Long-Term Outcomes of Nasopharyngectomy Using Partial Maxillectomy Approach

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1 The Laryngoscope VC 2015 The American Laryngological, Rhinological and Otological Society, Inc. Long-Term Outcomes of Nasopharyngectomy Using Partial Maxillectomy Approach Li Shia Ng, MMed (ORL); Chwee Ming Lim, MMed (ORL); Kwok Seng Loh, FRCS Objectives/Hypothesis: To determine the long-term outcomes of a prospective cohort of 20 patients who had nasopharyngectomy using an open partial-maxillectomy approach. Method: A prospective cohort study of the surgical outcomes of patients with recurrent T1 (rt1) and rt2 nasopharyngeal carcinoma recurrence. Results: There were 14 male and six female patients. The mean age was 49 years. The mean duration of follow-up was 60.4 months. All of the surgical margins were free of malignancy. Ten patients (50%) developed recurrences. The 5-year local control rate, disease-free, disease-specific, and overall survivals were 70%, 48.9%, 70.2%, and 66.7%, respectively. There were no major intraoperative complications. The most common morbidity was pain. The median length of hospitalization was 4 days. Conclusion: Early local recurrence of nasopharyngeal carcinoma can be treated surgically using a partial maxillectomy approach. The long-term outcomes are similar to nasopharyngectomy performed using the more common approaches. Key Words: Carcinoma, maxilla, nasopharynx, outcomes, recurrent, surgery, survival. Level of Evidence: 4. Laryngoscope, 126: , 2016 INTRODUCTION Approximately 10% of newly diagnosed nasopharyngeal carcinoma (NPC) patients will develop local recurrences after treatment. 1 Half of these local recurrences are small-volume recurrent (rt1) to rt2, and the other half are rt3 and rt4 recurrences. 1 Recurrences can be treated with curative intent by surgery. Surgery is a treatment option that avoids the risks of complications from a second course of radiation. Different surgical approaches to access the nasopharynx have been described over the years. Most of these approaches access the nasopharynx via the transpalatal and/or transmaxillary route. The outcomes of surgery using these approaches are reported to have a reasonable local control that is as good, if not better than, a second course of radiation. However, there have not been many reports of long-term outcomes of a homogenous population of recurrent NPC patients treated by a single surgical approach. The aim of this study is to report on the long-term outcomes of a partial maxillectomy approach for small-volume recurrent NPC. From the Department of Otolaryngology Head and Neck Surgery, National University Health System (L.S.N., C.M.L.); and Department Otolaryngology, National University of Singapore (K.S.L.), Singapore. Editor s Note: This Manuscript was accepted for publication October 14, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Dr. Kwok Seng Loh, Department of Otolaryngology Head and Neck Surgery, National University Health System, 1E Kent Ridge Road, Singapore entv5@nus.edu.sg DOI: /lary MATERIALS AND METHODS In this study, we included only patients with recurrent, undifferentiated nonkeratinizing NPC who underwent nasopharyngectomy via a partial maxillectomy approach. From 2004 to 2011, 30 patients were diagnosed with NPC, which required surgical treatment. Of these 30 patients, 10 were excluded from this study. Eight underwent endoscopic nasopharyngectomy. One patient had a combined partial maxillectomy and mandibulotomy approach to resect tumor that extended into the lateral pharyngeal wall; one patient had newly diagnosed NPC but required surgery because of previous radiation for tonsil squamous cell carcinoma. Of the 20 patients accrued into the study, nineteen had surgery performed via the lateral rhinotomy incision and one via the midfacial degloving approach. The patients were prospectively followed up, and the study accrual was stopped on December 31, The demographics, tumor-node-metastasis (TNM) staging, and surgical outcomes were analyzed and reported as of December 31, The primary outcomes included recurrence rate and local control rate, as well as survival outcomes. Recurrences were classified as local, regional, or distant. The secondary outcomes were postoperative complications and duration of hospitalization. The duration to the development of the recurrence was taken to be the time from nasopharyngectomy to the date of diagnosis of the first recurrence in months. The survival outcomes included 5-year disease-free, disease-specific, and overall survivals. The time period for disease-free survival was the time from nasopharyngectomy to the date of the first recurrence or last follow-up. The time period for disease-specific and overall survivals was defined as the time from nasopharyngectomy to death as a direct result of NPC or any cause, respectively. Kaplan-Meir survival analysis was performed, and parameters were analyzed. Partial Maxillectomy Approach Under general anaesthesia, an oral endotracheal tube is inserted. For the 19 patients who had lateral rhinotomy

2 our patients, resection did not breach the pharyngobasilar membrane because the tumor volume was small in general. Upon completion of resection, frozen sections are taken to ensure clear margins. The incision sites are closed, and nasal packs inserted for up to a week to allow for healing by secondary intention and to prevent blood stained nasal discharge. The patients are fed orally on the first postoperative day and oral antibiotics are prescribed for 1 week. These patients are discharged after a few days in the hospital. Fig. 1. Partial maxillectomy following lateral rhinotomy incision and osteotomies of anterior and medial walls of left maxilla. [Color figure can be viewed in the online issue, which is available at performed, the incision was made on the side of the nasopharynx in which the tumor bulk was located. The midfacial degloving approach was used in one patient. In both incisions, the anterior wall of the maxilla is exposed, with the nasal cavity forming the medial extent of exposure and the infraorbital nerve forming the lateral extent. To prevent epiphora, the nasolacrimal duct is marsupialized. Next, the anterior wall is burred with a high-speed drill, and the maxillary sinus is entered medial to the infraorbital nerve. The osteotomies are then created to remove the anteriormedial walls of the maxilla (Fig. 1). The inferior turbinate is removed, but the middle turbinate may be preserved. The posterior wall of the maxilla is then removed and the pterygoid plates are chiseled out. The sphenopalatine artery medially and the maxillary artery posteriorly have to be ligated. To allow exposure to the entire nasopharynx from the anterior direction, the posterior half of the nasal septum is resected completely. Once the nasopharynx is adequately exposed, resection of the tumor with margins is carried out. Superiorly, the sphenoid sinus is entered and the floor of the sinus is removed. This is next dissected continuous with the roof of the nasopharynx. The depth of the resection at the nasopharynx is brought to the level of the clivus, thus resecting the longus capitis muscle. Using monopolar diathermy, the tumor is then resected toward the lateral aspect, the limit being the lateral pterygoid muscle or guided by the extent of the recurrent tumor. The cartilaginous auditory tube, together with the tensor veli palatini and levator palatini muscles, is transected. The internal carotid artery is palpated for as the resection progresses, at a point posterior to the pterygoid plates. The pharyngobasilar membrane is also the anatomical barrier that aids in avoiding injury to the carotid artery. In RESULTS The demographics and clinical pathological parameters of the 20 patients are shown in Table I. There were 14 males and six females, with both the mean and median at 49 years of age. The majority were classified as having recurrent T1 disease. The mean and median duration of follow-up were 60.4 months and 58.5 months, respectively. Recurrences and outcomes are shown in Table II. Ten patients (50%) had recurrences, and the mean time to recurrence was 41 months. Of these recurrences, the majority were local and distant. The 3- and 5- year local control rates were 75% and 70%, respectively. The mean and median time to local recurrence postnasopharyngectomy were 32 months and 14 months, respectively (8 116 months). Of the seven patients with local recurrence, two were salvaged with further radiation. Of these two patients, one had persistent disease whereas the other remained free of disease. There were four patients who were deemed not salvageable because of intracranial involvement and concomitant distant disease. One patient underwent further nasopharyngectomy by the endoscopic approach. Twelve (60%) of the cohort studied were alive and eight (40%) were dead at the time of analysis. Of these eight, seven (35%) died of disease, whereas one (5%) died from other causes unrelated to NPC. The 5-year disease-free survival was 48.9% (Fig. 2); the 5-year disease-specific survival (Fig. 3) was 70.2%; and the 5-year overall survival was 66.7% (Fig. 4). The mean duration of surgery was 3 hours, and there was no major intraoperative complication in particular, carotid artery blowout. The most common postoperative side effect was pain. There was one patient with severe bleeding, which occurred 1 month postnasopharyngectomy as a result of hemorrhage from the sphenopalatine artery during cleaning of the crusts. This patient required intraoperative hemostasis. Another patient, with preexisting ankylosing spondylitis, developed atlantoaxial subluxation. None of the patients had increased trismus postoperatively. Speech and swallowing were well maintained, and diet was started on the first postoperative day. The median duration of hospitalization was 4 days. Four patients required more than 4 days of hospitalization, but three of them had concomitant radical neck dissection. DISCUSSION The preferred treatment of local recurrence in NPC is accepted by many to be nasopharyngectomy. This is because of concerns that a second dose of radiation is 57

3 TABLE I. Demographics and Clinical Pathological Parameters. Patient Age Gender TNM rtnm Hospitalization (days) Surgical Complication Pain F T1N2M0 T1N0M0 3 Nil Yes F T1N0M0 T1N0M0 3 Nil Yes M T4N0M0 T1 N0M0 3 Nil Yes M T2N0M0 T1 N0M0 3 Atlantoaxial subluxation Yes M T1N2M0 T1N1M0 5 Nil Yes M T2bN2M0 T1N0M0 4 Nil No M T2bN0M0 T1N0M0 3 Nil Yes M T3N2M0 T2bN0M0 4 Nil No M T3N0M0 T1N0M0 4 Nil Yes F T1N0M0 T1N0M0 4 Nil Yes F T2N2M0 T1N1M0 6 (L radical neck) Nil No F T2aN1M0 T2aN0M0 3 Nil Yes M T2aN2M0 T1N0M0 3 Nil No M T1N2M0 T1N1M0 8 (L radical neck with PM flap) Nil Yes F T1N0M0 T1N0M0 4 SPA bleeding No M T2N0M0 T1N0M0 3 Nil Yes M T2bN2M0 T1N0M0 4 Nil Yes M T4N2M0 T1N1M0 5 (L radical neck) Nil Yes M T1N2M0 T1N0M0 3 Nil No M T1N2M0 T1N0M0 4 Nil No F 5 female; L 5 left; M 5 male; PM 5 pectoralis major; rtnm 5 recurrent TNM staging; SPA 5 sphenopalatine artery; TNM 5 primary tumor-nodemetastasis staging. Patient Recurrence TABLE II. Recurrences and Outcomes. Time to Recurrence (months) Outcome Time to Death (months) 1. L,D 42 DD L 115 Alive 3. NER Alive 4. NER Alive 5. R,D 53 DD NER Alive 7. NER Alive 8. D 50 Alive 9. L 10 DD L 21 Alive 11. L,R 8 DD D 41 DD NER Alive 14. L,D 13 DD NER Alive 16. NER Alive 17. NER Alive 18. L,R 14 DD NER DU NER Alive D 5 distant recurrence; DD 5 died of disease; DU 5 died of unknown cause; L 5 local recurrence; NER 5 no evidence of recurrence; R 5 regional recurrence. associated with a high risk of complications. Several surgical approaches have been described, including endoscopic 2 4 ; infratemporal fossa 5 ; maxillary 6 or mandibular 7 swing; and more recently, the transoral robotic-assisted approach. 8 From the literature, the most time-tested and widely reported method is the maxillary swing approach described by Wei et al. 6 There is very sparse data that specifically compare the efficacy of different types of nasopharyngectomy. The data for open and endoscopic nasopharyngectomy seems Fig. 2. Disease-free survival. [Color figure can be viewed in the online issue, which is available at

4 TABLE III. Comparison of Outcomes of Nasopharyngectomy. Study (year published) Number Patients Overall Survival Disease-Free Survival Local Control Rate King et al. 13 (2000) 31 47% 42% 43% Wei et al. 10 (2011) 246 N/A 56% 74% Vlantis et al. 11 (2011) % 46.7% Bian et al. 9 (2012) % NA 53.5% Ng et al. (2015) % 48.9% 70% N/A 5 not applicable. Fig. 3. Disease-specific survival. [Color figure can be viewed in the online issue, which is available at Fig. 4. Overall survival. [Color figure can be viewed in the online issue, which is available at to suggest similar local control rates as well as overall survivals. 4,9 11 It has, however, been reported that the maxillary swing approach is associated with improved survivals in nasopharyngectomy for rt1 and rt2 disease compared to midfacial degloving transmaxillary approach. 12 At our center, our approach to local recurrences in NPC is to consider surgery if it is classified as rt1, rt2, or limited rt3. Most rt3 and all rt4 tumors are not considered for surgery and treated by chemotherapy and/or radiation. Because all tumors amenable to surgery are limited in volume, we used an open surgical approach via partial maxillectomy to access the nasopharynx and the adjacent area. We have found that the access to the midline via this approach is adequate, and the lateral extent of surgery can go as far as the pterygopalatine fossa. In addition, this approach allows adequate exposure for resection with clear margins in 100% of cases. This is of particular importance because positive margins are reported commonly to influence the local disease-free and overall survivals negatively We believed that partial maxillectomy is an alternative method for resecting locally recurrent NPC and proceeded to analyze the long-term outcomes of a homogenous group of patients with first-time locally recurrent undifferentiated NPC. This surgical approach was started in 2003, and this study was to assess the long-term outcomes of a cohort who had undergone open partial maxillectomy approach for nasopharyngectomy. Over the years, endoscopic approach has also become part of our algorithm for treatment of locally recurrent NPC. Endoscopic nasopharyngectomy may likely be the more common surgical approach for many centers, including ours. Although we have not analyzed our experience with endoscopic approaches, based on our experience, both open partial maxillectomy and endoscopic approaches are viable alternatives for small-volume NPC local recurrences. Our data shows that 60% of our cohort are alive, and at least 61% survived 5 years after nasopharyngectomy. The major failure remains local recurrent disease. In this study, results showed that at 5 years, the local recurrence rate was 30%, but longer-term surveillance revealed that 35% of the nasopharyngectomy cohort eventually recurred locally. Various studies reported local and locoregional recurrence rates ranging from 3% to 69% and 1.2% to 43%, respectively. 9,10,13 Studies reporting 5-year local control and survival rates postnasopharyngectomy include patients who have undergone surgery via mainly the maxillary swing and transpalatal approaches. In these studies, the 5-year local control rates ranged from 47% to 74%, 7,9 11 the 5- year disease-free survival from 42% to 63%, 7,10,13,14 and the 5-year overall survival from 42.1% to 51.9%. 9,11 13 Our 5-year local control rates (70%), disease-free survival (48.9%), and overall survival (66.7%) were similar to these reported series. Table III shows the 5-year overall survival, disease-free survival, and local control rate of series reported from the year We recognize that our cohort in this study was a selected group of smallvolume local recurrence and thus is expected to be similar to the higher end of the survival outcomes reported in other series. It does not necessarily reflect that this method is superior in terms of eventual outcomes. Rather, this data reaffirms our belief that open partial maxillectomy approach nasopharyngectomy for rt1 to 59

5 rt2 recurrent NPC is a viable alternative approach. None of our patients underwent elective postoperative radiation, which has been suggested to improve local tumor control rate and survival. 7,13 The main complication postnasopharyngectomy was that of pain. This was often reported by the patients as a headache or neck ache. The pain was controlled by analgesia and invariably resolved. Palatal fistula was not experienced in partial maxillectomy approach because it does not involve splitting of the palate. Other complications of maxillary and mandibular swing approaches, including significant trismus, nasal regurgitation, and dysphagia, 10,13,14 were not seen in our series of patients. There was no surgical mortality. The median hospitalization duration of 4 days was relatively shorter than the 13 days reported for other approaches. 10 The carotid artery frequently is not directly exposed or dissected as it ascends in the pterygopalatine area; therefore, no tissue flap was required and the resected area was left to heal by secondary intention. This significantly reduced operative time and the risk of posterior choanal stenosis associated with bulky flaps. The downside to healing by granulation was crusts that formed voraciously, and the resected nasopharyngeal bed had to be cleaned regularly for several months. One patient developed atlantoaxial subluxation, which might have been related to preexisting ankylosing spondylitis. We did not objectively quantify the aesthetic outcomes because the main goal of the study was to report the survival outcomes. Nonetheless, we noted that none of the patients complained of the aesthetic outcomes during follow-up, and no scar revision had to be performed. This may not be overly surprising because the lateral rhinotomy incision forms part of the incision used in maxillary swing approaches, for which good cosmesis outcomes have been reported. 10 One of the limitations of this study is that this approach to nasopharyngectomy is confined largely to rt1 and rt2 tumors, unlike the maxillary swing that has been performed on a significant number of patients with rt3 and rt4 tumors. 14 However, rt3 and rt4 NPC are associated with poor outcomes after surgery 1,9,10,13 with a significant number of positive margins. Hence, the practice in our institution is that surgery is advocated only for rt1 and rt2 NPC. We also recognize that we are reporting a relatively small number of patients. Nevertheless, this group of patients was followed prospectively. In addition, this was a long-term study of outcomes for which there are not many in the literature. It is also a report of the experience of a single surgeon versus a report of cases spanning over several decades reflecting the outcomes of different surgeons. CONCLUSION The partial maxillectomy approach to surgical resection of small-volume locally recurrent nasopharyngeal carcinoma is a viable option. The survival and local tumor control rates are similar to those reported using other nasopharyngectomy approaches. The exposure to the central and lateral aspect of the nasopharynx is adequate to achieve en-bloc resection and clear margins. In the long term, it does not appear to be associated with major complications. BIBLIOGRAPHY 1. Yu KH, Leung SF, Tung SY, et al. Survival outcome of patients with nasopharyngeal carcinoma with first local failure: a study by the Hong Kong Nasopharyngeal Carcinoma Study Group. Head Neck 2005;27: Wen YH, Wen WP, Chen HX, Li J, Zeng YH, Xu G. Endoscopic nasopharyngectomy for salvage in nasopharyngeal carcinoma: a novel anatomic orientation. 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