A new framework for analysis of three-dimensional shape and architecture of human skeletal muscles from in vivo imaging data

A new framework is presented for comprehensive analysis of the three-dimensional shape and architecture of human skeletal muscles from magnetic resonance and diffusion tensor imaging data. The framework comprises three key features: 1) identification of points on the surface of and inside a muscle that have a correspondence to points on and inside another muscle, 2) reconstruction of average muscle shape and average muscle fiber orientations, and 3) utilization of data on between-muscle variation to visualize and make statistical inferences about changes or differences in muscle shape and architecture. The general use of the framework is demonstrated by its application to three case studies. Analysis of data obtained before and after 8 wk of strength training revealed there was little regional variation in hypertrophy of the vastus medialis and vastus lateralis and no systematic change in pennation angle. Analysis of passive muscle lengthening revealed heterogeneous changes in shape of the medial gastrocnemius and confirmed the ability of the methods to detect subtle changes in muscle fiber orientation. Analysis of the medial gastrocnemius of children with unilateral cerebral palsy showed that muscles in the more-affected limb were shorter, thinner, and less wide than muscles in the less-affected limb and had slightly more pennate muscle fibers in the central and proximal part of the muscle. Among other applications, the framework can be used to explore the mechanics of muscle contraction, investigate adaptations of muscle architecture, build anatomically realistic computational models of skeletal muscles, and compare muscle shape and architecture between species. NEW &amp; NOTEWORTHY Muscle architecture is conventionally measured using simple scalar metrics such as muscle volume and average fascicle lengths. Here, a new framework is proposed for analysis of complex changes in three-dimensional architecture of whole human muscles from magnetic resonance and diffusion tensor imaging data. The general use of the framework is demonstrated through visualization, quantification, and statistical analysis of the effect of strength training, passive lengthening and cerebral palsy on three-dimensional muscle shape and architecture.</p

Transformation methods for estimation of subject-specific scapular muscle attachment sites

The parameters that describe the soft tissue structures are among the most important anatomical parameters for subject-specific biomechanical modelling. In this paper, we study one of the soft tissue parameters, namely muscle attachment sites. Two new methods are proposed for transformation of the muscle attachment sites of any reference scapula to any destination scapula based on four palpable bony landmarks. The proposed methods as well as one previously proposed method have been applied for transformation of muscle attachment sites of one reference scapula to seven other scapulae. The transformation errors are compared among the three methods. Both proposed methods yield significantly less (p < 0.05) prediction error as compared to the currently available method. Furthermore, we investigate whether there exists a reference scapula that performs significantly better than other scapulae when used for transformation of muscle attachment sites. Seven different scapulae were used as reference scapula and their resulting transformation errors were compared with each other. In the considered statistical population, no such a thing as an ideal scapula was found. There was, however, one outlier scapula that performed significantly worse than the other scapulae when used as a reference. The effect of perturbations in both muscle attachment sites and other muscle properties is studied by comparing muscle force predictions of a musculoskeletal model between perturbed and non-perturbed versions of the model. It is found that 10 mm variations in muscle attachments have more significant effect on muscle force predictions than 10% variations in any of the other four analysed muscle properties.</p

Architecture of the medial gastrocnemius muscle in people who have had a stroke: A diffusion tensor imaging investigation

People who have had a stroke often develop ankle contractures which may be caused by changes in architecture of calf muscles. Anatomically constrained diffusion tensor imaging has recently been used to make three-dimensional, whole-muscle measurements of muscle architecture. Here, we compared the architecture of the medial gastrocnemius muscle in the paretic and non-paretic sides of people who have had a hemiparetic stroke and control participants using novel imaging techniques. Methods: MRI techniques (diffusion tensor imaging and mDixon imaging) were used to obtain muscle volume, fascicle length, pennation angle, physiological cross-sectional area and curvature in 14 stroke patients (mean age 60 SD 13 years) and 18 control participants (mean age 66 SD 12 years). Findings: On average, the ankle on the paretic side had 11° (95% confidence interval 8 to 13°) less dorsiflexion range than on the non-paretic side, and 6° (1 to 13°) less dorsiflexion range than ankles of control participants. The medial gastrocnemius muscles on the paretic side were, on average, 15% (35.2 cm3, 95% confidence interval 5.2 to 65.2 cm3) smaller in volume than the muscles on the non-paretic side, and 16% (36.9 cm3, 95% confidence interval 3.1 to 70.6 cm3) smaller than in control participants. No statistically significant differences between paretic, non-paretic and control muscles were detected for fascicle length, pennation angle, physiological cross-sectional area or curvature. Conclusions: People with hemiparetic stroke and reduced range of motion have, on average, a smaller medial gastrocnemius muscle on the paretic side than on the non-paretic side. Other muscle architectural parameters appear unchanged.</p

Reliability and robustness of muscle architecture measurements obtained using diffusion tensor imaging with anatomically constrained tractography

For detailed analyses of muscle adaptation mechanisms during growth, ageing or disease, reliable measurements of muscle architecture are required. Diffusion tensor imaging (DTI) and DTI tractography have been used to reconstruct the architecture of human muscles in vivo. However, muscle architecture measurements reconstructed with conventional DTI techniques are often anatomically implausible because the reconstructed fascicles do not terminate on aponeuroses, as real muscle fascicles are known to do. In this study, we tested the reliability of an anatomically constrained DTI-based method for measuring three-dimensional muscle architecture. Anatomical magnetic resonance images and diffusion tensor images were obtained from the left legs of eight healthy participants on two occasions one week apart. Muscle volumes, fascicle lengths, pennation angles and fascicle curvatures were measured in the medial and lateral gastrocnemius, soleus and the tibialis anterior muscles. Averaged across muscles, the intraclass correlation coefficient was 0.99 for muscle volume, 0.81 for fascicle length, 0.73 for pennation angle and 0.76 for fascicle curvature. Measurements of muscle architecture obtained using conventional DTI tractography were highly sensitive to variations in the stopping criteria for DTI tractography. The application of anatomical constraints reduced this sensitivity significantly. This study demonstrates that anatomically constrained DTI tractography can provide reliable and robust three-dimensional measurements of whole-muscle architecture. The algorithms used to constrain tractography have been made publicly available.</p

Intramuscular Fat in the Medial Gastrocnemius Muscle of People Who Have Had a Stroke

Objective: To compare intramuscular fat fraction in people who have ankle contractures following stroke with the intramuscular fat fraction in control participants. Design: mDixon MRI images were used to quantify intramuscular fat fractions in the medial gastrocnemius muscles of people who had experienced a hemiparetic stroke (n = 14, mean age 60 ± 13 years) and control participants (n = 18, mean age 66 ± 12 years). Results: Intramuscular fat fractions were similar in the paretic and non-paretic sides of stroke patients (mean on paretic side 14.5%, non-paretic side 12.8%, difference 1.6%, 95% confidence interval −0.7 to 4.1%). The intramuscular fat fraction on the paretic side was higher than in the control group (mean intramuscular fat fraction in control muscles 7.6%; difference 7.8%, 95% confidence interval 4.6–10.9%). The difference between intramuscular fat fractions in non-paretic and control legs increased with age. Body mass index was similar in stroke patients and controls. There was no association between medial gastrocnemius intramuscular fat fraction and dorsiflexion range. Conclusion: Muscles of stroke patients had elevated intramuscular fat fractions compared to muscles from control participants which were not explained by differences in body mass index. There is no clear relationship between intramuscular fat in the medial gastrocnemius muscle and dorsiflexion range of motion.</p

Clinical applications of musculoskeletal modelling for the shoulder and upper limb

Musculoskeletal models have been developed to estimate internal loading on the human skeleton, which cannot directly be measured in vivo, from external measurements like kinematics and external forces. Such models of the shoulder and upper extremity have been used for a variety of purposes, ranging from understanding basic shoulder biomechanics to assisting in preoperative planning. In this review, we provide an overview of the most commonly used large-scale shoulder and upper extremity models and categorise the applications of these models according to the type of questions their users aimed to answer. We found that the most explored feature of a model is the possibility to predict the effect of a structural adaptation on functional outcome, for instance, to simulate a tendon transfer preoperatively. Recent studies have focused on minimising the mismatch in morphology between the model, often derived from cadaver studies, and the subject that is analysed. However, only a subset of the parameters that describe the model's geometry and, perhaps most importantly, the musculotendon properties can be obtained in vivo. Because most parameters are somehow interrelated, the others should be scaled to prevent inconsistencies in the model's structure, but it is not known exactly how. Although considerable effort is put into adding complexity to models, for example, by making them subject-specific, we have found little evidence of their superiority over current models. The current trend in development towards individualised, more complex models needs to be justified by demonstrating their ability to answer questions that cannot already be answered by existing models.</p

Contemporary image-based methods for measuring passive mechanical properties of skeletal muscles in vivo

Bilston LE, Bolsterlee B, Nordez A, Sinha S. Contemporary image-based methods for measuring passive mechanical properties of skeletal muscles in vivo. J Appl Physiol 126: 1454 –1464, 2019. First published September 20, 2018; doi:10.1152/japplphysiol.00672.2018.—Skeletal muscles’ primary function in the body is mechanical: to move and stabilize the skeleton. As such, their mechanical behavior is a key aspect of their physiology. Recent developments in medical imaging technology have enabled quantitative studies of passive muscle mechanics, ranging from measurements of intrinsic muscle mechanical properties, such as elasticity and viscosity, to three-dimensional muscle architecture and dynamic muscle deformation and kinematics. In this review we summarize the principles and applications of contemporary imaging methods that have been used to study the passive mechanical behavior of skeletal muscles. Elastography measurements can provide in vivo maps of passive muscle mechanical parameters, and both MRI and ultrasound methods are available (magnetic resonance elastography and ultrasound shear wave elastography, respectively). Both have been shown to differentiate between healthy muscle and muscles affected by a broad range of clinical conditions. Detailed muscle architecture can now be depicted using diffusion tensor imaging, which not only is particularly useful for computational modeling of muscle but also has potential in assessing architectural changes in muscle disorders. More dynamic information about muscle mechanics can be obtained using a range of dynamic MRI methods, which characterize the detailed internal muscle deformations during motion. There are several MRI techniques available (e.g., phase-contrast MRI, displacement-encoded MRI, and “tagged” MRI), each of which can be collected in synchrony with muscle motion and postprocessed to quantify muscle deformation. Together, these modern imaging techniques can characterize muscle motion, deformation, mechanical properties, and architecture, providing complementary insights into skeletal muscle function.</p

Muscle architecture in children with cerebral palsy and ankle contractures: an investigation using diffusion tensor imaging

Background: Children with cerebral palsy frequently have ankle contractures which may be caused by changes in architecture of calf muscles. Here, we compared the architecture of medial gastrocnemius muscles in children with unilateral cerebral palsy and typically developing children using novel imaging techniques. Methods and procedures: Muscle volumes, fascicle lengths, pennation angles and physiological cross-sectional areas were measured from diffusion tensor images and mDixon scans obtained from 20 ambulant children with unilateral spastic cerebral palsy who had ankle contractures (age 11 ± 3 years; mean ± standard deviation) and 20 typically developing children (11 ± 4 years). Findings: In children with cerebral palsy, the more-affected side had, on average, 13° less dorsiflexion range and the medial gastrocnemius muscle had 4.9 mm shorter fascicles, 50 cm3 smaller volume and 9.5 cm2 smaller physiological cross-sectional area than the less-affected side. Compared to typically developing children, the more-affected side had 10° less dorsiflexion range and the medial gastrocnemius muscle had 4.2 mm shorter fascicles, 51 cm3 smaller volume and 10 cm2 smaller physiological cross-sectional area. We did not detect differences between the less-affected and typically developing legs. Interpretation: Three-dimensional measurement of whole medial gastrocnemius muscles confirmed that the architecture of muscles on the more-affected side of children with cerebral palsy differs from the less-affected side and from muscles of typically developing children. Reductions in fascicle length, muscle volume and physiological cross-sectional area may contribute to muscle contracture.</p

Three-dimensional architecture of the human subscapularis muscle in vivo

Detailed analysis of skeletal muscle architecture provides insights into skeletal muscle function. To date, measurements of the human subscapularis architecture have been limited to cadaveric measurements. In this study we demonstrate the feasibility of using anatomically constrained fibre tractography to reconstruct and quantify the 3D architecture of the human subscapularis muscle, and provide the first quantitative measurements of the architecture of the human subscapularis muscle in vivo. mDixon and diffusion tensor magnetic resonance images were obtained from the right shoulders of 20 healthy young adults. Anatomically constrained fibre tractography, in which fascicle reconstructions were forced to terminate on the internal aponeurosis of the subscapularis, was used to reconstruct muscle fibre architecture of the subscapularis muscles. Qualitatively, architectural reconstructions resembled the known subscapularis anatomy well, demonstrating face validity of the reconstructions. Muscle architectural parameters (means ± SDs) were: muscle volume 138 ± 42 cm3, fascicle length 63.6 ± 5.9 mm, physiological cross-sectional area (PCSA) 22 ± 6 cm2, and pennation angle 16 ± 2°. Architectural measurements of the subscapularis fell within the range reported in cadaver studies and were relatively insensitive to variations in fibre tractography parameters. The anatomically detailed whole-muscle reconstructions can be used to quantify the effects of joint surgery on muscle architecture and to advance computational models of the human shoulder.</p

Intramuscular fat in children with unilateral cerebral palsy

Background: Many children with cerebral palsy develop muscle contractures. The mechanisms of contracture are not well understood. We investigated the possibility that, because fat is stiffer than passive muscle, elevated intramuscular fat contributes to contracture. In this cross-sectional study, we compared the quantity and distribution of intramuscular fat in muscles from typically developing children and children with cerebral palsy who have contractures. Methods: mDixon magnetic resonance images were obtained from the legs of 20 ambulant children with unilateral spastic cerebral palsy who had ankle contractures (mean age 11 SD 3 years, 13 male, mean moderate level contracture) and 20 typically developing children (mean age 11 SD 4 years, 13 male). The images were analyzed to quantify the intramuscular fat fraction of the medial gastrocnemius muscles. The amount and distribution of intramuscular fat were compared between muscles of children with cerebral palsy and typically developing children. Findings: In typically developing children, the medial gastrocnemius muscles had a mean intramuscular fat fraction of 4.7% (SD 1.6%). In children with cerebral palsy, the mean intramuscular fat fractions in the more- and less-affected medial gastrocnemius muscle were 11.4% (8.1%) and 6.9% (3.4%) respectively. There were small but statistically significant regional differences in the distribution of intramuscular fat. There was no evidence of a relationship between intramuscular fat fraction and severity of contracture. Interpretation: Children with cerebral palsy have higher proportions of intramuscular fat than typically developing children. There is no clear relationship between intramuscular fat fraction and dorsiflexion range of motion in children with cerebral palsy.</p