Is the tendon embryogenesis process resurrected during tendon healing?

The process of embryonic tendon development, including the nature and purpose of collagen fibril segments, is reviewed. It is proposed that tendon fibrillogenesis of repair is related to the fibrillogenesis of tendon embryonic development. The assembly of collagen fibril segment units into longer fibers occurs on the surface of tendon fibroblasts in embryonic tendon development. The biochemist's view of tendon healing, whereby the spontaneous polymerization of tropocollagen monomers regenerates lost tendon collagen fibers, needs to be reconsidered. Furthermore, the importance of direct fibroblast involvement in collagen fiber reassembly during tendon healing needs to be studied in tendon intrinsic regenerative repair.     

Is phylogeny driving tendon length in lizards?

Tulli, M.J., Herrel, A., Vanhooydonck, B. and Abdala, V. 2012. Is phylogeny driving tendon length in lizards?—Acta Zoologica (Stockholm) 93 : 319–329. Tendons transmit tensile forces generated by muscles and are a crucial part of the musculoskeletal system in vertebrates. Because tendons and tendon cells respond to altered mechanical load by increasing collagen synthesis, we hypothesized that a correlation between tendon morphology and the loading regime imposed by locomotor style or habitat use exists. This makes tendons an interesting model for studying the relationship between morphology and environment. In this study, we compare the general morphology of the palmar flexor plate, the length of the digital tendons, and the length of the flexor carpi ulnaris tendon in species of lizards that exploit a variety of structural habitats. The results from statistical analyses show that phylogenetic relatedness has a major impact on our ability to detect differences between habitat groups, and no differences in tendon length could be detected between iguanian species occupying different habitats when taking into account the relatedness between species. Our data for lizards diverge from the general mammalian paradigm where variation in tendon is often associated with habitat use or locomotor style.     

Should tendon and aponeurosis be considered in series?

Fibres, aponeuroses, and tendons are often considered mechanically "in series" in skeletal muscles. This notion has led to oversimplified calculations of fibre forces from tendon forces, to incorrect derivations of constitutive laws for aponeuroses, and to misinterpretations of the recovery of elastic energy in stretch-shortening cycles of muscles. Here, we demonstrate theoretically, using examples of increasing complexity, that tendon and aponeurosis are not in series in a muscle fibre-aponeurosis-tendon complex. We then demonstrate that assuming the tendon and aponeurosis to be in series can lead to the appearance of mechanical work creation in these passive viscoelastic structures, a result that is mechanically impossible. Finally, we explain the mechanical role of the incompressible muscle matrix in force transmission from fibres to aponeuroses and tendon, and emphasize that incompressibility necessitates the introduction of extra forces necessary to maintain this constraint. Unfortunately, this requirement eliminates, for all but the simplest cases, a theoretical approach of muscle modeling based on intuitive free-body diagrams.     

ISOFIT: a model-based method to measure muscle–tendon properties simultaneously

Summary Estimation of muscle parameters specifying force–length and force–velocity behavior requires in general a large number of sophisticated experiments often including a combination of isometric, isokinetic, isotonic, and quick-release experiments. This study validates a simpler method (ISOFIT) to determine muscle properties by fitting a Hill-type muscle model to a set of isovelocity data. Muscle properties resulting from the ISOFIT method agreed well with muscle properties determined separately in in vitro measurements using frog semitendinosus muscles. The force–length curve was described well by the results of the model. The force–velocity curve resulting from the model coincided with the experimentally determined curve above approximately 20% of maximum isometric force (correlation coefficient R>0.99). At lower forces and thus higher velocities the predicted curve underestimated velocity. The stiffness of the series elastic component determined with direct experiments was approximately 10% lower than that determined by the ISOFIT method. Use of the ISOFIT method can decrease experimental time up to 80% and reduce potential changes in muscle parameters due to fatigue.     

Identity of tendon stem cells – how much do we know?

Tendon stem cells are multi‐potent adult stem cells with broad differentiation plasticity that render them of great importance in cell‐based therapies for the repair of tendons. We called them tendon‐derived stem cells (TDSCs) to indicate the tissue origin from which the stem cells were isolated in vitro. Based on the work of other sources of MSCs and specific work on TDSCs, some properties of TDSCs have been characterized / implicated in vitro. Despite these findings, tendon stem cells remained controversial cells. This was because MSCs residing in different organs, although very similar, were not identical cells. There is evidence of differences in stem cell‐related properties and functions related to tissue origins. Similar to other stem cells, tendon stem cells were identified and characterized in vitro. Their in vivo identities, niche (both anatomical locations and regulators) and roles in tendons were less understood. This review aims to summarize the current evidence of the possible anatomical locations and niche signals regulating the functions of tendon stem cells in vivo. The possible roles of tendon stem cells in tendon healing and non‐healing are presented. Finally, the potential strategies for understanding the in vivo identity of tendon stem cells are discussed.     

Can the patellar tendon moment arm be predicted from anthropometric measurements?

The purpose of this study was to examine the relations between patellar tendon moment arm length and several relevant anthropometric characteristics of 22 healthy men. The patellar tendon moment arm length was measured using magnetic resonance imaging with two different methods: (1) measurement of patellar tendon moment arm length (d(PT)) with respect to the tibiofemoral contact point (d(PTCP)) and (2) measurement of d(PT) with respect to the intersection point of the anterior and posterior cruciate ligament (d(PTIP)). Pearson correlation coefficients and a stepwise linear regression analysis were used to examine the relationships between the d(PT) and anthropometric measurements taken. Furthermore, a Student's t-test was used to determine differences between the d(PTCP) and d(PTIP) values. Only knee circumference was a significant d(PTCP) predictor (P < 0.05) but with a very low R2 (0.139). None of the anthropometric parameters examined was found to be a significant d(PTIP) predictor. The correlation coefficients ranged from -0.04 to 0.42. The d(PTIP) values were significantly higher (by 0.84-1.89 cm) than the d(PTCP) values (P < 0.05). These results are in disagreement with previous in vitro findings that d(PT) variance may be explained by knee joint size differences. Hence, existing imaging-based methodologies remain necessary for accurate quantification of the patellar tendon moment arm.     

Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion?

Tendon elasticity is important for economical locomotion; however it is unknown whether tendon stiffness is appropriate to achieve an optimal efficiency in various muscles. Here we test the hypothesis that the Achilles tendon is of an appropriate stiffness to maximise medial gastrocnemius muscle efficiency during locomotion with different power requirements. To test this hypothesis we used a three element Hill muscle model to determine how muscle fascicles would be required to change length if the series elastic element stiffness is varied, whilst the limb kinematics and muscle properties are held constant. We applied a model of muscle energetics to these data to predict muscle efficiency for a range of stiffness values in both walking and running conditions. We also compared the model results to in vivo data collected using ultrasonography. The muscle model predicted that optimal series elastic element stiffness for maximising efficiency is equal or slightly higher than that of the average Achilles tendon in running and walking, respectively. Although the peak efficiency values for running (26%) and walking (27%) are similar, the range of stiffness values achieving high efficiency in running is much smaller than that during walking. These results suggest that a compliant tendon, such as the Achilles tendon, is required for efficient running. Such a finding is important, because it describes how the stiffness of a tendon may be adapted to achieve optimal efficiency for particular athletic pursuits. The influence of varying tendon stiffness on kinematic performance may, however, play an important role in determining the efficiency of the muscle.     

Medullary neurons mediating the inhibition of inspiration by intercostal muscle tendon organs?

Studies were conducted to test the hypothesis that nonrespiratory-modulated units are last-order interneurons mediating the effects of intercostal muscle tendon organs on medullary inspiratory neuron activity. Vagotomized, anesthetized, or decerebrate cats were used. Results show the following. 1) Afferents from different receptor types (i.e., intercostal tendon organs and chest wall cutaneous receptors) that inhibit medullary inspiratory neuron activities evoke the same units. 2) Gastrocnemius muscle group I afferent fibers evoke some of the same units as intercostal afferents but do not alter respiratory activity. 3) The "pneumotaxic center" and laryngeal nerve afferents, which inhibit medullary inspiratory activity, evoke different medullary units than intercostal afferents. 4) Evoked units are not active in spontaneously breathing cats. Additional results suggest that a few respiratory neurons near the retrofacial nucleus may be involved in the mediation of the inspiratory inhibitory effects of intercostal tendon organs. These results do not establish the mechanism by which intercostal muscle tendon organs reduces medullary inspiratory activity.     

Could intra-tendinous hyperthermia during running explain chronic injury of the human Achilles tendon?

Chronic tendinopathy of the human Achilles tendon (AT) is common but its injury mechanism is not fully understood. It has been hypothesised that heat energy losses from the AT during running could explain the degeneration of AT material seen with injury. A mathematical model of AT temperature distribution was used to predict what temperatures the core of the AT could reach during running. This model required input values for mechanical properties of the AT (stiffness, hysteresis, cross-sectional area (CSA), strain during running) which were determined using a combination of ultrasound imaging, kinematic and kinetic data. AT length data were obtained during hopping and treadmill running (12 kmph) using ultrasound images of the medial gastrocnemius (50 Hz) and kinematic data (200 Hz). AT force data were calculated from inverse dynamics during hopping and combined with AT length data to compute AT stiffness and hysteresis. AT strain was computed from AT length data during treadmill running. AT CSA was measured on transverse ultrasound scans of the AT. Mean ± sd tendon properties were: stiffness = 176 ± 41 Nmm(-1), hysteresis =17 ± 12%, strain during running =3.5 ± 1.8% and CSA = 42 ± 8 mm(2). These values were input into the model of AT core temperature and this was predicted to reach at least 41°C during running. Such temperatures were deemed to be conservative estimates but still sufficient for tendon hyperthermia to be a potential cause of tendon injury.     

Can Achilles tendon moment arm be predicted from anthropometric measures in pre-pubescent children?

Muscle-tendon moment arm magnitudes are essential variables for accurately calculating muscle forces from joint moments. Their measurement requires specialist knowledge and expensive resources. Research has shown that the patellar tendon moment arm length is related to leg anthropometry in children. Here, we asked whether the Achilles tendon moment arm (MA(AT)) can be accurately predicted in pre-pubescent children from surface anthropometry. Age, standing height, mass, foot length, inter-malleolar ankle width, antero-posterior ankle depth, tibial length, lower leg circumference, and distances from the calcaneus to the distal head of the 1st metatarsal and medial malleolus were determined in 49 pre-pubescent children. MA(AT) was calculated at three different ankle positions (neutral, 10° plantarflexion, and 10° dorsiflexion) by differentiating tendon excursion, measured via ultrasonography, with respect to ankle angle change using seven different differentiation techniques. Backwards stepwise regression analyses were performed to identify predictors of MA(AT.) When all variables were included, the regression analysis accounted for a maximum of 49% of MA(AT) variance at the neutral ankle angle when a third-order polynomial was used to differentiate tendon excursion with respect to ankle angle. For this condition, foot length and the distance between calcaneus and 1st metatarsal were the only significant predictors, accounting for 47% of the variance (p<0.05). The absolute error associated with this regression model was 3.8±4.4 mm, which would result in significant error (mean=14.5%) when estimating muscle forces from joint moments. We conclude that MA(AT) cannot be accurately predicted from anthropometric measures in children.     

Is echogenicity a viable metric for evaluating tendon properties in vivo?

Material properties of tissue in vivo present an opportunity for clinical analysis of healing progression and pathologies as well as provide an excellent research tool yielding quantified data for longitudinal and cross population studies. Echogenicity is a material?s ability to reflect sound and, using ultrasound, it has been shown to increase with tendon tension in vitro, though this non-invasive measurement technique for determining mechanical properties has not been tested in vivo. The aim of this study was to establish if echogenicity, seen by the increase in image brightness, could be correlated to stress within a tissue. 18 Achilles tendons were imaged in the sagittal and transverse planes while producing a series of isometric contractions starting from rest and producing the torque equivalent of 0.5, 1.0, 1.5, and 2.0× body weights. Manual tracing identified the tendon in each of the images. The cross-sectional area determined from the transverse plane images in conjunction with the tendon force yielded the tendon stress. The echogenicity of the tendon was determined from the mean brightness change from rest to each of the contraction cases, measured from the sagittal plane images. A weak correlation existed between the echogenicity and stress (R=0.25) but it was found that there was no significant change in axial area during contraction (p=0.683) establishing the tendon as incompressible. Echogenicity proved to be non-functional for measuring the mechanical properties of the Achilles tendon due to the additional factors included with in vivo testing e.g. tendon twist and multi-axial loading.     

Atomic force microscopy determination of Young׳s modulus of bovine extra-ocular tendon fiber bundles

Extra-ocular tendons (EOTs) transmit the oculorotary force of the muscles to the eyeball to generate dynamic eye movements and align the eyes, yet the mechanical properties of the EOTs remain undefined. The EOTs are known to be composed of parallel bundles of small fibers whose mechanical properties must be determined in order to characterize the overall behavior of EOTs. The current study aimed to investigate the transverse Young?s modulus of EOT fiber bundles using atomic force microscopy (AFM).     

Continuum description of the Poisson׳s ratio of ligament and tendon under finite deformation

Ligaments and tendons undergo volume loss when stretched along the primary fiber axis, which is evident by the large, strain-dependent Poisson?s ratios measured during quasi-static tensile tests. Continuum constitutive models that have been used to describe ligament material behavior generally assume incompressibility, which does not reflect the volumetric material behavior seen experimentally. We developed a strain energy equation that describes large, strain dependent Poisson?s ratios and nonlinear, transversely isotropic behavior using a novel method to numerically enforce the desired volumetric behavior. The Cauchy stress and spatial elasticity tensors for this strain energy equation were derived and implemented in the FEBio finite element software (www.febio.org). As part of this objective, we derived the Cauchy stress and spatial elasticity tensors for a compressible transversely isotropic material, which to our knowledge have not appeared previously in the literature. Elastic simulations demonstrated that the model predicted the nonlinear, upwardly concave uniaxial stress–strain behavior while also predicting a strain-dependent Poisson?s ratio. Biphasic simulations of stress relaxation predicted a large outward fluid flux and substantial relaxation of the peak stress. Thus, the results of this study demonstrate that the viscoelastic behavior of ligaments and tendons can be predicted by modeling fluid movement when combined with a large Poisson?s ratio. Further, the constitutive framework provides the means for accurate simulations of ligament volumetric material behavior without the need to resort to micromechanical or homogenization methods, thus facilitating its use in large scale, whole joint models.     

In vivo vastus lateralis force–velocity relationship at the fascicle and muscle tendon unit level

The force velocity relationship of in vivo human muscle fibers has often been derived from the torque-angular speed relationship during maximal voluntary isokinetic contractions. However, the assumption of a close association between joint performance and muscle mechanics is questionable. We aimed to determine the relationship between knee extension angular speeds, vastus lateralis fascicle and muscle tendon unit (MTU) shortening speeds, and maximal knee extensor force for the entire range of knee joint movement, for the isokinetic range, and for the ranges before, after and at peak torque occurrence, with different commonly used pre-loading conditions. Higher peak forces were observed when knee extensions were preceded by a pre-load, despite the similarity in fascicle shortening speeds. For the entire and the isokinetic range, MTU always shortened faster than fascicles, and this difference increased as joint speed increased. Interestingly, fascicle shortening velocities were greater before compared to after peak torque occurrence while the opposite happened at the MTU level. Assuming a close relationship between joint and fascicle dynamics results in an overestimation of muscle contractile component shortening velocity or force production at peak torque. The force velocity relationships obtained in vivo depend crucially on the test conditions, and the movement range used for analysis.     

Do the hamstrings operate at increased muscle–tendon lengths and velocities after surgical lengthening?

Children with crouch gait frequently walk with improved knee extension during the terminal swing and stance phases following hamstrings lengthening surgery; however, the mechanisms responsible for these improvements are unclear. This study tested the hypothesis that surgical lengthening enables the hamstrings of persons with cerebral palsy to operate at longer muscle-tendon lengths or lengthen at faster muscle-tendon velocities during walking. Sixty-nine subjects who had improved knee extension after surgery were retrospectively examined. The muscle-tendon lengths and velocities of the subjects' semimembranosus muscles were estimated by combining kinematic data from gait analysis with a three-dimensional computer model of the lower extremity. Log-linear analyses confirmed that the subjects who walked with abnormally short muscle-tendon lengths and/or slow muscle-tendon velocities preoperatively tended to walk with longer lengths (21 of 29 subjects, p<0.01) or faster velocities (30 of 40 subjects, p<0.01) postoperatively. In these cases, surgical lengthening may have slackened the subjects' tight hamstrings and/or diminished the hamstrings' spastic response to stretch. Other subjects walked with muscle-tendon lengths and velocities that were neither shorter nor slower than normal preoperatively (22 of 69 subjects), and the semimembranosus muscles of most of these subjects did not operate at increased lengths or velocities after surgery; in these cases, the subjects' postsurgical improvements in knee extension may have been unrelated to the hamstrings surgery. Analyses of muscle-tendon lengths and velocities may help to distinguish individuals who have "short" or "spastic" hamstrings from those who do not, and thus may augment conventional methods used to describe patients' neuromusculoskeletal impairments and gait abnormalities.     

Middle phalanx skeletal morphology in the hand: Can it predict flexor tendon size and attachments?

Specific sites on the palmar diaphysis of the manual middle phalanges provide attachment for the flexor digitorum superficialis (FDS) tendon. It has been assumed in the literature that lateral palmar fossae on these bones reflect locations for these attachments and offer evidence for relative size of the flexor tendon. This assumption has led to predictions about relative FDS muscle force potential from sizes of fossae on fossil hominin middle phalanges. Inferences about locomotor capabilities of fossil hominins in turn have been drawn from the predicted force potential of the flexor muscle. The study reported here provides a critical first step in evaluating hypotheses about behavioral implications of middle phalangeal morphology in fossil hominins, by testing the hypothesis that the lateral fossae reflect the size of the FDS tendon and the location of the terminal FDS tendon attachments on the middle phalanx. The middle phalangeal region was dissected in 43 individuals from 16 primate genera, including humans. Qualitative observations were made of tendon attachment locations relative to the lateral fossae. Length measurements of the fossae were tested as predictors of FDS tendon cross-sectional area and of FDS attachment tendon lengths. Our results lead to the conclusion that the hypothesis must be rejected, and that future attention should focus on functional implications of the palmar median bar associated with the lateral fossae.