Abstract
Nasopharynx is a complex region situated at the center of skull surrounded by various vital neurovascular structures. Surgical access to the nasopharyngeal space poses significant challenges due to the position of the internal carotid artery (ICA). Open approaches to nasopharynx utilize the lateral to medial anatomy but the endoscopic endo-nasal approach warrants knowledge about the medial to lateral anatomy. In this study we attempted to find the consistent surgical landmarks for parapharyngeal portion of internal carotid artery at the level of nasopharynx by means of cadaveric and radiological study. Eight fresh frozen cadavers (16 sides) and 30 CT angiography (60 sides) were included in the anatomical and radiological study respectively. Superior aspect of the torus tubarius was taken as the reference point in cadaveric study and C1–C2 interspace was used as the reference point for the radiological study. The distance between the ICA to the landmarks such as fossa of Rosenmullaer, torus tubarius, medial and lateral pterygoid plates were recorded. The mean distance of ICA to the fossa of Rosenmuller was 8.5 ± 1.4 mm and 9.1 ± 1.1 mm in the cadaveric and radiological study respectively. The mean distance between ICA to torus tubarius was 19.8 ± 1.3 mm in cadaveric and 20.6 ± 1.0 mm in radiological study. The mean distance of ICA to medial and lateral pterygoid plates were 25.3 ± 1.4 mm and 18.2 ± 1.4 mm in the cadaveric study and 25.9 ± 1.2 mm and 18.8 ± 1.3 mm in the radiological study respectively. On correlating the measurements between cadaveric and radiological study, the p values were not statistically significant (p > 0.05). The closest landmark to the ICA was the fossa of Rosenmuller. ICA was located at the same sagittal plane as that of the lateral pterygoid plate. The nasopharynx is a complex anatomical region closely related to ICA. Inadvertent injury to ICA is one of the dreaded complications of nasopharyngeal surgery. Fossa of Rosenmuller is only few millimeters away from the ICA and must be treated very cautiously. During the endoscopic approach, the ICA is at the sagittal plane as of the lateral pterygoid plate. This must be kept in mind when advancing toward the ICA by keeping intact the lateral pterygoid plate when possible and one should stay in the plane of medial pterygoid plate as the ICA lies posterolateral to it. Cadaveric dissections supported by radiological data would definitely aid surgeons to successfully perform surgeries in nasopharynx.
Keywords: Internal carotid artery, Parapharyngeal ICA, Endoscopic nasopharyngectomy, Cadaveric study, Radiological study
Introduction
Nasopharynx is a complex region situated at the center of skull surrounded by various vital neurovascular structures. Surgical access to the nasopharyngeal space poses significant challenges due to the position of the internal carotid artery (ICA), which is surrounded by soft tissue with very few reliable surgical landmarks [1–3]. A complete and systematic understanding of the ICA anatomy is a rate-limiting step to avoid surgical morbidity. Open approaches to nasopharynx utilize the lateral to medial anatomy but the endoscopic endo-nasal approach warrants knowledge about the medial to lateral anatomy [1, 2]. In this study we attempted to find the consistent surgical landmarks for parapharyngeal portion of internal carotid artery at the level of nasopharynx by means of cadaveric and radiological study.
Material and Methods
The anatomical (cadaveric) study was conducted as a part of Head and Neck Cadaveric Dissection Workshop conducted by the senior author at M S Ramaiah Advanced Learning Center, Bangalore. 8 fresh frozen cadavers (16 head and neck regions) were included in the anatomical study. The cadavers were positioned supine with neck extension. Maxillary swing approach performed and nasopharynx, infratemporal fossa and parapharyngeal space exposed. After the dissection, we measured the closest distance between the ICA and the mentioned anatomical landmarks at the reference level using a slide caliper and measurements were recorded in the proforma sheet. The reference level was taken at the level of superior margin of torus tubarius which corresponds to the level of C1–C2 interspace.
The radiological study was done at the Apollo Hospitals, Bangalore. 30 CT-Angiogram of neck (60 head and neck regions) were included in our study. None of the patients had any nasopharyngeal / maxillary / infratemporal fossa or parapharyngeal lesions or underwent nasopharyngeal / lateral neck surgeries that could alter the anatomy of area of interest. The obtained axial images of bone and soft tissue windows were reformatted into coronal and sagittal section images of 1 mm thickness and the digital images were reviewed. The C1–C2 interspace was taken as the reference point in the radiological study. The reference point was identified in the coronal section and the corresponding axial section image was used to measure the distance between ICA and the various landmarks. Fossa of Rosenmuller was identified as lateral air-soft tissue interface at the posterolateral aspect of nasopharynx.
The landmarks are; (both anatomical and radiological study, Figs. 1–4).
Soft tissue landmark—Fossa of Rosenmuller (FOR),
Cartilaginous landmark—Torus Tubarius (TT),
Bony landmarks—Medial pterygoid plate (MPP) and Lateral pterygoid plate (LPP).
Fig. 2.
Diagrammatic representation of measurement of distance from lateral pterygoid plate to ICA
Fig. 3.
Diagrammatic representation of measurement of distance from torus tubarius to ICA
Fig. 1.
Diagrammatic representation of measurement of distance from medial pterygoid plate to ICA
Fig. 4.
Diagrammatic representation of measurement of distance from fossa of Rosenmuller to ICA
Necessary approval for this study was obtained from Institutional Ethical Committee at Apollo Hospitals, Bangalore and MS Ramaiah Advanced Learning Centre, Bangalore. The findings were tabulated in the excel sheet using SPSS software and mean with standard deviation were calculated for all the measurements. The correlation between the cadaveric and radiological measurements was performed using unpaired T test and p value of < 0.05 was considered significant.
Results
Eight fresh frozen cadavers (16 sides) and 30 CT angiography (60 sides) were included in the anatomical and radiological study respectively. The mean distance of ICA to the fossa of Rosenmuller was 8.5 ± 1.4 mm and 9.1 ± 1.1 mm in the cadaveric and radiological study respectively. The mean distance between ICA to torus tubarius was 19.8 ± 1.3 mm in cadaveric and 20.6 ± 1.0 mm in radiological study. The mean distance of ICA to medial and lateral pterygoid plates were 25.3 ± 1.4 mm and 18.2 ± 1.4 mm in the cadaveric study and 25.9 ± 1.2 mm and 18.8 ± 1.3 mm in the radiological study respectively. On correlating the measurements between cadaveric and radiological study, the p values were not statistically significant (p > 0.05). Thus the measurements were similar between the cadaveric and radiological study (Table 1).
Table 1.
Table depicting correlation between anatomical and radiological measurements of landmarks from ICA
| Measurements | Side | Anatomical study | Radiological study | Unpaired t test | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| N | Mean (mm) | SD | N | Mean (mm) | SD | t | SE | p | ||
| ICA-FOR | R | 8 | 8.4 | 1.4 | 30 | 9.0 | 1.2 | 1.2 | 0.5 | 0.23 |
| L | 8 | 8.5 | 1.4 | 30 | 9.1 | 1.2 | 1.3 | 0.5 | 0.19 | |
| TOTAL | 16 | 8.5 | 1.4 | 60 | 9.1 | 1.1 | 1.8 | 0.3 | 0.07 | |
| ICA-TT | R | 8 | 19.8 | 1.3 | 30 | 20.7 | 1.0 | 2.0 | 0.4 | 0.06 |
| L | 8 | 19.9 | 1.3 | 30 | 20.6 | 1.0 | 1.7 | 0.4 | 0.09 | |
| TOTAL | 16 | 19.8 | 1.3 | 60 | 20.6 | 1.0 | 2.6 | 0.3 | 0.12 | |
| ICA-MPP | R | 8 | 25.2 | 1.5 | 30 | 25.6 | 1.5 | 0.6 | 0.6 | 0.52 |
| L | 8 | 25.3 | 1.4 | 30 | 25.5 | 1.5 | 0.4 | 0.6 | 0.68 | |
| TOTAL | 16 | 25.3 | 1.4 | 60 | 25.9 | 1.2 | 1.9 | 0.3 | 0.06 | |
| ICA-LPP | R | 8 | 18.1 | 1.5 | 30 | 18.8 | 1.4 | 1.3 | 0.5 | 0.19 |
| L | 8 | 18.3 | 1.5 | 30 | 18.8 | 1.3 | 0.9 | 0.5 | 0.35 | |
| TOTAL | 16 | 18.2 | 1.4 | 60 | 18.8 | 1.3 | 1.6 | 0.4 | 0.10 | |
The closest landmark to the ICA was the fossa of Rosenmuller and it was found lateral or posterolateral to the ICA. ICA was always found posterolateral to the medial pterygoid plate and it is located at the same sagittal plane as that of the lateral pterygoid plate (Figs. 5–11). Torus tubarius was found anteromedial to the ICA. We did not encounter any kinking or tortuous course of the internal carotid artery both in the cadaveric and radiological study.
Fig. 6.
Cadaveric dissection image depicting measurement of distance from lateral pterygoid plate to ICA
Fig. 7.
Diagrammatic representation of relationship of medial pterygoid plate to ICA
Fig. 8.
Radiological image depicting measurement of distance from fossa of Rosenmuller to ICA
Fig. 9.
Radiological image depicting measurement of distance from torus tubarius to ICA
Fig. 10.
Radiological image depicting measurement of distance from medial pterygoid plate to ICA
Fig. 5.
Cadaveric dissection image depicting the relationship of fossa of Rosenmuller and torus tubarius to ICA
Fig. 11.
Radiological image depicting measurement of distance from lateral pterygoid plate to ICA
Discussion
Advances in the technology have led to expansion of the horizon of endoscopic endonasal surgeries. Improved optics and visualization rendered by the endoscopes allow easy and minimally invasive access to even the difficult to access areas like nasopharynx and infratemporal fossa. Endoscopic technique confers additional advantage of reduced morbidity to the patients. Endoscopic nasopharyngectomy is being performed for the primary, secondary as well as recurrent nasopharyngeal carcinomas [1]. The main concern during the surgery is the internal carotid artery (ICA) which is surrounded by the soft tissue and hence surgical landmarks are difficult to establish. The published rate of ICA injury for traditional open approach ranges from 3–8% and 0.2–1.4% for endoscopic approach [1, 2]. The Injury to ICA leads to life threatening complications and leads to morbidity and even mortality to the patients. Hence it is pertinent to define the constant and reliable landmarks to locate ICA [3–6].
Internal carotid artery course has been divided into seven segments by Bouthilier et al. [7]. Mohamed et al. [4] had described six segments of ICA as encountered during endoscopic endonasal approach such as, parapharyngeal, petrous, paraclival, parasellar, paraclinoid and intradural segments. Parapharyngeal portion of the ICA is the most commonly encountered segment during endoscopic nasopharyngectomy. Various landmarks such as Eustachian tube isthmus, tensor vali palitini, levator vali palatini, longus capitis muscle, foramen ovale, foramen lacerum, stylopharyngeal fascia, pharyngeal recess and lateral pterygoid plate and pharyngeal tubercle have been mentioned in the literature to locate ICA [4–15].
We used maxillary swing technique for dissection in cadavers because it is an anterior approach similar to endoscopic approach and the landmarks encountered are same for both the approaches [3]. The closest landmark encountered was fossa of Rosenmuller at a distance of 7-10 mm and ICA was lateral or posterolateral to it in both cadaveric and radiological study which is consistent with the literature. ICA was located always posterolateral to torus tubarius and medial pterygoid plate. Lateral pterygoid plate was found at the same sagittal plane as that of ICA.
Fossa of Rosenmuller is the closest landmark but it is not constant as it is a soft tissue landmark. The soft tissue landmark like fossa of Rosenmuller and cartilaginous landmark like torus tubarius cannot be used in cases of carcinoma because these structures could be invaded or their location could be altered by the lesion. Hence bony landmarks can be considered as the most reliable landmarks to locate ICA. Lateral pterygoid plate when traced posteriorly, ICA is located at the distance of 17-19 mm in the same sagittal plane. The involvement of the ICA depends on the type and extension of the tumor. Limited lesions lead to obliteration of fossa of Rosenmuller. But large tumors or advanced cancers may lead to either pushing or encasement of ICA. Hence diligent examination of CT / MRI to be done to evaluate the extension of the lesion along with the involvement of ICA and its relation to the above mentioned landmarks in all the cases.
In our study, the measurement from ICA to FOR, TT, MPP and LPP were similar in both cadaveric and radiological study (p > 0.05). Thus the relationship and distance of ICA to these landmarks can be determined pre-operatively by the radiological imaging in order to identify any variations and to avoid injury to ICA during dissection. Fresh frozen cadavers without latex injection were used in our study which is similar to the live tissue. Thorough understanding of inside-out anatomy of nasopharynx along with pre-operative imaging leads to safer dissection without any injury to the ICA.
Conclusion
The nasopharynx is a complex anatomical region closely related to ICA. Inadvertent injury to ICA is one of the dreaded complications of nasopharyngeal surgery. Fossa of Rosenmuller is only few millimeters away from the ICA and must be treated very cautiously. During the endoscopic approach, the ICA is at the sagittal plane as of the lateral pterygoid plate. This must be kept in mind when advancing toward the ICA by keeping intact the lateral pterygoid plate when possible and one should stay in the plane of medial pterygoid plate as the ICA lies posterolateral to it. Cadaveric dissections supported by radiological data would definitely aid the surgeons to successfully perform surgeries in the nasopharynx.
Acknowledgement
Nil.
Authors' Contributions
Satish Nair: Substantial contributions to the conception or design of the work, revising it critically for important intellectual content, analysis and interpretation of data for the work and drafting the work and final approval of the version to be published. Namrata Srivastava, Brijith KVR: Substantial contributions to the acquisition of data for the work. Aishwarya J G: Substantial contributions to the acquisition of data for the work, revising it critically for important intellectual content and final approval of the version to be published.
Funding
Nil.
Declarations
Conflict of interest
Nil.
Footnotes
Publisher's Note
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References
- 1.Liu Y, Xie Y, Zou X, You R, Yang Q, Chen M. Techniques of endoscopic nasopharyngectomy for localized stage I nasopharyngeal carcinoma. Head Neck. 2020;42(4):807–812. doi: 10.1002/hed.26090. [DOI] [PubMed] [Google Scholar]
- 2.Herzallah I, Casiano R. endoscopic endonasal study of the internal carotid artery course and variations. Am J Rhinol. 2007;21(3):262–270. doi: 10.2500/ajr.2007.21.3030. [DOI] [PubMed] [Google Scholar]
- 3.Simon F, Vacher C, Herman P, Verillaud B. Surgical landmarks of the nasopharyngeal internal carotid using the maxillary swing approach: a cadaveric study. Laryngoscope. 2016;126:1562–1566. doi: 10.1002/lary.25870. [DOI] [PubMed] [Google Scholar]
- 4.LabibMA PrevedelloDM, Carrau R, Kerr EE, Naudy C, Abou AlShaar H, et al. A road map to the internal carotid artery in expanded endoscopic endonasal approaches to the ventral cranial base. Neurosurgery. 2014;10:448–471. doi: 10.1227/NEU.0000000000000362. [DOI] [PubMed] [Google Scholar]
- 5.Lee DL, McCoul ED, Anand VK, Schwartz TH. Endoscopic endonasal access to the jugular foramen: defining the surgical approach. J Neurol Surg B Skull Base. 2012;73:342–351. doi: 10.1055/s-0032-1322796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Liu J, Pinheiro-Neto CD, Fernandez-Miranda JC, Snyderman CH, Gardner PA, Hirsch BE, et al. Eustachian tube and internal carotid artery in skull base surgery: an anatomical study. Laryngoscope. 2015;124:2655–2664. doi: 10.1002/lary.24808. [DOI] [PubMed] [Google Scholar]
- 7.Bouthillier A, van Loveren HR, Keller JT. Segments of the internal carotid artery: a new classification. Neurosurgery. 1996;38:425–433. doi: 10.1097/00006123-199603000-00001. [DOI] [PubMed] [Google Scholar]
- 8.Ozgur Z, Celik S, Govsa F, Aktug H, Ozgur T. A study of the course of the internal carotid artery in the parapharyngeal space and its clinical importance. Eur Arch Otorhinolaryngol. 2007;264:1483–1489. doi: 10.1007/s00405-007-0398-6. [DOI] [PubMed] [Google Scholar]
- 9.Ekici F, Tekbas G, Onder H, Gumus H, Cetincakmak MG, Palanci Y, et al. Course anomalies of extracranial internal carotid artery and their relationship with pharyngeal wall: an evaluation with multislice CT. Surg Radiol Anat. 2012;34:625–631. doi: 10.1007/s00276-012-0958-3. [DOI] [PubMed] [Google Scholar]
- 10.Feigl G, Anderhuber F, Fasel JH, Likar R. Meaning of stylopharyngeal fascia in intraoral block techniques. Schmerz. 2007;21:28–33. doi: 10.1007/s00482-006-0497-0. [DOI] [PubMed] [Google Scholar]
- 11.Gardner PA, Tormenti MJ, Pant H, Fernandez-Miranda JC, Snyderman CH, Horo-witz MB. Carotid artery injury during endoscopic endonasal skull base surgery: incidence and outcomes. Neurosurgery. 2013;73:261–269. doi: 10.1227/01.neu.0000430821.71267.f2. [DOI] [PubMed] [Google Scholar]
- 12.Ho B, Jang DW, VanRompaey J, Figueroa R, Brown JJ, Carrau RL, et al. Landmarks for endoscopic approach to the parapharyngeal internal carotid artery: a radiographic and cadaveric study. Laryngoscope. 2014;124:1995–2001. doi: 10.1002/lary.24601. [DOI] [PubMed] [Google Scholar]
- 13.Gao Z, Chi FL. Anatomy relationship around internal carotid artery in the endoscopic surgery of nasopharynx: a study based on computed tomography angiography. J Neurol Surg B Skull Base. 2015;76(3):176–182. doi: 10.1055/s-0034-1395488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Battaglia P, Eesa M, Pietrobon G, Karligkiotis A, Castelnuovo P, Turri-Zanoni M. Practical guide for identification of internal carotid artery during endoscopic nasopharyngectomy. Laryngoscope. 2020 doi: 10.1002/lary.28778. [DOI] [PubMed] [Google Scholar]
- 15.Liu CL, Hsu NI, Shen PH. Endoscopic endonasal nasopharyngectomy: tensor veli palatine muscle as a landmark for the parapharyngeal internal carotid artery. Int Forum Allergy Rhinol. 2017;7(6):624–628. doi: 10.1002/alr.21921. [DOI] [PubMed] [Google Scholar]