The Anatomical Relationship Between the Eustachian Tube and Petrous Internal Carotid Artery

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1 The Laryngoscope VC 2012 The American Laryngological, Rhinological and Otological Society, Inc. The Anatomical Relationship Between the Eustachian Tube and Petrous Internal Carotid Artery Kayhan Ozturk, MD; Carl H. Snyderman, MD, MBA; Paul A. Gardner, MD; Juan C. Fernandez-Miranda, MD Objectives/Hypothesis: The aim of the present study was to investigate the relationship between the eustachian tube (ET) and petrous internal carotid artery (ICA) in whole-mount human temporal bone specimens. Study Design: Descriptive study. Methods: Histologically prepared serial sections of 10 adult temporal bones were included in the study. Five specific landmarks were selected to evaluate relationships between the petrous segment of the ICA and the ET. The selected distances were measured using computer software (Metamorph ; Molecular Devices, LLC, Sunnyvale, CA). Results: The ET and the ICA get close posteriorly, and the bony part of the ET and the ICA generally share the same wall. Conclusions: The junctional part of the ET may be a safe landmark to identify and protect the ICA during endoscopic endonasal surgery of the cranial base. Knowledge of the anatomical relationships of the ET and petrous part of the ICA, as well as their relationship with other surgical and radiological landmarks, would be useful to surgeons. Key Words: Eustachian tube, foramen ovale, foramen spinosum, internal carotid artery. Laryngoscope, 122: , 2012 INTRODUCTION Endoscopic endonasal surgery (EES) of the cranial base is made possible by technological advances in surgical endoscopy, instrumentation, and intraoperative navigational systems in combination with a new understanding of skull base anatomy from an endoscopic perspective. For coronal plane procedures that provide access to the middle cranial fossa and petrous apex, 1 5 Identification of the petrous segment of the internal carotid artery (ICA) is an important step. Surgical approaches are classified according to their relationship to the petrous segment of the ICA: suprapetrous and infrapetrous. The pterygoid canal with the vidian nerve and artery runs from the pterygopalatine fossa to the foramen lacerum and traverses the floor of the sphenoid sinus. This relationship between the vidian nerve and the petrous ICA is exploited during surgery to identify the genu of the ICA at the junction of the petrous and From the Department of Otolaryngology (K.O.), Selcuklu Faculty of Medicine, Selcuk University, Konya, Turkey; Department of Otolaryngology (C.H.S.) and Department of Neurological Surgery (C.H.S., P.A.G., J.C.F.-M.), University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, U.S.A. Editor s Note: This Manuscript was accepted for publication July 25, Dr. Kayhan Ozturk was supported by the Scientific and Technological Research Council of Turkey (TUBITAK). The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Kayhan Ozturk, Department of Otolaryngology, Selcuklu Faculty of Medicine, Selcuk University, Campus of Alaeddin Keykubat, 42075, Selcuklu, Konya, Turkey. kayhanozturk@selcuk.edu.tr DOI: /lary paraclival segments of the ICA. 1,6 8 The vidian artery is not consistently present but is also a useful landmark. EES of the nasopharynx and infrapetrous approaches to the skull base often result in transgression or resection of the medial aspect of the eustachian tube (ET). 9,10 In the current literature, there is limited knowledge that evaluates the relationship between the ET and petrous segment of the ICA. The aim of the present study was to investigate the relationship between the ET and petrous ICA in whole-mount human temporal bone specimens. MATERIALS AND METHODS Histologically prepared serial sections of 10 temporal bones were selected from the Sando temporal bone collection in the Department of Otolaryngology at the University of Pittsburgh School of Medicine. 11 The specimens were obtained from normal individuals without a history of congenital disease. Ages ranged from 18 to 88 years old (mean age, years). All specimens were obtained, prepared, and stained according to the technique described by Sando et al. 9 Serial 20 to 30 lmthick sections were cut from the nasopharyngeal orifice to the middle ear perpendicular to the long axis of the ET. In these sections, five specific landmarks were selected to evaluate relationships between the petrous segment of the ICA and the ET: 1) foramen ovale level, 2) foramen spinosum level, 3) cartilaginous and bony ET junctional point level, 4) bone part level of the ET, and 5) parapharyngeal part level of the ICA. When both the foramen ovale and V3 of the trigeminal nerve (mandibular nerve) were identified clearly on the histological section, this histopathological section was accepted as a foramen ovale level (Fig. 1). When both foramen spinosum and arteria meningia media were identified clearly, this section was accepted as foramen spinosum level (Fig. 2). When both cartilaginous and bony parts of the ET were identified on the section, it was accepted as the junctional point level (Fig. 3). The first identified bony

Fig. 1. Foramen ovale level. Histologic slide was obtained from a 52- year-old female eustachian tube specimen.

ICA ¼ internal carotid artery; LPM ¼ lateral pterygoid muscle; BT ¼ bone thickness of the petrous bone (temporal bone); UC ¼ the distance between the upper part of the eustachian tube lumen and the

eustachian tube lumen and the carotid canal; L ¼ lumen of the eustachian tube; RF ¼ Rosenmuller s fossa; OF ¼ Ostmann s fat tissue; ML ¼ medial lamina of the cartilage part of the eustachian tube;

com.] Fig. 3. Junction point level. Histologic slide was obtained from a 52- year-old female eustachian tube specimen.

2 Fig. 1. Foramen ovale level. Histologic slide was obtained from a 52- year-old female eustachian tube specimen. SB ¼ sphenoid bone; MF ¼ middle cranial fossa; GG ¼ Gasserian ganglion; TB ¼ temporal bone; FO ¼ foramen ovale; FOC ¼ the distance between the foramen ovale and the carotid canal; CC ¼ carotid canal; ICA ¼ internal carotid artery; LPM ¼ lateral pterygoid muscle; BT ¼ bone thickness of the petrous bone (temporal bone); UC ¼ the distance between the upper part of the eustachian tube lumen and the carotid canal; LS ¼ lateral side; MPM ¼ medial pterygoid muscle; LL ¼ lateral lamina of the cartilage part of the eustachian tube; MS ¼ medial side; BC ¼ the distance between the bottom level of the eustachian tube lumen and the carotid canal; L ¼ lumen of the eustachian tube; RF ¼ Rosenmuller s fossa; OF ¼ Ostmann s fat tissue; ML ¼ medial lamina of the cartilage part of the eustachian tube; TVPM ¼ tensor veli palatine muscle; LVPM ¼ levator veli palatine muscle; V3 ¼ mandibular nerve. Bar ¼ 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] Fig. 3. Junction point level. Histologic slide was obtained from a 52- year-old female eustachian tube specimen. MF ¼ middle cranial fossa; TTM ¼ tensor tympani muscle; SB ¼ sphenoid bone; C ¼ cartilage part of the eustachian tube; TMJ ¼ temporomandibular joint; UC ¼ the distance between the upper part of the eustachian tube lumen and the carotid canal; TB ¼ temporal bone; L ¼ lumen of the eustachian tube; ICA ¼ internal carotid artery; B ¼ bony part of the eustachian tube; BT ¼ bone thickness of the petrous bone (temporal bone); BC ¼ thedistancebetweenthebottomleveloftheeustachiantubelumen and the carotid canal; CC ¼ carotid canal; LS ¼ lateral side; MS ¼ medial side; PPF ¼ pterygopalatine fossa; LVPM ¼ levator veli palatine muscle. Bar ¼ 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] part section of the ET when following from nasopharyngeal orifice to the middle ear was accepted as the bone part level (Fig. 4), and finally, when the first whole parapharyngeal part of the ICA on the histopathological section was identified, it is accepted as the parapharyngeal part level (Fig. 5). Fig. 2. Foramen spinosum level. Histologic slide was obtained from a 52-year-old female eustachian tube specimen. MF ¼ middle cranial fossa; SB ¼ sphenoid bone; FS ¼ foramen spinosum; FSC ¼ distance between the foramen spinosum and the carotid canal; TB ¼ temporal bone; MMA ¼ middle meningeal artery; LL ¼ lateral lamina of the cartilage part of the eustachian tube; UC ¼ the distance between the upper part of the eustachian tube lumen and the carotid canal; ICA ¼ internal carotid artery; BT ¼ bone thickness of the petrous bone (temporal bone); CC ¼ carotid canal; LS ¼ lateral side; MPM ¼ medial pterygoid muscle; TVPM ¼ tensor veli palatine muscle; L ¼ lumen of the eustachian tube; ML ¼ medial lamina of the cartilage part of the eustachian tube; BC ¼ the distance between the bottom level of the eustachian tube lumen and the carotid canal; OF ¼ Ostmann s fat tissue; MS ¼ medial side; RF ¼ Rosenmuller s fossa; PPF ¼ pterygopalatine fossa; LVPM ¼ levator veli palatine muscle. Bar ¼ 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] Fig. 4. Bone part level of eustachian tube. Histologic slide was obtained from a 52-year-old female eustachian tube specimen. MF ¼ middle cranial fossa; TTM ¼ tensor tympani muscle; TMJ ¼ temporomandibular joint; SB ¼ sphenoid bone; UC ¼ the distance between the upper part of the eustachian tube lumen and the carotid canal; B ¼ bony part of the eustachian tube; L ¼ lumen of the eustachian tube; MS ¼ medial side; BC ¼ the distance between the bottom level of the eustachian tube lumen and the carotid canal; ICA ¼ internal carotid artery; TB ¼ temporal bone; CC ¼ carotid canal; LS ¼ lateral side; PPF ¼ pterygopalatine fossa; LVPM ¼ levator veli palatine muscle. Bar ¼ 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] 2659

3 Fig. 5. Parapharyngeal part level of the carotid artery. Histologic slide was obtained from a 52-year-old female eustachian tube specimen. MF ¼ middle cranial fossa; TMJ ¼ temporomandibular joint; SB ¼ sphenoid bone; TTM ¼ tensor tympani muscle; UC ¼ the distance between the upper part of the eustachian tube lumen and the carotid canal; B ¼ bony part of the eustachian tube; L ¼ lumen of the eustachian tube; TB ¼ temporal bone; BC ¼ the distance between the bottom level of the eustachian tube lumen and the carotid canal; CC ¼ carotid canal; MS ¼ medial side; LS ¼ lateral side; ICA ¼ internal carotid artery; PPF ¼ pterygopalatine fossa. Bar ¼ 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] All selected specimens were scanned at high resolution (1,200 dpi) with a flatbed scanner with transparency adapter. Calibration references were included in the initial scans. On each of five selected sections for each case, the vertical lumen length of the ET (VL), the distance between the upper part of the ET lumen and the carotid canal (UC), the bottom level of the ET lumen and the carotid canal (BC), the distance between the foramen ovale and the carotid canal (FOC), the distance between the foramen spinosum and the carotid canal (FSC), and the bone thickness between the ET and the carotid canal (BT) were measured using Metamorph software (Molecular Devices, LLC, Sunnyvale, CA). Mean values were given as mean 6 standard deviation. RESULTS The results of the UC, BC, FOC or FSC, BT, and VL measurements for specimens are given in Table I and Figure 6. For the foramen ovale level, the UC, BC, and FOC were mm (range, mm), mm (range, mm), and mm (range, mm), respectively. For foramen spinosum level, the mean UC, BC, and FSC were measured as mm (range, mm), mm (range, mm), and mm (range, mm). For junctional point level, the mean UC and BC were mm (range, mm), and mm (range, mm). The mean BT of specimens between the ET and the ICA at the foramen ovale level and foramen spinosum level were mm (range, mm) and mm (range, mm), respectively. DISCUSSION The anatomy of the skull base in the coronal plane of the ICA is very complex, with close proximity of TABLE I. The Mean Measurements and Standard Deviations at the Five Specific Sites in Temporal Bone Specimens. FOL FSL JPL BPL PPL UC BC FOC UC BC FSC UC BC UC BC UC BC Distance Range VL BT VL BT VL VL VL Distance Range Data are expressed in millimeters. FOL ¼ foramen ovale level; FSL ¼ foramen spinosum level; JPL ¼ junction point level; BPL ¼ bone part level of the ET; PPL ¼ parapharyngeal part level; UC ¼ distance between the upper part of the eustachian tube lumen and the carotid canal; BC ¼ distance between the bottom level of the eustachian tube lumen and the carotid canal; FOC ¼ distance between foramen ovale and the carotid canal; FSC ¼ distance between foramen spinosum and the carotid canal; VL ¼ vertical lumen length of the eustachian tube; BT ¼ bone thickness between the eustachian tube and the carotid canal. 2660

TABLE II. Distances Between the ICA and Foramen Ovale and Foramen Spinosum. Authors ICA and Foramen Ovale, mm ICA and Foramen Spinosum, mm Villavicencio et al. 13 3.8 5.2 Leonetti et al. 16 4.6 5.

The mean measurements in millimeters of the distance between the upper part of the eustachian tube lumen and the carotid canal (UC), the bottom level of the eustachian tube lumen and the carotid

4 TABLE II. Distances Between the ICA and Foramen Ovale and Foramen Spinosum. Authors ICA and Foramen Ovale, mm ICA and Foramen Spinosum, mm Villavicencio et al Leonetti et al Aslan et al Present study ICA ¼ internal carotid artery. Fig. 6. The mean measurements in millimeters of the distance between the upper part of the eustachian tube lumen and the carotid canal (UC), the bottom level of the eustachian tube lumen and the carotid canal (BC), the distance between the foramen ovale and the carotid canal (FOC), the distance between the foramen spinosum and the carotid canal (FSC), and the bone thickness between the eustachian tube and the carotid canal (BT) at the foramen ovale level (FOL), foramen spinosum level (FSL), junctional point level (JPL), bone part level (BPL), and parapharyngeal part level (PPL). VL ¼ vertical lumen length of the eustachian tube. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] important structures such as the ICA, sixth cranial nerve, trigeminal nerve, vidian nerve, middle meningeal artery, and greater petrosal nerve. 10,12 Numerous anatomical studies employing cadaveric dissections and radiological examinations of the petrous bone have described the relationship between these critical structures. Endoscopic endonasal approaches to the petrous apex and middle cranial fossa require recognition of these anatomical relationships, especially the relationships of the ICA. 1 The most important landmarks for localization of the petrous ICA are the vidian nerve, V2, V3, foramen spinosum, and the ET. 1 3,12 15 The Sando temporal bone collection is a unique resource that offers an opportunity to explore these anatomical relationships further. In the present study, normal whole-mount temporal bone specimens were used to evaluate anatomical relationships between the ICA and the ET, foramen ovale, and foramen spinosum. Therefore, all structures with surrounding soft tissues and bone can be examined in the same histological specimen without removal of tissue. In cadaveric specimens, exploration of these relationships requires extensive dissection of soft tissue and bone with the loss of anatomical information. Also, it can be difficult to obtain exact measurements of distances. In the present study, the objective analysis software was used to measure distances and minimize measurement errors. On the other hand, the process of preparing the temporal bone specimens for histopathology may introduce measurement artifact. 9 In the present study, we found that the average distances between the carotid canal and foramen ovale and foramen spinosum in the adult specimens were mm and mm, respectively. Our results are in good agreement with the results of radiological and cadaveric studies (Table II). On adult three-dimensional computed tomography images, Villavicencio et al. 13 reported that the average distance from the carotid artery to the foramen ovale was 3.8 mm, and the average distance from the carotid artery to the foramen spinosum was 5.2 mm. Leonetti et al. 16 showed that the average distance between foramen ovale and Fig. 7. Coronal magnetic resonance imaging sections of a 30-year-old female. One black arrow (A) shows the eustachian tube and the double black arrows (B) show foramen ovale and trigeminal nerve. 2661

5 the carotid artery was 4.6 mm, and the average distance between foramen spinosum and lateral wall of the carotid artery was 5.3 mm. Similarly, Aslan et al. 14 reported that the average distances between foramen ovale and internal carotid artery, and foramen spinosum and internal carotid artery were mm and , respectively, in the cadaveric dissection. We selected foramen ovale level, foramen spinosum level, junctional point level, bone part level, and parapharyngeal part level sections to analyze the relationship of the ET and the carotid artery for each subject because these structures can be identified during preoperative radiological examination or surgery (Figs. 1 5 and Fig. 7). The BT of specimens between the ET and the carotid artery was mm at the foramen ovale level. It is necessary to drill almost 2.2 mm of bone thickness to reach the carotid artery at the foramen ovale level. When following the ET from the nasopharyngeal orifice to its bony part, the ET and the carotid artery get closer posteriorly and the bony part of the ET and the carotid artery generally share the same wall (Figs. 1 5). The distance between the junctional part of the ET and the carotid artery was approximately 2 mm from the upper lumen and 3 mm from the bottom lumen. To prevent injury to the carotid artery during ET dissection, the surgeon should try to identify the junction of the cartilaginous and bony ET as a landmark (Fig. 3) by following the ET lumen from the nasopharyngeal orifice to the junctional part. Beyond this point, the surgeon should be careful, because the ICA and the ET get very close and generally share the same thin bony wall. CONCLUSION In the adult population, the junctional part of the ET may be selected as a safe landmark to identify and protect the petrous segment of the ICA, because there is adequate bone between the ET and the petrous carotid artery for each specimen. Anatomical knowledge of the relationships of the ET and ICA, as well as their relationships with other surgical and radiological landmarks, will be useful to surgeons performing EES in the coronal plane. Acknowledgments The authors thank Kira L. Lathrop for her assistance with image preparation and analysis, Dr. Nirmala Sundar Raj for providing the scanner and computer for imageacquisition,anddr.isamusandoforaccesstothe Sando temporal bone collection in the Department of Otolaryngology at the University of Pittsburgh School of Medicine. BIBLIOGRAPHY 1. Zanation AM, Snyderman CH, Carrau RL, Gardner PA, Prevedello DM, Kassam AB. Endoscopic endonasal surgery for petrous apex lesions. Laryngoscope 2009;119: Magro F, Solari D, Cavallo LM, et al. The endoscopic endonasal approach to the lateral recess of the sphenoid sinus via the pterygopalatine fossa: comparison of endoscopic and radiological landmarks. Neurosurgery 2006;59(4 suppl 2):ONS237 ONS Kassam AB, Gardner P, Snyderman C, Mintz A, Carrau R. Expanded endonasal approach: fully endoscopic, completely transnasal approach to the middle third of the clivus, petrous bone, middle cranial fossa, and infratemporal fossa. Neurosurg Focus 2005;19:E6, Georgalas C, Kania R, Guichard JP, Sauvaget E, Tran Ba Huy P, Herman P. Endoscopic transsphenoidal surgery for cholesterol granulomas involving the petrous apex. Clin Otolaryngol 2008;33: Zimmer LA, Hart C, Theodosopoulos PV. Endoscopic anatomy of the petrous segment of the internal carotid artery. Am J Rhinol Allergy 2009; 23: Osawa S, Rhoton AL Jr, Seker A, Shimizu S, Fujii K, Kassam AB. Microsurgical and endoscopic anatomy of the vidian canal. Neurosurgery 2009;64(5 suppl 2): Vescan AD, Snyderman CH, Carrau RL, et al. Vidian canal: analysis and relationship to the internal carotid artery. Laryngoscope 2007;117: Fortes FS, Sennes LU, Carrau RL, et al. Endoscopic anatomy of the pterygopalatine fossa and the transpterygoid approach: development of a surgical instruction model. Laryngoscope 2008;118: Sando I, Doyle WJ, Okuno H, Takahara T, Kitajiri M, Coury WJ III. A method for the histopathological analysis of the temporal bone and the Eustachian tube and its accessory structures. Ann Otol Rhinol Laryngol 1986;95 (3 pt 1): Liu XD, Xu QW, Che XM, Mao RL. Anatomy of the petrosphenoidal and petrolingual ligaments at the petrous apex. Clin Anat 2009;22: Sando I, Takasaki K, Hirsch BE. Clinical Atlas of the Company, Ltd; Temporal Bone and Eustachian Tube. Tokyo, Japan: Kanehara & Company, Ltd; Osawa S, Rhoton AL Jr, Tanriover N, Shimizu S, Fujii K. Microsurgical anatomy and surgical exposure of the petrous segment of the internal carotid artery. Neurosurgery 2008;63(4 suppl 2): Villavicencio AT, Leveque JC, Bulsara KR, Friedman AH, Gray L. Threedimensional computed tomographic cranial base measurements for improvement of surgical approaches to the petrous carotid artery and apex regions. Neurosurgery 2001;49: Aslan A, Balyan FR, Taibah A, Sanna M. Anatomic relationships between surgical landmarks in type b and type c infratemporal fossa approaches. Eur Arch Otorhinolaryngol 1998;255: Krayenbuhl N, Isolan GR, Al-Mefty O. The foramen spinosum: a landmark in middle fossa surgery. Neurosurg Rev 2008;31: Leonetti JP, Smith PG, Linthicum FH. The petrous carotid artery: anatomic relationships in skull base surgery. Otolaryngol Head Neck Surg 1990;102:

Analysis of the Petrous Portion of the Internal Carotid Artery: Landmarks for an Endoscopic Endonasal Approach

The Laryngoscope VC 2014 The American Laryngological, Rhinological and Otological Society, Inc. Analysis of the Petrous Portion of the Internal Carotid Artery: Landmarks for an Endoscopic Endonasal Approach