cm Pathology Hospitalization, days Complication Fragmentation Capsule Disruption Oral Diet NED, follow-up, months Patient 1 36 Male 4.0 Lymphoepithelial cyst 1 No Yes No 1 3 Patient 2 34 Female 4.7 Pleomorphic adenoma 2 No Yes No 1 1 Patient 3 51 Female 6.0 Basal cell adenoma 7 No Yes No 2 13 Patient 4 43 Female 5.4 Pleomorphic adenoma 7 No Yes No 1 15 O Malley et al 6 74 Male 3.0 Benign cyst 2 No No No N/A Female 2.5 Pleomorphic adenoma 1 No No Yes N/A Female 6.0 Pleomorphic adenoma 4 Pharyngeal dehiscence No No N/A Female 4.3 Pleomorphic adenoma 3 No No No N/A Female 5.8 Pleomorphic adenoma 5 No Yes No N/A Female 3.1 Pleomorphic adenoma 5 Pharyngeal dehiscence No Yes N/A Female 1.5 Benign cyst 4 No No No N/A Female 3.2 Pleomorphic adenoma 4 No No No N/A Male 7.0 Pleomorphic adenoma 3 Conversion to open No No N/A Female 2.9 Benign cyst 2 No No No N/A 12 De Virgilio et al 7 49 Female 4.0 Pleomorphic adenoma N/A No No No N/A N/A 43 Male 5.5 Pleomorphic adenoma N/A No No Yes N/A N/A 25 Male 8.5 Pleomorphic adenoma N/A Combined open No No N/A N/A 31 Male 8.6 Pleomorphic adenoma N/A Combined open No No N/A N/A 36 Male 6.0 Pleomorphic adenoma N/A Combined open No No N/A N/A 56 Male 5.0 Schwannoma N/A Combined open No No N/A N/A 39 Male 3.0 Pleomorphic adenoma N/A No No Yes N/A N/A 32 Male 4.0 Schwannoma N/A No No No N/A N/A 57 Female 4.0 Pleomorphic adenoma N/A No No No N/A N/A 24 Male 5.0 Pleomorphic adenoma N/A Combined open No No N/A N/A Park et al 8 42 Male N/A Pleomorphic adenoma 2 No No No 1 N/A 31 Male N/A Pleomorphic adenoma 2 No No No 1 N/A 39 Male N/A Pleomorphic adenoma 3 No No No 1 N/A 47 Female N/A Pleomorphic adenoma 3 No No No 1 N/A 57 Female N/A Pleomorphic adenoma 3 No No No 1 N/A 29 Male N/A Pleomorphic adenoma 2 No No No 1 N/A 21 Female N/A Pleomorphic adenoma 3 No No No 1 N/A 54 Female N/A Pleomorphic adenoma 3 No No No 1 N/A 30 Male N/A Pleomorphic adenoma 3 No No No 1 N/A 57 Female N/A Elongated styloid 2 No N/A N/A 1 N/A 55 Female N/A Elongated styloid 3 No N/A N/A 1 N/A Desai et al 9 68 Female N/A Vascular malformation 2 No N/A N/A 1 1 Lee et al Male 5.8 Schwannoma 5 No No No Male 5.0 Schwannoma 6 No No No 1 7 Arshad et al Male 6.6 Lipoma 1 No No No Male 3.1 Pleomorphic adenoma 0 No No No Male 2.6 Adenoid cystic carcinoma 1 No No No 1 6 Kim et al Male N/A Pleomorphic adenoma N/A N/A N/A N/A N/A N/A 40 Male N/A Pleomorphic adenoma N/A N/A N/A N/A N/A N/A O Malley et al 13 N/A N/A N/A Benign cyst 2 No No No 1 N/A Abbreviations: NED, no evidence of disease; N/A, not available. HEAD & NECK DOI /HED FEBRUARY
4 CHAN ET AL. TABLE 2. Outcome Combined overall outcomes of the 44 patients. Mean robot time (n 5 34) Mean total operating time (n 5 27) Mean estimated blood loss (n 5 40) Mean follow-up (n 5 41) Mean time to oral diets (n 5 22) Mean length of stay (n 5 32) Measure 68.8 min min 58.2 ml 18.5 mo 1.0 d 3.0 d intended capsular incisions. Thus, the total rate of unintended capsule violation of pleomorphic adenomas in this series was 24%, a rate much higher than with open approaches. Nonetheless, with a median follow-up of only 31.5 months, it is not possible to determine the true recurrence rate in this nascent series. Long-term follow-up with proper imaging studies is necessary, given the time to tumor recurrence averages approximately 10 years. 24 Transcervical approaches to the PPS have complication rates reported as high as 30% to 40%. 14,18,19,25,26 These complications include dysphagia, trismus, Frey syndrome, first bite syndrome, paresis of the marginal mandibular nerve, and paresis of the hypoglossal nerve. These complications, the morbidity of the surgical approach, and the TABLE 3. Summary of the patients with a diagnosis of pleomorphic adenoma. Pleomorphic adenoma (n 5 29) Mean age (range) 44.8 y (21 78) Sex Male 15 (51.8%) Female 14 (48.2%) Average length of stay (n 5 19) 3.1 d Average tumor size (n 5 18) 5.0 cm Tumor capsule violation or fragmentation (n 5 27) 7 (26%) Postoperative complications (n 5 27) 2 (7%) Required combined open approach (n 5 27) 5 (19%) Recurrences (n 5 29) 0 (0%) resultant scar of a transcervical approach constitute much of the impetus to revisit the transoral approach in the first place. Our analysis of TORS for PPS lesions found complications including 2 pharyngeal dehiscences that were treated conservatively with nasogastric tube feeding. There were no neurovascular injuries, trismus, or pain noted. No correlation between complications and tumor FIGURE 2. (A) Mean length of stay 1, 6 2, 8 3, 13 4, 11 5, 10 and 6, 9 7 (current case series). (B) Mean total operative time 1, 7 2, 6 3, 6 and 4, 10 5 (current case series). (C) Total robot time 1, 7 2, 6 3, 8 and 4, 11. (D) Mean estimated blood loss (EBL) 1, 7 2, 6 3, 8 4, 13 5, 11 and 6, 9 7 (current case series). Represents the mean values of the individual articles, with the adjacent number corresponding with the bibliography in superscript. w Represents the overall mean value with all the studies combined. 296 HEAD & NECK DOI /HED FEBRUARY 2015
5 TRANSORAL ROBOTIC SURGERY OF THE PARAPHARYNGEAL SPACE FIGURE 3. Axial CT scan with intravenous contrast illustrating a benign left parapharyngeal space mass with a surrounding fat plane. The arrow points at the left parapharyngeal space mass. size, capsule rupture, or fragmentation was appreciated. Park et al 8 also noted in their 11 patients that all patients were extremely satisfied with the cosmetic result, reflecting the avoidance of the transcervical scar. In addition, the comparable total operating time to open approaches, minimal blood loss, short length of stay, and almost immediate return to an oral diet support the feasibility of TORS in the treatment of PPS neoplasms. The use of the transoral approach begs 2 questions: (1) Is this approach truly minimally invasive and less morbid than a transcervical approach? and (2) Is this approach worth the avoidance of a visible cervical scar? Although the transoral approach offers the most direct access to the PPS, this approach requires division of the pharyngeal mucosa and superior constrictor musculature. This is associated with considerable postoperative pain and, without FIGURE 4. Photograph demonstrating tumor spillage and capsule disruption in a patient after transoral robotic resection of a right parapharyngeal space mass. The empty black arrow points toward the remaining intact capsule, the solid black arrow points at the area of capsule disruption and tumor spillage. direct comparison of speech, swallow, and pain outcomes to the transcervical approach, there is no conclusive evidence that this approach is truly minimally invasive. The desire of patients to avoid a visible cervical scar is certainly understandable. Although the transoral approach avoids a visible scar, this can also be accomplished via a transcervical approach via a retroauricular incision. Both of theseissuesshouldbekeptinmindwhenconsideringthe relative advantages and disadvantages of a transoral approach. Disadvantages of the TORS approach to PPS tumors include the need for an incision through the superior constrictor and soft palate muscles, as mentioned above, the inability to safely grasp the tumor capsule, sharp instrumentation, lack of haptic feedback, no bimanual manipulation, limited space to manipulate the tumor, awkward angulation as dissection proceeds laterally deep into the PPS, and lack of carotid artery protection. All of these factors likely contribute to the high rate of capsule violation in pleomorphic adenomas because of the ease of puncture of the delicate pseudocapsule with the robotic forceps during tumor manipulation. Therefore, blunt finger dissection is still often required in the transoral approach and when not feasible resulted in the conversion of a TORS case to a standard transcervical approach. 6 O Malley et al 27 recommend the use of a combination of the TORS technique as well as blunt instrument and finger dissection. This requires removing the robotic arms from the oral cavity and bluntly dissecting the deep and lateral aspect of the tumor with finger dissection, similar to the dissection via a transcervical approach. Limitations of this study include the small sample size and relatively short follow-up duration. Although this study supports the feasibility of TORS for resection of PPS neoplasms, there is insufficient long-term data to demonstrate an equivalent or decreased recurrence rate over an open approach, despite a higher rate of capsular rupture. This higher rate of tumor rupture noted may reflect a publication bias against negative results, explaining the lack of rupture documentation before this study. Therefore, further analysis will be needed to assess the functional outcomes, learning curve, and cost benefit in using TORS for resection of PPS neoplasms. CONCLUSION TORS resection of PPS neoplasms seems to be a safe and feasible technique with minimal complications when compared to traditional transcervical techniques. Caution should be taken with pleomorphic adenomas given the relatively high likelihood of capsular violation and insufficient long-term data on recurrence rates. Further evaluation and follow-up is needed to define the role of TORS with different types of neoplasms of the PPS. REFERENCES 1. Ducic Y, Oxford L, Pontius AT. Transoral approach to the superomedial parapharyngeal space. Otolaryngol Head Neck Surg 2006;134: Stell PM, Mansfield AO, Stoney PJ. Surgical approaches to tumors of the parapharyngeal space. Am J Otolaryngol 1985;6: Work WP, Hybels RL. A study of tumors of the parapharyngeal space. Laryngoscope 1974;84: Papadogeorgakis N, Petsinis V, Goutzanis L, Kostakis G, Alexandridis C. Parapharyngeal space tumors: surgical approaches in a series of 13 cases. Int J Oral Maxillofac Surg 2010;39: HEAD & NECK DOI /HED FEBRUARY
6 CHAN ET AL. 5. De Ceulaer J, De Clercq C, Swennen GR. Robotic surgery in oral and maxillofacial, craniofacial and head and neck surgery: a systematic review of the literature. Int J Oral Maxillofac Surg 2012;41: O Malley BW Jr, Quon H, Leonhardt FD, Chalian AA, Weinstein GS. Transoral robotic surgery for parapharyngeal space tumors. ORL J Otorhinolaryngol Relat Spec 2010;72: De Virgilio A, Park YM, Kim WS, Byeon HK, Lee SY, Kim SH. Transoral robotic surgery for the resection of parapharyngeal tumour: our experience in ten patients. Clin Otolaryngol 2012;37: Park YM, De Virgilio A, Kim WS, Chung HP, Kim SH. Parapharyngeal space surgery via a transoral approach using a robotic surgical system: transoral robotic surgery. J Laparoendosc Adv Surg Tech A 2013;23: Desai SC, Sung CK, Genden EM. Transoral robotic surgery using an image guidance system. Laryngoscope 2008;118: Lee HS, Kim J, Lee HJ, Koh YW, Choi EC. Transoral robotic surgery for neurogenic tumors of the prestyloid parapharyngeal space. Auris Nasus Larynx 2012;39: Arshad H, Durmus K, Ozer E. Transoral robotic resection of selected parapharyngeal space tumors. Eur Arch Otorhinolaryngol 2013;270: Kim GG, Zanation AM. Transoral robotic surgery to resect skull base tumors via transpalatal and lateral pharyngeal approaches. Laryngoscope 2012;122: O Malley BW Jr, Weinstein GS. Robotic skull base surgery: preclinical investigations to human clinical application. Arch Otolaryngol Head Neck Surg 2007;133: Khafif A, Segev Y, Kaplan DM, Gil Z, Fliss DM. Surgical management of parapharyngeal space tumors: a 10-year review. Otolaryngol Head Neck Surg 2005;132: Fisch U. Infratemporal fossa approach to tumours of the temporal bone and base of the skull. J Laryngol Otol 1978;92: Hughes KV III, Olsen KD, McCaffrey TV. Parapharyngeal space neoplasms. Head Neck 1995;17: Kolokythas A, Eisele DW, El-Sayed I, Schmidt BL. Mandibular osteotomies for access to select parapharyngeal space neoplasms. Head Neck 2009;31: Dimitrijevic MV, Jesic SD, Mikic AA, Arsovic NA, Tomanovic NR. Parapharyngeal space tumors: 61 case reviews. Int J Oral Maxillofac Surg 2010;39: Pang KP, Goh CH, Tan HM. Parapharyngeal space tumours: an 18 year review. J Laryngol Otol 2002;116: Zhi K, Ren W, Zhou H, Wen Y, Zhang Y. Management of parapharyngealspace tumors. J Oral Maxillofac Surg 2009;67: Witt RL. The significance of the margin in parotid surgery for pleomorphic adenoma. Laryngoscope 2002;112: Polat Ş, Serin GM, Ozt urk O, Uneri C. Pleomorphic adenomas recurrences within the parapharyngeal space. J Craniofac Surg 2011;22: Cassoni A, Terenzi V, Della Monaca M, et al. Parapharyngeal space benign tumours: our experience. J Craniomaxillofac Surg [Epub ahead of print]. 24. Henriksson G, Westrin KM, Carls o o B, Silfversw ard C. Recurrent primary pleomorphic adenomas of salivary gland origin: intrasurgical rupture, histopathologic features, and pseudopodia. Cancer 1998;82: Carrau RL, Myers EN, Johnson JT. Management of tumors arising in the parapharyngeal space. Laryngoscope 1990;100: Malone JP, Agrawal A, Schuller DE. Safety and efficacy of transcervical resection of parapharyngeal space neoplasms. Ann Otol Rhinol Laryngol 2001;110: O Malley BW Jr, Quon H, Leonhardt FD, Chalian AA, Weinstein GS. Transoral robotic surgery for parapharyngeal space tumors. ORL J Otorhinolaryngol Relat Spec 2010;72: HEAD & NECK DOI /HED FEBRUARY 2015
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