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. Author manuscript; available in PMC: 2022 Aug 1.
Published in final edited form as: Clin Biomech (Bristol). 2021 Jul 29;88:105442. doi: 10.1016/j.clinbiomech.2021.105442

Ligament Deformation Patterns of the Craniocervical Junction during Head Axial Rotation Tracked by Biplane Fluoroscopes

Chaochao Zhou 1,2, Runsheng Guo 1,2,5, Cong Wang 3, Tsung-Yuan Tsai 3, Yan Yu 4, Wei Wang 1,2,6, Guoan Li 1,*, Thomas Cha 1,2
PMCID: PMC8490296  NIHMSID: NIHMS1733303  PMID: 34390949

Abstract

Background:

Frequently, treatment decisions for craniocervical injuries and instability are based on imaging findings, but in vivo ligament kinematics were poorly understood. This study was to determine in vivo deformation patterns of primary ligaments in the craniocervical junction (i.e., C0-2), including the cruciform ligament, alar ligaments, and accessory ligaments, during dynamic head axial rotation.

Methods:

The skulls and cervical spines of eight asymptomatic female subjects were dynamically imaged using a biplane fluoroscopic imaging system, when they performed left and right head axial rotations. Using a 3D-to-2D registration technique, the in vivo positions and orientations of cervical segments were determined. An optimization algorithm was implemented to determine ligament wrapping paths, and the resulting ligament deformations were represented by percent elongations. Using paired t-tests, ligament deformations in the end-range position were compared to those in the neutral position.

Findings:

No significant differences were observed in segmental motions during left and right head rotations (p > 0.05). In general, slight deformations occurred in each component of the cruciform ligament. For the alar ligaments, the ipsilateral ligament was lengthened from −0.7 ± 13.8% to 16.6 ± 15.7% (p < 0.001*). For the accessory ligaments, the contralateral ligament was lengthened from −2.9 ± 7.5% to 10.1 ± 6.2% (p < 0.001*).

Interpretation:

This study reveals that there are distinct deformation patterns in craniocervical junction ligaments during dynamic axial head rotation. These ligament deformation data can enhance our understanding of the synergic function of craniocervical junction ligaments, and guide the treatment of craniocervical instability.

Keywords: Craniocervical junction, Head axial rotation, Ligament deformations, Segmental motion, In vivo, Biplane fluoroscopic imaging

1. Introduction

The craniocervical junction (CCJ) is composed of the occiput (C0), atlas (C1), and axis (C2) surrounded by connective tissues and muscles. Different from the lower (subaxial) cervical spine where there are intervertebral discs, the occipito-atlantal (C0-1) and atlanto-axial (C1-2) segments with more complex anatomy articulate through cartilaginous joints and are constrained mainly by ligaments. Correspondingly, the intrinsic stability of the CCJ region heavily relies on ligamentous constraints (Joaquim et al., 2014). Upper cervical injuries through fractures or ligament rupture can lead to craniocervical instability. Typically, C0, C1, and/or C2 fractures with clear ligamentous disruption, which can be inferred by craniocervical misalignment/dislocations, perched/locked facet joints, and an excessively large atlanto-dental interval (ADI) from medical images, require surgical treatments (e.g., fusion of C0-1/C1-2) (Joaquim et al., 2014; Walters et al., 2013). If no definitive ligamentous injuries are diagnosed, upper cervical traumatic injuries can be treated more conservatively (e.g., using external orthoses) (Joaquim et al., 2014; Li-Jun et al., 2014). However, inadequate treatments of these injuries may induce nonunion/malunion, neurological deficits, deformity, and refractory pain due to occult ligamentous instability (Joaquim et al., 2014). Therefore, an in-depth understanding of the ligamentous function involving their deformation patterns would be helpful in the decision-making process of craniocervical surgical treatments.

The role of ligamentous constraints on craniocervical segmental stability has been investigated by in vitro cadaveric tests and computational models. In a previously reported cadaveric test, CCJ specimens were tested by stepwise dissecting the transverse atlantal ligament (TAL) and the superior longitudinal band (SLB) in various loading scenarios (Li-Jun et al., 2014). It was observed that the SLB was capable of maintaining sufficient stability of the CCJ (i.e., ADI < 3 mm) in various loading scenarios, even when the TAL was dissected. Using finite element models, isolated and combined ligamentous injury patterns in the CCJ were simulated by decreasing the stiffness of capsular ligament, and/or dissecting various craniocervical ligaments (Brolin and Halldin, 2004; Phuntsok et al., 2019b, 2019a). It was shown that the TAL and capsular ligaments are the primary stabilizers for the CCJ, and their deteriorations potentially cause hypermobility and excessively increase the ADIs in various loading scenarios. Furthermore, ligament disruption has been considered a major source of whiplash pain. For the upper cervical spine, injury patterns which are sensitive to ligament nonlinear material properties in response to different impact accelerations have been predicted using dynamic simulation (Cronin et al., 2012; Fice and Cronin, 2012). However, it is challenging to accurately determine the actual functional ligament deformations, since ligament responses are sensitive to physiological joint motions caused by neuromuscular activations. Furthermore, due to the complex anatomy of the CCJ, primary ligaments would experience three-dimensional (3D) wrapping around the bony structures, which requires a robust contact analysis ability in finite element computational software.

Recently, we have implemented biplane fluoroscopic imaging combined with a 3D-to-2D registration technique to systematically quantify the in vivo segmental motions of the head-neck complex during dynamic axial rotation of the head (Guo et al., 2021). This study focused on quantifying the in vivo ligament deformations of the CCJ during head axial rotation. It has been showed that both C0-1 and C1-2 produced complex primary and coupled segmental motions in vivo needed for head axial rotations (Anderst et al., 2017; Ishii et al., 2004; Kang et al., 2019; Nagamoto et al., 2011; Zhou et al., 2020). Therefore, CCJ ligament kinematics and patterns in head axial rotations remain obscure, compared to those in other functional head movements. This study attempted to establish the relationship between the axial rotation angles of the CCJ and deformations of primary ligaments, including the alar ligaments, the accessory ligaments, as well as the cruciform ligament consisting of the TAL, SLB, and inferior longitudinal band (ILB). In particular, we compared ligament deformations (represented by percent elongations) in the end-range position to those in the neutral upright standing position during head axial rotation. It was hypothesized that there are characteristic deformation patterns (lengthening/shortening) in these ligaments during head axial rotation.

2. Methods

2.1. Collection of Image Data

The study was approved by the institutional review board at one of our institutions. Eight asymptomatic female subjects (mean age: 33.4±5.7 years; age range: 28 ~ 46 years; mean weight: 52.7±7.3 kg; mean height: 1.56±0.06 m; mean body mass index: 21.9±3.4 kg/m2; smoking status: none) subjects without prior diagnosed spinal disorders were included. Each subject signed an informed consent form before participating the imaging tests. The skull and cervical spine of each subject was scanned using a computed tomography (CT) scanner (SOMATOM Definition AS+, Siemens, Forchheim, Germany) in a supine position. The acquired CT images of each subject had a slice thickness of 0.60 mm and an image resolution of 512 pixels × 512 pixels, resulting in a voxel size of 0.86 mm × 0.86 mm × 0.60 mm.

Following the CT scanning, each subject was asked to perform left and right head rotations from the neutral position in their comfortable manners while they stood upright. Typically, each subject moved the head to either left or right side in 1 ~ 3 seconds, and held the end-range position for 1 ~ 2 second. The head and neck of each subject was dynamically imaged at a frequency of 30 frames per second with a pulse-width of 8 milliseconds using two orthogonally aligned C-arm fluoroscopes (BV Pulsera, Philips, Amsterdam, Netherlands). The total radiation exposure dose of CT and biplane fluoroscopes for each subject was estimated to be less than 4 mSv, approximately 20% of the average dose limit for occupational exposure in a year (Wrixon, 2008).

2.2. Reproduction of Craniocervical Junction Kinematics in Dynamic Head Rotations

3D bone surface models of the skull, atlas, and axis were constructed from the CT volume data Amira 6 (Thermo Fisher Scientific, Waltham, MA). To measure craniocervical segmental motions in different neck positions, local coordinate systems (Fig. 1) were established at the superior and inferior intervertebral joint articulations of the craniocervical vertebral models in Rhinoceros 5.0 (Robert McNeel & Associates, Seattle, WA). The definitions of these local coordinate systems conformed to the description in a previous study (Zhou et al., 2020); the x, y, and z axes pointed in the right, anterior, and superior directions, respectively (Fig. 1). Then, these 3D models were imported into a virtual environment of biplane fluoroscopes constructed in MATLAB R2017b (MathWorks, Inc., Natick, MA) that replicated the settings of the actual biplane fluoroscopes (Yu et al., 2017; Zhou et al., 2020). Using a previously validated 3D-to-2D registration technique (Yu et al., 2017; Zhou et al., 2020) (Fig. 2), each 3D anatomical model was independently translated and rotated in six degrees of freedom (DoFs), until their projections matched the osseous outlines/features captured on a pair of fluoroscopic images (both images had been pre-processed by an image calibration procedure as described in Appendix A). The registered 3D models, therefore, represented the in vivo positions/orientations of skull/vertebrae in 3D space (Fig. 2). For each subject, we registered six frames of biplane fluoroscopic images with approximately equal time intervals during each one-sided (left/right) head axial rotation from the neural position. Using the registration results during dynamic left and right head rotations, the primary and coupled segmental motions of C0-1, C1-2, and the overall CCJ (C0-2), including axial-twisting (AT), flexion-extension (FE), and lateral-bending (LB) rotations, were measured using the recommended Euler angles (Crawford et al., 1996). The rotation angles of the overall CCJ were monitored during the 3D-to-2D registration, and the posture with the maximal rotation angle was defined as the end-range position of the CCJ during the left/right head axial rotation.

Fig. 1:

Fig. 1:

The intervertebral local coordinate systems of the 3D CCJ anatomical model used to measure occipito-atlantal (C0-1) and atlanto-axial (C1-2) segmental motions. For all the local coordinate systems, the x(red), y (green), and z (blue) axes pointed in the right, anterior, and superior directions, respectively.

Fig. 2:

Fig. 2:

Illustration of the 3D-to-2D registration technique. As presented here, 3D anatomical models of the head and cervical vertebrae are registered to a pair of fluoroscopic images captured in the end-range position during left axial rotation of the head. In the registered 3D models, the CCJ involving the skull (C0), atlas (C1), and axis (C2) are highlighted. (F1 = fluoroscope 1; F2 = fluoroscope 2)

According to a previously reported validation study for the 3D-to-2D registration technique, the accuracy in measuring cadaveric ovine vertebrae was 0.4 mm, and the repeatability in reproducing in vivo six DoFs of human lumbar vertebrae was 0.3 mm in translations and 0.7° in orientations (Wang et al., 2008). By comparing the motion measurements using the 3D-to-2D registration against roentgen stereophotogrammetric analysis with implanted beads, the accuracy of this registration technique for the cervical spine represented by the root-mean-square error was less than 0.54 mm in measuring the superoinferior and anteroposterior vertebral translations (Yu et al., 2017). Recently, we further developed the 3D-to-2D registration technique for the craniocervical segments, by introducing newer fluoroscope modalities that can provide enhanced fluoroscopic images. Therefore, they enabled us to match 3D model projections of C0, C1 and C2 to their radiographic outlines/features on fluoroscopic images. As shown in Fig. A2 of Appendix A, we demonstrated the biplane fluoroscopic X-ray images of one subject captured from the neutral to the end-range positions during head rotation, as well as the corresponding registration results (i.e., 3D model projections on these pairs of X-ray images). The measurements of intervertebral motions of the entire head-neck complex during dynamic head axial rotation for the same group of subjects have been reported recently (Guo et al., 2021).

2.3. Analysis of Ligament Deformations of the Craniocervical Junction

We investigated the deformations of seven ligament structures, including the TAL, SLB, and ILB of the cruciform ligament, the left and right alar ligaments, and the left and right accessory ligaments (Fig. 3a). Each ligament was modeled by three evenly spaced ligament fiber bundles. The insertions of these ligaments were marked on the CCJ model of each subject in the supine CT-scanning position, according to the ligament anatomy described in the literature (Cramer, 2013; Dvorak et al., 1988; Krakenes and Kaale, 2006; Offiah and Day, 2017; Tubbs et al., 2011) and an online available head-neck 3D ligamentous model (https://human.biodigital.com/). These ligament insertions were further examined and confirmed by two experienced spine surgeons (authors: R. G. and T. C.). A path optimization algorithm, as used in knee ligament investigations (Rao et al., 2020), was developed to determine 3D wrapping of the CCJ ligaments around CCJ bone structures (Fig. 3). In particular, for the cruciform ligament, the SLB and ILB were connected to the superior and inferior bundles of the TAL, respectively, and these connections were updated as the TAL wrapping changed during head rotation.

Fig. 3:

Fig. 3:

Visualization of ligament wrapping configurations in the neutral (a), middle (b), and end (c) positions during left axial rotation of the CCJ (C0-2), corresponding to the rotation angles of −4.4°, 22.6°, and 43.2°, respectively. (TAL = transverse atlantal ligament; SLB = superior longitudinal band; ILB = inferior longitudinal band; AlrL = alar ligament; AccL = accessory ligament)

For simplicity, the length (l) of each ligament during head rotation were represented by the average length of three ligament fiber bundles belonging to that ligament (Fig. 3). The resulting ligament deformation were represented by the percent elongation (ε) (Englander et al., 2018; Fleming and Beynnon, 2004):

ε=ll0l0×100% (Eq. 1)

where l0 is the unloaded ligament length (Englander et al., 2018), measured in the supine CT-scanning position in this study.

According to our premilinary statistical analysis (using paired, two-tailed t-tests), no significant differences were found in the primary and coupled segmental ranges of motion (RoMs) in the left and right head axial rotations (p > 0.05, Table 1). Correspondingly, the resulting ligament lengths in head rotations to both sides were pooled together to establish the relationships between ligament deformations and the AT angels of the overall CCJ (C0-2). Concretely, we quantified the deformations of cruciform, alar, and accessory ligaments, when the overall CCJ was twisted to different angles (within a range of approximately 40°, Table 1) during one-sided head rotation. To describe the characteristic deformation patterns (lengthening/shortening) of these craniocervical ligaments, a paired, two-tailed t-test was used to compare the ligament percent elongations in the neutral and end-range positions during head rotation. The statistical significance was defined as p < 0.05. Additionally, post hoc power analysis was performed using the software of G*Power 3.1.

Table 1:

FE, LB, and AT RoMs (represented by mean ± one standard deviation, °) of C0-1, C1-2, and the overall CCJ (C0-2) in left and right head axial rotations. According to our definition of the right-hand Cartesian coordinate systems, extension, right LB, and left AT are indicated by positive values. Therefore, the same sign of LB as AT indicates contralateral LB.

FE RoM LB RoM AT RoM

Left Head Rotation Right Head Rotation Left Head Rotation Right Head Rotation Left Head Rotation Right Head Rotation
C0-C1 13.2 ± 3.3 11.1 ± 2.8 3.2 ± 1.5 −3.0 ± 1.0 1.2 ± 1.9 −2.6 ± 1.3
C1-C2 8.2 ± 4.2 9.1 ± 5.3 12.4 ± 7.2 −12.8 ± 5.6 37.6 ± 12.0 −36.2 ± 4.4
C0-C2 22.5 ± 5.7 20.8 ± 5.7 19.1 ± 6.7 −17.4 ± 4.9 39.8 ± 12.3 −39.6 ± 5.7

3. Results

3.1. Measurements of Segmental Kinematics

Due to the mirror symmetry of left and right head rotations, we only described segmental RoMs in the left head rotation. At C0-1 (Fig. 4a and Table 1), there was a large FE rotation (13.2±3.3°), while LB and AT rotations were small (3.2±1.5° and 1.2±1.9°, respectively). At C1-2 (Fig. 4b and Table 1), the primary AT rotation was largest (37.6±12.0°), followed by coupled LB and FE rotations (12.4±7.2° and 8.2±4.2°, respectively). For the overall CCJ (C0-2, Fig. 4c and Table 1), the AT, FE, and LB rotations were 39.8±12.3°, 22.5±5.7°, and 19.1±6.7°, respectively. It is noted that coupled extension and contralateral LB always occurred at C0-1, C1-2, and C0-2 (Fig. 4 and Table 1).

Fig. 4.

Fig. 4.

Primary (AT) and coupled (FE and LB) segmental rotations of C0-1 (a), C1-2 (b), and the overall CCJ, C0-2 (c) during left and right axial rotations of the head. (RFE = FE rotation; RLB = LB rotation; RAT = AT rotation). Shaded bands represent ± one standard deviation. On the horizontal axis, −100% ~ 0% and 0% ~ 100% represent the percentage range of left and right head axial rotations, respectively. On the vertical axis, “0°” indicates the neutral position; extension, right LB, and left AT are indicated by positive values, according to our definition of the right-hand Cartesian coordinate systems. Therefore, the same sign of LB as AT indicates contralateral LB.

3.2. Measurements of Ligament Deformations

Ligament wrapping paths during the left head axial rotation were graphically presented in Fig. 3. Here, we focused on the average deformation of each ligament; the deformations of individual bundles for each ligament can be found in Appendix B. Overall, each component of the cruciform ligament was slightly deformed during head rotation (Fig. 5a and Table 2). The deformations of TAL and ILB started from 0.1±1.1% and −4.4±6.5%, respectively, and remained almost invariant during head rotation (p=0.130 and p=0.557, respectively). The initial compression status of SLB (−3.9±4.3%) were restored to the unloaded length at the end-range position (p=0.005*). For the alar ligaments (Fig. 5b and Table 2), the ipsilateral ligament was tensioned from −0.7±13.8% to 16.6±15.7% (p<0.001*), while the contralateral ligament was compressed by −4.0±12.2% at 0°, −6.8±14.4% at 20°, and −2.0±13.7% at 40°, respectively (p=0.647). For the accessory ligaments (Fig. 5c and Table 2), the contralateral ligament was tensioned from −2.9±7.5% to 10.1±6.2% (p<0.001*), while the ipsilateral ligament was compressed from −6.1±7.9% to −11.2±7.3% (p=0.041*).

Fig. 5.

Fig. 5.

The relations between ligament elongations (%) and the AT angels (°) of the overall CCJ (C0-2). (TAL = transverse atlantal ligament; SLB = superior longitudinal band; ILB = inferior longitudinal band; AlrL = alar ligament; AccL = accessory ligament). Shaded bands represent ± one standard deviation. (a) The TAL, SLB, and ILB of the cruciform ligament. (b) The ipsilateral and contralateral alar ligaments. (c) The ipsilateral and contralateral accessory ligaments.

Table 2:

Comparison of elongations (%) of each ligament in the neutral and maximal positions during head axial rotation. The p values with statistical significance were marked by asterisk signs. Powers of statistical comparisons were also presented.

Neutral position Maximal position p values Powers
Transverse atlantal ligament 0.1 ± 1.1 1.2 ± 2.5 0.130 49.7%
Superior longitudinal band −3.9 ± 4.3 0.0 ± 3.1 0.005* 96.4%
Inferior longitudinal band −4.4 ± 6.5 −5.7 ± 4.9 0.557 14.7%
Ipsilateral alar ligament −0.7 ± 13.8 16.6 ± 15.7 <0.001* 100.0%
Contralateral alar ligament −4.0 ± 12.2 −2.0 ± 13.7 0.647 12.4%
Ipsilateral accessory ligament −6.1 ± 7.9 −11.2 ± 7.3 0.041* 76.2%
Contralateral accessory ligament −2.9 ± 7.5 10.1 ± 6.2 <0.001* 100.0%

4. Discussion

Using biplane fluoroscopic imaging in combination with a 3D-to-2D registration technique, this study determined in vivo CCJ ligament deformation patterns during dynamic head axial rotation. Our primary findings are that the TAL, SLB, and ILB of the cruciform ligament was minimally deformed during head rotation. The ipsilateral alar ligament was elongated, while the contralateral alar ligament was compressed; in contrast, the exact opposite occurred for the ipsilateral and contralateral accessory ligaments. These data supported our hypothesis that there are distinct deformation patterns in these primary CCJ ligaments. The physiological ligament deformations may not be trivially reproduced using in vitro tests or computational models, as they are dependent on the complex primary and coupled motions needed for head axial rotation.

As the atlas and axis are commonly obscured by the mandible in fluoroscopic images, the in vivo segmental motions of the CCJ were less measured (Anderst et al., 2017; Zhong et al., 2021; Zhou et al., 2020). Correspondingly, the physiological deformation patterns of the CCJ ligaments depending on in vivo segmental motions were poorly known, as they have various insertion locations (the SLB, ILB, and alar ligaments connect between C0 and C2; the accessory ligaments connect between C1 and C2; the TAL connects C1 itself). The upgraded fluoroscope modality adopted in this study provided a higher image resolution, and facilitated us to accurately reproduce in vivo segmental motions of the CJJ in dynamic head axial rotation. Moreover, the implementation of the 3D ligament wrapping algorithm enabled us to describe high-fidelity deformations of the CCJ ligaments.

As the TAL is considered to be the one with the maximal volume, thickness and strength among the CCJ ligaments (Debernardi et al., 2011), our data show that the TAL deformed slightly during head rotation, even when the AT rotation between C1 and C2 reached approximately 40° (Fig. 5a). Consequently, the TAL retains the odontoid process within the anterior arch of C1. This is in agreement with previously reported findings in in vitro tests (Li-Jun et al., 2014) and computer simulation (Phuntsok et al., 2019b), which have demonstrated that the TAL is the most crucial stabilizing component to prevent abnormal anterior translation of C1 with respect to C2, as indicated by a small range of ADI (< 3 mm) for an intact atlanto-axial segment specimen (Li-Jun et al., 2014). However, we observed that both the SLB and ILB were slightly compressed during head rotation, although the SLB restored to no deformation in the end-range position (Fig. 5a). The non-functioning of both longitudinal bands potentially result from the coupled extension of CCJ during head rotation.

This study further reveals the coordination of the alar and accessory ligaments in maintaining the stability of the CCJ. In vitro studies have shown that both the alar and accessory ligaments play primary roles in restraining the AT rotation of the CJJ, while the accessory ligaments are less strong as the alar ligaments (Panjabi et al., 1991; Tubbs et al., 2004). The detailed deformation patterns of these ligaments were further investigated by our study. For the alar ligaments, the ipsilateral ligament was elongated (Fig. 5b), suggesting that it more preferentially restrained coupled contralateral LB during head rotation (Fig. 4c). Consistent with previously reported in vivo measurements, coupled contralateral LB occurred in the CCJ to maintain the head to rotate horizontally, since the lower (subaxial) cervical spine commonly produces ipsilateral LB during head rotation (Nagamoto et al., 2011; Zhou et al., 2020). For the accessory ligaments, the contralateral ligament was elongated (Fig. 5c), leading to a more straightforward implication for their function in restraining the AT rotation of C1-2 (the accessory ligaments connect between C1 and C2).

Generally, it has been well established that disruptions of the cruciform and alar ligaments are highly associated with abnormal motions, misalignment, and instability of the CCJ (Debernardi et al., 2011; Dvorak et al., 1988; Hidalgo-García et al., 2020). Although isolated avulsion of the accessory ligaments may cause less discernable laxity of the atlanto-axial segment, the stability of the CCJ would be more markedly influenced by their damages together with bony fractures and other ligamentous disruptions (Debernardi et al., 2011). For example, Jefferson fracture of the atlas may cause rupture of both the TAL and accessory ligaments, since their insertions are close to each other on the atlas (Smith et al., 2018). As a direct visualization of the integrity of these structures is difficult, the approach based on dynamic radiographs in this study is promising to examine ligamentous disruptions, by comparing to the normal ligament deformation patterns (Fig. 5). In particular, this could be applied to the diagnosis of refractory pain whose source is hard to identify. In addition, it is also anticipated that our data can be leveraged to improve the fidelity of CCJ ligamentous computational models, by calibrating the model-predicted ligament deformations to the physiological patterns (Fig. 5).

However, we acknowledge that the deformations of more ligaments and membranes of the CCJ in more scenarios of dynamic functional head movements need to be quantified to establish appropriate assessment criteria. Whether the baseline deformations are sensitive to movement speeds should be also established to help elucidate mechanisms of injury. Furthermore, the potential variations depending on genders and ages on spinal structures and mechanics (Yoganandan et al., 2017) were not considered, due to the small sample size. After excluding two subjects in which one was diagnosed with congenital fusion at C2-3 from CT images and another one’s CT images failed to be retrieved from the CT scanner, only eight subjects were included in this study to investigate the CCJ ligament deformations during head rotation. Since CCJ segmental kinematics of these subjects were mirror-symmetric during left and right head axial rotations, we pooled together the kinematics data in head rotations to either side. Such processing could strengthen the evidence regarding the ligament deformation characteristics, and the preliminary data have demonstrated the feasibility of the new approach for investigating physiological ligament kinematics. Future work should further expand the sample size to validate if the reported ligament deformation characteristics exist in a population. In addition, we adopted the well-established definition of ligament percent elongation to quantify the ligament deformations, as described in the Methods Section 2.3. We acknowledge that the unloaded ligament length is sensitive to the positions of subjects during CT scanning, that may differ among these subjects. However, it should be noted that we performed statistical comparisons of ligament deformations in the end-range position with those in the neutral position using paired t-tests. That is, we examined if a ligament was lengthened / shortened during head axial rotation from the neural to end-range positions; the characteristic ligament deformation pattern should not be sensitive to the selection of the reference unloaded ligament status. Regarding the cruciform ligament, we ignored the interaction between the TAL and the longitudinal bands; that is, the length changes of one component did not influence the width change of another component. Therefore, it is necessary to develop more detailed model of the cruciform ligament considering such interaction.

5. Conclusion

This study determined the physiological relation of the CCJ ligament deformations with the AT rotational angles of the CCJ during dynamic head axial rotations. It is shown that there are distinct deformation patterns in these CCJ ligaments. The cruciform ligament including TAL, SLB, and ILB were slightly deformed during head axial rotation, while the ipsilateral part of the alar ligaments and the contralateral part of the accessory ligaments were tensioned, in response to the coupled (contralateral) LB and primary AT rotations of the CCJ, respectively. This study enhanced the understanding of the synergic functions of the CCJ ligaments, and could help guide the treatment of craniocervical instability.

Supplementary Material

1

Highlights.

  • Motions of the craniocervical junction during head rotation were measured.

  • Deformation patterns of the primary craniocervical ligaments were determined.

  • The cruciform ligament was marginally deformed.

  • The ipsilateral alar ligament and the contralateral accessory ligament were elongated.

  • Ligament deformation patterns can help diagnose craniocervical instability.

Acknowledgements

This study was supported by National Institutes of Health (1R03AG056897), USA.

Abbreviations

2D

Two-dimensional

3D

Three-dimensional

ADI

Atlanto-dental interval

AT

Axial twisting

C0

Occiput

C1

Atlas

C2

Axis

CCJ

Craniocervical junction

CT

Computed tomography

DoF

Degree of freedom

FE

Flexion-extension

ILB

Inferior longitudinal band

LB

Lateral bending

RoM

Range of motion

SLB

Superior longitudinal band

TAL

Transverse atlantal ligament

Footnotes

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Conflict of Interest

The authors declare that there is no conflict of interest.

Ethical Review Approval

This study was approved by the institutional review board at Tongji Hospital, Shanghai, China (certificate #: K-2017-008). Each subject signed an informed consent form before participating the imaging tests.

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