Anatomy and mobility in the adult cadaveric craniocervical junction.

Genetic diseases with craniofacial malformations can be associated with anomalies of the craniocervical joint (CCJ). The functions of the CCJ are thus impaired, as mobility may be either limited by abnormal bone fusion causing headaches, or exaggerated in the case of hypermobility, which may cause irreparable damage to the spinal cord. Restoring the balance between mobility and stability requires surgical correction in children. The anatomy and biomechanics of the CCJ are quite unique, yet have been overlooked in the past decades. Pediatric evidence is so scarce, that investigating the adult CCJ is our best shot to disentangle the form-function relationships of this anatomical region. The motivation of the present study was to understand the morphological and functional basis of motion in the CCJ, in the hope to find morphological features accessible from medical imaging able to predict mobility. To do so, we have quantified the in-vitro kinematics of the CCJ in nine cadaveric asymptomatic adults, and estimated a wide range of mobility variables covering the complexity of spinal motion. We compared these variables with the shape of the occipital, the atlas and the axis, obtained using a dense geometric morphometric approach. Morphological joint congruence was also quantified. Our results suggest a strong relationship between bone shape and motion, with the overall geometry predicting best the primary movements, and the joint facets predicting best the secondary movements. We propose a functional hypothesis stating that the musculoligamental system determines movements of great amplitude, while the shape and congruence of joint facets determine the secondary and coupled movements, especially by varying the geometry of bone stops and the way ligaments are tensioned. We believe this work will provide valuable insights in understanding the biomechanics of the CCJ. Furthermore, it should help surgeons treating CCJ anomalies by enabling them to translate objectives of functional and clinical outcome into clear objectives of morphological outcome.

Geometric growth of the normal human craniocervical junction from 0 to 18 years old.

The craniocervical junction (CCJ) forms the bridge between the skull and the spine, a highly mobile group of joints that allows the mobility of the head in every direction. The CCJ plays a major role in protecting the inferior brainstem (bulb) and spinal cord, therefore also requiring some stability. Children are subjected to multiple constitutive or acquired diseases involving the CCJ: primary bone diseases such as in FGFR-related craniosynostoses or acquired conditions such as congenital torticollis, cervical spine luxation, and neurological disorders. To design efficient treatment plans, it is crucial to understand the relationship between abnormalities of the craniofacial region and abnormalities of the CCJ. This can be approached by the study of control and abnormal growth patterns. Here we report a model of normal skull base growth by compiling a collection of geometric models in control children. Focused analyses highlighted specific developmental patterns for each CCJ bone, emphasizing rapid growth during infancy, followed by varying rates of growth and maturation during childhood and adolescence until reaching stability by 18 years of age. The focus was on the closure patterns of synchondroses and sutures in the occipital bone, revealing distinct closure trajectories for the anterior intra-occipital synchondroses and the occipitomastoid suture. The findings, although based on a limited dataset, showcased specific age-related changes in width and closure percentages, providing valuable insights into growth dynamics within the first 2 years of life. Integration analyses revealed intricate relationships between skull and neck structures, emphasizing coordinated growth at different stages. Specific bone covariation patterns, as found between the first and second cervical vertebrae (C1 and C2), indicated synchronized morphological changes. Our results provide initial data for designing inclusive CCJ geometric models to predict normal and abnormal growth dynamics.

New diagnostic criteria for metopic ridges and trigonocephaly: a 3D geometric approach.

BACKGROUND: Trigonocephaly occurs due to the premature fusion of the metopic suture, leading to a triangular forehead and hypotelorism. This condition often requires surgical correction for morphological and functional indications. Metopic ridges also originate from premature metopic closure but are only associated with mid-frontal bulging; their surgical correction is rarely required. Differential diagnosis between these two conditions can be challenging, especially in minor trigonocephaly. METHODS: Two hundred seven scans of patients with trigonocephaly (90), metopic rigdes (27), and controls (90) were collected. Geometric morphometrics were used to quantify skull and orbital morphology as well as the interfrontal angle and the cephalic index. An innovative method was developed to automatically compute the frontal curvature along the metopic suture. Different machine-learning algorithms were tested to assess the predictive power of morphological data in terms of classification. RESULTS: We showed that control patients, trigonocephaly and metopic rigdes have distinctive skull and orbital shapes. The 3D frontal curvature enabled a clear discrimination between groups (sensitivity and specificity > 92%). Furthermore, we reached an accuracy of 100% in group discrimination when combining 6 univariate measures. CONCLUSION: Two diagnostic tools were proposed and demonstrated to be successful in assisting differential diagnosis for patients with trigonocephaly or metopic ridges. Further clinical assessments are required to validate the practical clinical relevance of these tools.

Paediatric skull growth models: A systematic review of applications to normal skulls and craniosynostoses.

INTRODUCTION: Craniosynostoses affect 1/2000 births and their incidence is currently increasing. Without surgery, craniosynostosis can lead to neurological issues due to restrained brain growth and social stigma due to abnormal head shapes. Understanding growth patterns is essential to develop surgical planning approaches and predict short- and long-term post-operative results. Here we provide a systematic review of normal and pathological cranial vault growth models. MATERIAL AND METHODS: The systematic review of the literature identified descriptive and comprehensive skull growth models with the following criteria: full text articles dedicated to the skull vault of children under 2 years of age, without focus on molecular and cellular mechanisms. Models were analysed based on initial geometry, numerical method, age determination method and validation process. RESULTS: A total of 14 articles including 17 models was reviewed. Four descriptive models were assessed, including 3 models using statistical analyses and 1 based on deformational methods. Thirteen comprehensive models were assessed including 7 finite element models and 6 diffusion models. Results from the current literature showed that successful models combined analyses of cranial vault shape and suture bone formation. DISCUSSION: Growth modelling is central when assessing craniofacial architecture in young patients and will be a key factor in the development of future customized treatment strategies. Recurrent technical difficulties were encountered by most authors when generalizing a specific craniosynostosis model to all types of craniosynostoses, when assessing the role of the brain and when attempting to relate the age with different stages of growth.

Insights into the mechanical interaction between an active cranial implant and the skull subjected to moderate impact loadings.

In the context of cochlear implants, which are now widely used, and innovative active devices, the cranial implantation of electronic devices raises new questions about the mechanical interactions between the implant and the skull. The aim of this study was to build a methodology using experimental data and numerical simulations to evaluate the mechanical interactions between the skull and the WIMAGINE® active cranial implant intended for use for tetraplegic patients. A finite element model of the implant housing and a simplified model of the three-layered skull were developed. 2.5 J-hammer impact tests were performed on implant housings and ovine cadaver heads for model calibration. The two models were then combined to analyze the interactions between the skull and the implant and compared against impact tests. The implant dissipates a certain amount of the impact energy which could be a parameter to include in implant design in addition to the implant integrity, tending to increase the implant stiffness. The non-implanted as well as the implanted lamb heads demonstrated an overall good resistance to the impact tests. The models correlated well with the experimental data, and improvements of the model through more realistic geometry (CT-scans) and more complex material behavior could now be implemented. Such a model could then be used with human head geometries and help for future implant design optimizations using numerical models of the implant-skull and even implant-head complex.

Personalised gravitational loading of the cervical spine from biplanar X-rays for asymptomatic and clinical subjects in neutral standing position.

BACKGROUND: As a leading cause of disability with a high societal and economic cost, it is crucial to better understand risk factors of neck pain and surgical complications. Getting subject-specific external loading is essential for quantifying muscle forces and joint loads but it requires exertion trials and load cells which are uncommon in clinical settings. METHODS: This paper presents a method to compute the gravitational loading at four levels of the cervical spine (C3C4, C4C5, C5C6, C6C7) in neutral standing position from biplanar radiographs exclusively. The resulting load was decomposed in local disc frames and its components were used to compare different populations: 118 asymptomatic subjects and 46 patients before and after surgery (anterior cervical discectomy and fusion or total disc replacement). Comparisons were performed at C6C7 and the upper level adjacent to surgery. FINDINGS: Significant changes in gravitational loading were observed with age in healthy subjects as well as in patients after surgery and have been associated with changes in posture. INTERPRETATION: This approach quantifies the influence of postural changes on gravitational loading on the cervical spine. It represents a simple way to obtain necessary input for muscle force quantification models in clinical routine and to use them for patient evaluation. The study of the subsequent subject-specific spinal loading could help further the understanding of cervical spine biomechanics, degeneration mechanisms and complications following surgery.

Johnson-Cook Parameter Identification for Commercially Pure Titanium at Room Temperature under Quasi-Static Strain Rates.

BACKGROUND: To simulate mechanical shocks on an intracranial implant called WIMAGINE®, Clinatec chose a Johnson-Cook model to account for the viscoplastic behavior of grade 2 titanium in a dynamic study using Radioss©. METHODS: Thirty tensile specimens were subjected to tensile tests at room temperature, and the influence of the strain rate (8 × 10-3 and 8 × 10-2 s-1) and sandblasting was analyzed. Relaxations were included in the tests to analyze viscosity phenomena. RESULTS: A whole set of parameters was identified for the elastic and plastic parts. Strain rate influence on stress was negligible at these strain rates. As expected, the sandblasting hardened the material during the tests by decreasing the hardening parameters, while local necking occurred at an earlier strain. CONCLUSIONS: This article provides the parameters of a Johnson-Cook model to simulate the elastoplastic behavior of pure titanium (T40, grade 2) in Finite Element Model (FEM) software.

Modeling of muscular activation of the muscle-tendon complex using discrete element method.

The tearing of a muscle-tendon complex (MTC) is caused by an eccentric contraction; however, the structures involved and the mechanisms of rupture are not clearly identified. The passive mechanical behavior the MTC has already been modeled and validated with the discrete element method. The muscular activation is the next needed step. The aim of this study is to model the muscle fiber activation and the muscular activation of the MTC to validate their active mechanical behaviors. Each point of the force/length relationship of the MTC (using a parabolic law for the force/length relationship of muscle fibers) is obtained with two steps: 1) a passive tensile (or contractile) test until the desired elongation is reached and 2) fiber activation during a position holding that can be managed thanks to the Discrete Element model. The muscular activation is controlled by the activation of muscle fiber. The global force/length relationship of a single fiber and of the complete MTC during muscular activation is in agreement with literature. The influence of the external shape of the structure and the pennation angle are also investigated. Results show that the different constituents of the MTC (extracellular matrix, tendon), and the geometry, play an important role during the muscular activation and enable to decrease the maximal isometric force of the MTC. Moreover, the maximal isometric force decreases when the pennation angle increases. Further studies will combine muscular activation with a stretching of the MTC, until rupture, in order to numerically reproduce the tearing of the MTC.

Surface reconstruction from routine CT-scan shows large anatomical variations of falx cerebri and tentorium cerebelli.

BACKGROUND: Finite element modeling of the human head offers an alternative to experimental methods in understanding the biomechanical response of the head in trauma brain injuries. Falx, tentorium, and their notches are important structures surrounding the brain, and data about their anatomical variations are sparse. OBJECTIVE: To describe and quantify anatomical variations of falx cerebri, tentorium cerebelli, and their notches. METHODS: 3D reconstruction of falx and tentorium was performed by points identification on 40 brain CT-scans in a tailored Matlab program. A scatter plot was obtained for each subject, and 8 anatomical landmarks were selected. A reference frame was defined to determine the coordinates of landmarks. Segments and areas were computed. A reproducibility study was done. RESULTS: The height of falx was 34.9 ± 3.9 mm and its surface area 56.5 ± 7.7 cm2. The width of tentorium was 99.64 ± 4.79 mm and its surface area 57.6 ± 5.8 cm2. The mean length, height, and surface area of falx notch were respectively 96.9 ± 8 mm, 41.8 ± 5.9 mm, and 28.8 ± 5.8 cm2 (range 15.8-40.5 cm2). The anterior and maximal widths of tentorial notch were 25.5 ± 3.5 mm and 30.9 ± 2.5 mm; its length 54.9 ± 5.2 mm and its surface area 13.26 ± 1.6 cm2. The length of falx notch correlated with the length of tentorial notch (r = 0.62, P < 0.05). CONCLUSION: We observe large anatomical variations of falx, tentorium, and notches, crucial to better understand the biomechanics of brain injury, in personalized finite element models.

Corrigendum: An Initial Passive Phase That Limits the Time to Recover and Emphasizes the Role of Proprioceptive Information.

[This corrects the article DOI: 10.3389/fneur.2018.00986.].

An Initial Passive Phase That Limits the Time to Recover and Emphasizes the Role of Proprioceptive Information.

In the present experiments, multiple balance perturbations were provided by unpredictable support-surface translations in various directions and velocities. The aim of this study was to distinguish the passive and the active phases during the pre-impact period of a fall. It was hypothesized that it should be feasible if one uses a specific quantitative kinematic analysis to evaluate the dispersion of the body segments trajectories across trials. Moreover, a multi-joint kinematical model was created for each subject, based on a new 3-D minimally invasive stereoradiographic X-ray images to assess subject-specific geometry and inertial parameters. The simulations allowed discriminating between the contributions of the passive (inertia-induced properties) and the active (neuromuscular response) components during falls. Our data show that there is limited time to adjust the way one fall from a standing position. We showed that the pre-impact period is truncated of 200 ms. During the initial part of a fall, the observed trajectory results from the interaction between the destabilizing external force and the body: inertial properties intrinsic to joints, ligaments and musculotendinous system have then a major contribution, as suggested for the regulation of static upright stance. This passive phase is later followed by an active phase, which consists of a corrective response to the postural perturbation. We believe that during a fall from standing height, it takes about 300 ms for postural responses to start correcting the body trajectory, while the impact is expected to occur around 700 ms. It has been argued that this time is sufficient to change the way one falls and that this makes it possible to apply safer ways of falling, for example by using martial arts fall techniques. Also, our results imply visual and vestibular information are not congruent with the beginning of the on-going fall. This consequence is to be noted as subjects prepare to the impact on the basis of sensory information, which would be uniquely mainly of proprioceptive origin at the fall onset. One limitation of the present analysis is that no EMG was included so far but these data are the subject of a future study.

Inconsistent anticipatory postural adjustments (APAs) in rugby players: a source of injuries?

BACKGROUND: We are developing since 2010 with Thales and the Fédération Française de Rugby (FFR) M-Rex, a new kind of rugby scrum simulator. The study questioned whether it could improve safety and protect players from injury by using it as a tool for training/coaching the packs. AIM: To explore the anticipatory postural adjustments (APAs) during the engagement of the ruck, because these predictive neck and back muscles contractions protect the spinal cord at the time of impacts, which is crucial to prevent injuries. METHODS: We quantified the kinematics and the EMG activities in high-level front row players during their initial engagement, when scrummaging with M-Rex. All studies were performed with one player interacting with the robot, at first, and then with the three players acting together. RESULTS: For most of the tested high-level players, the APA latencies were highly variable from trial to trial even though the engagement resulted in similar impacts. At time, the onset of the electromyography activity in the neck and back muscles showed latencies inferior to 50 ms or even close to zero prior to the impact, which rendered muscle contractions inefficient as APAs. We were also unable to identify clear muscular synergies underlying the APAs because of their great variability on a trial-to-trial basis. Finally, the APAs were not related to the amplitude of the ensuing impact and were asymmetric in most trials. All these characteristics held true, whether the player was playing alone or with two other frontline players. CONCLUSION: Our result suggest that APAs should be systematically tested in high-level rugby players as well as in any high-level sport men at risk of neck and back injuries. Because APAs can be efficiently trained, our study paves the way to design individual position-specific injury prevention programme.

A subject-specific biomechanical control model for the prediction of cervical spine muscle forces.

BACKGROUND: The aim of the present study is to propose a subject-specific biomechanical control model for the estimation of active cervical spine muscle forces. METHODS: The proprioception-based regulation model developed by Pomero et al. (2004) for the lumbar spine was adapted to the cervical spine. The model assumption is that the control strategy drives muscular activation to maintain the spinal joint load below the physiological threshold, thus avoiding excessive intervertebral displacements. Model evaluation was based on the comparison with the results of two reference studies. The effect of the uncertainty on the main model input parameters on the predicted force pattern was assessed. The feasibility of building this subject-specific model was illustrated with a case study of one subject. FINDINGS: The model muscle force predictions, although independent from EMG recordings, were consistent with the available literature, with mean differences of 20%. Spinal loads generally remained below the physiological thresholds. Moreover, the model behavior was found robust against the uncertainty on the muscle orientation, with a maximum coefficient of variation (CV) of 10%. INTERPRETATION: After full validation, this model should offer a relevant and efficient tool for the biomechanical and clinical study of the cervical spine, which might improve the understanding of cervical spine disorders.

Collaborative sensorimotor intelligence: the scrum as a model.

AIM: Using M-Rex, a rugby scrum simulator, we developed tools to describe scrummaging forces and to prevent accident. METHODS: We tested three groups of frontliners at national level. The simulator was passive or responded to the player(s) to simulate the reaction of opposite players. Sensors in the beam measured the force exerted by each of the players. Their movements were recorded with a Codamotion system. RESULTS: The force signals exhibited two phases: a transient phase, similar to a damped sinusoid with a dominant frequency around 5 Hz when the players scrummaged alone and with a wider range when playing together; then, a sustained phase could be decomposed in two components: a DC component remained stable whether frontliners played alone or together. In contrast, its variability decreased when the frontliners played together compared with when they played alone. As for the oscillations, the frontliners exhibited a large variability in their ability to synchronise their efforts during the sustained phase. The synchronisation between the hooker and the props was quite efficient, while it was always missing between two props. Finally, we were able to study postural readjustments and their synchronisation among players during the sustained phase. CONCLUSION: This study shows that by using adequate methods, it is possible to assess the frontline collective intelligence. These findings may pave the way for innovative methods of training to improve players' collective behaviour.

An Attempt of Early Detection of Poor Outcome after Whiplash.

The main concern with whiplash is that a large proportion of whiplash patients experience disabling symptoms or whiplash-associated disorders (WAD) for months if not years following the accident. Therefore, identifying early prognostic factors of WAD development is important as WAD have widespread clinical and economic consequences. In order to tackle that question, our study was specifically aimed at combining several methods of investigation in the same WAD patients at the acute stage and 6 months later. Our longitudinal, open, prospective, multi-center study included 38 whiplash patients, and 13 healthy volunteers matched for age, gender, and socio-economic status with the whiplash group. Whiplash patients were evaluated 15-21 days after road accident, and 6 months later. At each appointment, patients underwent a neuropsychological evaluation, a full clinical neurological examination, neurophysiological and postural tests, oto-neurological tests, cervical spine cord magnetic resonance imaging (MRI) with tractography (DTI). At 6 months, whiplash patients were categorized into two subgroups based on the results of the Diagnostic and Statistical Manual of Mental Disorders as having either favorable or unfavorable progression [an unfavorable classification corresponding to the presence of post-concussion symptom (PCS)] and we searched retrospectively for early prognostic factors of WAD predicting the passage to chronicity. We found that patients displaying high level of catastrophizing at the acute stage and/or post-traumatic stress disorder associated with either abnormalities in head or trunk kinematics, abnormal test of the otolithic function and at the Equitest or a combination of these syndromes, turned to chronicity. This study suggests that low-grade whiplash patients should be submitted as early as possible after the trauma to neuropsychological and motor control tests in a specialized consultation. In addition, they should be evaluated by a neuro-otologist for a detailed examination of vestibular functions, which should include cervical vestibular evoked myogenic potential. Then, if diagnosed at risk of WAD, these patients should be subjected to an intensive preventive rehabilitation program, including vestibular rehabilitation if required.

Non-invasive assessment of human multifidus muscle stiffness using ultrasound shear wave elastography: A feasibility study.

There is a lack of numeric data for the mechanical characterization of spine muscles, especially in vivo data. The multifidus muscle is a major muscle for the stabilization of the spine and may be involved in the pathogenesis of chronic low back pain (LBP). Supersonic shear wave elastography (SWE) has not yet been used on back muscles. The purpose of this prospective study is to assess the feasibility of ultrasound SWE to measure the elastic modulus of lumbar multifidus muscle in a passive stretching posture and at rest with a repeatable and reproducible method. A total of 10 asymptotic subjects (aged 25.5 ± 2.2 years) participated, 4 females and 6 males. Three operators performed 6 measurements for each of the 2 postures on the right multifidus muscle at vertebral levels L2-L3 and L4-L5. Repeatability and reproducibility have been assessed according to ISO 5725 standard. Intra-class correlation coefficients (ICC) for intra- and inter-observer reliability were rated as both excellent [ICC=0.99 and ICC=0.95, respectively]. Reproducibility was 11% at L2-L3 level and 19% at L4-L5. In the passive stretching posture, shear modulus was significantly higher than at rest (µ < 0.05). This preliminary work enabled to validate the feasibility of measuring the shear modulus of the multifidus muscle with SWE. This kind of measurement could be easily introduces into clinical routine like for the medical follow-up of chronic LBP or scoliosis treatments.

Kinetic DTI of the cervical spine: diffusivity changes in healthy subjects.

INTRODUCTION: The study aims to assess the influence of neck extension on water diffusivity within the cervical spinal cord. METHODS: IRB approved the study in 22 healthy volunteers. All subjects underwent anatomical MR and diffusion tensor imaging (DTI) at 1.5 T. The cervical cord was imaged in neutral (standard) position and extension. Segmental vertebral rotations were analyzed on sagittal T2-weighted images using the SpineView® software. Spinal cord diffusivity was measured in cross-sectional regions of interests at multiple levels (C1-C5). RESULTS: As a result of non-adapted coil geometry for spinal extension, 10 subjects had to be excluded. Image quality of the remaining 12 subjects was good without any deteriorating artifacts. Quantitative measurements of vertebral rotation angles and diffusion parameters showed good intra-rater reliability (ICC = 0.84-0.99). DTI during neck extension revealed significantly decreased fractional anisotropy (FA) and increased radial diffusivity (RD) at the C3 level and increased apparent diffusion coefficients (ADC) at the C3 and C4 levels (p < 0.01 Bonferroni corrected). The C3/C4 level corresponded to the maximal absolute change in segmental vertebral rotation between the two positions. The increase in RD correlated positively with the degree of global extension, i.e., the summed vertebral rotation angle between C1 and C5 (R = 0.77, p = 0.006). CONCLUSION: Our preliminary results suggest that DTI can quantify changes in water diffusivity during cervical spine extension. The maximal differences in segmental vertebral rotation corresponded to the levels with significant changes in diffusivity (C3/C4). Consequently, kinetic DTI measurements may open new perspectives in the assessment of neural tissue under biomechanical constraints.

Experimental characterization of post rigor mortis human muscle subjected to small tensile strains and application of a simple hyper-viscoelastic model.

In models developed for impact biomechanics, muscles are usually represented with one-dimensional elements having active and passive properties. The passive properties of muscles are most often obtained from experiments performed on animal muscles, because limited data on human muscle are available. The aim of this study is thus to characterize the passive response of a human muscle in tension. Tensile tests at different strain rates (0.0045, 0.045, and 0.45 s⁻¹) were performed on 10 extensor carpi ulnaris muscles. A model composed of a nonlinear element defined with an exponential law in parallel with one or two Maxwell elements and considering basic geometrical features was proposed. The experimental results were used to identify the parameters of the model. The results for the first- and second-order model were similar. For the first-order model, the mean parameters of the exponential law are as follows: Young's modulus E (6.8 MPa) and curvature parameter α (31.6). The Maxwell element mean values are as follows: viscosity parameter η (1.2 MPa s) and relaxation time τ (0.25 s). Our results provide new data on a human muscle tested in vitro and a simple model with basic geometrical features that represent its behavior in tension under three different strain rates. This approach could be used to assess the behavior of other human muscles.

Study on cervical muscle volume by means of three-dimensional reconstruction.

PURPOSE: To quantify the cervical muscle volume variation by means of three-dimensional reconstruction from MRI images. MATERIALS AND METHODS: Sixteen subjects were scanned using a Philips MRI scanner, including 11 men and 5 women, aged from 23 to 33 years, weighting between 49-80 kg. The deformation of a parametric specific object method was used to develop three-dimensional muscle models from contours on a small number of MRI images. Six subjects were reconstructed by two observers for evaluating the reliability by means of intraclass correlation coefficient (ICC). The results were also compared with in vivo measurement on a single specimen from a reference literature. The difference in left and right muscles volumes was assessed with a paired Wilcoxon signed rank test. RESULTS: The results showed good reliability by means of ICC study and were consistent with the in vivo specimen measurements. The left and right paired muscle volumes showed no significant difference. Interindividual variance was large that could reach 364 cm(3) , but the ratio of a given muscle volume to the total volume was less variable, always lower than 13%. The maximum cross sectional areas of cervical muscles varied greatly between individuals and the maximum values were mostly found at the C6-C7 level. CONCLUSION: This study provides initial results which could be used as reference data for clinical evaluation and biomechanical model development.