The Jugular Foramen is Rather a Canal With Distinctive Morphological Configuration Concerning Its Clinical Anatomy and Surgical Implications: Morphological Analysis
Status Publisher Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
GAUK No. 266222
Grantova Agentura, Univerzita Karlova
PubMed
40498516
DOI
10.1227/ons.0000000000001654
PII: 01787389-990000000-01622
Knihovny.cz E-zdroje
- Klíčová slova
- Jugular canal, Jugular foramen, Jugular foramen syndrome, Skull base,
- Publikační typ
- časopisecké články MeSH
BACKGROUND AND OBJECTIVES: The jugular foramen (JF) is rather a complex anatomical structure with internal configuration. Its osteomorphology was assessed to redefine this rather long bony passage as a jugular canal (JC) based on its morphometric data. METHODS: The JF was endocranially and exocranially observed and measured by a digital Vernier caliper bilaterally in 402 dry skulls with opened cranial cavity. The following parameters were measured and analyzed statistically: (1) external and internal widths in the mediolateral dimension, (2) external and internal lengths in the anteroposterior dimension, and (3) depth between the external and internal planes of the foramen. The JF/canal was classified based on its appearance and its morphometric features. RESULTS: The mean length of the JC was approximately 12 mm (12.25 mm-right, 11.76 mm-left) and was longer on the right side (P = .05, 95% CI). Its external opening was found to be slightly larger than the internal opening (P = .07-right, P = .06-left). The JC took 3 distinctive course patterns of straight (47.6%), curved (45.5%), and angulated (6.9%). Its openings exhibited 3 types based on their morphometric analysis: 14.4% Type-I (width = length ±1 mm), 9.8% Type-II (width > length), and 75.9% Type-III (width < length). The size of the external opening into the JC was larger than its internal opening (straight: P = .08-right and P = .07-left), (curved: P = .03-right and P = .03-left), (angulated: P = .03-right and P = .04-left). CONCLUSION: The JF should be regarded clinically as a canal. It is composed of internal and external openings where the jugular fossa resides in between. The provided osteomorphological variations of the JC would enhance the diagnostics and surgical planning in JF syndromes radioimaging and surgical interventions.
Department of Anatomy 2nd Faculty of Medicine Charles University Prague Czech Republic
Department of Anatomy Faculty of Medicine Masaryk University Brno Czech Republic
Department of Neurosurgery České Budějovice Hospital České Budějovice Czech Republic
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Ayeni SA, Ohata K, Tanaka K, Hakuba A. The microsurgical anatomy of the jugular foramen. J Neurosurg. 1995;83(5):903-909.
Rhoton AL Jr. Jugular foramen. Neurosurgery. 2000;47(3 Suppl):S267-S285.
Van Loveren HR, Liu SS, Pensak ML, Keller JT. Anatomy of the jugular foramen: the neurosurgical perspective. Oper Tech Otolaryngol Head Neck Surg. 1996;7(2):90-94.
Vlajković S, Vasović L, Daković-Bjelaković M, Stanković S, Popović J, Cukuranović R. Human bony jugular foramen: some additional morphological and morphometric features. Med Sci Monit. 2010;16(5):BR140-BR146.
Skrzat J, Mróz I, Spulber A, Walocha J. Morphology, topography and clinical signi cance of the jugular foramen. Folia Med Cracov. 2016;56(1):71-80.
Sturrock RR. Variations in the structure of the jugular foramen of the human skull. J Anat. 1988;160:227-230.
Liang L, Qu L, Chu X, et al. Meningeal architecture of the jugular foramen: an anatomic study using plastinated histologic sections. World Neurosurg. 2019;127:e809-e817.
Komune N, Matsuo S, Miki K, et al. Microsurgical anatomy of the jugular process as an anatomical landmark to access the jugular foramen: a cadaveric and radiological study. Oper Neurosurg. 2019;16(4):486-495.
Akdag UB, Ogut E, Barut C. Intraforaminal dural septations of the jugular foramen: a cadaveric study. World Neurosurg. 2020;141:e718-e727.
Ma SC, Liu S, Agazzi S, Jia W. The jugular process: a key anatomical landmark for approaches to the jugular foramen. World Neurosurg. 2020;135:e686-e694.
Singh O, Das JM. Anatomy, head and neck: jugular foramen. In: StatPearls. StatPearls Publishing; 2023.
Weber AL, McKenna MJ. Radiologic evaluation of the jugular foramen. Anatomy, vascular variants, anomalies, and tumors. Neuroimaging Clin N Am. 1994;4(3):579-598.
Gupta C, Kurian P, Seva KN, Kalthur SG, D’Souza AS. A morphological and morphometric study of jugular foramen in dry skulls with its clinical implications. J Craniovertebr Junction Spine. 2014;5(3):118-121.
Das SS, Saluja S, Vasudeva N. Complete morphometric analysis of jugular foramen and its clinical implications. J Craniovertebr Junction Spine. 2016;7(4):257-264.
Freitas CAF, Santos LRMD, Santos AN, Amaral Neto ABD, Brandão LG. Anatomical study of jugular foramen in the neck. Braz J Otorhinolaryngol. 2020;86(1):44-48.
Bond JD, Zhang M. Compartmental subdivisions of the jugular foramen: a review of the current models. World Neurosurg. 2020;136:49-57.
Komune N, Suzuki T, Miyamoto Y, et al. Anatomy of small canals around the jugular foramen: special reference to Jacobson's and Arnold's nerves. Clin Anat. 2023;36(4):599-606.
Hovelacque A. Le crâne dans son ensemble Ostéologie,Vol 2. Doin and Cie; 1934:155-156.
Shapiro R. Compartmentation of the jugular foramen. J Neurosurg. 1972;36(3):340-343.
Katsuta T, Rhoton AL Jr, Matsushima T. The jugular foramen: microsurgical anatomy and operative approaches. Neurosurgery. 1997;41(1):149-202.
Bernard F, Zemmoura I, Cottier JP, Fournier HD, Terrier LM, Velut S. The interperiosteodural concept applied to the jugular foramen and its compartmentalization. J Neurosurg. 2018;129(3):770-778.
Hesselink JR, Davis KR, Taveras JM. Selective arteriography of glomus tympanicum and jugulare tumors: techniques, normal and pathologic arterial anatomy. AJNR Am J Neuroradiol. 1981;2(4):289-297.
Caldemeyer KS, Mathews VP, Azzarelli B, Smith RR. The jugular foramen: a review of anatomy, masses, and imaging characteristics. RadioGraphics. 1997;17(5):1123-1139.
Erol FS, Kaplan M, Kavakli A, Ozveren MF. Jugular foramen syndrome caused by choleastatoma. Clin Neurol Neurosurg. 2005;107(4):342-346.
Moritani T, Aihara T, Oguma E, et al. Magnetic resonance venography of achondroplasia: correlation of venous narrowing at the jugular foramen with hydrocephalus. Clin Imaging. 2006;30(3):195-200.
Gleeson M. Jugular foramen tumors. Skull Base. 2009;19(1):1.
Bakar B. Jugular foramen meningiomas: review of the major surgical series. Neurol Med Chir (Tokyo). 2010;50(2):89-97.
Florisson JM, Barmpalios G, Lequin M, et al. Venous hypertension in syndromic and complex craniosynostosis: the abnormal anatomy of the jugular foramen and collaterals. J Craniomaxillofac Surg. 2015;43(3):312-318.
Thomas AJ, Wiggins RH 3rd, Gurgel RK. Nonparaganglioma jugular foramen tumors. Otolaryngol Clin North Am. 2015;48(2):343-359.
Distriquin Y, Vital JM, Ella B. Biomechanical analysis of skull trauma and opportunity in neuroradiology interpretation to explain the post-concussion syndrome: literature review and case studies presentation. Eur Radiol Exp. 2020;4(1):66.
Ishak C, Danda V. Jugular foramen paragangliomas: preoperative transcatheter particle embolization. J Cerebrovasc Endovasc Neurosurg. 2020;22(4):273-281.
Gul B, Samanci C, Uluduz DU, et al. Does measurement of the jugular foramen diameter on MRI help to differentiate transverse sinus thrombosis from unilateral transverse sinus hypoplasia? Radiol Med. 2021;126(3):430-436.
Pang S, Kolarich AR, Brinjikji W, Nakaji P, Hepworth E, Hui F. Interventional and surgical management of internal jugular venous stenosis: a narrative review. J NeuroInterv Surg. 2022;14(5):503-507.
Schweinfurth JM, Johnson JT, Weissman J. Jugular foramen syndrome as a complication of metastatic melanoma. Am J Otolaryngol. 1993;14(3):168-174.
Rich PM, Cox TC, Hayward RD. The jugular foramen in complex and syndromic craniosynostosis and its relationship to raised intracranial pressure. AJNR Am J Neuroradiol. 2003;24(1):45-51.
Ong CK, Fook-Hin Chong V. Imaging of jugular foramen. Neuroimaging Clin N Am. 2009;19(3):469-482.
Brinjikji W, Graffeo CS, Perry A, et al. Moving target: transient rotational stenosis precipitating jugular bow hunter's syndrome. J Neurointerv Surg. 2017;9(7):e28.
Saliou G, Dirks P, Slater LA, Krings T. Is jugular bulb stenosis in vein of Galen aneurysmal malformation associated with bony remodeling of the jugular foramina? J Neurosurg Pediatr. 2016;18(1):92-96.
Monteiro F, Oliveira P, Peneda J, Condé A. Vernet syndrome: intracranial extension of a slow-growing mass. BMJ Case Rep. 2019;12(5):e228039.
Bento RA, Rodrigues D, Levy J, Eça T, Oliveira V, Luís L. Bilateral severely stenotic jugular foramen: diagnosis and management from the otologist/neurotologist point of view. Case Rep Otolaryngol. 2020;2020:1530310.
Bruneau M, George B. The juxtacondylar approach to the jugular foramen. Neurosurgery. 2008;62(3 Suppl 1):75-81.
Sedney CL, Nonaka Y, Bulsara KR, Fukushima T. Microsurgical management of jugular foramen schwannomas. Neurosurgery. 2013;72(1):42-46.
Samii M, Alimohamadi M, Gerganov V. Surgical treatment of jugular foramen schwannoma: surgical treatment based on a new classification. Neurosurgery. 2015;77(3):424-432.
Tang J, Zhang L, Zhang J, et al. Microsurgical management of primary jugular foramen meningiomas: a series of 22 cases and review of the literature. Neurosurg Rev. 2016;39(4):671-683.
Cömert E, Kiliç C, Cömert A. Jugular bulb anatomy for lateral skull base approaches. J Craniofac Surg. 2018;29(7):1969-1972.
Basma J, Michael LM 2nd, Sorenson JM, Robertson JH. Deconstruction of the surgical approach to the jugular foramen region: anatomical study. J Neurol Surg B Skull Base. 2019;80(5):518-526.
Constanzo F, Gerhardt J, Ramina R. How I do it: retrosigmoid suprajugular approach to the jugular foramen. Acta Neurochir (Wien). 2019;161(11):2271-2274.
Luzzi S, Giotta Lucifero A, Del Maestro M, et al. Anterolateral approach for retrostyloid superior parapharyngeal space schwannomas involving the jugular foramen area: a 20-year experience. World Neurosurg. 2019;132:e40-e52.
Matsushima K, Kohno M. Transjugular transsigmoid approach for triple dumbbell-shaped jugular foramen schwannomas. Acta Neurochir (Wien). 2019;161(4):739-743.
Constanzo F, Coelho Neto M, Nogueira GF, Ramina R. Microsurgical anatomy of the jugular foramen applied to surgery of glomus jugulare via craniocervical approach. Front Surg. 2020;7:27.
Liu J, Pinheiro-Neto CD, Yang D, et al. Comparison of endoscopic endonasal approach and lateral microsurgical infratemporal fossa approach to the jugular foramen: an anatomical study. J Neurol Surg B Skull Base. 2022;83(Suppl 2):e474-e483.
Constanzo F, Pinto J, Coelho Neto M, Ramina R. Retrosigmoid infralabyrinthine (suprajugular) approach to the jugular foramen: indications, limitations, and surgical nuances. Oper Neurosurg. 2022;23(2):e102-e107.
Hawsawi AH, Bawazir M, Basindwah SA, Alqurashi A, Ajlan A. Modified retrosigmoid extended approach to jugular tubercle meningioma: a video abstract. Surg Neurol Int. 2022;13:289.
Zhang C, Harris L, Itum H, et al. Potential surgical implications of internal jugular stenosis in a craniocervical junction meningioma. Cureus. 2022;14(6):e26403.
Sen C, Hague K, Kacchara R, Jenkins A, Das S, Catalano P. Jugular foramen: microscopic anatomic features and implications for neural preservation with reference to glomus tumors involving the temporal bone. Neurosurgery. 2001;48(4):838-848.
Lai PF, Wu X, Lan SH, Tang B, Huang HY, Hong T. Anatomical study of a surgical approach through the neck to the jugular foramen under endoscopy. Surg Radiol Anat. 2021;43(2):251-260.
Roche PH, Mercier P, Sameshima T, Fournier HD. Surgical anatomy of the jugular foramen. Adv Tech Stand Neurosurg. 2008;33:233-263.
Dichiro G, Fisher RL, Nelson KB. The jugular foramen. J Neurosurg. 1964;21:447-460.
Vogl TJ, Bisdas S. Differential diagnosis of jugular foramen lesions. Skull Base. 2009;19(1):3-16.
Wang M, Wu X, Lan D, et al. Differentiation between anatomical slenderness and acquired stenosis of the internal jugular veins. CNS Neurosci Ther. 2022;28(11):1849-1860.