Basic ScienceIn vitro biomechanics of the craniocervical junction—a sequential sectioning of its stabilizing structures
Introduction
The occipitocervical region comprised the occiput (C0), the atlas (C1), and the axis (C2). It is a unique part of the spine, where the anatomy permits more flexion-extension (FE) and axial rotation (AR) than anywhere else in the cervical region [1], [2], [3], [4], [5], [6]. The large motions occur because of the geometry of the articulating joints working in concert with the attached ligaments, which span two levels to create a stabilizing linkage for the entire joint complex. It is also well noted that this region exhibits coupled motion, meaning there are secondary rotations accompanying primary motion, such as incidental lateral bending that occurs during applied AR [7], [8]. With the absence of capsular intervertebral discs, maintaining stability requires these ligaments to be present at the craniocervical junction, unlike other regions of the spine [3], [6].
There are four layers of ligamentous stabilizers of the craniocervical junction. The most anterior structure is the anterior atlantooccipital membrane that extends from the clivus to the anterior arch of the atlas. It is located immediately posterior to the rectus capitis muscles and anterior to the alar ligaments [9]. The second layer of anterior cervical restraining ligaments, the apical and alar ligaments, is located in the plane of the odontoid and also attached to the odontoid. The alar ligaments are strong, rounded cords extending obliquely from the cranial, lateral aspect of the odontoid to the medial aspect of the occipital condyles (Fig. 1B). The apical odontoid ligament extends from the tip of the odontoid ligament to the clivus. The third layer of anterior cervical ligaments, posterior to the odontoid, contains the cruciate ligament. The cruciate ligament consists of three structures: the transverse ligament (Fig. 1C), superior crus, and inferior crus. The transverse ligament of the atlas is a thick band that crosses the ring of the atlas, encircling the odontoid. It is firmly attached to the medial surface of the lateral mass of the atlas. It is an anterior-posterior (AP) restraint of translation of the atlas on the axis. As it crosses the odontoid process, a small fasciculus (crus superius) extends rostrally to insert on the clivus and another (crus inferius) caudally to insert on the C2 body. The superior and inferior crurae originate from the superficial or posterior fibers of the ligament. The entire third layer is, therefore, termed the cruciate ligament of the axis [9]. Although it is the strongest, thickest, and the most important of the internal craniocervical ligaments, it is surprisingly susceptible to disruption from external forces [2], [3], [6], [10], [11]. The fourth, and deepest, layer is the tectorial membrane. It is a prolongation of the posterior longitudinal ligament extending from the posterior surface of the body of the axis to the clivus. It covers the odontoid but does not insert on the odontoid. It is the most posterior ligamentous structure located immediately anterior to the dura. There is also a posterior atlantooccipital membrane from the occipital bone to the posterior arch of C1 immediately posterior to the dura.
Traumatic dislocations of the occipitocervical region, such as those caused by motor vehicle accidents, involve separation and translation of the craniocervical joints because of destruction of stabilizing ligaments [12], [13], [14], [15], [16], [17], [18]. Occipitocervical dislocations can be either unilateral or bilateral and may involve the occipitoatlantal joints, the atlantoaxial (C1–C2) joints, or combined occipitoatlantoaxial dislocations [15], [19], [20], [21], [22]. Based largely on the historical biomechanical studies, the cruciate ligaments are considered the primary stabilizer of the occipitoatlantal and atlantoaxial junctions, and the alar ligaments as the secondary stabilizers of the occipitoatlantal junction [23]. Isolated occipitoatlantal, atlantoaxial, and occipitoatlantoaxial axial dislocations have been observed and reported by several authors [14], [15], [24], [25], [26], [27], [28], [29].
However, there are reported clinical cases of occipitocervical dislocations with intact ligaments [29], challenging the traditional belief that the alar and cruciate ligaments are the main craniocervical stabilizers [29], [30], [31]. There are also cases of ligamentous injury without traumatic occipitoatlantal or atlantoaxial dislocation. The joint capsules have been observed to be secondary stabilizers of the occipitoatlantal articulation that may distinguish occipitoatlantal versus combined occipitoatlantal and C1–C2 dislocations, but this observation has not been biomechanically proven [29].
Understanding the biomechanical properties of the ligaments may be useful for injury diagnosis and reconstruction. It is well understood that certain ligament and joint complexes likely contribute to specific motion profiles. To the authors’ knowledge, the native craniocervical junction stability has not been studied using modern biomechanical techniques. The purpose of this study was to define the relative contributions of various ligamentous structures (vertical stabilizers inserting onto the clivus with the alar ligaments, transverse ligaments, and joint capsules) to the overall craniocervical stability and to build a model of craniocervical dissociative injuries to facilitate further study. The authors hypothesize that destruction of joint capsules, along with the removal of the vertical structures with the alar ligaments and transverse ligaments, would create pathologic translation and joint subluxation. Furthermore, the authors hypothesize that the joint capsules are main stabilizers and assist in stability similar to the cruciate ligament complex at the atlantoaxial joint. To the authors’ knowledge, there lacks quantification of the craniocervical joint capsules role, in terms of stability, in such traumatic cases. A reproducible model of craniocervical instability would facilitate future studies on operative and nonoperative craniocervical stabilizations. Furthermore, understanding the natural motion and translations observed during rotation of this region in all planes simultaneously could assist in identifying proper fixation methods.
Section snippets
Materials and methods
Five of the authors are paid employees of Globus Medical, Inc., where all testings were performed. The three other authors have various royalties, consultant contracts, and affiliations with various companies and organizations.
Results
All information can be found in Table 1, Table 2, Table 3 and Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8 with intact primary and secondary ROM summarized in Table 1, Table 2, Table 3 (FE, LB, and AR, respectively).
Discussion
Despite the prevalence of craniocervical trauma, basic craniocervical biomechanics and the function of ligamentous stabilizers are not well known. Contrary to the historical studies, we have found that the occipitoatlantal joint capsules are the main restraints to occipitoatlantal motion. The vertical band of the cruciate ligament is the primary restraint to C1–C2 lateral bending, and the transverse ligament restrains almost all other C1–C2 motions, with the exception of AR. Additionally, we
Conclusions
The transverse ligament is the main restraint to instability across the C0–C2 region. Contrary to the previous biomechanical studies, the occipitoatlantal joint capsules are the main restraints to occipitoatlantal motion and the vertical ligaments connecting to the clivus and the C0–C1 capsules are secondary stabilizers. Also in contrast to the previous studies, the alar ligaments appear to function as secondary stabilizers to lateral bending and not to AR. Additionally, the normal
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2021, World NeurosurgeryCitation Excerpt :Importantly, the stability of the craniocervical junction is complex and relies on bony, ligamentous, and capsular structures. Biomechanical studies have classified the transverse and alar ligaments as primary stabilizers and the atlanto-occipital membrane and condylar joint capsules as secondary stabilizers.3 Thus, where possible, preservation of key structures plays a role in limiting postoperative instability.
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2020, Journal of Clinical NeuroscienceBiomechanical contribution of the alar ligaments to upper cervical stability
2020, Journal of BiomechanicsCitation Excerpt :The etiology of chronic whiplash associated disorder remains unknown, but the upper cervical spinal ligaments, specifically the alar ligaments, have been implicated as a possible source of long-term morbidity associated with whiplash injuries (Dvorak et al., 1988; Fice and Cronin, 2012; Kaale et al., 2005; Krakenes et al., 2002; Shateri and Cronin, 2015). The alar ligaments may be damaged in whiplash injuries (Lindgren et al., 2009) and more severe damage to these ligaments may also occur as a result of an occipito-cervical dislocation (Radcliff et al., 2015). Magnetic resonance imaging (MRI) of the upper cervical spine offers objective measurement of compositional changes within the substance of the alar ligaments, but MRI diagnosis of alar injury remains highly variable (Krakenes and Kaale, 2006; Li et al., 2013; Lindgren et al., 2009; Myran et al., 2011; Wilmink and Patijn, 2001).
Anatomy of Alar Ligament Part III: Biomechanical Study
2017, World NeurosurgeryCitation Excerpt :Thorough knowledge of the biomechanical properties is of clinical importance considering it will determine their susceptibility to rupture and lesions. There are reports of occipitocervical dislocations with no evidence of ligamentous rupture, thus confronting the function of the alar and cruciate ligaments as main stabilizers.6,18-21 Though we found the alar ligaments to have a high tensile strength, forces applied to obtain the measurements were only of a distracting nature.
FDA device/drug status: Not applicable.
Author disclosures: KER: Royalties: Globus Medical (A); Consulting: Globus Medical (C); Speaking and/or Teaching Arrangements: Medtronic (C); Grants: Depuy (C, Paid directly to institution), Medtronic (B, Paid directly to institution), Paradigm spine (B, Paid directly to institution). ADN: Nothing to disclose. PWM: Stock Ownership: Globus Medical (E). MMH: Other: Globus Medical (Paid Employee, E per yr). MM: Other: Globus Medical, Inc. (Salaried Employee). NK: Other: Globus Medical, Inc. (Salaried Employee, E per year); Stock Ownership: Globus Medical, Inc. (750 stock options currently endowed but not held); Research Support (Investigator Salary, Staff/Materials): Globus Medical, Inc. (Salaried Employee, E per year; travel to conferences for other Global Medical–sponsored studies also covered). ARV: Royalties: DePuy (B–C), Medtronics (F), Stryker Spine (F), Biomet Spine (F), Globus (F), Aesculap (0–B), Nuvasive (F); Stock Ownership: Replication Medica (B), Globus (F), K-2 Medical (F), Paradigm Spine (F), Stout Medical (F), Spine Medica (C-D), Computational Biodynamics (B), Progressive Spinal Technologies (F), Spinology (B–C), Small Bone Innovations (D–E), Cross Current (D–E), Syndicom (B), In Vivo (B), Flagship Surgical (C–D), Advanced Spinal Intellectual Properties (co-owner), Cytonics (B), Bonovo Orthopedics (D–E), Electrocore (C–D), Gamma Spine (B), Location-Based Intelligence (C–D), FlowPharma (B), R.S.I. (0–B), Rothman Institute and Related Properties (F), Innovative Surgical Design, Spinicity (C–D); Consulting: Stout Medical (F), Gerson Lehrman Group (B), Guidepoint Global (B), Medacorp (B), Innovative Surgical Design, Orthobullets; Board of Directors: AO Spine, Innovative Surgical Design, Association of Collaborative Spine Research, Spinicity; Grants: Styrker Spine, NuVasive, Cerapedics (F). TJA: Royalties: DePuy (F), Biomet (F); Stock Ownership: Paradigm Spine (C-D), ASIP (B), Biomerix (C–D), Breakaway Imaging (C–D), Crosstree Capital Partners (C–D), In Vivo Therapeutics (B), Invuity (C–D), Pioneer Surgical (C–D), Vertech (B), Gentis (C–D); Consulting: Facetlink (B–C), DePuy (B–C), United Healthcare (B), Biomet Spine (B–C); Speaking and/or Teaching Arrangements: DePuy Spine (B–C); Board of Directors: United Healthcare, Rothman Institute and Related Properties (F); Scientific Advisory Board/Other Office: Gentis (B), United Healthcare (B). SK: Other: Globus Medical Inc. (Salaried Employee). BB: Other: Globus Medical (Salary).
The disclosure key can be found on the Table of Contents and at www.TheSpineJournalOnline.com.
Although no specific funding was provided, some authors are salaried employees of a medical device company in which there is a research budget, whereas other authors have royalty/consultant affiliations.