Sage Journals: Discover world-class research

Abstract

Objectives: The ascending pharyngeal artery (APA) travels with the parapharyngeal internal carotid artery (pICA) in the parapharyngeal space (PPS). This study aimed to investigate the anatomical variations of the APA, and to explore their implications for endoscopic surgery in the PPS. Methods: Dissection of the APA in the PPS was performed on 10 cadaveric specimens (20 sides). The relationship between APA and PPS tumors was retrospectively reviewed in 20 patients, attempting to ascertain the APA during the resection of 10 pre-styloid and 10 retro-styloid PPS tumors. Results: During the cadaveric dissections, the APA was identified at the medial, posteromedial, or bilateral aspects of the pICA in 12 (60%) and 4 (20%) sides, respectively. In the remaining 4 sides (20%), the APA branched into several subcategory arteries lying at the medial and lateral aspects of the pICA. Branches of the APA were observed in 13/20 sides (65%). Two branches were found in 9/13 sides and 3 branches in 4/13, respectively. The APA was only identifiable in 1/10 (10%) of pre-styloid tumors, a patient with basal cell adenoma. In contrast, the APA was encountered surrounding the pICA in 8/10 (80%) of patients with retro-styloid tumors, all of which were schwannomas. No inadvertent injury of the APA or the pICA occurred in this cohort. Conclusions: With identification of the ascending pharyngeal artery on preoperative magnetic resonance imaging, it may serve as an additional landmark during the endoscopic extirpation of tumors arising in the PPS.

Keywords

ascending pharyngeal artery parapharyngeal space internal carotid artery tumor extirpation

Introduction

The parapharyngeal space (PPS) lies at the posterior aspect of the infratemporal fossa and above the inferior border of the medial pterygoid muscle.¹ The PPS is divided into the pre- and retro-styloid compartments by the styloid process and the attached stylopharyngeal aponeurosis.² Adipose tissue, lymph node, and the deep lobe of the parotid gland are the main structures within the pre-styloid space; whereas the retro-styloid compartment contains the parapharyngeal internal carotid artery (pICA), internal jugular vein, and lower cranial nerves (CN IX to XII).^3,4 Due to the complex neurovascular relationships of the PPS, extirpation of tumors arising from the PPS still carry great challenges.⁵

Multiple minimally invasive approaches have been adopted to address lesions arising from the PPS, among which the endoscopic transnasal and transoral corridors have gained popularity during the past 3 decades.^6-8 Using these and other approaches for the resection of benign lesions in the PPS yield satisfactory outcomes with a low incidence of complications or sequelae.^9,10 Of note, various anatomical structures, such as the foramen ovale, posterior trunk of V₃, lateral pterygoid plate, and tensor veli palatini muscle, have been advocated as landmarks to guide surgical procedures within the PPS and the infratemporal fossa.^11-13

Identification and protection of the pICA is critical for any procedure in the PPS,¹¹ especially when using minimally invasive corridors in a medial to lateral trajectory (ie, transnasal and transoral approaches).¹⁴ Prior studies have shown that the ascending pharyngeal artery (APA) accompanies the pICA as it traverses in the PPS,^1,3 and these studies identified its course and anatomical variations, as well as variable correlations with the pICA.^15,16

The APA supplies the lower cranial nerves (CN IX to XII) and connects the vertebrobasilar system through collateral communications.^17,18 Moreover, the APA may contribute to the blood supply the tumors arising from the PPS.¹⁹ Therefore, intraoperative identification of the APA may provide an additional reference to locate the pICA and to avoid its inadvertent injury. A strategy for intraoperative identification and protection of the APA in this context has not been sufficiently explored and proposed.

This study hypothesized that the APA may serve as an additional landmark for tumor removal in the PPS. Therefore, this study aims to assess anatomical variations of the APA, its correlation with the pICA, and to elucidate surgical implications for the extirpation of benign tumors arising in the PPS.

Materials and Methods

Cadaveric Dissection

The APA in PPS was dissected and assessed on 10 cadaveric heads (20 sides). Course variations of the APA to the pICA were recorded. The cadaveric dissections were conducted at the Anatomy Laboratory Toward Visuospatial Surgical Innovations in Otolaryngology and Neurosurgery (ALT-VISION) at the Wexner Medical Center of The Ohio State University. ALT-VISION and all coauthors were certified by local regulatory agencies dealing with the use of human tissues and cadaveric studies.

Visualization was achieved using rigid rod-lens endoscopes (4-mm diameter, 18-cm length) with 0° scope (Karl Storz Endoscopy; Karl Storz, Tuttlingen, Germany), coupled to a high-definition camera and video monitor. Both video and standard digital images were recorded during dissections using the AIDA recording system (Karl Storz Endoscopy; Karl Storz, Tuttlingen, Germany). A high-resolution CT scan was performed before the dissection and the data were exported to a surgical navigation system (Stryker, Kalamazoo, MI, USA).

Clinical Data

The study comprised a retrospective analysis of patients who underwent an endoscopic transoral extirpation of PPS tumors from January 1, 2014 to December 31, 2018. Informed consent was obtained from all patients and the study protocol was approved by the Ethics Committee of Beijing Tongren Hospital, Capital Medical University in China (no. TRECKY2016-036). During the tumor removal, the course of the APA, its relationship to the pICA, and the tumor in the PPS were assessed and recorded.

Results

Cadaveric Dissection

Technical nuances of surgical access into the PPS have been previously described in detail.¹ Following removal of the adipose tissue in the pre-styloid compartment, the stylopharyngeal aponeurosis was exposed (Figure 1A). The stylopharyngeal aponeurosis was subsequently peeled in a medial to lateral fashion, and the APA was encountered prior to exposing the pICA (Figure 1B). The APA was located at the medial aspect of the tensor veli palatini muscle in all 20 sides (Figure 1C).

Figure 1.

Left side of the specimen, viewed by 0° scope. (A) The stylopharyngeal aponeurosis of the left side was exposed (arrow); (B) after peeling of the stylopharyngeal aponeurosis (arrow), the APA was encountered; and (C) the APA located at the lateral aspect of the TVPM. APA, ascending pharyngeal artery; ET: Eustachian tube; TVPM, tensor veli palatini muscle.

The APA was found to travel at the medial (Figure 2A) and posteromedial (Figure 2B) aspects of the pICA in 12 (60%) and 4 (20%) sides, respectively. In the remaining 4 sides (20%), the APA branched into several subcategory arteries lying at the medial and lateral aspects of the pICA (Figure 2C), respectively.

Figure 2.

Left side of the specimen, viewed by 0° scope. The APA (left side) courses vertically upward at the medial (A) or posteromedial (B) aspect of the pICA; (C) the branches of APA course at the medial (green arrow) and lateral (blue arrow) aspect of the pICA. APA, ascending pharyngeal artery; pICA, parapharyngeal internal carotid artery.

In 13/20 sides of the specimens (65%), branches of the APA were identified (Figure 3A). Two branches were identified in 9 sides and 3 branches in 4 sides, respectively. At the superior aspect of the PPS close to the skull base, the APA coursed vertically at the medial or posteromedial aspect of the pICA (Figure 3B). Branches of the APA passing through the hypoglossal canal and the jugular foramen could also be observed (Figure 3C).

Figure 3.

Left side of the specimen, viewed by 0° scope. (A) The branches of APA (blue and green arrows); (B) when coursed upward close to the HGC, the APA located at the posteromedial aspect of the pICA; (C) the branches of APA nurturing the HGC (green arrow) and JF (blue arrow). APA, ascending pharyngeal artery; HGC, hypoglossal canal; JF, jugular foramen; pICA, parapharyngeal internal carotid artery.

Intraoperative Validation

The technical details of the endoscopic transoral approach for extirpation of tumors arising from the PPS has been previously reported.^8,20 Tumors arising in the pre-styloid compartment in this cohort included pleomorphic adenoma (n = 7), basal cell adenoma (n = 1), and cavernous hemangioma (n = 2). The APA was not encountered in any of the patients with pleomorphic adenoma or cavernous hemangioma (n = 9, 90%). In the patient with a basal cell adenoma (pre-styloid compartment; Figure 4A), however, both the APA and the pICA had been displaced to the medial aspect of the tumor. The tumor was subsequently removed en bloc with preservation of both vessels (Figure 4B).

Figure 4.

Left PPS, viewed by 0° scope. (A) The tumor located anterior to the SP; (B) intraoperative identification of the APA and the pICA. APA, ascending pharyngeal artery; pICA, parapharyngeal internal carotid artery; SP, styloid process.

All retro-styloid compartment tumors included in this cohort were schwannomas (n = 10). In all these 10 patients, the pICA was displaced into the anteromedial aspect of the tumor (Figure 5A). While the APA was identified in 8 patients (80%) on the preoperative magnetic resonance imaging (MRI) at the anteromedial aspect of the pICA (Figure 5B).

Figure 5.

(A) The pICA was displaced into the anteromedial aspect of the tumor; (B) the branches of APA (green arrows) and pICA (red arrows) on preoperative MRI. APA, ascending pharyngeal artery; MRI, magnetic resonance imaging; pICA, parapharyngeal internal carotid artery.

During the transoral resection of tumors arising in the retro-styloid compartment, the APA served as a sentinel landmark for the pICA (Figure 6A). The pICA was identified at the posterior aspect of the APA in 8 patients (80%, Figure 6B), which was in accordance with the presence of APA in MRI scan. All tumors were removed without injury of these arteries. Branches of the APA were observed coursing vertically in 3 patients (37.5%, Figure 6C). In the remaining 2 patients with retro-styloid tumors, the APA was not encountered, and the medial border of the tumor was dissected following identification and preservation of the pICA.

Figure 6.

Left PPS, viewed by 0° scope. (A) The APA locates at the anteromedial aspect of the tumor; (B) the pICA locates at the posterior aspect of the APA; (C) branches of APA (green arrows). APA, ascending pharyngeal artery; pICA, parapharyngeal internal carotid artery; PPS, parapharyngeal space.

Discussion

The complex neurovascular relationships within the PPS, pose significant challenges for extirpation of lesions originally arising from the PPS.²¹ Therefore, additional surgical landmarks like the APA may help complete a safe surgical procedure in the PPS.¹⁵ Anatomical variations of the APA and their implications were explored using cadaveric dissections and confirmed in live surgeries; thus, adding to our knowledge of the PPS surgical anatomy.

The APA routinely branched from the external carotid artery and coursed vertically upward toward the skull base.^3,22 The APA has several branches, including the superior pharyngeal branch and the meningeal branch.^17,23 In this cadaveric study, the APA was detected to constantly course surrounding the pICA (at the medial and posteromedial aspects of the pICA in 60% and 20% of specimens respectively) at the retro-styloid compartment; and as such, the APA may serve as an additional landmark to localize the pICA intraoperatively, especially when employing an endoscopic approach.

Others described the external carotid artery traveling vertically or diagonally in the retro-styloid compartment, whereas the branches of the APA may course in both the pre- and retro-styloid compartments.^15,19 This cadaveric study demonstrated that the APA was identified in the retro-styloid compartment in all 20 sides. In this cohort of 10 patients with pre-styloid tumors; however, the APA was intraoperatively encountered in one patient only (10%). We analyzed this phenomenon in our previous publication, considering that the basal cell adenoma was arising from the small salivary gland around the styloid process, masquerading as a retro-styloid PPS tumor to displace the carotid artery and APA medially.²⁰ In the clinical setting, we also observed that the main trunk of the external carotid artery was occasionally encountered during the procedures in the pre-styloid space, whereas the APA was rarely exposed during pre-styloid PPS tumor removal. Therefore, we may consider that the role of APA for procedures within the pre-styloid compartment is relatively limited.

External approaches including the transcervical, transcervical-parotid with or without mandibulotomy have been routinely performed for the extirpation of tumors in the retro-styloid compartment.^24,25 The pICA is often displaced to the medial or anteromedial aspect of these tumors.⁸ Although the potential risk of injury to the pICA exists, endoscopic approaches have been successfully applied for resection of retro-styloid tumors.^8,26 In this cohort of retro-styloid tumors, the pICA was displaced into the anteromedial aspect of the tumor, and the APA was identified to at the anterior aspect of the pICA in 80% of preoperative MRIs and validated in surgical dissections. In these 8 patients, the APA could be adequately revealed and protected, and it is not necessary to sacrifice the artery. Therefore, suggesting that the APA serve as a valuable landmark for endoscopic procedures within the retro-styloid compartment. However, the APA was not constantly presented for all patients who harbored the schwannoma (20% absence). Compressing the artery by the tumor might constitute the contributing factor; and as such, presence of the APA on preoperative MRI may be a valuable reference factor to facilitate its intraoperative usage. Moreover, the paraganglioma often arises from the vagus or the sympathetic trunk in the retro-styloid space, and the open approaches are traditionally adopted for management of these paragangliomas. It is not difficult to control the APA from an open incision; and as such, the role of APA for paraganglioma management is limited via the open approach.

Given that the APA can branch to supply the lower cranial nerves (CN IX to XII) and has collateral communication with the vertebrobasilar artery system, the intraoperative identification and protection of the APA may be of critical importance.¹⁷ A preoperative high-resolution MRI screening can help in its identification and to define its relationship with the tumor and the pICA. Moreover, the APA may supply tumors arising in the PPS, especially for paragangliomas in the PPS. A preoperative digital subtraction angiography can help determine if the APA is the dominant nurturing vessel.¹⁸ In this regard, it may advantageous to embolize the APA preoperatively especially for vascular tumors such as paragangliomas.²⁷ Based on our experience, however, the APA was rarely detected to supply the schwannoma. Therefore, for patients with schwannoma selected in this cohort, the nutrition function by the APA to the schwannoma was limited.

Based on our observation, the tumor size does not impact the relationship between the APA and the tumor in PPS. Instead, the tumor origin from the pre- or retro-styloid compartment may determine the relative relationship between the tumor and the artery. To extirpate the tumor in the PPS en bloc via the transoral approach, we have previously reported that the maximal diameter of the tumor was 5 cm.^8,20 For schwannomas arising from the retro-styloid space, however, the diameter is not the determining factor due to the fact that the tumor can be removed in an intracapsular and piece-by-piece fashion.

In a previous study, the tensor veli palatini muscle was used as the landmark for intraoperative identification of the pICA via an endonasal corridor.²⁸ Based on this cadaveric dissection, however, the APA was identified lying between the tensor veli palatini muscle and the pICA in 60% of specimens. Therefore, following identification of the tensor veli palatini muscle, the APA may serve as a complementary landmark for identification of the pICA through an endonasal or transoral corridor. Furthermore, particular attention is desirable when elevating and dividing the tensor veli palatini muscle, in case to avoid inadvertent injury of the APA.

The authors acknowledge the significant limitations included in the present study. All cadaveric dissection involved in the PPS was performed through an endonasal corridor, whereas all tumors in the clinical series were resected an endoscopic transoral corridor. Although a significant bias may exist, the anatomical principles and the neurovascular relationships within the PPS are adequately described. Moreover, while the value of using the APA as a landmark for procedures within the PPS has been validated for the endoscopic transoral corridor, its implication for endonasal resection remains undefined. In addition, one should note that the transoral corridor for resection of retro-styloid tumors is associated with significant technical difficulty and risk; thus, should only be performed by surgical teams with adequate experience in skull base and infratemporal fossa.

Conclusion

With identification of the APA on preoperative MRI, it may serve as an additional landmark for extirpation of tumors arising in the retro-styloid PPS via the endoscopic approaches.

Footnotes

Authors’ Note

Abstract was accepted as poster presentation at the Chinese Annual Meeting of Otolaryngology–Head and Neck Surgery, Suzhou, November 2021.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Declaration of Conflicting Interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: N. London holds stock in Navigen Pharmaceuticals and was a consultant for Cooltech Inc. The other authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This article was supported by the Beijing Municipal Administration of Hospitals Incubating Program (PX2024008).

ORCID iDs

Lifeng Li

Nyall R. London

References

London

Jr Prevedello

Carrau

. Endonasal endoscopic transpterygoid approach to the upper parapharyngeal space. Head Neck. 2020;42:2734-2740.

Fang

Zhou

Jiang

. The anatomy of the parapharyngeal segment of the internal carotid artery for endoscopic endonasal approach. Neurosurg Rev. 2020;43:1391-1401.

London

Jr Prevedello

Carrau

. Anatomy based corridors to the infratemporal fossa: implications for endoscopic approaches. Head Neck. 2020;42:846-853.

London

Prevedello

Carrau

. Endonasal access to lower cranial nerves: from foramina to upper parapharyngeal space. Head Neck. 2021;43:3225-3233.

Hosseini

Razfar

Carrau

, et al. Endonasal transpterygoid approach to the infratemporal fossa: correlation of endoscopic and multiplanar CT anatomy. Head Neck. 2012;34:313-320.

Mohamed

Paleri

George

. A cadaveric study quantifying the anatomical landmarks of the facial artery and its parapharyngeal branches for safe transoral surgery. Head Neck. 2019;41:3389-3394.

Boyce

Curry

Luginbuhl

Cognetti

. Transoral robotic approach to parapharyngeal space tumors: case series and technical limitations. Laryngoscope. 2016;126:1776-1782.

London

Jr Gao

Carrau

Chen

. Endoscopic transoral approach for resection of retrostyloid parapharyngeal space tumors: retrospective analysis of 16 patients. Head Neck. 2020;42:3531-3537.

Chen

Sun

Tang

. Surgical treatment of primary parapharyngeal space tumors: a single-institution review of 28 cases. J Oral Maxillofac Surg. 2019;77:1520.e1521-1520.e1516.

10.

Chen

, et al. Excision of tumors in the parapharyngeal space using an endoscopically assisted transoral approach: a case series and literature review. J Int Med Res. 2019;47:1103-1113.

11.

Tanjararak

Upadhyay

Thiensri

, et al. Potential surgical exposure of the parapharyngeal internal carotid artery by endonasal, transoral, and transcervical approaches. J Neurol Surg B Skull Base. 2018;79:241-249.

12.

Sun

Yan

Truong

Borghei-Razavi

Snyderman

Fernandez-Miranda

. A comparative analysis of endoscopic-assisted transoral and transnasal approaches to parapharyngeal space: a cadaveric study. J Neurol Surg B Skull Base. 2018;79:229-240.

13.

London

Jr Prevedello

Carrau

. Anatomical variations and relationships of the infratemporal fossa: foundation of a novel endonasal approach to the foramen ovale. J Neurol Surg B Skull Base. 2021;82:668-674.

14.

Roger

Patron

Moreau

Kanagalingam

Babin

Hitier

. Extended endonasal approach versus maxillary swing approach to the parapharyngeal space. Head Neck. 2018;40:1120-1130.

15.

Wang

Kundaria

Fernandez-Miranda

Duvvuri

. A description of arterial variants in the transoral approach to the parapharyngeal space. Clin Anat. 2014;27:1016-1022.

16.

Robinson

. Vascular lesions of the skull base: endovascular prospective for the otolaryngologist. Otolaryngol Clin North Am. 2005;38:737-771.

17.

Martins

Yasuda

Campero

Ulm

Tanriover

Rhoton

Jr.

Microsurgical anatomy of the dural arteries. Neurosurgery. 2005;56:211-251; discussion 211-251.

18.

Cavalcanti

Reis

Hanel

, et al. The ascending pharyngeal artery and its relevance for neurosurgical and endovascular procedures. Neurosurgery. 2009;65:114-120; discussion 120.

19.

Hacein-Bey

Daniels

Ulmer

, et al. The ascending pharyngeal artery: branches, anastomoses, and clinical significance. Am J Neuroradiol. 2002;23:1246-1256.

20.

London

Jr Li

Chen

Carrau

. Endoscopic transoral approach for resection of basal cell adenoma arising in parapharyngeal space. J Neurol Surg B Skull Base. 2021;82:675-681.

21.

Battaglia

Turri-Zanoni

Dallan

, et al. Endoscopic endonasal transpterygoid transmaxillary approach to the infratemporal and upper parapharyngeal tumors. Otolaryngol Head Neck Surg. 2014;150:696-702.

22.

Lemos-Rodriguez

Sreenath

Rawal

Overton

Farzal

Zanation

. Carotid artery and lower cranial nerve exposure with increasing surgical complexity to the parapharyngeal space. Laryngoscope. 2017;127:585-591.

23.

Weber

Patel

. Jugulotympanic paragangliomas. Otolaryngol Clin North Am. 2001;34:1231-1240, x.

24.

Grilli

Suarez

Munoz

Costales

Llorente

. Parapharyngeal space primary tumours. Acta Otorrinolaringol Esp. 2017;68:138-144.

25.

Okamoto

Tsukahara

Sato

. Parapharyngeal space tumor surgery using a modified cervical-parotid approach. Acta Otolaryngol. 2018;138:165-169.

26.

Strohl

El-Sayed

. Contemporary management of parapharyngeal tumors. Curr Oncol Rep. 2019;21:103.

27.

Chen

, et al. Management of multiple head and neck paragangliomas with assistance of a 3-D model. Ear Nose Throat J. 2023;103:362-368.

28.

Liu

Hsu

Shen

. Endoscopic endonasal nasopharyngectomy: tensor veli palatine muscle as a landmark for the parapharyngeal internal carotid artery. Int Forum Allergy Rhinol. 2017;7:624-628.

Anatomical Variations of the Ascending Pharyngeal Artery: Implications for Endoscopic Surgery in the Parapharyngeal Space

Abstract

Keywords

Introduction

Materials and Methods

Cadaveric Dissection

Clinical Data

Results

Cadaveric Dissection

Intraoperative Validation

Discussion

Conclusion

Footnotes

Authors’ Note

Data Availability Statement

Declaration of Conflicting Interests

Funding

ORCID iDs

References