Leitlinien & Studien

Image
LABORATORY INVESTIGATION  
C1–2 hypermobility and its impact on the spinal cord:  
a finite element analysis  
Arpan A. Patel, MD,1,2 Jacob K. Greenberg, MD, MSCI,3 Michael P. Steinmetz, MD,1,2  
Sarel Vorster, MD,1,2 Edin Nevzati, MD,4,5 and Alexander Spiessberger, MD1,2  
1Center for Spine Health, Cleveland Clinic, Cleveland, Ohio; 2Department of Neurosurgery, Cleveland Clinic Lerner College of  
Medicine, Cleveland, Ohio; 3Department of Neurological Surgery, Washington University School of Medicine, St. Louis, Missouri;  
4Department of Neurosurgery, Cantonal Hospital of Lucerne, Switzerland; and 5Faculty of Medicine, University of Basel,  
Switzerland  
OBJECTIVE The authors present a finite element analysis (FEA) evaluating the mechanical impact of C1–2 hypermobil-  
ity on the spinal cord.  
METHODS The Code_Aster program was used to perform an FEA to determine the mechanical impact of C1–2 hyper-  
mobility on the spinal cord. Normative values of Young’s modulus were applied to the various components of the model,  
including bone, ligaments, and gray and white matter. Two models were created: 25° and 50° of C1-on-C2 rotation, and  
2.5 and 5 mm of C1-on-C2 lateral translation. Maximum von Mises stress (VMS) throughout the cervicomedullary junc-  
tion was calculated and analyzed.  
RESULTS The FEA model of 2.5 mm lateral translation of C1 on C2 revealed maximum VMS for gray and white matter  
of 0.041 and 0.097 MPa, respectively. In the 5-mm translation model, the maximum VMS for gray and white matter was  
0.069 and 0.162 MPa. The FEA model of 25° of C1-on-C2 rotation revealed maximum VMS for gray and white matter of  
0.052 and 0.123 MPa. In the 50° rotation model, the maximum VMS for gray and white matter was 0.113 and 0.264 MPa.  
CONCLUSIONS This FEA revealed significant spinal cord stress during pathological rotation (50°) and lateral transla-  
tion (5 mm) consistent with values found during severe spinal cord compression and in patients with myelopathy. While  
this finite element model requires oversimplification of the atlantoaxial joint, the study provides biomechanical evidence  
that hypermobility within the C1–2 joint leads to pathological spinal cord stress.  
KEYWORDS finite element analysis; Ehlers-Danlos syndrome; atlantoaxial instability; hypermobility; cervical  
hlErs-Danlos syndromes (EDSs) have been asso-  
(CMS) with symptoms of syncope, dizziness, sleep apnea,  
autonomous dysregulation, motor weakness, and hyperre-  
ciated with a constellation of spinal conditions as  
a consequence of underlying ligamentous laxity,  
2,4  
E
flexia. Similar to hypermobility within the occiput–C1  
including craniocervical instability (CCI), atlantoaxial  
joint leading to brainstem functional impairment, liga-  
mentous laxity in the transverse and alar ligaments within  
1–5  
instability (AAI), and basilar invagiation. AAI, in par-  
1,4  
ticular, is observed in multiple disorders of connective  
tissue including Marfan syndrome, Down syndrome, and  
the C1–2 junction can lead to hypermobility and AAI.  
However, the mechanism of brainstem injury in AAI may  
be secondary to repetitive strain and stress rather than  
compression. Our study aims to examine various normal  
and hypermobile anatomical scenarios within the atlanto-  
axial joint to evaluate whether hypermobility can lead to  
significant spinal cord stress using finite element analysis  
(FEA).  
1
rheumatoid arthritis. The deficient ligamentous architec-  
ture and consequential hypermobility in conditions such  
as CCI can lead to cranial settling and clivoaxial kypho-  
1–3  
sis. This well-studied phenomenon (cranial settling and  
clivoaxial kyphosis) has been shown to lead to brainstem  
compression and associated cervicomedullary syndrome  
ABBREVIATIONS AAI = atlantoaxial instability; CAD = computer-aided design; CCI = craniocervical instability; CMS = cervicomedullary syndrome; EDS = Ehlers-Danlos  
syndrome; FEA = finite element analysis; FEM = finite element modeling; VMS = von Mises stress.  
SUBMITTED December 5, 2023. ACCEPTED February 21, 2024.  
INCLUDE WHEN CITING Published online May 3, 2024; DOI: 10.3171/2024.2.SPINE231327.  
©AANS 2024, except where prohibited by US copyright law  
J Neurosurg Spine May 3, 2024  
1
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
FIG. 1. CAD developed within the Code_Aster program. Components of the discretization process are labeled. Figure is available  
in color online only.  
Previous studies have utilized finite element modeling  
unteer was used to develop a 3D finite element model of  
the human cervical osteoligamentous spine and spinal  
cord. Thin-sectioned (1-mm) DICOM files were used to  
model the C1–2 junction, which was subsequently used to  
develop a computer-aided design (CAD) model (Fig. 1).  
The FEA program, Code_Aster, was used to compute the  
magnitude and location of stress within the spinal cord.  
Similar to the Spinal Cord Stress Injury Assessment sys-  
tem, FEM provides a model of the brainstem with sim-  
plified biomechanics including isotropy of gray and white  
(FEM) to investigate the mechanical impact on neural  
structures associated with pathological or postsurgical  
conditions within the craniocervical junction such as  
Chiari malformation, basilar invagination, degenerative  
cervical myelopathy, spinal cord contusion, and surgical  
6–13  
decompression and fusion. These studies have signifi-  
cantly improved our understanding of the relationship be-  
tween the biomechanics of the cervical spine and their  
mechanical impact on the spinal cord through assessing  
stress and strain. Additionally, FEA allows the study of  
unique anatomical and pathological scenarios that would  
be difficult to produce in ex vivo cadaveric studies due  
to tissue quality, high cost, and limited measurement of  
11,14  
matter and constant material property. A complete list  
of biomechanical properties, including Young’s modulus  
and Poisson’s ratio for anatomical components, is found in  
15–18  
Table 1.  
All measures of stress were reported in mega-  
6,12  
pascal (MPa).  
biomechanical parameters. Our study contributes to  
the collective understanding of cervical biomechanics  
derived from FEA studies by investigating the gray and  
white matter von Mises stress (VMS) in two anatomical  
settings: C1–2 lateral displacement and C1–2 rotation.  
Using FEM, we simulated the pathological, supraphysi-  
ological C1–2 movement that can be found in conditions  
such as EDS and evaluated its mechanical impact on the  
spinal cord.  
Finite Element Model Testing  
Two different anatomical conditions were simulated,  
including lateral displacement of C1 on C2 (2.5 and 5.0  
mm) and rotation of C1 on C2 (25° and 50°). When simu-  
lating C1-on-C2 motion, boundary constraints were ap-  
plied to the model to mimic physiological motion. The  
degrees of freedom for C2 were minimal, while C1 was  
allowed to laterally translate and rotate upon C2. In mod-  
eling rotation, a moment boundary was applied at the axis  
of rotation line that centered around the dens (Fig. 2A and  
B). The caudal aspect of the spinal cord was constrained in  
degrees of freedom while the cranial aspect was allowed  
Methods  
Study Materials  
A cervical MR image from an 18-year-old healthy vol-  
TABLE 1. Components of the discretization process of the upper cervical spine with Young’s modulus and Poisson’s  
ratio reported for each component  
Material (element type)  
Anatomy  
Young’s Modulus (MPa) Poisson’s Ratio Thickness (mm)  
Linear elastic (cubic)  
Linear elastic (cubic)  
Linear elastic (tetrahedron)  
Linear elastic (cubic)  
Linear elastic  
Gray matter  
White matter  
0.277  
0.656  
14.8  
0.45  
0.45  
0.48  
0.45  
0.45  
0.28  
0.3  
0.3  
Subarachnoid space (CSF)  
Dura mater  
31.5  
Epidural space  
31.5  
Linear elastic  
Cortical bone  
15000  
100  
Linear (2D shell elements)  
Dentate ligaments  
2
J Neurosurg Spine May 3, 2024  
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
FIG. 2. A: Inferior view of C2 (green arrow) with degree of freedom constraints defined by dotted circles. B: Moment boundary  
applied to the axis of rotation (arrows) through the dens for C1–2 rotation. C: Sliding contact settings between C1 and C2 and the  
epidural space. Figure is available in color online only.  
to move. VMS (in MPa), an aggregate calculation to de-  
termine yield criteria, was calculated for each voxel and  
graphically presented in a contour map. This calculation  
was performed individually for both gray and white mat-  
ter throughout the lower brainstem and spinal cord. The  
maximum values were utilized to compare the mechani-  
cal impact of different anatomical scenarios. The force  
transfer path began with movement of C1 and C2 with  
sliding contact between the osseous structures and the  
epidural space (Fig. 2C). The sliding contact coefficient of  
friction was defined as 0.1. The force was then transferred  
from the epidural space to the dura mater, then to the sur-  
rounding CSF and dentate ligaments, and finally to gray  
and white matter.  
contour map revealed a trend toward higher VMS values  
in the anterior aspect of the gray and white matter of the  
spinal cord in both the 2.5- and 5-mm translation models  
(Fig. 3). During 2.5 mm of C1-on-C2 lateral translation,  
the spinal cord was also noted to be laterally displaced by  
approximately 2.5 mm. Similarly, in 5 mm of C1-on-C2  
lateral translation, the spinal cord was laterally displaced  
by approximately 5 mm (Fig. 4).  
Rotation  
In the FEA performed for 25° of C1-on-C2 rotation,  
the maximum VMS for gray and white matter was 0.052  
and 0.123 MPa. In the 50° rotation model, the maximum  
VMS for gray and white matter was 0.113 and 0.264 MPa  
(Table 2). Similar to the lateral translation model, the con-  
tour map revealed a trend toward higher VMS values in  
the anterior aspect of the gray and white matter of the spi-  
nal cord for both the 25° and 50° rotation models (Fig.  
5). In the 25° rotation model, the posterior aspect of the  
Principles of FEA Modeling  
FEA of the spine uses a discretization process of re-  
ducing a continuous anatomical system into discrete parts  
of bones, ligaments, and neural structures. The 3D repre-  
sentation is often built from CT or MR imaging and rep-  
resented as geometric shapes. The material properties of  
the discrete components are assigned. The stiffness of the  
tissue can either be interpreted from CT or MR imaging  
or be based on existing literature. Once the model is devel-  
oped, unique loading conditions are applied to the system  
to evaluate the clinically relevant biomechanical param-  
eters such as stress and strain on the brainstem, intradiscal  
TABLE 2. Minimum, maximum, and average VMS for each clinical  
condition simulated  
VMS (MPa)  
Clinical Condition  
Min  
Max  
Average  
6,11,12  
pressure, or segmental rotation.  
Lateral translation  
2.5 mm  
Results  
Gray matter  
White matter  
5 mm  
0
0.041  
0.097  
0.014  
0.023  
Two types of C1–2 motion were considered: lateral  
translation and rotation. Lateral translation movement was  
subdivided into 2.5 mm (physiological range of motion)  
and 5.0 mm (supraphysiological range of motion). Rota-  
tion was subdivided into 25° (physiological range of mo-  
tion) and 50° (supraphysiological range of motion).  
0.001  
Gray matter  
White matter  
Rotation  
0.001  
0.002  
0.069  
0.162  
0.028  
0.048  
25°  
Lateral Translation  
Gray matter  
White matter  
50°  
0.001  
0.001  
0.052  
0.123  
0.016  
0.029  
In the FEA performed for 2.5-mm lateral translation of  
C1 on C2, maximum VMS for gray and white matter was  
0.041 and 0.097 MPa, respectively. In the 5-mm transla-  
tion model, the maximum VMS for gray and white mat-  
ter was 0.069 and 0.162 MPa, respectively (Table 2). The  
Gray matter  
White matter  
0.002  
0.003  
0.113  
0.034  
0.063  
0.264  
J Neurosurg Spine May 3, 2024  
3
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
FIG. 3. FEA modeling 2.5 and 5.0 mm of C1-on-C2 lateral translation. Distribution of VMS throughout the gray and white matter is  
reported and axial distribution of the VMS is represented. Figure is available in color online only.  
spinal cord was noted to undergo up to approximately 4  
mm of lateral displacement in the direction of the rotation,  
while the anterior midline aspect of the cord remained un-  
changed. Similarly, in the 50° model, the posterior aspect  
of the spinal cord was noted to undergo approximately 7.7  
mm of lateral displacement, while the anterior midline re-  
mained in its neutral location. The rotation of C1 on C2  
around the axis of the dens resulted in similar rotation and  
displacement of the spinal cord around an axis in the an-  
terior midline (Fig. 6).  
Using diagnostic criteria for Fielding type 1 AAI,  
25° of rotation of C1 on C2 is considered within normal  
physiological conditions, while 50° of rotation is consid-  
19  
ered a pathological state. Additionally, 2.5 mm of lateral  
translation was considered as a potentially normal physi-  
ological finding, while 5 mm of translation was consid-  
19–21  
ered pathological.  
As expected, the FEA found higher  
values of VMS all throughout the gray and white matter  
of the C1–2 junction during 50° of rotation when com-  
pared with the maximum VMS during 25° rotation. Simi-  
larly, the maximum VMS during 5 mm of lateral trans-  
lation was higher than the maximum during 2.5 mm of  
movement. The maximum discrete values of VMS dur-  
ing both 5 mm of lateral movement and 50° of rotation  
are consistent with values of pathological stress that are  
Discussion  
Our study aimed to provide insight into the mechanical  
impact of supraphysiological movement within atlantoax-  
ial segments on the spinal cord. Using a healthy volunteer  
to generate a finite element model, we tested normal and  
supraphysiological movement in C1–2 lateral translation  
and rotation. Although we aimed to better understand the  
pathophysiology of spinal cord injury in patients with liga-  
mentous laxity and hypermobility, we used a healthy vol-  
unteer to generate the CAD because the osseous structures  
of a patient with EDS are similar to the osseous structures  
in a healthy volunteer. In this model, the Young’s modulus  
of the ligaments was estimated to have little influence on  
the mechanical impact exerted by the osseous structures  
found in settings of severe spinal cord compression and  
7,11,18  
patients with myelopathy.  
Evaluating the distribution  
of stress throughout the white and gray matter of the spi-  
nal cord revealed a trend toward increased VMS values in  
the anterior horn of the gray matter, anterior corticospinal  
tract, and anterior spinothalamic tract. Given the location  
of stress in the upper spinal cord, the expected symptoms  
were similar to those of CMS such as upper- and lower-  
extremity weakness, autonomic dysfunction, numbness,  
swallowing difficulties, and imbalance. With higher stress  
values in the anterior spinal cord, there may be a predilec-  
tion for motor symptoms. During 50° of C1–2 rotation,  
there was approximately 7.7 mm of displacement noted  
in the posterior aspect of the spinal cord, while the ante-  
rior aspect remained relatively in its neutral position (Fig.  
6). This finding correlated with increased VMS values in  
11,14  
on the spinal cord, thus normative values were utilized.  
The simulated hypermobility within a healthy spine was  
an acceptable method to evaluate the mechanical impact  
of supraphysiological lateral translation and rotation on  
the spinal cord.  
4
J Neurosurg Spine May 3, 2024  
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
the anterior aspect of the spinal cord as the inability to  
displace during rotational movement resulted in increased  
torsional stress.  
The maximum VMS of both gray and white matter  
during 2.5 mm of lateral translation was noted to be less  
than the maximum VMS in both gray and white matter  
during 25° of rotation. Given that 25° of C1-on-C2 rota-  
tion is well accepted as normal physiological motion, this  
finding may suggest that 2.5 mm of lateral translation of  
C1 on C2 can be an acceptable finding. Rotational move-  
ment in the C1–2 segment led to overall higher maximum  
VMS in both gray and white matter when compared to  
displacement. This effect may be seen due to motion cou-  
pling, in which rotation in the atlantoaxial joint is coupled  
to lateral displacement and lateral bending, thus leading  
to more strain and stress applied to the spinal cord.  
Clinically, dynamic spinal cord stress and strain in an  
unstable spine is associated with chronic spinal cord in-  
jury and dysfunction. Repetitive shear forces due to in-  
stability can induce localized mechanical axonal injury.  
Both tensile and compressive stress forces can lead to in-  
creased intramedullary pressure, reduced perfusion, and  
22  
ischemic injury in the spinal cord. Through this FEA  
we found that specific anatomical movements within the  
atlantoaxial segment result in distinct amounts of spinal  
cord stress, with certain movements generating stress val-  
ues similar to those found in patients with severe spinal  
11,18  
cord compression. Yang et al. evaluated the maximum  
spinal cord stress associated with C4–5 stenosis in pa-  
tients with cervical myelopathy. Spinal cord stress dur-  
ing loading conditions at the C4–5 level in a control pa-  
tient ranged from 0.00014 to 0.001 MPa, while the stress  
values within a diseased myelopathic spinal cord ranged  
FIG. 4. FEA evaluating the total displacement of the spinal cord during  
2.5 and 5.0 mm of C1-on-C2 lateral translation. Figure is available in  
color online only.  
18  
from 0.0194 to 0.039 MPa. Although the stress values  
generated from specific models in different regions of the  
spinal cord cannot be directly compared with the values  
generated within this study, a trend was identified, with  
higher values associated with pathological states. Simi-  
larly, previous studies have shown that increased spinal  
cord VMS as measured by FEA in craniocervical con-  
modalities. Consequentially, identification of atlantoaxial  
hypermobility or CCI is often missed on static imaging  
7,11  
4
ditions correlates clinically with increased disability.  
modalities. As the most mobile segment of the spine, the  
Henderson et al. noted within their finite element model  
of craniocervical compression that clinical improve-  
ment following decompression correlated with a 68%  
atlantoaxial joint is prone to developing instability. Range-  
of-motion studies report maximum global head rotation in  
a single direction as 70°–90°, with the C1–2 segment re-  
11  
23–25  
reduction in modeled stress values (e.g., 0.7–0.13 MPa).  
sponsible for 50%–60% of the movement.  
The maxi-  
Within our study, we noted a 53.4% and 54.0% reduction  
in VMS between 50° and 25° of rotation when compar-  
ing the maximum VMS in white (0.264–0.123 MPa) and  
gray matter (0.113–0.52 MPa), respectively. Similarly, the  
maximum VMS in white matter and gray matter when  
comparing 5 to 2.5 mm of lateral translation resulted in  
a 40.1% (0.162–0.97 MPa) and 40.6% (0.162–0.041 MPa)  
reduction, respectively. The relative differences between  
the VMS scores of 25° of rotation and 2.5 mm of lateral  
translation when compared with 50° rotation and 5 mm  
of lateral translation suggest a similar relationship of non-  
pathological and pathological states between these ranges  
of motion.  
mum rotation of C1 relative to C2 in normative settings is  
23,25  
reported to be between 36° and 43°.  
In vivo kinematic  
studies reveal coupled motion, including lateral bending  
and flexion/extension of the C1–2 segment, during upright  
rotation as well as lateral translation and axial rotation of  
23,26  
C1–2 during cervical lateral bending.  
Although there  
is a paucity of data regarding the normative lateral trans-  
lation of C1 on C2 during maximal lateral bending, a few  
studies have suggested that 1–2 mm of ipsilateral C1-on-  
C2 overhang may be within normal parameters, while >  
3.5 mm of translation is associated with hypermobility  
20,21  
and AAI.  
Our investigation suggests that both 50° of  
rotation and 5 mm of lateral translation are associated with  
pathologic amounts of stress within the spinal cord. In the  
clinical evaluation of patients with EDS and hypermobil-  
ity, dynamic films revealing 50° of C1-on-C2 rotation or  
Defining parameters of abnormal atlantoaxial motion  
continues to be challenging due to the dynamic nature of  
the underlying pathology and the static nature of imaging  
J Neurosurg Spine May 3, 2024  
5
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
FIG. 5. FEA modeling 25° and 50° of C1-on-C2 rotation. Distribution of VMS throughout the gray and white matter is reported and  
axial distribution of VMS is represented. Figure is available in color online only.  
5 mm of lateral translation during lateral bending may be  
an indication of instability and need for stabilization. Fur-  
thermore, our investigation suggests that 2.5 mm of C1-  
on-C2 lateral translation leads to comparatively less stress  
on the spinal cord than 25° of C1-on-C2 rotation. Given  
that 25° of C1-on-C2 rotation is well defined as within nor-  
mal physiological range, our investigation suggests that 2.5  
mm of lateral translation should also be considered within  
normal physiological range.  
as a solid element with equivalent fluid properties, thus  
the fluid is unable to displace under force. While there are  
many intrinsic limitations to FEM of the craniocervical  
spine, we believe these studies provide useful insight into  
biomechanics that would be difficult to ascertain through  
cadaveric studies.  
CoWneclhuasveiountislized FEM to evaluate spinal cord stress in  
the atlantoaxial junction during normative and pathologi-  
cal ranges of motion. The FEA performed revealed signifi-  
cant spinal cord stress during pathological rotation (50°)  
and lateral translation (5 mm). During these movements,  
there is significant stress within the anterior horn of the  
gray matter, anatomically corresponding to projections of  
anterior corticospinal and anterior spinothalamic tracts.  
In a clinical scenario, stress within this region can be as-  
sociated with symptoms similar to CMS with autonomic  
dysfunction, motor weakness, numbness, and imbalance.  
While FEA of the craniocervical junction requires over-  
simplification of a complex anatomical region, the study  
provides biomechanical insight into spinal cord stress in  
C1–2 hypermobility.  
Limitations of the Study  
Overall, FEM of the craniocervical junction requires  
simplification of the most mobile and complex anatomi-  
cal region of the spine. In the absence of an intervertebral  
disc, the atlantoaxial segment has a multitude of ligaments  
that play an important role in limiting segmental motion.  
FEA requires the simplification of such ligaments and re-  
duction to linear material properties. In our study, we used  
normative values for Young’s modulus despite investigat-  
ing the mechanical impact of hypermobility on the spinal  
cord. This was an acceptable limitation for our analysis as  
the FEM can simulate hypermobile movement indepen-  
dent of Young’s modulus of the ligaments. The focus of  
our investigation was evaluating spinal cord stress gener-  
ated by motion of the osseous structures. Furthermore,  
within our model the spinal cord was designed to be fixed  
caudally with no degrees of freedom and allowed to move  
cranially. This fixation method can impact the results as  
the ability of the spinal cord to displace can directly im-  
pact the VMS measured. Additionally, CSF was modeled  
Acknowledgments  
No sponsor contribution to the design and conduct of the  
study; collection, management, analysis, or interpretation of data;  
or preparation, review, or approval of the manuscript was given by  
the Ehlers-Danlos Syndrome Initiative Germany.  
6
J Neurosurg Spine May 3, 2024  
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
6. Singhal I, Harinathan B, Warraich A, et al. Finite element  
modeling of the human cervical spinal cord and its applica-  
tions: a systematic review. N Am Spine Soc J. 2023;15:100246.  
7. Xue F, Deng H, Chen Z, et al. Effects of cervical rotatory  
manipulation on the cervical spinal cord complex with ossifi-  
cation of the posterior longitudinal ligament in the vertebral  
canal: a finite element study. Front Bioeng Biotechnol. 2023;  
11:1095587.  
8. Zhu R, Chen YH, Yu QQ, et al. Effects of contusion load on  
cervical spinal cord: a finite element study. Math Biosci Eng.  
2020;17(3):2272-2283.  
9. Stoner KE, Abode-Iyamah KO, Fredericks DC, Viljoen S,  
Howard MA, Grosland NM. A comprehensive finite element  
model of surgical treatment for cervical myelopathy. Clin  
Biomech (Bristol, Avon). 2020;74:79-86.  
10. Vedantam A, Harinathan B, Warraich A, Budde MD, Yo-  
ganandan N. Differences in spinal cord biomechanics after  
laminectomy, laminoplasty, and laminectomy with fusion for  
degenerative cervical myelopathy. J Neurosurg Spine. 2023;  
39(1):28-39.  
11. Henderson FC, Wilson WA, Mott S, et al. Deformative stress  
associated with an abnormal clivo-axial angle: a finite ele-  
ment analysis. Surg Neurol Int. 2010;1(1):30.  
12. Wang MC, Kiapour A, Massaad E, Shin JH, Yoganandan  
N. A guide to finite element analysis models of the spine for  
clinicians. J Neurosurg Spine. 2023;40(1):38-44.  
13. Naoum S, Vasiliadis AV, Koutserimpas C, Mylonakis N,  
Kotsapas M, Katakalos K. Finite element method for the  
evaluation of the human spine: a literature overview. J Funct  
Biomater. 2021;12(3):43.  
14. Wong KH, Choi J, Wilson W, Berry J, Henderson FC Sr.  
Spinal cord stress injury assessment (SCOSIA): clinical ap-  
plications of mechanical modeling of the spinal cord and  
brainstem. Proc SPIE. 2009;7261:726106.  
15. Phuntsok R, Mazur MD, Ellis BJ, Ravindra VM, Brockmeyer  
DL. Development and initial evaluation of a finite element  
model of the pediatric craniocervical junction. J Neurosurg  
Pediatr. 2016;17(4):497-503.  
FIG. 6. FEA evaluating the total displacement of the spinal cord during  
25° and 50° of C1-on-C2 rotation. Global Z-proj = a calculation provided  
by the Code_Aster program that allows us to verify the amount of rota-  
tion. Figure is available in color online only.  
16. Astin JH, Wilkerson CG, Dailey AT, Ellis BJ, Brockmeyer  
DL. Finite element modeling to compare craniocervical mo-  
tion in two age-matched pediatric patients without or with  
Down syndrome: implications for the role of bony geometry  
in craniocervical junction instability. J Neurosurg Pediatr.  
2020;27(2):218-224.  
17. Czyż M, Scigała K, Jarmundowicz W, Będziński R. Numeri-  
cal model of the human cervical spinal cord—the develop-  
ment and validation. Acta Bioeng Biomech. 2011;13(4):51-58.  
18. Yang S, Qu L, Yuan L, et al. Finite element analysis of spinal  
cord stress in a single segment cervical spondylotic myelopa-  
thy. Front Surg. 2022;9:849096.  
References  
1. Henderson FC Sr, Austin C, Benzel E, et al. Neurological and  
spinal manifestations of the Ehlers-Danlos syndromes. Am J  
Med Genet C Semin Med Genet. 2017;175(1):195-211.  
2. Henderson FC Sr, Francomano CA, Koby M, Tuchman K,  
Adcock J, Patel S. Cervical medullary syndrome secondary  
to craniocervical instability and ventral brainstem compres-  
sion in hereditary hypermobility connective tissue disorders:  
5-year follow-up after craniocervical reduction, fusion, and  
stabilization. Neurosurg Rev. 2019;42(4):915-936.  
19. Fielding JW, Hawkins RJ. Atlanto-axial rotatory fixation.  
(Fixed rotatory subluxation of the atlanto-axial joint.) J Bone  
Joint Surg Am. 1977;59(1):37-44.  
20. Henderson FC Sr, Rosenbaum R, Narayanan M, et al. Atlan-  
to-axial rotary instability (Fielding type 1): characteristic  
clinical and radiological findings, and treatment outcomes  
following alignment, fusion, and stabilization. Neurosurg  
Rev. 2021;44(3):1553-1568.  
3. Spiessberger A, Dietz N, Gruter B, Virojanapa J. Ehlers-  
Danlos syndrome-associated craniocervical instability with  
cervicomedullary syndrome: comparing outcome of cranio-  
cervical fusion with occipital bone versus occipital condyle  
fixation. J Craniovertebr Junction Spine. 2020;11(4):287-292.  
4. Lohkamp LN, Marathe N, Fehlings MG. Craniocervical  
instability in Ehlers-Danlos Syndrome-a systematic review  
of diagnostic and surgical treatment criteria. Global Spine J.  
2022;12(8):1862-1871.  
21. Hariharan KV, Terhorst L, Maxwell MD, Bise CG, Timko  
MG, Schneider MJ. Inter-examiner reliability of radiographic  
measurements from open-mouth lateral bending cervical  
radiographs. Chiropr Man Therap. 2020;28(1):32.  
22. Henderson FC, Geddes JF, Vaccaro AR, Woodard E, Berry  
KJ, Benzel EC. Stretch-associated injury in cervical spon-  
dylotic myelopathy: new concept and review. Neurosurgery.  
2005;56(5):1101-1113.  
5. Milhorat TH, Bolognese PA, Nishikawa M, McDonnell NB,  
Francomano CA. Syndrome of occipitoatlantoaxial hyper-  
mobility, cranial settling, and Chiari malformation type I in  
patients with hereditary disorders of connective tissue. J Neu-  
rosurg Spine. 2007;7(6):601-609.  
23. Anderst W, Rynearson B, West T, Donaldson W, Lee J. Dy-  
namic in vivo 3D atlantoaxial spine kinematics during up-  
right rotation. J Biomech. 2017;60:110-115.  
J Neurosurg Spine May 3, 2024  
7
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Patel et al.  
24. González DCN, Ardura Aragón F, Sanjuan JC, et al. C1-C2  
rotatory subluxation in adults “a narrative review.” Diagnos-  
tics (Basel). 2022;12(7):1615.  
Author Contributions  
Conception and design: Patel, Greenberg, Steinmetz, Nevzati,  
Spiessberger. Analysis and interpretation of data: Patel, Vorster,  
Spiessberger. Drafting the article: Patel. Critically revising the  
article: all authors. Reviewed submitted version of manuscript: all  
authors. Approved the final version of the manuscript on behalf  
of all authors: Patel. Statistical analysis: Patel. Study supervision:  
Spiessberger.  
25. Pang D, Li V. Atlantoaxial rotatory fixation: part 1—biome-  
chanics of normal rotation at the atlantoaxial joint in chil-  
dren. Neurosurgery. 2004;55(3):614-626.  
26. Ishii T, Mukai Y, Hosono N, et al. Kinematics of the cervical  
spine in lateral bending: in vivo three-dimensional analysis.  
Spine (Phila Pa 1976). 2006;31(2):155-160.  
Correspondence  
Arpan A. Patel: Cleveland Clinic, Cleveland, OH. patela16@  
Disclosures  
ccf.org.  
Dr. Steinmetz reported receiving royalties from Elsevier and  
royalties/honoraria from Globus outside the submitted work. Dr.  
Nevzati reported receiving grants from Deutsche Ehlers Danlos  
Gesellschaft during the conduct of the study. Dr. Spiessberger  
reported that this study was financially supported by a patient  
advocacy group (EDS Germany, 4000 USD).  
8
J Neurosurg Spine May 3, 2024  
Authenticated gshasby@thejns.org | Downloaded 05/06/24 04:12 PM UTC  
Wir benutzen Cookies

Wir nutzen Cookies auf unserer Website. Einige von ihnen sind essenziell für den Betrieb der Seite, während andere uns helfen, diese Website und die Nutzererfahrung zu verbessern (Tracking Cookies). Sie können selbst entscheiden, ob Sie die Cookies zulassen möchten. Bitte beachten Sie, dass bei einer Ablehnung womöglich nicht mehr alle Funktionalitäten der Seite zur Verfügung stehen.

Wir benutzen Cookies

Wir nutzen Cookies auf unserer Website. Einige von ihnen sind essenziell für den Betrieb der Seite, während andere uns helfen, diese Website und die Nutzererfahrung zu verbessern (Tracking Cookies). Sie können selbst entscheiden, ob Sie die Cookies zulassen möchten. Bitte beachten Sie, dass bei einer Ablehnung womöglich nicht mehr alle Funktionalitäten der Seite zur Verfügung stehen.