Intraoral and extraoral approach for surgical treatment of Eagle's syndrome: a retrospective study

Eagle's syndrome is not uncommon in clinical work. Because of its atypical symptoms, it is easy to be misdiagnosed as other diseases, further leading to misdiagnosis and mistreatment. At present, there is no expert consensus or treatment guidelines for the disease. We evaluated the clinical characteristics and postoperative efficacy of 103 patients with Eagle’s syndrome based on their clinical symptoms, radiological studies, and physical examination. Through the multicenter clinical study of Tongji Medical College and Dalian Medical University, we found some characteristics of Eagle’s syndrome in operation and imaging. In total, 103 patients with Eagle’s syndrome (treated from January 2010 to January 2020) were retrospectively enrolled. The postoperative curative effect was analyzed by three surgical methods: styloid process resection through the external cervical approach (styloid process could not be touched through the mouth or could be touched under the jaw or when the CT scan showed that the inclination angle was not large), tonsillectomy + styloidectomy, and preservation of the tonsil for styloidectomy (the styloid process bone could be touched directly during intraoral palpation or in whom the distal part of the styloid process could not be directly touched, but the CT scan showed that the bone inclined toward the oropharynx and its distal part was relatively close to the oropharynx cavity; whether tonsillectomy was performed depended on whether the patient’s tonsil was too large to affect the surgical incision). According to the Quality of Well-Being Scale (QWB), we calculated the W value of the scale before operation and 30 days, 3 months, 6 months and 12 months after operation, and compared the W value of each group. The average length of the styloid process was 33 mm (range 25–61 mm). The patients were followed up for 12–36 months (average 15 months). Of the 103 patients, 21 underwent styloid process resection through the external cervical approach, 49 underwent tonsillectomy and styloidectomy, and 33 underwent styloidectomy with preservation of the tonsil. The treatment cured 48 (46%) cases, was effective in 35 (34%) and was ineffective in 20 (20%). The R language 3.6.3 software was used to perform the nonparametric rank sum test, differences in characteristics between groups were analyzed using the Kruskal–Wallis test with Dunn post hoc tests ( R package FSA) for categorical variables, and there was no significant difference between the three types of operations (H = 0.491, P = 0.782). QWB showed that the quality of life after operation was improved compared with that before operation. Operation is an effective method for treating Eagle’s syndrome. There were no significant differences between the effects of the intraoral and external cervical approaches. Imaging examination—especially CT scanning and 3D reconstruction of the styloid process—is very helpful for diagnosis, but not an absolute criterion for the selection of surgery protocol.


Introduction
Symptoms of Eagle's syndrome can be divided into two types: classic Styloid syndrome and stylo-carotid-artery syndrome [1][2][3]. Styloid process truncation has a clear curative effect on patients with Eagle's syndrome, and can significantly reduce the symptoms of pharyngalgia, swallowing pain, cervicodynia. Because of the variety of clinical manifestations of the disease, it can be easily misdiagnosed as chronic pharyngitis, cervical spondylosis, chronic tonsillitis, glossopharyngeal neuralgia, temporomandibular joint disorder [4,5]. The diagnosis mainly depends on the patient's clinical symptoms, physical examination (primarily via digital palpation of the tonsillar fossa), and radiological studies (X-ray and computed tomography [CT] scans of the Styloid process, followed by a three-dimensional [3D] reconstruction) [6,7]. In China, surgical treatment for this disease is generally performed by the otolaryngology department. However, the clinical symptoms of some patients are not solved through surgery [8]. Therefore, this retrospective study aimed to evaluate the surgical treatment of this disease through statistical analysis of various postoperative outcome measures, providing a reference for the treatment of such patients in the future.

Data and patients
A total of 103 patients were treated at the First Affiliated Hospital of Dalian Medical University (39 cases) and Tongji Hospital ( affiliated to Tongji Medical College of Huazhong University of Science and Technology, 64 cases) from January 2010 to January 2020 were enrolled as research subjects. The patients were provided informed consent, and the relevant institutional review boards granted ethical clearance for the study. The selection criteria were as follows: (1) patients complained of either pharyngeal pain, Pharyngeal foreign body sensation, unilateral neck shoulder radiation pain, or radiation ear pain; (2) a bony eminence was palpable in the fossa; (3) either the 3D CT reconstruction of the Styloid process or the anteroposterior, lateral X-ray film of the Styloid process met the diagnostic criteria, and the length of the Styloid process was > 25 mm. Patients with severe cardiovascular diseases, neuropsychiatric diseases, and neuromuscular diseases were excluded.

Radiological studies
Radiological studies were performed with a Siemens 64-slice double helix machine (Siemens, Munich, Germany). The patient was put in a supine position with the mandible raised, such that the auditory orbital line was perpendicular to the scanning table. The measurement method used was as follows [7,9]: based on the 3D CT reconstruction image, the length of the Styloid process was measured as the distance between its root and the distal end. On the anteroposterior image, a perpendicular line was drawn parallel to the skull base, and the angle between the centre line of the Styloid process and the perpendicular measurement line was noted as the inward angle [10]. An acoustic orbital line (a perpendicular line connecting the upper edge of the outer ear hole and the lower edge of the orbit) was drawn on the reconstructed image, and the internal deviation angle was measured as the angle between the perpendicular line and the centre line of the Styloid process. If the length of the Styloid process was greater than 25 mm [11], the Styloid process was considered too long. In this case, the angle of inclination (inward or forward) was greater than 25° and was called the abnormal azimuth angle (Fig. 1). The anteroposterior, lateral X-ray film of the Styloid process was examined as follows: for scanning, the patient (either standing or reclining) was instructed to keep their head in a lateral position and slightly tilt their body. After scanning, the data was transmitted to a picture archiving and communication system workstation to measure the azimuth angle and the length of the Styloid process using the same method as before.

Surgical indications
At present, patients diagnosed with Eagle's syndrome are not uncommon. Some patients with a long Styloid process undergo conservative treatments such as non-steroidal antiinflammatory drugs and glucocorticoids [12,13], although it has a short-term effect, can easily relapse. The inclusion criteria for surgery were the same as the selection criteria for this study. All three criteria (1, 2, and 3) were considered necessary conditions and were strictly observed, and the imaging data were carefully analysed. The 3D CT scan of the Styloid process is more accurate in displaying the details, and accurate judgement of deflection, interruption, and ossification of the hyoid ligament [10].

Selection of the operation method
The patients were placed under general anaesthesia and the appropriate surgical method was selected based on their oropharyngeal palpation, 3D CT reconstruction of the Styloid process, and specific selection criteria: (1) for patients in whom the Styloid process bone could be touched directly during intraoral palpation, or in whom the distal part of the Styloid process could not be directly touched but the CT scan showed that the bone inclined toward the oropharynx and its distal part was relatively close to the oropharynx cavity (which does not cause excessive injury in the Parapharyngeal space), Styloid process resection was selected for transoral surgery. Whether tonsillectomy was performed depending on whether the patient's tonsil was too large to affect the surgical incision; (2) for patients whose Styloid process could not be touched through the mouth or could be touched under the jaw, or when the CT scan showed that the inclination angle was not large, the external cervical approach was selected. The selection of appropriate surgical methods can lower operation time, injury, postoperative pharyngalgia, and the probability of complications.

Transoral surgery
The index finger of one hand was placed in the affected tonsillar fossa, and the other finger was placed behind or under the ipsilateral ramus of the Mandible [14]. Of 82 patients who underwent surgery using the intraoral approach, 50 patients could either touch the hard cord in the unilateral or bilateral tonsillar fossa, or felt tenderness, fullness, or other discomforts at the touchpoint; 12 patients could touch the hard cord behind or under the ramus of the mandible. The other 20 patients could not touch any abnormality. Specific surgical methods: (1) the tonsillar fossa approach: if the tonsil was too large and affected the exposure of the whole Styloid process, tonsillectomy was performed first. Based on the position and course of the Styloid process, a sickle knife was used to cut the mucosa of the palatoglossal or palatopharyngeal arch to separate the superior pharyngeal muscle and expose the distal Styloid process. Following this, the Styloid process periosteum was cut, and soft tissues such as the muscle and Styloid hyoid ligament were excised. The Styloid process was covered with a small ethmoid curette from the free end and walked along the Styloid process (which was clipped with a vascular clamp), then cut and removed with bone-biting forceps. The cut-off length was 10-38 mm. If the residual Styloid process was long, it was further stripped and shortened. During the operation, it was necessary to clamp the broken end of the Styloid process with a vascular clamp as it is difficult to find once it slips. Small incisions were not sutured; however, large incisions were sutured with 3-0 absorbable sutures to eliminate large spaces and prevent Parapharyngeal space infection. In patients with tonsillectomy, it was not necessary to suture the tonsillar fossa completely. (2) Using the palatoglossal arch-soft palate approach, the mucosa was cut between the medial sides of the opsigenes on the palatoglossal arch, and the incision was extended to the upper soft palate to a length of 2.5 cm. The remaining steps were the same as those described for surgical procedure 1.

External cervical approach
An arc-shaped incision was made around the mandibular angle, approximately 1-2 cm from the posterior edge of the ramus to the inferior edge of the mandible. The length of the incision was approximately 4 cm. The skin was cut, and the layers of subcutaneous tissue and Platysma were separated. The parotid masseteric fascia was exposed to protect its superficial layer and to cross the facial nerve. The mandibular angle was fully exposed, and the Styloid mandibular ligament was located. The Styloid process was located, and the attached Mandibular ligament of the Styloid process and Styloid hyoid ligament was cut. The attachment site of the Styloid process was approached using the ethmoid curette, and a small pair of bone-biting forceps was inserted along the Styloid process.

Statistical analyses
The R language 3.6.3 software was used to perform the nonparametric rank sum test, differences in characteristics between groups were analyzed using the Kruskal-Wallis test with Dunn post hoc tests ( R package FSA) for categorical variables, and there was no significant difference between the three types of operations (H = 0.491, P = 0.782). According to the QWB, we calculated the average values of W of the scale before operation and 30 days, 3 months, 6 months and 12 months after operation, and compared the W value of each group. When the average values of W is between 0.32 and 1.00, 0.32 represent the death of the case at the evaluation time, and 1. 00 represent without any deterioration in quality of life. When the average values of W is between 0.32 and 1.00, the higher the W value is, the better the quality of life is [15,16].

Results
There were 47 men and 56 women with an average age of 44 ± 10.6 years (range, 24-68 years). The disease course was 3-60 months. Of the 103 cases, 68 had unilateral disease and 35 had bilateral diseases; 21 patients underwent Styloid process resection through the external cervical approach, 49 underwent tonsillectomy as well as Styloid process shortening, and 33 underwent Styloid process shortening along with tonsil preservation. The average length of the Styloid process was 33 mm (range, 25-61 mm). The patients were followed up for 12-36 months (average, 15 months).
The visual analogue scale(VAS) score was 4.23 ± 0.25 before the operation and 1.62 ± 1.21 after the operation, and the difference was statistically significant (P < 0.05). Single case statistics: according to the results of VAS score before treatment, if the score was reduced by 0-2 points, it was cured; if the score was reduced by 3-5 points, it was effective; if the symptom was reduced by less than 2 points, it was ineffective (Table 1 for specific data). The main complaints were Swallowing pain, pharyngalgia, Foreign body sensation in the pharynx (with one of them) and the cure rate was 70%. Most of the above symptoms were significantly relieved after wound healing. The complaints were headache, earache, dizziness and tinnitus (with one of them), the cure rate was 58%, Most of the aforementioned symptoms were relieved after surgery, and the postoperative symptoms of these patients were gradually relieved after 3-6 months. A small amount of tonsillar haemorrhage occurred in 2 patients 1 week after the operation, no parapharyngeal space infection or facial nerve paralysis. Persistent dry throat and pharyngeal foreign body sensation were reported in individual cases but were tolerable without special intervention. The postoperative pain lasted 5 days longer in patients who underwent surgery using the extraoral approach compared to those who underwent the intraoral approach. The results of the rank-sum tests were not statistically significant (H = 0.491, P = 0.782).

Quality of Well-Being Scale (QWB)
The results showed that the quality of life after operation was improved compared with that before operation. The improvement of the quality of life 30 days after operation was more obvious than that before operation, and the change of the quality of life 3 months to 1 year after operation was less. There was no significant difference among the groups (Table 2) Case report Case 1: a 54 years old female patient, complained of " pharyngalgia for half a year". This case was a typical Styloid process truncation with preservation of tonsils through the oral approach. Through CT, we could clearly see the length, anteversion, and inclination of the Styloid process, and judge that the Styloid process was toward the oropharynx cavity. Palpation through the tonsil fossa also further confirms that the Styloid process was too long, and the bone of the Styloid process could be seen protruding to the tonsil fossa. Such a typical patient was relatively rare. After the operation, the wound in the mouth was very small and healed quickly. The patient's pharyngalgia was obviously improved. (Fig. 2).
Case 2: a 47 years old male patient, was admitted with " pharyngalgia for half a year", a case of an extremely long Styloid process on both sides. CT accurately measured the true length of the Styloid process, which was consistent with the intraoperative findings. It could be seen that CT threedimensional reconstruction has diagnostic value for the disease. Two weeks after the operation, the symptoms improved significantly. (Fig. 3).

Discussion
In this study, 103 patients were enrolled, most patients have been diagnosed with chronic pharyngitis, chronic tonsillitis, or otitis before surgery, Eagle's syndrome can also cause these symptoms, which makes it difficult to differentiate from other diseases that can cause neck or facial pain and abnormal sensations. Special examination-especially   . 2 A and B CT examination shows the bilateral Styloid process growing downward, inward, and forward. The length of the right Styloid process is 44.1 mm, the inclination angle is 27.2°, the anteversion angle is 29.6° to the superior margin of the axis, the lower segment of the right Styloid process bends, and the inclination angle increases to the medial. C During the operation, the right tonsil fossa is palpated, and a hard rod-like protrusion is found. D The Styloid process is completely truncated during the operation, and no ligament or soft tissue attachment is left around the Styloid process. E and F wound recovery on the third and sixth days after the operation. There are small wounds in the mouth with a little white membrane attached to the surface, and the surrounding mucosa is intact without redness, swelling, or congestion. The wound recovered 6 days after the operation Fig. 3 a-c The length of the right Styloid process is 58.8 mm and the inclination angle is 30.3°; the length of the left Styloid process is 55.6 mm and the inclination angle is 26.7°, CT can clearly show the course and length of Styloid process. d Bilateral Styloid process was completely truncated during operation tonsillar fossa and neck palpation-has become the key diagnosis in such cases. If the long Styloid process can be touched or causes obvious tenderness, foreign body sensation, and fullness, the diagnosis is confirmed. Imaging technology, especially CT scanning and 3D reconstruction of the Styloid process, can clearly show the Styloid process length, shape, internal deflection angle, and ligament ossification [7]. These examinations allow relatively accurate observation and measurement. This study found that there was no significant difference in the efficacy of intraoral and extraoral approaches. We found that imaging studies-especially CT scanning and 3D reconstruction of the Styloid process-are very helpful for diagnosis, but not an absolute criterion for the selection of surgery protocol. In some cases, although CT scans showed that the bone was continuous, it was found to be interrupted during the operation, in these cases, the effect of the operation was often not very good. In some cases, CT scans showed that the Styloid process was too long, but intraoperative exploration, especially in the case of sufficient exposure to the external cervical approach, the Styloid process was not too long, which may be related to the incomplete ossification of Styloid ligament. In this study, we set the Styloid process length at > 25 mm; however, most other related studies set it at > 30 mm [17], the main consideration is that the length cut-off is not universal; some patients have a Styloid process length of 25-30 mm, but their symptoms are obvious, the hard Styloid process can be felt on tonsillar fossa examination, and surgical treatment is also feasible. Therefore, imaging examinations can only be used as an important auxiliary tool in clinical practice and cannot become a definitive diagnosis.
Styloid process truncation has a clear curative effect on patients with Eagle's syndrome, and can significantly reduce the symptoms of pharyngalgia, swallowing pain, cervicodynia, earache, and pharyngeal foreign body sensation [6,18]. However, the symptoms of patients with Tinnitus, Headache, and Dizziness are not significantly relieved. The surgeon in this study is proficient in the above three surgical methods, who presents no technical differences. However, some scholars believe that the lateral cervical region approach can ensure the safety of operations and reduce the probability of postoperative complications [19], it is also suggested that the Styloid process truncation should be performed through the external cervical approach because it allows clear surgical vision and less damage to peripheral blood vessels and nerves [14,20]. However, extensive facial anatomy and long operation times can easily cause epidermal nerve injuries, such as sensory abnormalities of the great auricular nerve and facial nerve branch injury [21]. Open surgery should be selected when the Styloid process grows towards the lateral cervical region, so as to avoid excessive operation in the parapharyngeal space, longer operation times, and higher operating costs. Through the surgical procedures used in this study, the wound in the mouth had a small internal diameter and the recovery time was short (6 days after the operation), there was no incision or scar on the outside. Although the field of vision was smaller, the Styloid process could be fully exposed in most cases [22]. These selection criteria can help reduce the risk of Parapharyngeal space infection and nerve injury [23]. In general, it is very important to choose the appropriate surgical method according to the experience of the operator and the different pathological characteristics of the patients.

Conclusion
Surgery is an effective method for treating Styloid process syndrome. However, in view of the imprecise curative effect of surgery in some cases and postoperative discomfort (dry throat and foreign body sensation in the pharynx), and the imaging studies were also inconsistent with the intraoperative findings, it is very important to strengthen the preoperative evaluation (length and angle judgement of the Styloid process via imaging, digital palpation), select surgical protocols according to the symptoms.
Author contributions Zhi bin Wang and Yan Liu: study conception and design, acquisition of data, kai Sheng Yan analyzes and processes data. Jing Wang: drafting of the manuscript. All authors have read and approved the manuscript.

Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Declarations
Ethics approval This study was conducted in agreement with the Ethics Committee of Tongji Hospital Affiliated to Tongji Medical College and The First Affiliated Hospital of Dalian Medical University.
Consent to participate All participants had provided written informed consent.