Endoscopic Transoral Approach for Resection of Basal Cell Adenoma Arising in Parapharyngeal Space

Abstract

Objectives  The clinical and radiological characteristics of the basal cell adenoma (BCA) and its association with the internal carotid artery (ICA) in the parapharyngeal space (PPS), have not been sufficiently explored. This study aims to analyze the characteristics of patients with BCA arising in the PPS and to evaluate the feasibility of a total resection via an endoscopic transoral corridor.

Design and Main Outcome Measures  The clinical, radiological, and histopathological characteristics of four patients with BCA arising in the PPS were retrospectively analyzed. The endoscopic transoral approach was performed for resection of BCA. Its technical nuances, perioperative comorbidities, and outcomes are introduced.

Results  The clinical presentation, symptoms, and signs of patients with BCA are variable. The tumor was lateral to the ICA in two patients and anterior to the ICA in the remaining two. All four BCA were successfully removed en bloc ( n  = 3) or by piecemeal ( n  = 1) via an endoscopic transoral approach. The ICA was not injured, and no additional nerve damage, venous bleeding, postoperative infection, or salivary gland fistula were encountered in any of the four patients. Cystic degeneration is the predominant appearance of BCA on MRI; however, they are difficult to differentiate from other lesions arising in the PPS. No recurrence was detected at the time of the study analysis.

Conclusion  BCA of the PPS could have variable relationships with the ICA. An endoscopic transoral approach can provide an adequate corridor for total resection of BCA in PPS with seemingly low morbidity.

Introduction

Advancements of endoscopic instrumentation and techniques, minimally invasive approaches (e.g., transnasal, endoscopic transoral corridor) for access into the infratemporal fossa (ITF) and parapharyngeal space (PPS) have been described previously. ^{1 2 3 4} Satisfactory outcomes have been reported following the adoption of minimally invasive techniques for the resection of benign tumors located in both the ITF and PPS. ^{5 6}

The PPS is traditionally divided into the prestyloid and retro-styloid compartments by the styloid process and the stylopharyngeal aponeurosis. ^{4 7} The prestyloid PPS mainly comprises adipose tissue, minor salivary glands, lymph node, and the deep lobe of the parotid gland. Neurovascular structures including the parapharyngeal segment of the internal carotid artery (ICA), internal jugular vein, lower cranial nerves (IX to XII), and sympathetic nerve chain are located in the retro-styloid compartment. ⁸

As described in previous studies, tumors arising from the prestyloid PPS (e.g., pleomorphic adenoma and cavernous hemangioma) often displace the ICA in a posterior or posterolateral direction; and as such, it provides the rationale to remove these tumors via a medial corridor (transnasal or transoral) reducing the potential of ICA injury. ⁹ The tumors originating from the retro-styloid compartment, however, demonstrate variable relationships with the ICA depending on the lesions' origin and histopathological types. ¹⁰ Schwannomas arising from the lower cranial nerves may displace the ICA into an anteromedial direction, which may thereby constitute a relative contraindication for transnasal or transoral access for dissection from the anterior and medial surgical corridors. ¹¹ Lesions arising from the sympathetic chain or metastatic lesions to retropharyngeal lymphnodes may displace the ICA in a posterior or posterolateral direction. ⁹

Due to the potential for spillage and subsequent recurrence, en bloc removal of tumors is required for pleomorphic adenoma, which most frequently arise from the deep lobe of the parotid gland or small salivary glands in the prestyloid compartment. ¹² For other types of benign but large sized tumors of the PPS (e.g., schwannoma and paraganglioma); however, a piecemeal removal with internal debulking is not contraindicated. ¹³ Although pleomorphic adenoma and basal cell adenoma (BSA) share a salivary gland origin is similar, recurrence rates are seemingly different. Recurrence of pleomorphic adenoma are frequently reported. ⁶ However, reports of BSA in PPS are sparse. ¹⁴

During a retrospective analysis of patients with benign tumors of the PPS resected via an endoscopic transoral corridor, we identified that four patients with a histopathological diagnosis of BSA. The purpose of this study was to retrospectively analyze the clinical and radiological characteristics of patients with BSA in the PPS, and to evaluate the feasibility of endoscopic transoral approach for resection.

Materials and Methods

Clinical Data

Four patients with histopathologic diagnosis of BSA arising in PPS who underwent endoscopic transoral approach for resection from January 1, 2014 to December 31, 2018 at Beijing Tongren Hospital, Capital Medical University were identified and enrolled in this study. Tumors with irregular borders or deemed potentially of malignant as assessed by a preoperative magnetic resonance imaging (MRI), or tumors with other histopathologic diagnoses were excluded from this study. Informed consent was obtained from these subjects upon admission, and the study protocol was approved by the ethics committee of Beijing Tongren Hospital.

Preoperative contrast enhanced CT and gadolinium contrasted MRI were performed to evaluate the relationships of the tumor with adjacent neurovascular structures. All surgeries were performed under endoscopic visualization by a senior author (X.H.C.).

Surgical Technique

Video 1

Endoscopic transoral resection of the basal cell adenoma arising from the parapharyngeal space.

Download video file ^{(155.9MB, mp4)}

Patients were intubated nasotracheally after induction with general anesthesia. A two-surgeon, four-handed technique was performed. Visualization was achieved using rigid rod-lens endoscopes (4-mm diameter and 18-cm length) with 0 and 45 degrees lenses coupled to a high-definition camera and video monitor (Karl Storz Endoscopy; Karl Storz, Tuttlingen, Germany). Both video ( Video 1 ) and standard digital images were recorded during dissections using the AIDA recording system (Karl Storz Endoscopy; Karl Storz, Tuttlingen, Germany).

Under visualization with a 0-degree scope, a mucosal incision was made 1 cm medial to the second molar teeth started close to the gingiva of the hard palate, directed downward to the third molar, then extended inferolaterally along the glossopalatine arch, and ended at the inferior pole of the palatine tonsil ( Fig. 1A ). The posterior branches arising from the lesser palatine artery and nerve may affected or even transected by the hard palate incision, whereas their anterior branches and those of the greater palatine and nerve course anteriorly after exiting their corresponding foramen in the hard palate are unlikely to be affected.

Fig. 1.

( A ) The incision on the left side (arrow), the polygon represents the third molar teeth; ( B ) after incision of the superior pharyngeal constrictor muscle (arrow), the adipose tissue in prestyloid compartment was encountered (polygon); ( C ) the corridor (enclosed dot lines) was created under the medial pterygoid muscle.

Following the elevation of the mucosa and submucosal tissue, one encounters the superior pharyngeal constrictor muscle, which can be then vertically incised to enter and expose the adipose tissue in the prestyloid PPS ( Fig. 1B ). A surgical corridor is continued under the inferior border of the medial pterygoid muscle ( Fig. 1C ).

The adipose tissue within the prestyloid PPS compartment was carefully cauterized and removed with a bipolar cautery enhancing the visualization of the anterior facet of the tumor ( Fig. 2A ). Dissection around the tumor exposed its superior, inferior, and lateral borders ( Fig. 2B ). To facilitate exposure and separation, an endoscope with a 45-degree lens was adopted to enhance visualization. If the ICA was displaced to the medial aspect of the tumor, one must identify the ICA and the ascending pharyngeal artery were prior to dissecting the medial border of the tumor ( Fig. 2C ). An atraumatic forceps can be used to grasp the carotid sheath and displace the ICA anteromedially, thus protecting the vessel before its separation from the medial border of the tumor ( Fig. 2D ).

Fig. 2.

( A ) The front facet of the tumor on left side; ( B ) the superior (red arrow), lateral (green arrow), and inferior borders (blue arrow) of the tumor were exposed; ( C ) the ICA and ascending pharyngeal artery were identified at first; ( D ) an atraumatic forceps retracting the carotid sheath (green arrow) medially to protect the ICA. ICA, internal carotid artery.

The styloid process is a good landmark to differentiate tumors arising from the prestyloid or retro-styloid compartment ( Fig. 3A ). Exposure of the superior border of tumors located at the upper PPS is often difficult. In addition to using of an angled endoscope (45 degrees), the removal of the lower aspect of the pterygoid process including the pterygoid hamulus ( Fig. 3B ) enhances the exposure of the superior pole.

Fig. 3.

( A ) The styloid process (arrow, left side) is a good landmark. ( B ) The pterygoid hamulus (arrow, left side).

After all border of the tumor have been clearly visualized, total separation of tumors from adjacent structures was performed. The tumor was removed en bloc ( Fig. 4A ) or by piecemeal with internal debulking ( Fig. 4B ), which correlates intimately with tumor size.

Fig. 4.

( A ) The tumor with small size on left side was removed en bloc . ( B ) The tumors with large size on left side was removed by piecemeal with internal debulking (arrow).

Following the complete removal of the tumor, the surgical field was carefully inspected, and hemostasis ensured. A thin closed suction drain was placed into the intraoperative cavity and fixed at the corner of the mouth. The incision was reapproximated using absorbable suture.

Results

Demographics, tumor size, histopathological classification, recurrence, relative location of the ICA to the tumor, and follow-up of these four patients are demonstrated in Table 1 . There were two men and two women with ages ranging from 61 to 66 years old. All four patients underwent an endoscopic transoral resection of the tumor, and no major vascular injuries occurred.

Table 1. The demographics, laterality, tumor size (cm ³ ), histopathology, location of the internal carotid artery relative to tumor body, recurrence, and follow-up (months) for the four patients with basal cell adenoma .

No.	Sex	Age	Laterality	Tumor size	Histopathology	ICA to TB	Recurrence	Follow-up
1	Female	61	Left	3.2 × 2.9 × 2.3	Solid	Posterior	No	52
2	Female	62	Right	5.2 × 4.5 × 2.9	Cystic	Medial	No	38
3	Male	66	Right	2.8 × 2.0 × 2.5	Solid	Posterior	No	32
4	Male	66	Left	3.3 × 2.8 × 2.4	Tubular	Medial	No	8

Abbreviations: ICA, internal carotid artery; TB, tumor body.

Symptoms and signs of patients with BSA in the PPS were atypical, and tumors were often incidentally identified. Patients presented with foreign body sensation ( n  = 1) and neck mass ( n  = 1), the remaining two patients were asymptomatic. During physical examination, nasopharyngeal and oropharyngeal swelling was observed in one patient.

On MRI, all four patients' tumors had a clear delineated margin, signs of heterogeneity with moderate enhancing after contrast with gadolinium, and cystic degeneration within the tumor were identified ( Fig. 5A ). In two patients, the ICA was displaced adjacent to the medial aspect of the tumor body ( Fig. 5B ). The ICA was located at the posterior aspect of the tumor body in the remaining two patients ( Fig. 5C ), among which the lateral border of the tumor was closely to the deep lobe of the parotid gland ( Fig. 5D ).

Fig. 5.

( A ) Cystic degeneration was common in patients with basal cell adenoma in parapharyngeal space; ( B ) the ICA (arrow) located at the medial aspect of the tumor body (T); ( C ) the ICA was displaced to the posterior aspect of the tumor body (T); and ( D ) the tumor body (T) was in continuous with the deep lobe of parotid gland (Pa, green arrow). ICA, internal carotid artery.

In three patients (75%), the tumor was resected en bloc . Their maximum diameter was less than 3.2 cm; however, the maximum diameter of the remaining tumor (25%) was 5.2 cm requiring internal debulking and piecemeal resection.

A nasogastric tube was placed in all patients for nutritional support after surgery and removed 1 week later. With respect to postoperative complications, trismus was seen in one patient and resolved after 3 months of mouth-opening exercises. No airway obstruction or reintubation, postoperative infection or abscess formation, bleeding, delayed healing of the surgical incision, postoperative cranial nerve injury, CSF leak, or intracranial infections were encountered in any of these four patients.

Follow-up ranged from 8 months to 52 months (mean = 32.50 ± 18.36 months). There was no sign of recurrence at the time of this study analysis.

Discussion

Pleomorphic adenoma is the most commonly reported salivary gland tumor arising in the prestyloid PPS. ¹⁵ Clinical and radiological characteristics of BSA in the PPS, however, is rarely described. ¹⁴ The present study demonstrates that BSAs arising in the PPS have a variable anatomical relationship with the ICA (lying lateral or anterior to the ICA). However, an endoscopic transoral corridor is feasible for the resection of BSAs in the PPS, even with the ICA lying at its medial aspect. ¹⁶

Wu et al reported three patients with BSAs in the PPS resected via a transoral approach. ¹⁴ Regarding the relationship between the ICA and the tumor, the ICA was reported to be displaced medially in one patient; nonetheless, the relationship was not specified in the other two patients. In the present study, the ICA was displaced medial to the tumor in two patients; thus, mandating the identification and protection of the ICA.

In our experience, use of atraumatic forceps to retract the carotid sheath and henceforth displace the ICA anteromedially helps to adequately expose the medial border of tumor and protect the ICA ( Fig. 2D ). This is a similar technique to that used for a transcervical approach and TORS. ^{12 16} Consequently, no rupture of ICA happened in this case series. A DSA including a balloon occlusion test are not routinely performed in our institution. This is reserved for select paraganglioma, or tumors with malignant potential, or those encroaching the great vessels.

Early in our experience we tried the operating microscope and found that it did not offer an adequate exposure of the upper, posteromedial, and posterolateral borders of the tumor in the upper PPS, did not allow angle views and the instrumentation of the surgical field led to some blind spots. We strongly prefer the use of endoscopes with 0 and 45 degrees lenses. The steps prior to expose the anterior facet of the tumor were employed using a 0-degree scope; as the angled lenses offer the advantages of exposure and visualization of previously inaccessible regions in the upper PPS. Moreover, removal of pterygoid hamulus and the lower part of the pterygoid process expands the exposure of the superior border of the tumor, especially when the tumor abuts the skull base.

Use of an endoscopic transoral approach for resection of tumors in the PPS is not new, and a similar concept has been also adopted for the management of anterior craniovertebral junction compressive pathologies. ^{17 18 19} Compared with open approaches (i.e., transcervical, transcervical-parotid, transmastoid-parotid, transcervical-parotid with mandibulectomy, and ITF approach), the endoscopic transoral approach demonstrates explicit advantages, including the avoidance of comorbidities such as esthetic defects or injury of the facial nerve and parotid gland. ²⁰ However, the disadvantages of a transoral approach are also significant and should be considered, including the potential of postoperative infection and abscess formation in PPS, difficulty in controlling the great vessels, oropharyngeal fistula, and emergent postoperative airway obstruction. ¹⁶ Therefore, the appropriate surgical approach needs to be individually selected.

Tumor spillage and recurrence of pleomorphic adenoma in the prestyloid PPS can occur if the tumor capsule is ruptured. ²¹ The consideration of a pleomorphic adenoma is not a contraindication for a transoral resection (either endoscopic assisted or by transoral robotic surgery). However, to avoid the potential of capsular rupture (pleomorphic adenoma) resulting in tumor spillage and recurrence, only those tumors with a maximal diameter of lesser than 4 cm was indicated for an endoscopic transoral en bloc resection. We have not attempted transoral resection of pleomorphic adenoma larger than 4 cm. In addition, employment of fine needle aspiration biopsy or thru-cut biopsy was not performed routinely in patients with tumors arising at the PPS, especially for those with suspicion of pleomorphic adenoma based on enhanced MRI.

Both the basal cell and pleomorphic adenomas may originate from the parotid gland or small salivary glands. ²² The radiologic appearance of BSA is not consistent or diagnostic, cystic degeneration, and heterogeneity with moderate enhancing after contrast with gadolinium were common characteristics on MRI. Therefore, it is difficult to differentiate these two tumors preoperatively. In general, we do not recommend a transoral approach if we suspect a pleomorphic adenoma greater than 4 cm or if a malignancy is suspected. In this series, one patient had a large tumor (5.2 cm); however, the tumor demonstrated a clear border and an obvious separation plane from adjacent structures, and furthermore, it seems to protrude into the oropharynx. In addition, the patient expressed a strong preference to undergo a transoral resection, and in case the tumor could not be resected en bloc , we were prepared to transition to an open or hybrid approach. A transoral resection was thereby attempted with the intraoperative ascertainment of BSA, which was ultimately removed piecemeal.

Tumors arising in the PPS have a variable relationship with the ICA that depends on its tissue of origin (salivary gland, node, cranial nerves, and sympathetic nerve chain), location (pre- or retro-styloid compartment), and histopathological types. ²³ Analysis of the four patients with BSA included in this study, the ICA was located at the medial aspect of the tumor and no connection with the deep lobe of the parotid gland in two patients, masquerading as a retro-styloid PPS tumor on radiological assessment. Therefore, we may speculate that the BSA with displacement of ICA into a medial aspect may be originated from the minor salivary gland around the styloid process. The remaining two patients with tumors lying anterior to the ICA, however, may originate from the deep lobe of the parotid gland.

BSA exhibit a variable histopathological features, which mainly include membranous and other patterns (i.e., solid, cystic, trabecular, and tubular). ²⁴ Overall, BSAs have a good prognosis, except for the membranous type that has a recurrence rate of 25%. ²⁴ All four patients in the present study demonstrated a pattern that was different from the membranous type.

At the term of follow-up, no recurrence has been detected in any of these patients. Moreover, since only benign PPS tumors are being managed with an endoscopic transoral resection, those with a suspected malignancy are eliminated as candidates. Nonetheless, one must consider a differential diagnosis that includes basal cell carcinomatous transformation, malignant pleomorphic adenoma and adenoid cystic carcinoma. ²⁵ Therefore, if the tumor were to be deemed malignant by intraoperative frozen biopsy (e.g., pleomorphic adenoma coexisted with malignancy), we would transition to an open approach to expand the resection to adjacent tissues.

There are significant limitations to this study. It is a retrospective study with a small sample size, and as such, it cannot provide a strong recommendation in respect to BSAs arising in PPS. Moreover, the mean follow-up time is 32.50 ± 18.36 months, which cannot accurately predict recurrence rate in the long run (more than 10 years).

Conclusion

BSAs arising in PPS may lie lateral or anterior to the ICA. Endoscopic transoral approach can provide a reasonable corridor for total resection of BSA arising in PPS with seemingly low morbidity.