Acta Oto-Laryngologica
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution Fenglin Sun, Yan Yan, Dongmin Wei, Wenming Li, Shengda Cao, Dayu Liu, Guojun Li, Xinliang Pan & Dapeng Lei To cite this article: Fenglin Sun, Yan Yan, Dongmin Wei, Wenming Li, Shengda Cao, Dayu Liu, Guojun Li, Xinliang Pan & Dapeng Lei (2017): Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution, Acta Oto-Laryngologica, DOI: 10.1080/00016489.2017.1378433 To link to this article: http://dx.doi.org/10.1080/00016489.2017.1378433
Published online: 05 Oct 2017.
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ACTA OTO-LARYNGOLOGICA, 2017 https://doi.org/10.1080/00016489.2017.1378433
RESEARCH ARTICLE
Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution Fenglin Suna,b, Yan Yanc, Dongmin Weia, Wenming Lia, Shengda Caoa, Dayu Liua, Guojun Lid,e, Xinliang Pana and Dapeng Leia a
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Department of Otorhinolaryngology, Qilu Hospital, Shandong University, Key Laboratory of Otolaryngology, NHFPC (Shandong University), Jinan, Shandong, P. R. China; bDepartment of Otorhinolaryngology, Zibo Central Hospital, Zibo, Shandong, P. R. China; cDepartment of Surgery, Qilu Hospital, Shandong University, Jinan, Shandong, P. R. China; dDepartments of Head and Neck Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; eDepartments of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
ABSTRACT
ARTICLE HISTORY
Purpose: To evaluate clinical features, diagnosis, surgical management, and treatment of parapharyngeal space tumors in a single-center setting due to limited knowledge of diagnosis and treatment of parapharyngeal space. Methods: Clinical records of 103 patients were included for the analysis of such clinical characteristics. Results: A total of 29 different types of tumors were diagnosed after operation: 20 benign and 9 malignant. With a follow-up of 31–84 months for 90 benign cases, 84 cases had no recurrence and 6 cases were lost to follow-up. In contrast, with an 8- to 51-month follow-up for 13 malignant cases, 11 patients died and 2 were lost to follow-up. Furthermore, for postoperative complications, 3 cases had Horner syndrome, 2 had hoarseness, 2 had facial nerve dysfunction, and each for other types. Conclusions: Surgery remains the first choice for the treatment of parapharyngeal space tumors, with the transcervical approach used for most tumors. Moreover, CT or MRI may assist in making decisions about operation schemes.
Received 19 June 2017 Revised 18 August 2017 Accepted 26 August 2017 KEYWORDS
Parapharyngeal space tumors; head and neck neoplasms; diagnostic imaging; surgical treatment
Abbreviations: PPS: parapharyngeal space; CT: computed tomography; MRI: magnetic resonance imaging; FNAB: fine-needle aspiration biopsy; AMS: average of maximum size of the tumor; MMS: mean maximum size; HB: House-Brackman grading of facial nerve; LCN: low cranial nerves.
Introduction The parapharyngeal space (PPS) is a deep neck space in the lateral pharyngeal region. The PPS is in the shape of an inverted pyramid, with the greater cornu of the hyoid bone as its apex and the skull base as its floor [1]. It is divided into an anterior muscular compartment and a posterior neurovascular compartment by muscular aponeurotic partition [2]. A wide spectrum of benign and malignant primary pathologies has been encountered in this complex anatomic region. PPS tumors are rare, comprising only 0.5% of the neoplasms of the head and neck [1]. A variety of primary tumors arise from the normal structures of the PPS; 80% are benign and 20% malignant. The most common benign neoplasms are salivary pleomorphic adenomas [3], followed by paragangliomas and neurogenic tumors. Salivary gland neoplasms are the most common primary malignant tumor [4]. Various surgical approaches have been reported, including transcervical, transparotid, and transoral approaches – separately or combined for more exposure and resection of PPS tumors – as well as the use of a robot [5].
Because primary PPS tumors are hidden and have diverse characteristics and anatomical complexities, they are challenging to treat for otorhinolaryngology head and neck surgeons. There is currently little information about the clinical features, diagnoses, surgical approaches, and treatment outcomes of PPS tumors. The purpose of this study was to collect data on these tumors by analyzing our institution’s 15-year experience in the treatment of PPS tumors.
Materials and methods Patients with PPS tumors who were treated from January 1999 to June 2014 at our institution were identified through a database search, and their medical records were retrospectively evaluated and analyzed. The patients with congenital branchial cysts, metastatic neoplasms, and primary tumors originating from other regions involving PPS were excluded. Data regarding patient age, sex, clinical features, diagnosis, characteristics of the PPS mass, surgical approaches, complications, and outcomes were collected and analyzed.
CONTACT Xinliang Pan [email protected]; Dapeng Lei [email protected] Department of Otorhinolaryngology, Qilu Hospital, Shandong University; Key Laboratory of Otolaryngology, NHFPC (Shandong University), 107 West Wenhua Road, Jinan 250012, Shandong, P. R. China These authors contributed equally. ß 2017 Acta Oto-Laryngologica AB (Ltd)
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F. SUN ET AL.
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Table 1. Incidence and frequency of clinical symptoms.
Table 2. Incidence and frequency of clinical signs.
Types of symptoms
No.
%
Pain Foreign body sensation pharynx Dysphagia Snoring Hoarseness Dysarthria Rhinocleisis Dyspnea Hearing impairment Asymptomatic Total
17 12 10 8 4 3 2 1 1 45 103
16.5 11.6 9.7 7.8 3.9 2.9 1.9 1.0 1.0 43.7 100.0
All patients had received a thorough interrogation about their medical history and a detailed physical examination. In addition to preoperative examinations including electrocardiography, chest radiography, and hematologic laboratory examination, all patients underwent enhanced multi-slice spiral computed tomography (CT) of the neck. The surgical approach was dictated by the location of the tumor, its dimensions, its relationship to anatomic structures (carotid artery, jugular vein, cranial nerves), and the degree of suspicion of malignancy. Follow-up data had been obtained through personal interviews, examinations, and/or telephone conversations with patients or family members. We used the SPSS (SPSS Inc., Chicago, IL) statistical package for data analysis to describe and analyze the clinical features, diagnoses, surgical approaches, and treatment outcomes of patients with PPS tumors.
Results We identified a total of 103 patients (56 males and 47 females) with PPS masses who met the inclusion criteria. The mean age was 42 years (range, 4–78 years); six patients were children under 10 years of age. Five patients were referred to our department after treatment in another hospital; the remaining patients were treated in our hospital for the first time. The average time from onset to treatment was 21.0 months. In this cohort, 30 (29.1%) of the tumors were found to be located in prestyloid space, while 73 (70.9%) originated from poststyloid space. The main clinical symptoms of patients are summarized in Table 1. The most frequent symptoms were pain (16.5%), foreign body sensation (11.6%), and dysphagia (9.7%). A significantly high number of patients (45 patients; 43.7%) had asymptomatic growth detected during a routine checkup or while scanning for other reasons. In this study, the most frequent clinical signs were neck mass (59.2%), oropharyngeal mass (8.7%), and parotid mass (3.9%), while approximately 23.4% of patients had no clinical signs (Table 2). In addition to CT in all patients, five patients with disease highly suspicious of carotid body paraganglioma showing untidy margins with the carotid artery underwent digital subtraction angiography (DSA) preoperatively, and seven patients underwent fine-needle aspiration biopsy (FNAB) at other hospitals preoperatively. Apart from tumors with suspicion for vascular tumors, cysts, accessory nerve ganglion cells, and suggested nerve sheath tumors by CT scanning
Signs
No.
%
Neck mass Oropharyngeal mass Parotid mass Hemiprosoplegia Hypoglossus paralysis No signs Total
61 9 4 3 2 24 103
59.2 8.7 3.9 2.9 1.9 23.4 100
Table 3. Surgical approaches and tumor size. Surgical approaches
No.
%
MMS (cm)
Transcervical Transparotid Transoral Mandibulotomy Total
75 11 8 9 103
72.8 10.7 7.7 8.8 100
5.8 4.1 4.4 6.9 5.6
MMS: the mean of maximum sizes of the tumors.
before operation, 41 patients had intraoperative frozen section biopsies, according to that the preoperative assessment showed evidence of malignancy and whether patients were willing to undergo this examination. All patients underwent postoperative pathological examination. The surgical approaches and mean maximum sizes (MMSs) of the tumors are shown in Table 3. The transcervical surgical approach was most frequently used (75 cases, 72.8%). In these patients, tumors were generally located between the carotid sheath and pharyngeal constrictor muscles and in the deep posterior belly of the digastric muscle. Eleven patients with tumors located in the deep lobe of the parotid gland in the prestyloid space underwent a transparotid approach. The key was to identify, elevate, and preserve the facial nerve and its branches, especially the marginal mandibular branch. In the group who received a transoral approach, four cases had en bloc resection. Another four cases had intracapsular excision because the tumors were larger than 5.0 cm and complete exposure was difficult. The major steps were to expose the tumor capsule through the intraoral incision first, then cut open the capsule following block resection of the tumor tissue, and finally remove the capsule. In the case of mandibulotomy, all the patients who underwent tracheotomy were all successfully decannulated from 8 to 15 days postoperatively. All the patients underwent histopathological tests after operation. The results are presented in Table 4. A total of 41 patients underwent intraoperative frozen section examination, and their results were in agreement with the postoperative pathologic diagnosis. A total of 29 different types of tumors were diagnosed, including 20 types of benign tumors and nine types of malignant tumors. The overall frequencies of benign and malignant tumors were 87.2 and 12.8%, respectively. Of the 90 cases with benign tumors, neurilemoma was the most common type (33.0%), followed by pleomorphic adenoma (15.5%). For malignant tumors, the most frequent type was lymphoma (3.9%), followed by leiomyosarcoma (1.9%). Complications caused by surgical treatment were found in 10 patients. In cases adopting transparotid approaches, nine patients had normal VII nerve function (HB I), and
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ACTA OTO-LARYNGOLOGICA
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two had HB II in the immediate postoperative period. At the end of 6 months, the two patients recovered to HB I (Table 5). Patients with carotid body paragangliomas had the highest rate of LCN palsies, followed by Neurilemoma (Table 6). Horner Syndrome was observed in two patients with carotid body paraganglioma and one patient with neurilemoma, and this complication showed no improvement after 3–5 years of follow-up. Carotid body paraganglioma postoperative hoarseness in two patients caused by ipsilateral paralysis of the vocal cord disappeared after 6 months of conservative treatment. Hypoglossal nerve palsy was noted in one patient with neurilemoma and faded gradually after 3 weeks. Dyspnea in one patient with neurilemoma due to local bleeding improved after tracheotomy and clearing hematoma. In addition, contralateral hemiplegia caused by carotid-cavernous fistula was found in one patient with carotid body paraganglioma who underwent artificial vascular graft and anastomosis during the operation.
Among the benign tumor group of 90 patients, the patients did not receive any further treatment postoperatively. Six patients were lost to follow-up and 84 patients were followed-up for 31–84 months with no recurrence. In contrast, for malignant tumors, postoperative radiotherapy was applied in four patients with lymphoma and combined chemo-radiotherapy was given to five patients, including two with leiomyosarcoma, one with myxofibrosarcoma, one with liposarcoma, and one with malignant rhabdomyoma. The auxiliary treatment was unknown in one patient with clear cell carcinoma. The remaining three patients in the malignant tumor group refused any postoperative treatment. Thirteen patients with malignant tumors were followed-up for 8–51 months. Seven patients died, of which three patients died of recurrence of leiomyosarcoma, myxofibrosarcoma, or liposarcoma. Four patients died of metastasis, including one with malignant rhabdomyoma and three with lymphoma. Two patients with a malignant tumor were lost to follow-up.
Table 4. Histopathological diagnosis of 103 PPS tumors.
Discussion
Diagnosis Benign Neurilemoma/schwannoma Pleomorphic adenoma Carotid body paraganglioma Hemangioma Inflammatory tissue Neurofibroma Salivary gland lymphoma Vascular tumor Lipoma Cyst Others Malignant Lymphoma, non-Hodgkin Leiomyosarcoma Others Total
No.
%
34 16 8 5 5 4 2 2 2 2 10
33.0 15.5 7.7 4.8 4.8 3.8 1.9 1.9 1.9 1.9 10.0
4 2 7 103
3.9 1.9 7.0 100.0
Table 5. Preoperative and postoperative VII nerve function in transparotid approach cases. Cranial VII nerve HBI HBII HBIII HBIV HBV HBVI
Preoperative
Immediate
After 6 months
11 – – – – –
9 2 – – – –
11 – – – – –
HB: House-Brackman grading of facial nerve.
Traditionally, the PPS has been divided into the prestyloid and poststyloid compartments. In recent decades, new compartmentalization of this complex area has been proposed for the selection of appropriate surgical approaches. According to the compartmentalization of the PPS suggested by Shahinian et al. [6], Kanzaki and Nameki [7], Prasad et al. [8], proposed that the PPS could be divided into three compartments; the upper (between the skull base and the line joining the lower borders of the lateral pterygoid muscles of both sides), middle (between the line joining the lower borders of the lateral pterygoid muscles and the line joining the angle of mandible on both sides), lower part (between line joining the lower borders of the angle of the mandible and the plane of the hyoid). PPS tumors are always a challenge for surgeons to diagnose because of their rarity, atypical clinical manifestations and diverse pathological types. In this paper, we found that 87.2% of PPS tumors were benign and 12.8% were malignant, which is in agreement with a previous study that reported 80% benign and 20% malignant PPS tumors [9]. In addition, only 5.8% of the cases were found in children under the age of 10. The most common PPS tumor in our study was neurilemoma, followed by pleomorphic adenoma and paraganglioma, which differs from what has been reported previously [2,3,10].
Table 6. LCN deficits in relation to the histopathology of tumor. CRP CN CN CN CN HS
IX X XI XII
Preoperative 0 1 0 0 0
Neurilemoma Postoperative 0 3 0 0 2
Preoperative 0 3 0 0 0
Postoperative 0 3 0 1 1
Malignant tumors Preoperative 0 0 0 0 0
Postoperative 0 0 0 0 0
LCN: low cranial nerves; CRP: carotid body paraganglioma; CN IX: glossopharyngeal nerve; CN X: vagus nerve; CN XI: spinal accessory nerve; CN XII: hypoglossal nerve; HS: Horners syndrome.
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F. SUN ET AL.
Due to the concealment of the location of PPS tumors and the characteristic slow growth of these tumors, most patients tend to have large tumors at diagnosis. In our study, the longest mean diameter of the tumors was 5.6 cm, and the average time from onset to treatment was 21.0 months. The common symptoms and clinical characteristics may be diverse and non-specific. Although patients may suffer from a wide variety of symptoms and signs, the most common symptom and sign in this study were pain and the presence of a neck mass, which were the same as those from previous reports [2,3,10]. However, 43.7% of the patients had no symptoms and 23.4% of the patients had no signs, which is a potential challenge for surgeons. Imaging is essential to evaluate the location and extent of PPS neoplasms because of the limitations of physical examination in this anatomical area [11]. Arteriography is performed infrequently for the diagnostic purposes. In rare instances, it can be used to evaluate cervicocerebral collateral circulation, which may necessitate the sacrifice of major blood vessels [5]. DSA is helpful for surgeons to understand the compensation of the blood supply to the brain and Wills rings and then to properly assess the safety of resection of tumor adhering to the internal carotid artery. In this study, five patients underwent DSA and were diagnosed with carotid body paraganglioma postoperatively. Among them, three cases could not be resected directly because of severe adhesion to the internal carotid artery and common carotid artery, so vascular prosthesis bypass grafting was performed after resection. To reduce intraoperative blood loss, one patient with neurilemoma that invaded the intervertebral foramen underwent ascending cervical artery superselective embolization and vertebral artery balloon embolization. This provided strong protection for the complete resection of the tumor. It is important to have an accurate diagnosis by pathological examination preoperatively. Whether FNAB can be applied to preoperative examination of PPS tumors remains controversial. Peroral or transcervical FNAB is up to 90–95% accuracy among these cases and can be performed under CT or ultrasound guidance [12, 13]. Nevertheless, a non-diagnostic aspirate has been reported in 25–60% of cases due to the lack of cellular material, excessive bleeding, or other technical problems [5]. In our practice, FNAB was performed in seven cases and the rate of accuracy was only approximately 28.6% (2/7). There were five cases in which FNAB did not agree with our diagnosis, including four cases of neurilemoma and one case of malignant ameloblastoma. However, among 41 patients, including 11 with malignant tumors, who had intraoperative frozen section biopsy, the diagnostic accuracy reached 100. The low rate of accuracy of FNAB may result from the following: (a) more non-neurogenic tissues in neurogenic tumors, (b) no standard FNAB techniques in the nation, leading to the application of intraoperative frozen section biopsy instead of preoperative FNAB in our clinical practice. Surgical management is the main treatment for PPS tumors. However, how to appropriately choose the surgical approach and decrease the risk of surgical complications is a great challenge for surgeons. The successful resection of PPS
tumors depends mainly on two conditions: (a) correct identification and exposition of tumors for complete removal and prevention of potential recurrence and (b) minimum functional and aesthetic morbidity taking into account the risk of surgery in this space [14]. The transoral approach is commonly used for removing tumors involved only in oropharynx, small benign avascular tumors, and those not palpable in the neck or parotid regions [2,13,15]. However, this approach is considered not safe enough, for it fails to effectively avoid the neck great vessels and the cranial nerves in some cases, possibly leading to some severe complications, such as excessive hemorrhage and damage to cranial nerves. In our clinic, we used this approach to perform intracapsular resection in four cases without recurrence. In contrast, the transparotid approach is considered for small tumors located in the deep lobe of the parotid gland. It works well for patients with the prestyloid tumors or deep-lobe parotid neoplasms extending into the PPS, who require the superficial parotidectomy in advance. This approach requires identification and preservation of the main trunk of the facial nerve [16]. In the current study, the transparotid approach was applied to 11 cases, and the mean of the maximum sizes of the tumors was 4.1 cm. Our experience was that some branches of the facial nerve could be shifted in order to reveal the tumor as much as possible. If necessary, partial resection of the superficial or deep lobe of the parotid gland could be performed and the mandibular angle was pulled forward. The transcervical approach can be performed to successfully resect most PPS tumors [2,5,9,12,16]. Its advantage is that it can achieve a satisfactory exposure to tumors and the important blood vessels and nerves around them. Thus, it may be indicated for large tumors (benign and malignant), particularly for malignant tumors, whose margins are hard to determine unless touched by surgeons themselves. In this series, this approach was performed in 72.8% of the cases and the mean of maximum sizes of the tumors was 5.8 cm. We used the following skills to maximally expose the tumors: (1) cut the posterior belly of the digastric, resect the partial hyoid bone, and shift the submandibular gland medially; (2) resect partial non-functional soft tissue in the cervical sublevels IB and IIA; and (3) push down tumors from the oral cavity. These techniques can prevent greater trauma and the potential pollution of the field from other combined approaches. Mandibulotomy to improve surgical access to the PPS should be considered for selected patients, including those with malignant neoplasms, recurrent neoplasms, large benign neoplasms, and highly vascular neoplasms [17]. It can be combined with other PPS approaches and is performed mainly when a wide surgery field is required. Mandibulotomy reduces the intraoperative risks as a result of adequate exposure [3]. One or more osteotomies are involved in mandibulotomy and therefore such operations takes more time and requires experienced surgeons. In addition, the transmandibular approach can vary with the location and amount of amputated bones. In this study, nine patients underwent this approach with tracheotomy, of which four cases were malignant tumors and the
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ACTA OTO-LARYNGOLOGICA
others were very large benign neoplasms with mean tumor sizes >8 cm. Tumor histology, vascularity, size, as well as anatomical location are important factors in the determination of the appropriate surgical approach. Many surgical approaches to PPS tumors have been previously reported. However, few reports on a standard surgical approach are related to tumor location, except that Prasad et al. has proposed an algorithm for the selection of appropriate surgical approaches in the management of PPS tumors [8]. Potential complications should be explained to patients before surgery. All complications need to be managed appropriately to facilitate rehabilitation [18]. Preoperative clinical assessment of the LCN is an important factor to be taken into consideration in the management of PPS tumors [8]. In this study, postoperative neurological deficits in patients accounted for 80% (8/10) of all complications, with 50% (4/8) of these in carotid body paragangliomas. The possible reasons may be transposition of cranial nerves X and XI and the cervical sympathetic trunk caused by carotid body paraganglioma and the large number of blood vessels resulting in a bleeding field. In this study, we found that contralateral compensation plays a critical part in the cases of X and XII palsies over a period of time after surgery. Postoperative complications of vascular injury were uncommon, but often more serious. Contralateral hemiplegia caused by carotid-cavernous fistula was reported in one patient with carotid body paraganglioma who underwent artificial vascular graft and anastomosis during the operation. Such complications showed no improvement after 14-month follow-up. Besides surgery, no other treatment was administered for the benign tumors in our series, as reported by others [19,20]. In this study, the benign tumors had no recurrence, while for the malignant tumors, the 5-year survival rates were low, even though the patients received surgery combined with radiotherapy and/or chemotherapy. This suggests a poor prognosis for primary malignant tumors in PPS. In conclusion, PPS tumors are rare and have atypical clinical manifestations and diverse pathological types. Surgery is the first choice of treatment for PPS tumors, and the transcervical approach can be applied to most tumors. Furthermore, examination of CT or MRI is useful to help evaluate the tumor size, location, and possible sources and to plan the operation. Finally, PPS benign tumors have a good prognosis, while malignant tumors have a poor prognosis.
5
Funding This work was supported by the Taishan Scholars Program (No. tshw20130950), Shandong Province; the Department of Science and Technology of Shandong Province (No. ZR2013HM107, ZR2014HM005, 2015GSF118014, and 2015GSF118030); Science Foundation of Qilu Hospital of Shandong University; and the Fundamental Research Funds of Shandong University (No. 2014QLKY05).
References [1]
[2]
[3]
[4] [5]
[6] [7]
[8]
[9] [10] [11] [12]
[13]
[14]
[15]
[16]
[17]
Disclosure statement The authors declare no competing financial interests or conflict of interest.
[18]
Ethical approval
[19]
All procedures performed in studies involving human participates were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.
[20]
Maheshwar AA, Kim EY, Pensak ML, et al. Roof of the parapharyngeal space: defining its boundaries and clinical implications. Ann Otol Rhinol Laryngol. 2004;113:283–288. Dimitrijevic MV, Jesic SD, Mikic AA, et al. Parapharyngeal space tumors: 61 case reviews. Int J Oral Maxillofac Surg. 2010;39:983–989. Papadogeorgakis N, Petsinis V, Goutzanis L, et al. Parapharyngeal space tumors: surgical approaches in a series of 13 cases. Int J Oral Maxillofac Surg. 2010;39:243–250. Olsen KD. Tumours and surgery of the parapharyngeal space. Laryngoscope. 1994;104:1–28. Bradley PJ, Bradley PT, Olsen KD. Update on the management of parapharyngeal tumours. Curr Opin Otolaryngol Head Neck Surg. 2011;19:92–98. Shahinian H, Dornier C, Fisch U. Parapharyngeal space tumors: the infratemporal fossa approach. Skull Base Surg. 1995;5:73–81. Kanzaki S, Nameki H. Standardised method of selecting surgical approaches to benign parapharyngeal space turnouts, based on pre-operative images. J Laryngol Otol. 2008;122:628–634. Prasad SC, Piccirillo E, Chovanec M, et al. Lateral skull base approaches in the management of benign parapharyngeal space tumors. Auris Nasus Larynx. 2015;42:189–198. Cohen SM, Burkey BB, Netterville JL. Surgical management of parapharyngeal space masses. Head Neck. 2005;27:669–675. Panda S, Behera SK, Ray R. Parapharyngeal tumors: a review of 16 cases. J India Med Assoc. 2010;108:357–359. Gupta A, Chazen JL, Phillips CD. Imaging evaluation of the parapharyngeal space. Otolaryngol Clin North Am. 2012;45:1223–1232. Oliai BR, Sheth S, Burroughs FH, et al. “Parapharyngeal Space” tumors: a cytopathological study of 24 cases on fine-needle aspiration. Diagn Cytopathol. 2005;32:11–15. Bozza F, Vigili MG, Ruscito P, et al. Surgical management of parapharyngeal space tumours: results of 10-year follow-up . Acta Otorhinolaryngol Ital. 2009;29:10–15. Infante-Cossio P, Gonzalez-Cardero E, Gonzalez-Perez LM, et al. Management of parapharyngeal giant pleomorphic adenoma. Oral Maxillofac Surg. 2011;15:211–216. Ducic Y, Oxford L, Pontius AT. Transoral approach to the superomedial parapharyngeal space. Otolaryngol Head Neck Surg. 2006;134:466–470. Cassoni A, Terenzi V, Della Monaca M, et al. Parapharyngeal space benign tumors: our experience. J Craniomaxillofac Surg. 2014;42:101–105. Vikatmaa P, Makitie AA, Railo M, et al. Midline mandibulotomy and interposition grafting for lesions involving the internal carotid artery below the skull base. J Vasc Surg. 2009;49:86–92. Riffat F, Dwivedi RC, Palme C, et al. A systematic review of 1143 parapharyngeal space tumors reported over 20 years. Oral Oncol. 2014;50:421–430. Kuet ML, Kasbekar AV, Masterson L, et al. Management of tumors arising from the parapharyngeal space: a systematic review of 1,293 cases reported over 25 years. Laryngoscope. 2015;125:1372–1381. Cosetti M, Linstrom C, Alexiades G, et al. Glomus tumors in patients of advanced age: a conservative approach. Laryngoscope. 2008;118:270–274.
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution Fenglin Sun, Yan Yan, Dongmin Wei, Wenming Li, Shengda Cao, Dayu Liu, Guojun Li, Xinliang Pan & Dapeng Lei To cite this article: Fenglin Sun, Yan Yan, Dongmin Wei, Wenming Li, Shengda Cao, Dayu Liu, Guojun Li, Xinliang Pan & Dapeng Lei (2017): Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution, Acta Oto-Laryngologica, DOI: 10.1080/00016489.2017.1378433 To link to this article: http://dx.doi.org/10.1080/00016489.2017.1378433
Published online: 05 Oct 2017.
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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [Stony Brook University]
Date: 06 October 2017, At: 10:51
ACTA OTO-LARYNGOLOGICA, 2017 https://doi.org/10.1080/00016489.2017.1378433
RESEARCH ARTICLE
Surgical management of primary parapharyngeal space tumors in 103 patients at a single institution Fenglin Suna,b, Yan Yanc, Dongmin Weia, Wenming Lia, Shengda Caoa, Dayu Liua, Guojun Lid,e, Xinliang Pana and Dapeng Leia a
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Department of Otorhinolaryngology, Qilu Hospital, Shandong University, Key Laboratory of Otolaryngology, NHFPC (Shandong University), Jinan, Shandong, P. R. China; bDepartment of Otorhinolaryngology, Zibo Central Hospital, Zibo, Shandong, P. R. China; cDepartment of Surgery, Qilu Hospital, Shandong University, Jinan, Shandong, P. R. China; dDepartments of Head and Neck Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; eDepartments of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
ABSTRACT
ARTICLE HISTORY
Purpose: To evaluate clinical features, diagnosis, surgical management, and treatment of parapharyngeal space tumors in a single-center setting due to limited knowledge of diagnosis and treatment of parapharyngeal space. Methods: Clinical records of 103 patients were included for the analysis of such clinical characteristics. Results: A total of 29 different types of tumors were diagnosed after operation: 20 benign and 9 malignant. With a follow-up of 31–84 months for 90 benign cases, 84 cases had no recurrence and 6 cases were lost to follow-up. In contrast, with an 8- to 51-month follow-up for 13 malignant cases, 11 patients died and 2 were lost to follow-up. Furthermore, for postoperative complications, 3 cases had Horner syndrome, 2 had hoarseness, 2 had facial nerve dysfunction, and each for other types. Conclusions: Surgery remains the first choice for the treatment of parapharyngeal space tumors, with the transcervical approach used for most tumors. Moreover, CT or MRI may assist in making decisions about operation schemes.
Received 19 June 2017 Revised 18 August 2017 Accepted 26 August 2017 KEYWORDS
Parapharyngeal space tumors; head and neck neoplasms; diagnostic imaging; surgical treatment
Abbreviations: PPS: parapharyngeal space; CT: computed tomography; MRI: magnetic resonance imaging; FNAB: fine-needle aspiration biopsy; AMS: average of maximum size of the tumor; MMS: mean maximum size; HB: House-Brackman grading of facial nerve; LCN: low cranial nerves.
Introduction The parapharyngeal space (PPS) is a deep neck space in the lateral pharyngeal region. The PPS is in the shape of an inverted pyramid, with the greater cornu of the hyoid bone as its apex and the skull base as its floor [1]. It is divided into an anterior muscular compartment and a posterior neurovascular compartment by muscular aponeurotic partition [2]. A wide spectrum of benign and malignant primary pathologies has been encountered in this complex anatomic region. PPS tumors are rare, comprising only 0.5% of the neoplasms of the head and neck [1]. A variety of primary tumors arise from the normal structures of the PPS; 80% are benign and 20% malignant. The most common benign neoplasms are salivary pleomorphic adenomas [3], followed by paragangliomas and neurogenic tumors. Salivary gland neoplasms are the most common primary malignant tumor [4]. Various surgical approaches have been reported, including transcervical, transparotid, and transoral approaches – separately or combined for more exposure and resection of PPS tumors – as well as the use of a robot [5].
Because primary PPS tumors are hidden and have diverse characteristics and anatomical complexities, they are challenging to treat for otorhinolaryngology head and neck surgeons. There is currently little information about the clinical features, diagnoses, surgical approaches, and treatment outcomes of PPS tumors. The purpose of this study was to collect data on these tumors by analyzing our institution’s 15-year experience in the treatment of PPS tumors.
Materials and methods Patients with PPS tumors who were treated from January 1999 to June 2014 at our institution were identified through a database search, and their medical records were retrospectively evaluated and analyzed. The patients with congenital branchial cysts, metastatic neoplasms, and primary tumors originating from other regions involving PPS were excluded. Data regarding patient age, sex, clinical features, diagnosis, characteristics of the PPS mass, surgical approaches, complications, and outcomes were collected and analyzed.
CONTACT Xinliang Pan [email protected]; Dapeng Lei [email protected] Department of Otorhinolaryngology, Qilu Hospital, Shandong University; Key Laboratory of Otolaryngology, NHFPC (Shandong University), 107 West Wenhua Road, Jinan 250012, Shandong, P. R. China These authors contributed equally. ß 2017 Acta Oto-Laryngologica AB (Ltd)
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Table 1. Incidence and frequency of clinical symptoms.
Table 2. Incidence and frequency of clinical signs.
Types of symptoms
No.
%
Pain Foreign body sensation pharynx Dysphagia Snoring Hoarseness Dysarthria Rhinocleisis Dyspnea Hearing impairment Asymptomatic Total
17 12 10 8 4 3 2 1 1 45 103
16.5 11.6 9.7 7.8 3.9 2.9 1.9 1.0 1.0 43.7 100.0
All patients had received a thorough interrogation about their medical history and a detailed physical examination. In addition to preoperative examinations including electrocardiography, chest radiography, and hematologic laboratory examination, all patients underwent enhanced multi-slice spiral computed tomography (CT) of the neck. The surgical approach was dictated by the location of the tumor, its dimensions, its relationship to anatomic structures (carotid artery, jugular vein, cranial nerves), and the degree of suspicion of malignancy. Follow-up data had been obtained through personal interviews, examinations, and/or telephone conversations with patients or family members. We used the SPSS (SPSS Inc., Chicago, IL) statistical package for data analysis to describe and analyze the clinical features, diagnoses, surgical approaches, and treatment outcomes of patients with PPS tumors.
Results We identified a total of 103 patients (56 males and 47 females) with PPS masses who met the inclusion criteria. The mean age was 42 years (range, 4–78 years); six patients were children under 10 years of age. Five patients were referred to our department after treatment in another hospital; the remaining patients were treated in our hospital for the first time. The average time from onset to treatment was 21.0 months. In this cohort, 30 (29.1%) of the tumors were found to be located in prestyloid space, while 73 (70.9%) originated from poststyloid space. The main clinical symptoms of patients are summarized in Table 1. The most frequent symptoms were pain (16.5%), foreign body sensation (11.6%), and dysphagia (9.7%). A significantly high number of patients (45 patients; 43.7%) had asymptomatic growth detected during a routine checkup or while scanning for other reasons. In this study, the most frequent clinical signs were neck mass (59.2%), oropharyngeal mass (8.7%), and parotid mass (3.9%), while approximately 23.4% of patients had no clinical signs (Table 2). In addition to CT in all patients, five patients with disease highly suspicious of carotid body paraganglioma showing untidy margins with the carotid artery underwent digital subtraction angiography (DSA) preoperatively, and seven patients underwent fine-needle aspiration biopsy (FNAB) at other hospitals preoperatively. Apart from tumors with suspicion for vascular tumors, cysts, accessory nerve ganglion cells, and suggested nerve sheath tumors by CT scanning
Signs
No.
%
Neck mass Oropharyngeal mass Parotid mass Hemiprosoplegia Hypoglossus paralysis No signs Total
61 9 4 3 2 24 103
59.2 8.7 3.9 2.9 1.9 23.4 100
Table 3. Surgical approaches and tumor size. Surgical approaches
No.
%
MMS (cm)
Transcervical Transparotid Transoral Mandibulotomy Total
75 11 8 9 103
72.8 10.7 7.7 8.8 100
5.8 4.1 4.4 6.9 5.6
MMS: the mean of maximum sizes of the tumors.
before operation, 41 patients had intraoperative frozen section biopsies, according to that the preoperative assessment showed evidence of malignancy and whether patients were willing to undergo this examination. All patients underwent postoperative pathological examination. The surgical approaches and mean maximum sizes (MMSs) of the tumors are shown in Table 3. The transcervical surgical approach was most frequently used (75 cases, 72.8%). In these patients, tumors were generally located between the carotid sheath and pharyngeal constrictor muscles and in the deep posterior belly of the digastric muscle. Eleven patients with tumors located in the deep lobe of the parotid gland in the prestyloid space underwent a transparotid approach. The key was to identify, elevate, and preserve the facial nerve and its branches, especially the marginal mandibular branch. In the group who received a transoral approach, four cases had en bloc resection. Another four cases had intracapsular excision because the tumors were larger than 5.0 cm and complete exposure was difficult. The major steps were to expose the tumor capsule through the intraoral incision first, then cut open the capsule following block resection of the tumor tissue, and finally remove the capsule. In the case of mandibulotomy, all the patients who underwent tracheotomy were all successfully decannulated from 8 to 15 days postoperatively. All the patients underwent histopathological tests after operation. The results are presented in Table 4. A total of 41 patients underwent intraoperative frozen section examination, and their results were in agreement with the postoperative pathologic diagnosis. A total of 29 different types of tumors were diagnosed, including 20 types of benign tumors and nine types of malignant tumors. The overall frequencies of benign and malignant tumors were 87.2 and 12.8%, respectively. Of the 90 cases with benign tumors, neurilemoma was the most common type (33.0%), followed by pleomorphic adenoma (15.5%). For malignant tumors, the most frequent type was lymphoma (3.9%), followed by leiomyosarcoma (1.9%). Complications caused by surgical treatment were found in 10 patients. In cases adopting transparotid approaches, nine patients had normal VII nerve function (HB I), and
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two had HB II in the immediate postoperative period. At the end of 6 months, the two patients recovered to HB I (Table 5). Patients with carotid body paragangliomas had the highest rate of LCN palsies, followed by Neurilemoma (Table 6). Horner Syndrome was observed in two patients with carotid body paraganglioma and one patient with neurilemoma, and this complication showed no improvement after 3–5 years of follow-up. Carotid body paraganglioma postoperative hoarseness in two patients caused by ipsilateral paralysis of the vocal cord disappeared after 6 months of conservative treatment. Hypoglossal nerve palsy was noted in one patient with neurilemoma and faded gradually after 3 weeks. Dyspnea in one patient with neurilemoma due to local bleeding improved after tracheotomy and clearing hematoma. In addition, contralateral hemiplegia caused by carotid-cavernous fistula was found in one patient with carotid body paraganglioma who underwent artificial vascular graft and anastomosis during the operation.
Among the benign tumor group of 90 patients, the patients did not receive any further treatment postoperatively. Six patients were lost to follow-up and 84 patients were followed-up for 31–84 months with no recurrence. In contrast, for malignant tumors, postoperative radiotherapy was applied in four patients with lymphoma and combined chemo-radiotherapy was given to five patients, including two with leiomyosarcoma, one with myxofibrosarcoma, one with liposarcoma, and one with malignant rhabdomyoma. The auxiliary treatment was unknown in one patient with clear cell carcinoma. The remaining three patients in the malignant tumor group refused any postoperative treatment. Thirteen patients with malignant tumors were followed-up for 8–51 months. Seven patients died, of which three patients died of recurrence of leiomyosarcoma, myxofibrosarcoma, or liposarcoma. Four patients died of metastasis, including one with malignant rhabdomyoma and three with lymphoma. Two patients with a malignant tumor were lost to follow-up.
Table 4. Histopathological diagnosis of 103 PPS tumors.
Discussion
Diagnosis Benign Neurilemoma/schwannoma Pleomorphic adenoma Carotid body paraganglioma Hemangioma Inflammatory tissue Neurofibroma Salivary gland lymphoma Vascular tumor Lipoma Cyst Others Malignant Lymphoma, non-Hodgkin Leiomyosarcoma Others Total
No.
%
34 16 8 5 5 4 2 2 2 2 10
33.0 15.5 7.7 4.8 4.8 3.8 1.9 1.9 1.9 1.9 10.0
4 2 7 103
3.9 1.9 7.0 100.0
Table 5. Preoperative and postoperative VII nerve function in transparotid approach cases. Cranial VII nerve HBI HBII HBIII HBIV HBV HBVI
Preoperative
Immediate
After 6 months
11 – – – – –
9 2 – – – –
11 – – – – –
HB: House-Brackman grading of facial nerve.
Traditionally, the PPS has been divided into the prestyloid and poststyloid compartments. In recent decades, new compartmentalization of this complex area has been proposed for the selection of appropriate surgical approaches. According to the compartmentalization of the PPS suggested by Shahinian et al. [6], Kanzaki and Nameki [7], Prasad et al. [8], proposed that the PPS could be divided into three compartments; the upper (between the skull base and the line joining the lower borders of the lateral pterygoid muscles of both sides), middle (between the line joining the lower borders of the lateral pterygoid muscles and the line joining the angle of mandible on both sides), lower part (between line joining the lower borders of the angle of the mandible and the plane of the hyoid). PPS tumors are always a challenge for surgeons to diagnose because of their rarity, atypical clinical manifestations and diverse pathological types. In this paper, we found that 87.2% of PPS tumors were benign and 12.8% were malignant, which is in agreement with a previous study that reported 80% benign and 20% malignant PPS tumors [9]. In addition, only 5.8% of the cases were found in children under the age of 10. The most common PPS tumor in our study was neurilemoma, followed by pleomorphic adenoma and paraganglioma, which differs from what has been reported previously [2,3,10].
Table 6. LCN deficits in relation to the histopathology of tumor. CRP CN CN CN CN HS
IX X XI XII
Preoperative 0 1 0 0 0
Neurilemoma Postoperative 0 3 0 0 2
Preoperative 0 3 0 0 0
Postoperative 0 3 0 1 1
Malignant tumors Preoperative 0 0 0 0 0
Postoperative 0 0 0 0 0
LCN: low cranial nerves; CRP: carotid body paraganglioma; CN IX: glossopharyngeal nerve; CN X: vagus nerve; CN XI: spinal accessory nerve; CN XII: hypoglossal nerve; HS: Horners syndrome.
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Due to the concealment of the location of PPS tumors and the characteristic slow growth of these tumors, most patients tend to have large tumors at diagnosis. In our study, the longest mean diameter of the tumors was 5.6 cm, and the average time from onset to treatment was 21.0 months. The common symptoms and clinical characteristics may be diverse and non-specific. Although patients may suffer from a wide variety of symptoms and signs, the most common symptom and sign in this study were pain and the presence of a neck mass, which were the same as those from previous reports [2,3,10]. However, 43.7% of the patients had no symptoms and 23.4% of the patients had no signs, which is a potential challenge for surgeons. Imaging is essential to evaluate the location and extent of PPS neoplasms because of the limitations of physical examination in this anatomical area [11]. Arteriography is performed infrequently for the diagnostic purposes. In rare instances, it can be used to evaluate cervicocerebral collateral circulation, which may necessitate the sacrifice of major blood vessels [5]. DSA is helpful for surgeons to understand the compensation of the blood supply to the brain and Wills rings and then to properly assess the safety of resection of tumor adhering to the internal carotid artery. In this study, five patients underwent DSA and were diagnosed with carotid body paraganglioma postoperatively. Among them, three cases could not be resected directly because of severe adhesion to the internal carotid artery and common carotid artery, so vascular prosthesis bypass grafting was performed after resection. To reduce intraoperative blood loss, one patient with neurilemoma that invaded the intervertebral foramen underwent ascending cervical artery superselective embolization and vertebral artery balloon embolization. This provided strong protection for the complete resection of the tumor. It is important to have an accurate diagnosis by pathological examination preoperatively. Whether FNAB can be applied to preoperative examination of PPS tumors remains controversial. Peroral or transcervical FNAB is up to 90–95% accuracy among these cases and can be performed under CT or ultrasound guidance [12, 13]. Nevertheless, a non-diagnostic aspirate has been reported in 25–60% of cases due to the lack of cellular material, excessive bleeding, or other technical problems [5]. In our practice, FNAB was performed in seven cases and the rate of accuracy was only approximately 28.6% (2/7). There were five cases in which FNAB did not agree with our diagnosis, including four cases of neurilemoma and one case of malignant ameloblastoma. However, among 41 patients, including 11 with malignant tumors, who had intraoperative frozen section biopsy, the diagnostic accuracy reached 100. The low rate of accuracy of FNAB may result from the following: (a) more non-neurogenic tissues in neurogenic tumors, (b) no standard FNAB techniques in the nation, leading to the application of intraoperative frozen section biopsy instead of preoperative FNAB in our clinical practice. Surgical management is the main treatment for PPS tumors. However, how to appropriately choose the surgical approach and decrease the risk of surgical complications is a great challenge for surgeons. The successful resection of PPS
tumors depends mainly on two conditions: (a) correct identification and exposition of tumors for complete removal and prevention of potential recurrence and (b) minimum functional and aesthetic morbidity taking into account the risk of surgery in this space [14]. The transoral approach is commonly used for removing tumors involved only in oropharynx, small benign avascular tumors, and those not palpable in the neck or parotid regions [2,13,15]. However, this approach is considered not safe enough, for it fails to effectively avoid the neck great vessels and the cranial nerves in some cases, possibly leading to some severe complications, such as excessive hemorrhage and damage to cranial nerves. In our clinic, we used this approach to perform intracapsular resection in four cases without recurrence. In contrast, the transparotid approach is considered for small tumors located in the deep lobe of the parotid gland. It works well for patients with the prestyloid tumors or deep-lobe parotid neoplasms extending into the PPS, who require the superficial parotidectomy in advance. This approach requires identification and preservation of the main trunk of the facial nerve [16]. In the current study, the transparotid approach was applied to 11 cases, and the mean of the maximum sizes of the tumors was 4.1 cm. Our experience was that some branches of the facial nerve could be shifted in order to reveal the tumor as much as possible. If necessary, partial resection of the superficial or deep lobe of the parotid gland could be performed and the mandibular angle was pulled forward. The transcervical approach can be performed to successfully resect most PPS tumors [2,5,9,12,16]. Its advantage is that it can achieve a satisfactory exposure to tumors and the important blood vessels and nerves around them. Thus, it may be indicated for large tumors (benign and malignant), particularly for malignant tumors, whose margins are hard to determine unless touched by surgeons themselves. In this series, this approach was performed in 72.8% of the cases and the mean of maximum sizes of the tumors was 5.8 cm. We used the following skills to maximally expose the tumors: (1) cut the posterior belly of the digastric, resect the partial hyoid bone, and shift the submandibular gland medially; (2) resect partial non-functional soft tissue in the cervical sublevels IB and IIA; and (3) push down tumors from the oral cavity. These techniques can prevent greater trauma and the potential pollution of the field from other combined approaches. Mandibulotomy to improve surgical access to the PPS should be considered for selected patients, including those with malignant neoplasms, recurrent neoplasms, large benign neoplasms, and highly vascular neoplasms [17]. It can be combined with other PPS approaches and is performed mainly when a wide surgery field is required. Mandibulotomy reduces the intraoperative risks as a result of adequate exposure [3]. One or more osteotomies are involved in mandibulotomy and therefore such operations takes more time and requires experienced surgeons. In addition, the transmandibular approach can vary with the location and amount of amputated bones. In this study, nine patients underwent this approach with tracheotomy, of which four cases were malignant tumors and the
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others were very large benign neoplasms with mean tumor sizes >8 cm. Tumor histology, vascularity, size, as well as anatomical location are important factors in the determination of the appropriate surgical approach. Many surgical approaches to PPS tumors have been previously reported. However, few reports on a standard surgical approach are related to tumor location, except that Prasad et al. has proposed an algorithm for the selection of appropriate surgical approaches in the management of PPS tumors [8]. Potential complications should be explained to patients before surgery. All complications need to be managed appropriately to facilitate rehabilitation [18]. Preoperative clinical assessment of the LCN is an important factor to be taken into consideration in the management of PPS tumors [8]. In this study, postoperative neurological deficits in patients accounted for 80% (8/10) of all complications, with 50% (4/8) of these in carotid body paragangliomas. The possible reasons may be transposition of cranial nerves X and XI and the cervical sympathetic trunk caused by carotid body paraganglioma and the large number of blood vessels resulting in a bleeding field. In this study, we found that contralateral compensation plays a critical part in the cases of X and XII palsies over a period of time after surgery. Postoperative complications of vascular injury were uncommon, but often more serious. Contralateral hemiplegia caused by carotid-cavernous fistula was reported in one patient with carotid body paraganglioma who underwent artificial vascular graft and anastomosis during the operation. Such complications showed no improvement after 14-month follow-up. Besides surgery, no other treatment was administered for the benign tumors in our series, as reported by others [19,20]. In this study, the benign tumors had no recurrence, while for the malignant tumors, the 5-year survival rates were low, even though the patients received surgery combined with radiotherapy and/or chemotherapy. This suggests a poor prognosis for primary malignant tumors in PPS. In conclusion, PPS tumors are rare and have atypical clinical manifestations and diverse pathological types. Surgery is the first choice of treatment for PPS tumors, and the transcervical approach can be applied to most tumors. Furthermore, examination of CT or MRI is useful to help evaluate the tumor size, location, and possible sources and to plan the operation. Finally, PPS benign tumors have a good prognosis, while malignant tumors have a poor prognosis.
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Funding This work was supported by the Taishan Scholars Program (No. tshw20130950), Shandong Province; the Department of Science and Technology of Shandong Province (No. ZR2013HM107, ZR2014HM005, 2015GSF118014, and 2015GSF118030); Science Foundation of Qilu Hospital of Shandong University; and the Fundamental Research Funds of Shandong University (No. 2014QLKY05).
References [1]
[2]
[3]
[4] [5]
[6] [7]
[8]
[9] [10] [11] [12]
[13]
[14]
[15]
[16]
[17]
Disclosure statement The authors declare no competing financial interests or conflict of interest.
[18]
Ethical approval
[19]
All procedures performed in studies involving human participates were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.
[20]
Maheshwar AA, Kim EY, Pensak ML, et al. Roof of the parapharyngeal space: defining its boundaries and clinical implications. Ann Otol Rhinol Laryngol. 2004;113:283–288. Dimitrijevic MV, Jesic SD, Mikic AA, et al. Parapharyngeal space tumors: 61 case reviews. Int J Oral Maxillofac Surg. 2010;39:983–989. Papadogeorgakis N, Petsinis V, Goutzanis L, et al. Parapharyngeal space tumors: surgical approaches in a series of 13 cases. Int J Oral Maxillofac Surg. 2010;39:243–250. Olsen KD. Tumours and surgery of the parapharyngeal space. Laryngoscope. 1994;104:1–28. Bradley PJ, Bradley PT, Olsen KD. Update on the management of parapharyngeal tumours. Curr Opin Otolaryngol Head Neck Surg. 2011;19:92–98. Shahinian H, Dornier C, Fisch U. Parapharyngeal space tumors: the infratemporal fossa approach. Skull Base Surg. 1995;5:73–81. Kanzaki S, Nameki H. Standardised method of selecting surgical approaches to benign parapharyngeal space turnouts, based on pre-operative images. J Laryngol Otol. 2008;122:628–634. Prasad SC, Piccirillo E, Chovanec M, et al. Lateral skull base approaches in the management of benign parapharyngeal space tumors. Auris Nasus Larynx. 2015;42:189–198. Cohen SM, Burkey BB, Netterville JL. Surgical management of parapharyngeal space masses. Head Neck. 2005;27:669–675. Panda S, Behera SK, Ray R. Parapharyngeal tumors: a review of 16 cases. J India Med Assoc. 2010;108:357–359. Gupta A, Chazen JL, Phillips CD. Imaging evaluation of the parapharyngeal space. Otolaryngol Clin North Am. 2012;45:1223–1232. Oliai BR, Sheth S, Burroughs FH, et al. “Parapharyngeal Space” tumors: a cytopathological study of 24 cases on fine-needle aspiration. Diagn Cytopathol. 2005;32:11–15. Bozza F, Vigili MG, Ruscito P, et al. Surgical management of parapharyngeal space tumours: results of 10-year follow-up . Acta Otorhinolaryngol Ital. 2009;29:10–15. Infante-Cossio P, Gonzalez-Cardero E, Gonzalez-Perez LM, et al. Management of parapharyngeal giant pleomorphic adenoma. Oral Maxillofac Surg. 2011;15:211–216. Ducic Y, Oxford L, Pontius AT. Transoral approach to the superomedial parapharyngeal space. Otolaryngol Head Neck Surg. 2006;134:466–470. Cassoni A, Terenzi V, Della Monaca M, et al. Parapharyngeal space benign tumors: our experience. J Craniomaxillofac Surg. 2014;42:101–105. Vikatmaa P, Makitie AA, Railo M, et al. Midline mandibulotomy and interposition grafting for lesions involving the internal carotid artery below the skull base. J Vasc Surg. 2009;49:86–92. Riffat F, Dwivedi RC, Palme C, et al. A systematic review of 1143 parapharyngeal space tumors reported over 20 years. Oral Oncol. 2014;50:421–430. Kuet ML, Kasbekar AV, Masterson L, et al. Management of tumors arising from the parapharyngeal space: a systematic review of 1,293 cases reported over 25 years. Laryngoscope. 2015;125:1372–1381. Cosetti M, Linstrom C, Alexiades G, et al. Glomus tumors in patients of advanced age: a conservative approach. Laryngoscope. 2008;118:270–274.
