Surgical management of recurrent nasopharyngeal carcinoma

Oral Oncology xxx (2013) xxx–xxx Contents lists available at ScienceDirect Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology Surgical management of recurrent nasopharyngeal carcinoma Jimmy Yu Wai Chan ⇑ Division of Head and Neck Surgery, Department of Surgery, University of Hong Kong Li Ka Shing Faculty of Medicine, Queen Mary Hospital, Hong Kong Special Administrative Region a r t i c l e i n f o Article history: Available online xxxx Keywords: Recurrent Nasopharyngeal carcinoma Nasopharyngectomy Maxillary swing Transoral robotic surgery (TORS) s u m m a r y Objectives: Nasopharyngeal carcinoma is a unique tumour which is endemic in Southern China including Hong Kong. While the treatment results for primary cancer has been encouraging, management of persistent or recurrent tumours has been challenging. Compared to other surgical approaches, the maxillary swing operation provides spacious access to the bilateral nasopharynx and the ipsilateral parapharyngeal space, allowing resection of tumours with wide margins. In this article, we will present our results in the surgical management of recurrent nasopharyngeal carcinoma. Materials and Methods: Retrospective review. Results: Over the years, we have performed salvage maxillary swing nasopharyngectomy for 312 patients. Microscopic negative resection margins were achieved in the majority (79.5%) of the patients. The overall local recurrence rate after surgery was 13.1%, the risk of which was significantly higher in patients with previous positive resection margins. The overall 5-year actuarial local tumour control and overall survival was 74% and 62%, respectively, which was significantly higher in patients with clear resection. For small tumours located in the posterior wall, minimally invasive approach can be used, which included the endoscopic resection, or more recently, the transoral robotic (TORS) assisted approach. Conclusion: The result of surgical salvage of recurrent nasopharyngeal carcinoma is promising. Every effort should be made to ensure microscopic clearance of disease as well as to minimize the potential complications of surgery that may adversely affect the subsequent quality of life. Ó 2013 Elsevier Ltd. All rights reserved. Introduction Nasopharyngeal carcinoma (NPC) is unique among other head and neck malignancies in its epidemiology, pathology and treatment outcome. It is endemic in southern China and Southeast Asia, affecting 10–50 per 100,000 populations per year [1]. The primary treatment is radiotherapy or concurrent chemoradiation depending on the stage of disease on presentation [2], while surgery is reserved for persistent or recurrent tumours after the initial therapy [3]. In general, local recurrence rates after primary treatment of NPC is approximately 10% [4]. Treatment of recurrent tumour in the nasopharynx is either by surgical salvage or a second course of radiation. Studies showed that surgery potentially offers better local tumour control and survival [5] as well as less post-treatment morbidities than reirradiation [6], and the risk of major complications can be as high as 57% [7]. Long term complications of a second course of radiation include multiple cranial nerve palsies, which lead to dysphagia and aspiration, and hence malnutrition and recurrent ⇑ Address: Division of Head and Neck Surgery, Department of Surgery, University of Hong Kong Li Ka Shing Faculty of Medicine, Queen Mary Hospital, 102 Pokfulam Road, Hong Kong Special Administrative Region. Tel.: +852 2255 4394; fax: +852 2819 3780. E-mail address: chanjyw@gmail.com pneumonia. Severe osteoradionecrosis may also occur, which is often debilitating and sometimes life-threatening. Internal carotid blowout is not an infrequent cause of death in these patients, and other complications, such as radiation myelitis, can cause peripheral weakness of limbs, severe hearing loss, and visual impairment. Surgery in the nasopharynx, however, is not without obstacles. The nasopharynx is deep seated in the central part of the skull, being at least 10 cm from the nasal vestibule anteriorly, and is obscured by the cranium superiorly, the maxilla anteriorly, the palate inferiorly, the mandible laterally, and the cervical spine posteriorly. In this chapter, we will describe the different surgical approaches to the nasopharynx and the outcome after nasopharyngectomy for recurrent NPC. Preoperative assessment Patients with NPC treated by radiotherapy should have regular endoscopic assessment after the initial therapy. In addition, those who complained of new symptoms, including nasal obstruction, persistent headache, blood stained sputum, facial numbness or cranial nerve palsies should have nasopharyngsocopy arranged. This should be followed by biopsy under local anaesthesia even if there is no gross abnormality under endoscopic examination. Submucosal tumour invasion is not uncommon after radiotherapy, and deep 1368-8375/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.oraloncology.2013.05.003 Please cite this article in press as: Chan JYW. Surgical management of recurrent nasopharyngeal carcinoma. Oral Oncol (2013), http://dx.doi.org/10.1016/ j.oraloncology.2013.05.003 2 J.Y.W. Chan / Oral Oncology xxx (2013) xxx–xxx biopsy is often necessary to confirm the diagnosis of tumour recurrence. Nevertheless, endoscopic diagnosis of early recurrent NPC is often challenging. Narrow-band imaging (NBI) in the detection of NPC has been studied, and it was found that it is potentially useful in such circumstances [8]. It can offer a timely, convenient, and a highly reliable way to assess recurrent tumours in the nasopharynx. It may also guide endoscopic resection during nasopharyngectomy [9]. Imaging is useful to assess the loco-regional extent of the recurrent tumour. It is also helpful in patients with high suspicion of tumour recurrence, and yet repeated nasopharyngeal biopsies are negative. MRI allows better tissue delineation and definition than CT scan, which is crucial for the assessment of prevertebral fascial invasion, parapharyngeal extension and petrosal internal carotid artery (ICA) involvement, and retropharyngeal lymph node metastasis [10]. The presence of skull base erosion and dural involvement should be identified, and in particular, extension through the foramen rotundum, foramen ovale, foramen lacerum and invasion of the cavernous sinus. The imaging should also cover the neck to rule out the presence of synchronous cervical nodal metastasis. More recently, [18F]-FDG PET-CT scan is available and is particularly useful for systemic work-up before surgery. It is also invaluable in the diagnosis of isolated retropharyngeal lymph node metastasis after radiotherapy, where image guided biopsy is impossible due to the location. Circulating cell free Epstein–Barr virus (EBV) deoxyribonucleic acid (DNA) is useful as a molecular marker in the monitoring of treatment response. Chan et al. studied 31 patients with undifferentiated NPC, and at a median follow up of 33.7 months, 6 distant and 3 locoregional failures were detected. Plasma EBV DNA was found to be significantly elevated in 88.9% of patients with treatment failure, while remained undetectable for those in remission [11]. For patients with recurrent NPC, the pre-operative plasma EBV DNA also predicts the chance of resection with clear margins [12], which may help to stratify patients who may benefit from adjuvant treatment. However, 15.6% of patients with recurrent NPC have no detectable plasma EBV DNA before operation, despite the presence of histologically proven, EBER positive, undifferentiated carcinoma in the nasopharynx. Pre-operative measurement should be performed in order to identify this group of patients as they cannot rely on the molecular marker to monitor the treatment response. Surgical options for recurrent nasopharyngeal carcinoma Apart from small recurrent tumours in the nasopharynx which can be treated by intracavitary [13] or interstitial [14] brachytherapy, majority of the persistent or recurrent tumours are managed by formal surgical resection. It is indicated when the disease cannot be managed by brachytherapy, either being too extensive or being located in a unfavourable position, such as the cartilage of the Eustachian tube, where the gold grains cannot be implanted securely. It is indicated when the parapharyngeal space is invaded by the tumour, where en-bloc removal of the cancer with preservation of the internal carotid artery is crucial. As mentioned before, the nasopharynx is located in a difficult position such that oncologic extirpation has been a technical challenge. The difficulty was addressed by Wilson in 1950 [15]. Over the years, efforts had been made to explore different approaches to this difficult area. The superior, trans-skull base technique had been described. After craniotomy, the frontal lobe can be lifted and retracted, allowing the resection of lesions at the clivus, nasopharynx to as low as the second cervical vertebra [16]. Complications such as meningitis, leakage of cerebrospinal fluid, formation of encephalocele and development of diabetes insipidus have been reported [17]. The lateral, infratemporal fossa approach has been described in 1979 [18]. The internal carotid artery is exposed and safeguarded during operation, but the associated morbidities include conductive hear- ing loss and trigeminal nerve dysfunction. The exposure is also not optimal for nasopharyngeal tumours that extended to the contralateral nasopharynx. When the tumour is located in the posterior wall of the nasopharynx, resection can be performed via the inferior/transpalatal approach [19]. The soft palate is retracted anteriorly and the nasopharyngeal region is approached from below. In order to improve the exposure, a transverse incision can be made between the soft and hard palate junction and the soft palate retracted posteriorly. Alternatively, the soft palate can be split in the midline and retracted laterally for better exposure [20]. However, it is difficult to manipulate the surgical instruments in the palatal wound, and the exposure of the parapharyngeal space in limited. Currently, there are two surgical techniques commonly employed for the resection of cancer of the nasopharynx. Maxillary swing nasopharyngectomy The nasopharynx and the anterior skull base are obscured from surgical approach by the maxillary antrum anteriorly. It has been reported that the whole maxilla can be removed to facilitate resection of tumours in the region. At the completion of surgery, it is possible to reinsert the maxilla as a free bone graft and no bone resorption is demonstrated at 15 months post-operation [21]. Nevertheless, in patients with previous radiotherapy, wound healing may be suboptimal and the non-vascularized bone graft may be resorped with the formation of sequestra. It is beneficial to preserve the blood supply to the maxillary antrum so that it is swung out as an osteocutaneous flap [22]. The surgical approach involves a Weber Ferguson facial incision as in maxillectomy, incision on the palate, osteotomies of the anterior wall, medial wall of the maxillary antrum, and lower portion of the zygomatic arch (Fig. 1). The pterygoid plates are also separated from the maxillary tuberosity. The maxillary osteocutaneous unit can then be swung out while maintaining its blood supply from the branches of the external carotid artery. This anterolateral approach provides complete exposure of the ipsilateral nasopharynx down to the oropharynx and the associated parapharyngeal space. With the removal of the posterior part of the nasal septum the contralateral nasopharynx can also be exposed, although access to the contralateral parapharyngeal space is limited. Because of the wide exposure, persistent or recurrent cancer of the nasopharynx can be removed with adequate margins. Resection is also possible for tumours with parapharyngeal space invasion or those with retropharyngeal lymph node metastasis [23]. In such scenario, the resection of tumours in the parapharyngeal space en-bloc with the pharyngobasilar fascia ensures microscopic tumour clearance on the surface of the ICA. The artery can be identified and safe-guarded by palpation, intra-operative ultrasound, or CT navigation. Temporalis muscle flap or microvascular free flap is frequently employed in such circumstances to protect the exposed ICA. After the tumour is resected, the surgical margins are sent for frozen section examination. If one or more of the margins showed the presence of microscopic tumour deposits, further resection would be performed, if possible. Upon the completion of surgery, the maxillary osteocutaneous unit was returned into position and the osteotomy sites were fixed with titanium mini plates and screws. A pre-fabricated dental obturator was fitted to ensure accurate dental positioning. Tracheostomy was performed for airway protection and nasogastric tube was inserted for feeding during the early post-operative period. Over the past 2 decades, we have performed salvage nasopharyngectomy for 312 patients using the maxillary swing approach [24]. Majority (94.6%) of the tumours were undifferentiated carcinoma which were Epstein-Barr virus encoded RNA (EBER) positive. Please cite this article in press as: Chan JYW. Surgical management of recurrent nasopharyngeal carcinoma. Oral Oncol (2013), http://dx.doi.org/10.1016/ j.oraloncology.2013.05.003 J.Y.W. Chan / Oral Oncology xxx (2013) xxx–xxx 3 Figure 1. (Left) Patient with recurrent nasopharyngeal carcinoma involving the left nasopharynx. Left maxillary swing nasopharyngectomy was performed via the left Weber Ferguson Longmire incision. (Middle) After the osteotomies, the maxillary osteocutaneous unit (M) was swung out to expose the tumour in the ipsilateral nasopharynx. (Right) Specimen after nasopharyngectomy showing the tumour (T) resected with wide margins. The cartilaginous portion of the Eustachian tube (splinted with yellow tube) was resected en-bloc with the tumour. The median interval between the initial radiotherapy and the detection of tumour recurrence was 22 months. Macroscopic tumour clearance was achieved in all patients. Microscopically clear resection margins was achieved in 79.5% of the subjects, and these patients had received subsequent adjuvant treatment, if possible. All patients survived the operation, and the mean hospital stay was 12 days. After a median follow up of 34 months, the overall 5-year actuarial local tumour control was 74%, which was significantly higher in patients with clear resection margins (79% vs. 57%, p = 0.000). The 5-year overall survival was 62%, which, again, was significantly higher in patients with clear resection (63% vs. 37%, p = 0.000). Tumor size and the resection margin status were the two independent factors that significantly influence the surgical outcome. With improving experience, larger tumours can be resected with oncologically satisfactory results. Tumours with parapharyngeal invasion or retropharyngeal lymph node metastasis, the lesion can be resected down to and including the pharyngobasilar fascia. For tumours with encasement of the ICA or erosion of the skull base around the carotid canal, the tumour can be removed in staged operations. In the first stage surgery, the cerebral perfusion is secured using an extra-cranial intra-cranial bypass vascular graft. This is followed by the second stage operation, when the tumour is resected en-bloc with the petrosal ICA and skull base bone using a combined cranio-facial resection. The resultant defect is usually reconstructed by microvascular free flaps. With such an extended approach, 81.8% of curative resection rate can be achieved in our group of 22 patients [23]. None of the patients had neurovascular complications after surgery. Except for 1 patient who was found to have local recurrence and systemic metastasis soon after surgery, the rest of the patients remained disease free. The local recurrence rate after salvage nasopharyngectomy is 13.1% [25], the risk of which is significantly higher in patients with positive resection margins at the previous nasopharyngectomy (39.6% vs. 6.9%, p = 0.006). The recurrence can occur at the ipsilateral (60.6%) or contralateral (30.3%) nasopharynx, as well as the nasal side of the soft palate (9.1%). Overall, 63.6% of these patients are amenable for further surgery. The most common reason for inoperability is intracranial extension with cavernous sinus invasion, followed by encasement of ICA with substantial paraspinal infiltration. Depending on the location of the recurrent tumour, the proportion of patients where further surgery is feasible is 50% for ipsilateral tumour, 80% for contralateral recurrence, and 100% for nasal floor recurrence. More than half of the patients operated required flap coverage of the exposed skull base and the ICA to prevent subsequent osteoradionecrosis and carotid blowout. In a longitudinal study of the quality of life (QOL) in patients after maxillary swing nasopharyngectomy, it was found that there is no significant change in the mean global health system score after surgery [26]. Five functioning domains were studied, including physical, role, emotion, cognitive and social functions. Majority of them were satisfactory after surgery, apart from social functioning, which scored slightly lower than the others. The presence of post-operative palatal fistula significantly affects the QOL, resulting in weight loss and poor social eating. In view of this, a modification of the palatal incision is now adopted [27]. By using a curvilinear incision over the ipsilateral side of the palate, the mucosal incision is no longer overlapping with the palatal osteotomy site, thereby effectively reducing the rate of palatal fistula from 24% to 4.3%. The other post-operative complication that significantly affects the QOL after surgery is the development of skull base osteoradionecrosis (ORN). The presence of ORN is associated with significantly more pain, more consumption of analgesics, and poorer social contact. To prevent this complication, coverage of the raw bone after nasopharyngectomy is mandatory. Small area of exposed bone can be resurfaced by the use of the posteriorly pedicled middle turbinate mucoperiosteal flap [28] or nasal septal mucosal flap [29]. For wide area of raw bone, especially those with exposed petrosal ICA, microvascular free flap remains the best option for coverage. In general, the QOL is good for patients after salvage nasopharyngectomy using the maxillary swing approach. Attention should be paid to achieve curative resection and to avoid complications, such as palatal fistula and ORN after surgery. The mean hospital stay for patients after maxillary swing nasopharyngectomy is 8.2 days. The mean operative time is 382 min and 8.3% of patients require blood transfusion during surgery, and the mean transfusion requirement is 1.2 l of pack red cells. All patients can resume oral feeding upon discharge. Common complications after surgery include facial numbness (7.4%), ectropion (1.8%), epiphora (6.5%), trismus (9.2%), palatal fistula (4.3%) and middle ear effusion (37.8%). Minimally invasive nasopharyngectomy With improvements in the visualization, instrumentation and technology in endoscopic sinus surgery, surgeons have extended their practice to nasal cavity and sinus malignancy surgery. After Please cite this article in press as: Chan JYW. Surgical management of recurrent nasopharyngeal carcinoma. Oral Oncol (2013), http://dx.doi.org/10.1016/ j.oraloncology.2013.05.003 4 J.Y.W. Chan / Oral Oncology xxx (2013) xxx–xxx Figure 2. (Above, left) T2 weighted MRI showed the presence of recurrent nasopharyngeal carcinoma (white arrow) at the posterior wall of the nasopharynx with no parapharyngeal extension. (Above, right) Endoscopic view of the recurrent tumour (T) at the posterior nasopharyngeal wall. (Below, left) In order to provide working space for the robotic instruments, the soft palate was split longitudinally and retracted with the help of the Dingman retractor. (Below, right) Magnified view of the surgical field at the console. The tumour is removed under direct vision using the grasping forceps and scissors with monopolar diathermy. the first report of trans-septal endoscopic nasopharyngectomy by Yoshizaki et al. [30], further modification of the techniques are described to improve the exposure for resection, including removing the inferior turbinate [31]. Adequate resection of small tumour located in the posterior wall of the nasopharynx can be achieved with the endoscope approach, and the oncological result has been encouraging. While much has been made about obviating the need for an incision in endoscopic nasopharyngectomy, the major advantage may well truly be the improved visualisation. En bloc resection of tumour is made easier using electric knife with an adjustable angle of knifepoint [32] or laser [33]. The ordinary instruments for nasoendoscopic surgery, however, limits the oncological resection of larger tumours, especially on the lateral wall of the nasopharynx. There are increasing reports on the efficacy of transoral robotic surgery (TORS) in head and neck surgery, particularly for pathology in the oropharynx [34], supraglottic larynx [35] and upper hypopharynx [36]. Its use on removing recurrent tumours in the nasopharynx has also been described [37]. Access to the nasopharynx is facilitated by a longitudinal split of the soft palate (Fig. 2). The tumour is visualised using a 0° 8-mm dual channel camera introduced transorally, and it is removed using a 5-mm Maryland grasping forceps mounted to left robotic arm and a 8-mm scissors with monopolar diathermy mounted to the right robotic arm. The threedimensional camera of the surgical robot provides excellent visualization, and the maneuverability of the robotic instruments with the Endowrist design is a major advantage over the traditional nasoendoscopic instruments, especially for deep and small area like the nasopharynx. When the sphenoid bone has to be removed due to tumour involvement, the procedure can be performed by a combined transnasal endoscopic and transoral robotic assisted approach [38]. The major drawback of the TORS nasopharyngectomy is the lack of tactile sensation, and currently, the procedure is limited to the resection of small recurrent tumours with minimal parapharyngeal invasion. If major resection of the parapharyngeal space is necessary, it is advisable to identify and protect the ICA through neck to the skull base before tumour extirpation is contemplated. Conclusion Surgical salvage of recurrent NPC is an effective treatment modality with acceptable morbidity. 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