Evaluation of a method to scale muscle strength for gait simulations of children with cerebral palsy

Cerebral palsy (CP) is a neurological disorder that results in life-long mobility impairments. Musculoskeletal models used to investigate mobility deficits for children with CP often lack subject-specific characteristics such as altered muscle strength, despite a high prevalence of muscle weakness in this population. We hypothesized that incorporating subject-specific strength scaling within musculoskeletal models of children with CP would improve accuracy of muscle excitation predictions in walking simulations. Ten children (13.5 ± 3.3 years; GMFCS level II) with spastic CP participated in a gait analysis session where lower-limb kinematics, ground reaction forces, and bilateral electromyography (EMG) of five lower-limb muscles were collected. Isometric strength was measured for each child using handheld dynamometry. Three musculoskeletal models were generated for each child including a ‘Default’ model with the generic musculoskeletal model’s muscle strength, a ‘Uniform’ model with muscle strength scaled allometrically, and a ‘Custom’ model with muscle strength scaled based on handheld dynamometry strength measures. Muscle-driven gait simulations were generated using each model for each child. Simulation accuracy was evaluated by comparing predicted muscle excitations and measured EMG signals, both in the duration of muscle activity and the root-mean-square difference (RMSD) between signals. Improved agreement with EMG were found in both the ‘Custom’ and ‘Uniform’ models compared to the ‘Default’ model indicated by improvement in RMSD summed across all muscles, as well as RMSD and duration of activity for individual muscles. Incorporating strength scaling into musculoskeletal models can improve the accuracy of walking simulations for children with CP.     

Subject-specific hip geometry and hip joint centre location affects calculated contact forces at the hip during gait

Hip loading affects the development of hip osteoarthritis, bone remodelling and osseointegration of implants. In this study, we analyzed the effect of subject-specific modelling of hip geometry and hip joint centre (HJC) location on the quantification of hip joint moments, muscle moments and hip contact forces during gait, using musculoskeletal modelling, inverse dynamic analysis and static optimization. For 10 subjects, hip joint moments, muscle moments and hip loading in terms of magnitude and orientation were quantified using three different model types, each including a different amount of subject-specific detail: (1) a generic scaled musculoskeletal model, (2) a generic scaled musculoskeletal model with subject-specific hip geometry (femoral anteversion, neck-length and neck-shaft angle) and (3) a generic scaled musculoskeletal model with subject-specific hip geometry including HJC location. Subject-specific geometry and HJC location were derived from CT. Significant differences were found between the three model types in HJC location, hip flexion–extension moment and inclination angle of the total contact force in the frontal plane. No model agreement was found between the three model types for the calculation of contact forces in terms of magnitude and orientations, and muscle moments. Therefore, we suggest that personalized models with individualized hip joint geometry and HJC location should be used for the quantification of hip loading. For biomechanical analyses aiming to understand modified hip joint loading, and planning hip surgery in patients with osteoarthritis, the amount of subject-specific detail, related to bone geometry and joint centre location in the musculoskeletal models used, needs to be considered.     

Level of subject-specific detail in musculoskeletal models affects hip moment arm length calculation during gait in pediatric subjects with increased femoral anteversion

Biomechanical parameters of gait such as muscle's moment arm length (MAL) and muscle-tendon length are known to be sensitive to anatomical variability. Nevertheless, most studies rely on rescaled generic models (RGMo) constructed from averaged data of cadaveric measurements in a healthy adult population. As an alternative, deformable generic models (DGMo) have been proposed. These models integrate a higher level of subject-specific detail by applying characteristic deformations to the musculoskeletal geometry. In contrast, musculoskeletal models based on magnetic resonance (MR) images (MRMo) reflect the involved subject's characteristics in every level of the model. This study investigated the effect of the varying levels of subject-specific detail in these three model types on the calculated hip MAL during gait in a pediatric population of seven cerebral palsy subjects presenting aberrant femoral geometry. Our results show large percentage differences in calculated MAL between RGMo and MRMo. Furthermore, the use of DGMo did not uniformly reduce inter-model differences in calculated MAL. The magnitude of these percentage differences stresses the need to take these effects into account when selecting the level of subject-specific detail one wants to integrate in musculoskeletal. Furthermore, the variability of these differences between subjects and between muscles makes it very difficult to a priori estimate their importance for a biomechanical analysis of a certain muscle in a given subject.     

Subject-specific tendon-aponeurosis definition in hill-type model predicts higher muscle forces in dynamic tasks

Neuromusculoskeletal models are a common method to estimate muscle forces. Developing accurate neuromusculoskeletal models is a challenging task due to the complexity of the system and large inter-subject variability. The estimation of muscles force is based on the mechanical properties of tendon-aponeurosis complex. Most neuromusculoskeletal models use a generic definition of the tendon-aponeurosis complex based on in vitro test, perhaps limiting their validity. Ultrasonography allows subject-specific estimates of the tendon-aponeurosis complex's mechanical properties. The aim of this study was to investigate the influence of subject-specific mechanical properties of the tendon-aponeurosis complex on a neuromusculoskeletal model of the ankle joint. Seven subjects performed isometric contractions from which the tendon-aponeurosis force-strain relationship was estimated. Hopping and running tasks were performed and muscle forces were estimated using subject-specific tendon-aponeurosis and generic tendon properties. Two ultrasound probes positioned over the muscle-tendon junction and the mid-belly were combined with motion capture to estimate the in vivo tendon and aponeurosis strain of the medial head of gastrocnemius muscle. The tendon-aponeurosis force-strain relationship was scaled for the other ankle muscles based on tendon and aponeurosis length of each muscle measured by ultrasonography. The EMG-driven model was calibrated twice - using the generic tendon definition and a subject-specific tendon-aponeurosis force-strain definition. The use of subject-specific tendon-aponeurosis definition leads to a higher muscle force estimate for the soleus muscle and the plantar-flexor group, and to a better model prediction of the ankle joint moment compared to the model estimate which used a generic definition. Furthermore, the subject-specific tendon-aponeurosis definition leads to a decoupling behaviour between the muscle fibre and muscle-tendon unit in agreement with previous experiments using ultrasonography. These results indicate the use of subject-specific tendon-aponeurosis definitions in a neuromusculoskeletal model produce better agreement with measured external loads and more physiological model behaviour.     

Ultrasound-based subject-specific parameters improve fascicle behaviour estimation in Hill-type muscle model

The estimation of muscle fascicle behaviour is decisive in a Hill-type model as they are related to muscle force by the force–length–velocity relationship and the tendon force–strain relationship. This study was aimed at investigating the influence of subject-specific tendon force–strain relationship and initial fascicle geometry (IFG) on the estimation of muscle forces and fascicle behaviour during isometric contractions. Ultrasonography was used to estimate the in vivo muscle fascicle behaviour and compare the muscle fascicle length and pennation angle estimated from the Hill-type model. The calibration–prediction process of the electromyography-driven model was performed using generic or subject-specific tendon definition with or without IFG as constraint. The combination of subject-specific tendon definition and IFG led to muscle fascicle behaviour closer to ultrasound data and significant lower forces of the ankle dorsiflexor and plantarflexor muscles compared to the other conditions. Thus, subject-specific ultrasound measurements improve the accuracy of Hill-type models on muscle fascicle behaviour.     

Validation of subject-specific musculoskeletal models using the anatomical reachable 3-D workspace

A novel metric for the validation of musculoskeletal models is proposed, the reachable 3-D workspace (RWS). This new metric was used to compare a generic model scaled in a standard manner to a more subject-specific model. An experimental protocol for assessing the RWS was performed by ten participants for four distinct hand-payload cases. In addition, isometric individual strength measurements were collected for 12 different directions. The strength of subject-specific musculoskeletal models was then computed using the following assumptions: (1) standard routines including the length-mass-fat (LMF) scaling law; (2) the isometric strengths of the muscle elements were optimized to the individual strength measurements using joint strength factors (JSF). The RWS of each participant was subsequently estimated from each of the scaling approaches, LMF and JSF, for the four load cases. The experimental RWS showed that the volume and shape decreased with increasing hand-payload for every participant. The lateral and frontal far-from-torso aspects of the RWS were reduced the most. These trends were reproduced by both strength scaling approaches, but the LMF-scaled models were not able to track the overall RWS volume decrease with increasing payload, since they proved to be weaker than the participants. On the other hand, the optimised JSF subject-specific models performed better on the prediction of the RWS for all payload cases across participants. The RWS can potentially be further used as a subject-specific musculoskeletal model validation, enabling quantification of the volume and shape differences between experimentally and model-predicted RWSs.     

The non-linear response of a muscle in transverse compression: assessment of geometry influence using a finite element model

Most recent finite element models that represent muscles are generic or subject-specific models that use complex, constitutive laws. Identification of the parameters of such complex, constitutive laws could be an important limit for subject-specific approaches. The aim of this study was to assess the possibility of modelling muscle behaviour in compression with a parametric model and a simple, constitutive law. A quasi-static compression test was performed on the muscles of dogs. A parametric finite element model was designed using a linear, elastic, constitutive law. A multi-variate analysis was performed to assess the effects of geometry on muscle response. An inverse method was used to define Young's modulus. The non-linear response of the muscles was obtained using a subject-specific geometry and a linear elastic law. Thus, a simple muscle model can be used to have a bio-faithful, biomechanical response.     

Atlas-based non-rigid image registration to automatically define line-of-action muscle models: A validation study

Research has raised a growing concern about the accuracy of rescaled generic musculoskeletal models for estimating a subject's musculoskeletal geometry. Information extracted from magnetic resonance (MR) images can improve the subject-specific detail and accuracy of musculoskeletal models. Nevertheless, methods that allow efficient, automated definition of subject-specific muscular models for use in biomechanical analysis of gait have not yet been published to the best of our knowledge. We report a novel method for automated definition of subject-specific muscle paths using non-rigid image registration between an atlas image and the subject's MR images. We validated this approach quantitatively by measuring the distance between automatically and manually defined coordinates of muscle attachment sites. Data was collected for 34 muscles in each lower limb of 5 paediatric subjects diagnosed with diplegic cerebral palsy and presenting varying degrees of increased femoral anteversion. Distances showed an overall median Euclidean error of 6.1 mm: 2.0 mm along the medio-lateral direction, 1.8 mm along the anterior–posterior direction and 3.8 mm along the superior–inferior direction. A qualitative validation between automatically defined muscle points and the muscular geometry observed in the subject's medical image data corroborated the quantitative validation. This automated approach followed by visual inspection and, if needed, correction to the muscle paths, reduced the time required for defining 34 lower-limb muscle paths from around 3.5 to 1 h. Furthermore, the method was also applicable to aberrant skeletal geometry. Using the proposed method, defining MR-based musculoskeletal models becomes a time efficient and more accurate alternative to rescaling generic models.     

Effects of geometric individualisation of a human spine model on load sharing: neuro-musculoskeletal simulation reveals significant differences in ligament and muscle contribution

In spine research, two possibilities to generate models exist: generic (population-based) models representing the average human and subject-specific representations of individuals. Despite the increasing interest in subject specificity, individualisation of spine models remains challenging. Neuro-musculoskeletal (NMS) models enable the analysis and prediction of dynamic motions by incorporating active muscles attaching to bones that are connected using articulating joints under the assumption of rigid body dynamics. In this study, we used forward-dynamic simulations to compare a generic NMS multibody model of the thoracolumbar spine including fully articulated vertebrae, detailed musculature, passive ligaments and linear intervertebral disc (IVD) models with an individualised model to assess the contribution of individual biological structures. Individualisation was achieved by integrating skeletal geometry from computed tomography and custom-selected muscle and ligament paths. Both models underwent a gravitational settling process and a forward flexion-to-extension movement. The model-specific load distribution in an equilibrated upright position and local stiffness in the L4/5 functional spinal unit (FSU) is compared. Load sharing between occurring internal forces generated by individual biological structures and their contribution to the FSU stiffness was computed. The main finding of our simulations is an apparent shift in load sharing with individualisation from an equally distributed element contribution of IVD, ligaments and muscles in the generic spine model to a predominant muscle contribution in the individualised model depending on the analysed spine level.

     

Knee medial and lateral contact forces in a musculoskeletal model with subject-specific contact point trajectories

Contact point (CP) trajectory is a crucial parameter in estimating medial/lateral tibio-femoral contact forces from the musculoskeletal (MSK) models. The objective of the present study was to develop a method to incorporate the subject-specific CP trajectories into the MSK model. Ten healthy subjects performed 45 s treadmill gait trials. The subject-specific CP trajectories were constructed on the tibia and femur as a function of extension-flexion using low-dose bi-plane X-ray images during a quasi-static squat. At each extension-flexion position, the tibia and femur CPs were superimposed in the three directions on the medial side, and in the anterior-posterior and proximal-distal directions on the lateral side to form the five kinematic constraints of the knee joint. The Lagrange multipliers associated to these constraints directly yielded the medial/lateral contact forces. The results from the personalized CP trajectory model were compared against the linear CP trajectory and sphere-on-plane CP trajectory models which were adapted from the commonly used MSK models. Changing the CP trajectory had a remarkable impact on the knee kinematics and changed the medial and lateral contact forces by 1.03 BW and 0.65 BW respectively, in certain subjects. The direction and magnitude of the medial/lateral contact force were highly variable among the subjects and the medial-lateral shift of the CPs alone could not determine the increase/decrease pattern of the contact forces. The suggested kinematic constraints are adaptable to the CP trajectories derived from a variety of joint models and those experimentally measured from the 3D imaging techniques.     

Alterations of musculoskeletal models for a more accurate estimation of lower limb joint contact forces during normal gait: A systematic review

Musculoskeletal modelling is a methodology used to investigate joint contact forces during a movement. High accuracy in the estimation of the hip or knee joint contact forces can be obtained with subject-specific models. However, construction of subject-specific models remains time consuming and expensive. The purpose of this systematic review of the literature was to identify what alterations can be made on generic (i.e. literature-based, without any subject-specific measurement other than body size and weight) musculoskeletal models to obtain a better estimation of the joint contact forces. The impact of these alterations on the accuracy of the estimated joint contact forces were appraised.The systematic search yielded to 141 articles and 24 papers were included in the review. Different strategies of alterations were found: skeletal and joint model (e.g. number of degrees of freedom, knee alignment), muscle model (e.g. Hill-type muscle parameters, level of muscular redundancy), and optimisation problem (e.g. objective function, design variables, constraints). All these alterations had an impact on joint contact force accuracy, so demonstrating the potential for improving the model predictions without necessarily involving costly and time consuming medical images. However, due to discrepancies in the reported evidence about this impact and despite a high quality of the reviewed studies, it was not possible to highlight any trend defining which alteration had the largest impact.     

Modeling the contraction of the pelvic floor muscles

We performed numerical simulation of voluntary contraction of the pelvic floor muscles to evaluate the resulting displacements of the organs and muscles. Structures were segmented in Magnetic Resonance (MR) images. Different material properties and constitutive models were attributed. The Finite Element Method was applied, and displacements were compared with dynamic MRI findings. Numerical simulation showed muscle magnitude displacement ranging from 0 to 7.9 mm, more evident in the posterior area. Accordingly, the anorectum moved more than the uterus and bladder. Dynamic MRI showed less 0.2 mm and 4.1 mm muscle dislocation in the anterior and cranial directions, respectively. Applications of this model include evaluating muscle impairment, subject-specific mesh implant planning, or effectiveness of rehabilitation.     

Subject-specific musculoskeletal model of the lower limb in a lying and standing position

Accurate estimation of joint loads implies using subject-specific musculoskeletal models. Moreover, as the lines of action of the muscles are dictated by the soft tissues, which are in turn influenced by gravitational forces, we developed a method to build subject-specific models of the lower limb in a functional standing position. Bones and skin envelope were obtained in a standing position, whereas muscles and a set of bony landmarks were obtained from conventional magnetic resonance images in a lying position. These muscles were merged with the subject-specific skeletal model using a nonlinear transformation, taking into account soft tissue movements and gravitational effects. Seven asymptomatic lower limbs were modelled using this method, and results showed realistic deformations. Comparing the subject-specific skeletal model to a scaled reference model rendered differences in terms of muscle length up to 4% and in terms of moment arm for adductor muscles up to 30%. These preliminary findings enlightened the importance of subject-specific modelling in a functional position.     

Relation between subject-specific hip joint loading, stress distribution in the proximal femur and bone mineral density changes after total hip replacement

In the prediction of bone remodelling processes after total hip replacement (THR), modelling of the subject-specific geometry is now state-of-the-art. In this study, we demonstrate that inclusion of subject-specific loading conditions drastically influences the calculated stress distribution, and hence influences the correlation between calculated stress distributions and changes in bone mineral density (BMD) after THR.For two patients who received cementless THR, personalized finite element (FE) models of the proximal femur were generated representing the pre- and post-operative geometry. FE analyses were performed by imposing subject-specific three-dimensional hip joint contact forces as well as muscle forces calculated based on gait analysis data. Average values of the von Mises stress were calculated for relevant zones of the proximal femur. Subsequently, the load cases were interchanged and the effect on the stress distribution was evaluated. Finally, the subject-specific stress distribution was correlated to the changes in BMD at 3 and 6 months after THR.We found subject-specific differences in the stress distribution induced by specific loading conditions, as interchanging of the loading also interchanged the patterns of the stress distribution. The correlation between the calculated stress distribution and the changes in BMD were affected by the two-dimensional nature of the BMD measurement.Our results confirm the hypothesis that inclusion of subject-specific hip contact forces and muscle forces drastically influences the stress distribution in the proximal femur. In addition to patient-specific geometry, inclusion of patient-specific loading is, therefore, essential to obtain accurate input for the analysis of stress distribution after THR.     

Wrist tendon moment arms: Quantification by imaging and experimental techniques

Subject-specific musculoskeletal models require accurate values of muscle moment arms. The aim of this study was to compare moment arms of wrist tendons obtained from non-invasive magnetic resonance imaging (MRI) to those obtained from an in vitro experimental approach. MRI was performed on ten upper limb cadaveric specimens to obtain the centrelines for the flexor carpi radialis (FCR), flexor carpi ulnaris (FCU), extensor carpi radialis longus (ECRL), extensor carpi radialis brevis (ECRB), extensor carpi ulnaris (ECU), and abductor pollicis longus (APL) tendons. From these, the anatomical moment arms about each of the flexion-extension (FE) and radioulnar deviation (RUD) axes of the wrist were calculated. Specimens were mounted on a physiologic wrist simulator to obtain functional measurements of the moment arms using the tendon excursion method. No differences were observed between anatomical and functional values of the FE and RUD moment arms of FCR, ECRL and ECRB, and the RUD moment arm of ECU (p > .075). Scaling the anatomical moment arms relative to ECRB in FE and ECU in RUD reduced differences in the FE moment arm of FCU and the RUD moment arm of APL to less than 15% (p > .139). However, differences persisted in moment arms of FCU in RUD, and ECU and APL in FE (p < .008). This study shows that while measurements of moment arms of wrist tendons using imaging do not always conform to values obtained using in vitro experimental approaches, a stricter protocol could result in the acquisition of subject-specific moment arms to personalise musculoskeletal models.     

Muscle geometry affects accuracy of forearm volume determination by magnetic resonance imaging (MRI)

Upper extremity musculoskeletal modeling is becoming increasingly sophisticated, creating a growing need for subject-specific muscle size parameters. One method for determining subject-specific muscle volume is magnetic resonance imaging (MRI). The purpose of this study was to determine the validity of MRI-derived muscle volumes in the human forearm across a variety of muscle sizes and shapes. Seventeen cadaveric forearms were scanned using a fast-spoiled gradient echo pulse sequence with high isotropic spatial resolution (1mm(3) voxels) on a 3T MR system. Pronator teres (PT), extensor carpi radialis brevis (ECRB), extensor pollicis longus (EPL), flexor carpi ulnaris (FCU), and brachioradialis (BR) muscles were manually segmented allowing volume to be calculated. Forearms were then dissected, muscles isolated, and muscle masses obtained, which allowed computation of muscle volume. Intraclass correlation coefficients (ICC(2,1)) and absolute volume differences were used to compare measurement methods. There was excellent agreement between the anatomical and MRI-derived muscle volumes (ICC = 0.97, relative error = 12.8%) when all 43 muscles were considered together. When individual muscles were considered, there was excellent agreement between measurement methods for PT (ICC = 0.97, relative error = 8.4%), ECRB (ICC = 0.93, relative error = 7.7%), and FCU (ICC = 0.91, relative error = 9.8%), and fair agreement for EPL (ICC = 0.68, relative error = 21.6%) and BR (ICC = 0.93, relative error = 17.2%). Thus, while MRI-based measurements of muscle volume produce relatively small errors in some muscles, muscles with high surface area-to-volume ratios may predispose them to segmentation error, and, therefore, the accuracy of these measurements may be unacceptable.     

The influence of simulation model complexity on the estimation of internal loading in gymnastics landings

Evaluating landing technique using a computer simulation model of a gymnast and landing mat could be a useful tool when attempting to assess injury risk. The aims of this study were: (1) to investigate whether a subject-specific torque-driven or a subject-specific muscle-driven model of a gymnast is better at matching experimental ground reaction forces and kinematics during gymnastics landings, (2) to calculate their respective simulation run times and (3) to determine what level of model complexity is required to assess injury risk. A subject-specific planar seven-link wobbling mass model of a gymnast and a multi-layer model of a landing mat were developed for this study. Subject-specific strength parameters were determined which defined the maximum voluntary torque/angle/angular velocity relationship about each joint. This relationship was also used to produce subject-specific 'lumped' muscle models for each joint. Kinetic and kinematic data were obtained during landings from backward and forward rotating gymnastics vaults. Both torque-driven and muscle-driven models were capable of producing simulated landings that matched the actual performances (with overall percentage differences between 10.1% and 18.2%). The torque-driven model underestimated the internal loading on joints and bones, resulting in joint reaction forces that were less than 50% of those calculated using the muscle-driven model. Simulation time increased from approximately 3 min (torque driven) to more than 10 min (muscle driven) as model complexity increased. The selection of a simulation model for assessing injury risk must consider the need for determining realistic internal forces as the priority despite increases in simulation run time.     

Moving muscle points provide accurate curved muscle paths in a model of the cervical spine

Muscle paths in musculoskeletal models have been modeled using several different methods; however, deformation of soft tissue with changes in posture is rarely accounted for, and often only the neutral posture is used to define a muscle path. The objective of this study was to model curved muscle paths in the cervical spine that take into consideration soft tissue deformation with changes in neck posture. Two subject-specific models were created from magnetic resonance images (MRI) in 5 different sagittal plane neck postures. Curved paths of flexor and extensor muscles were modeled using piecewise linear lines-of-action in two ways; (1) using fixed via points determined from muscle paths in the neutral posture and (2) using moving muscle points that moved relative to the bones determined from muscle paths in all 5 postures. Accuracy of each curved modeled muscle path was evaluated by an error metric, the distance from the anatomic (centroid) muscle path determined from the MRI. Error metric was compared among three modeled muscle path types (straight, fixed via and moving muscle point) using a repeated measures one-way ANOVA (α=0.05). Moving muscle point paths had 21% lower error metric than fixed via point paths over all 15 pairs of neck muscles examined over 5 postures (3.86 mm vs. 4.88 mm). This study highlights the importance of defining muscle paths in multiple postures in order to properly define the changing curvature of a muscle path due to soft tissue deformation with posture.     

Subject-specific geometry affects acetabular contact pressure during gait more than subject-specific loading patterns

Abstract

Finite element modeling (FEM) can predict hip cartilage contact mechanics. This study investigated how subject-specific boundary conditions and joint geometry affect acetabular cartilage contact mechanics using a multi-scale workflow. For two healthy subjects, musculoskeletal models calculated subject-specific hip kinematics and loading, which were used as boundary conditions for FEM. Cartilage contact mechanics were predicted using either generic or subject-specific FEM and boundary conditions. A subject-specific mesh resulted in a more lateral contact. Effects of subject-specific boundary conditions varied between both subjects. Results highlight the complex interplay between loading and kinematics and their effect on cartilage contact mechanics.     

Subject-specific geometrical detail rather than cost function formulation affects hip loading calculation*

This study assessed the relative importance of introducing an increasing level of medical image-based subject-specific detail in bone and muscle geometry in the musculoskeletal model, on calculated hip contact forces during gait. These forces were compared to introducing minimization of hip contact forces in the optimization criterion. With an increasing level of subject-specific detail, specifically MRI-based geometry and wrapping surfaces representing the hip capsule, hip contact forces decreased and were more comparable to contact forces measured using instrumented prostheses (average difference of 0.69 BW at the first peak compared to 1.04 BW for the generic model). Inclusion of subject-specific wrapping surfaces in the model had a greater effect than altering the cost function definition.