Activation of neuromuscular sub-regions of supraspinatus and infraspinatus during common rehabilitative exercises

‘Regional activation’ has been identified within the supraspinatus and infraspinatus. Previous EMG studies have provided insight on the different functions of the sub-regions within the supraspinatus and infraspinatus, however, to date timing of peak EMG activation has not been investigated. To assess how theses sub-regions function during commonly prescribed rehabilitation exercises, electrodes were inserted into the supraspinatus - anterior and posterior- and infraspinatus - superior and middle - of 22 healthy participants. For each sub-region, normalized EMG data - amplitude and timing - was collected from nine rehabilitation exercises - three with an elastic band and six an exercise ball. Supraspinatus posterior and infraspinatus superior had similar activation levels between elastic band exercises, but the timing of peak activation was exercise specific. In all elastic band exercises, supraspinatus posterior activated prior to supraspinatus anterior. All ball exercises elicited low-amplitude muscle activation; dynamic ball exercises had higher peak muscle activation than their static counterparts.     

Temperature-dependent viscoelastic properties of the human supraspinatus tendon

Temperature effects on the viscoelastic properties of the human supraspinatus tendon were investigated using static stress-relaxation experiments and the quasi-linear viscoelastic (QLV) theory. Twelve supraspinatus tendons were randomly assigned to one of two test groups for tensile testing using the following sequence of temperatures: (1) 37, 27, and 17 °C (Group I, n=6), or (2) 42, 32, and 22 °C (Group II, n=6). QLV parameter C was found to increase at elevated temperatures, suggesting greater viscous mechanical behavior at higher temperatures. Elastic parameters A and B showed no significant difference among the six temperatures studied, implying that the viscoelastic stress response of the supraspinatus tendon is not sensitive to temperature over shorter testing durations. Using regression analysis, an exponential relationship between parameter C and test temperature was implemented into QLV theory to model temperature-dependent viscoelastic behavior. This modified approach facilitates the theoretical determination of the viscoelastic behavior of tendons at arbitrary temperatures.     

Effect of partial-thickness tear on loading capacities of the supraspinatus tendon: a finite element analysis

Partial-thickness tears of the supraspinatus tendon frequently occur at its insertion on the greater tubercule of the humerus, causing pain and reduced strength and range of motion. The goal of this work was to quantify the loss of loading capacity due to tendon tears at the insertion area. A finite element model of the supraspinatus tendon was developed using in vivo magnetic resonance images data. The tendon was represented by an anisotropic hyperelastic constitutive law identified with experimental measurements. A failure criterion was proposed and calibrated with experimental data. A partial-thickness tear was gradually increased, starting from the deep articular-sided fibres. For different values of tendon tear thickness, the tendon was mechanically loaded up to failure. The numerical model predicted a loss in loading capacity of the tendon as the tear thickness progressed. Tendon failure was more likely when the tendon tear exceeded 20%. The predictions of the model were consistent with experimental studies. Partial-thickness tears below 40% tear are sufficiently stable to persist physiotherapeutic exercises. Above 60% tear surgery should be considered to restore shoulder strength.     

Determination of the compressive material properties of the supraspinatus tendon

A methodology was developed for determining the compressive properties of the supraspinatus tendon, based on finite element principles. Simplified three-dimensional models ure re reated based on anatomical thickness measurements of unloaded supraspinatus tendons over 15 points. The tendon material was characterized as a composite structure of' longitudinally arranged collagen fibers within an extrafibrillar matrix. The matrix was formulated as a hyperelastic material described by the Ogden form of the strain energy potential. The hyperelastic material parameters were parametrically manipulated until the analytical load-displacement results were similar to the results obtaizned from indentation testinrg. In the geometrically averaged tendon, the average ratio of experimental to theoretical maximum indentation displacement was 1.00 (SD: 0.01). The average normalization of residuals was 2.1 g (SD: 0.9 g). Therefjore, the compressive material properties of the supraspinatus tendo'n extrafibrillar matrix were adequately derived with a first-order hyperelastic formulation. The initial comnpressive elastic modulus ranged from 0.024 to 0.090 MPa over the tendon surface and increased nonlinearly with additional compression. Using these material properties, the stresses induced during acromional impingement can be analyzed.     

Regional activation of supraspinatus and infraspinatus sub-regions during dynamic tasks performed with free weights

Growing evidence supports the existence of distinct anatomical sub-regions within supraspinatus and infraspinatus, but only recently has attention turned to exploring their potential functional differences. Using indwelling fine-wire electromyography, muscle activity was investigated from these sub-regions in 15 participants (mean 34 yr, 170 cm, 71.9 kg) during dynamic external rotation (ER), abduction, flexion, and scaption tasks with and without free weights corresponding to 50% and 75% of the participant’s five repetition maximum. Electromyography data were normalized to isometric and isokinetic maximal voluntary contractions and activation ratios for each sub-region compared.Differences in mean regional activation ratios for supraspinatus and infraspinatus varied by arm posture, but were not influenced by load. Relative activation of posterior supraspinatus was greater during an ER task performed in side lying compared to an ER task performed with 90° of humeral elevation in seated and prone postures. Relative activation of superior infraspinatus was greater during an ER task in prone and side lying postures compared to flexion and scaption. Similar results were found when comparing regional muscle activation ratios for infraspinatus between tasks regardless of normalization method employed. These findings may impact exercise selection in the non-operative management of rotator cuff tears.     

Sub-regional activation of supraspinatus and infraspinatus muscles during activities of daily living is task dependent

The supraspinatus and infraspinatus muscles each have multiple sub-regions that may activate differentially in activities of daily living. Awareness of these differential demands critically informs rehabilitation of rotator cuff muscle following injury, particularly if centered on recovering and strengthening the rotator cuff to perform daily tasks. This study quantified muscle activation of supraspinatus and infraspinatus sub-regions during the performance of six activities of daily living. Twenty-three participants (mean: 22.6 ± 2.6 years) completed the following tasks: opening a jar, reaching at shoulder height, overhead reaching, pouring water from a pitcher, eating with a spoon, and combing hair. Indwelling electromyography was collected from the anterior and posterior supraspinatus and superior, middle, and inferior infraspinatus. Tasks requiring high arm elevations (e.g. reaching at shoulder and overhead height) activated anterior supraspinatus between 21 and 28% MVC. The posterior supraspinatus consistently activated between 10 and 30% MVC across all tasks. All sub-regions of infraspinatus activated highly (between 18 and 25% MVC) in tasks requiring high arm elevations in flexion. These findings may be leveraged to define effective measures to increase rotator cuff function in daily tasks.     

Comparing surface and indwelling electromyographic signals of the supraspinatus and infraspinatus muscles during submaximal axial humeral rotation

This study quantified the relationship between EMG signals recorded by surface and indwelling electrodes for the infraspinatus and supraspinatus during submaximal axial humeral rotation. Muscular activity was measured on 20 participants during 82 submaximal isometric internal or external axial humeral rotations in a range of postures and intensities. Equations to predict indwelling magnitudes from surface data were generated and the effects of humeral angle and intensity on this relationship were also evaluated.Supraspinatus surface data explained 72–76% of the variance in the indwelling data. Surface data overestimated indwelling data by up to 30% of maximal voluntary contraction (MVC). Infraspinatus surface data explained 62–64% of the variance in the indwelling data, but overestimated by 72% and 400% MVC in external and internal axial humeral rotation trials, respectively. Humeral abduction angle and exertion intensity both altered the relationship between electrode types modestly (p < 0.01) for most muscles and exertions. Better variance explanation was achieved for these submaximal exertions than previously reported values for maximal exertions.These results help inform electrode type selection for the recording of supraspinatus and infraspinatus EMG. Caution is recommended when interpreting surface recordings as indicators of indwelling recordings for exertions where the muscle studied is not a primary mover.     

Biaxial tensile testing and constitutive modeling of human supraspinatus tendon

The heterogeneous composition and mechanical properties of the supraspinatus tendon offer an opportunity for studying the structure-function relationships of fibrous musculoskeletal connective tissues. Previous uniaxial testing has demonstrated a correlation between the collagen fiber angle distribution and tendon mechanics in response to tensile loading both parallel and transverse to the tendon longitudinal axis. However, the planar mechanics of the supraspinatus tendon may be more appropriately characterized through biaxial tensile testing, which avoids the limitation of nonphysiologic traction-free boundary conditions present during uniaxial testing. Combined with a structural constitutive model, biaxial testing can help identify the specific structural mechanisms underlying the tendon's two-dimensional mechanical behavior. Therefore, the objective of this study was to evaluate the contribution of collagen fiber organization to the planar tensile mechanics of the human supraspinatus tendon by fitting biaxial tensile data with a structural constitutive model that incorporates a sample-specific angular distribution of nonlinear fibers. Regional samples were tested under several biaxial boundary conditions while simultaneously measuring the collagen fiber orientations via polarized light imaging. The histograms of fiber angles were fit with a von Mises probability distribution and input into a hyperelastic constitutive model incorporating the contributions of the uncrimped fibers. Samples with a wide fiber angle distribution produced greater transverse stresses than more highly aligned samples. The structural model fit the longitudinal stresses well (median R(2) ≥ 0.96) and was validated by successfully predicting the stress response to a mechanical protocol not used for parameter estimation. The transverse stresses were fit less well with greater errors observed for less aligned samples. Sensitivity analyses and relatively affine fiber kinematics suggest that these errors are not due to inaccuracies in measuring the collagen fiber organization. More likely, additional strain energy terms representing fiber-fiber interactions are necessary to provide a closer approximation of the transverse stresses. Nevertheless, this approach demonstrated that the longitudinal tensile mechanics of the supraspinatus tendon are primarily dependent on the moduli, crimp, and angular distribution of its collagen fibers. These results add to the existing knowledge of structure-function relationships in fibrous musculoskeletal tissue, which is valuable for understanding the etiology of degenerative disease, developing effective tissue engineering design strategies, and predicting outcomes of tissue repair.     

Effect of preconditioning and stress relaxation on local collagen fiber re-alignment: inhomogeneous properties of rat supraspinatus tendon

Repeatedly and consistently measuring the mechanical properties of tendon is important but presents a challenge. Preconditioning can provide tendons with a consistent loading history to make comparisons between groups from mechanical testing experiments. However, the specific mechanisms occurring during preconditioning are unknown. Previous studies have suggested that microstructural changes, such as collagen fiber re-alignment, may be a result of preconditioning. Local collagen fiber re-alignment is quantified throughout tensile mechanical testing using a testing system integrated with a polarized light setup, consisting of a backlight, 90 deg-offset rotating polarizer sheets on each side of the test sample, and a digital camera, in a rat supraspinatus tendon model, and corresponding mechanical properties are measured. Local circular variance values are compared throughout the mechanical test to determine if and where collagen fiber re-alignment occurred. The inhomogeneity of the tendon is examined by comparing local circular variance values, optical moduli and optical transition strain values. Although the largest amount of collagen fiber re-alignment was found during preconditioning, significant re-alignment was also demonstrated in the toe and linear regions of the mechanical test. No significant changes in re-alignment were seen during stress relaxation. The insertion site of the supraspinatus tendon demonstrated a lower linear modulus and a more disorganized collagen fiber distribution throughout all mechanical testing points compared to the tendon midsubstance. This study identified a correlation between collagen fiber re-alignment and preconditioning and suggests that collagen fiber re-alignment may be a potential mechanism of preconditioning and merits further investigation. In particular, the conditions necessary for collagen fibers to re-orient away from the direction of loading and the dependency of collagen reorganization on its initial distribution must be examined.     

Effect of age on collagen fibril diameter in rabbit patellar tendon repair

The effect of aging on soft tissue repair is poorly understood. We examined collagen fibril diameter in repairing patellar tendons from young adult and aging rabbits. We hypothesized that repairing tendons from older (geriatric) rabbits would have similar diameter fibrils compared with the younger (young adult) rabbits. Full-length, full-thickness, central-third (2.5 to 3 mm) patellar tendon injuries were made by cutting out the center of the tendon in twelve 1-y-old and thirteen 4- to 5.5 (average, 4.25)-y-old female New Zealand White rabbits. The contralateral tendon served as an unoperated control. The rabbits were euthanized at 6, 12, and 26 wk after surgery. The collagen fibril diameter was examined by electron microscopy at the patellar end, middle, and tibial end of the patellar tendon. There was no significant decline in collagen fibril diameter at any location in the aging rabbit healing patellar tendons compared with those of the 1-y-old rabbits. This study found that collagen fibril diameter was not altered with increasing age in the healing rabbit patellar tendon.     

Perivascular cells of the supraspinatus tendon express both tendon- and stem cell-related markers

Tendons and ligaments are often affected by mechanical injuries or chronic impairment but other than muscle or bone they possess a low healing capacity. So far, little is known about regeneration of tendons and the role of tendon precursor cells in that process. We hypothesize that perivascular cells of tendon capillaries are progenitors for functional tendon cells and are characterized by expression of marker genes and proteins typical for mesenchymal stem cells and functional tendon cells. Immunohistochemical characterization of biopsies derived from intact human supraspinatus tendons was performed. From these biopsies perivascular cells were isolated, cultured, and characterized using RT-PCR and Western blotting. We have shown for the first time that perivascular cells within tendon tissue express both tendon- and stem/precursor cell-like characteristics. These findings were confirmed by results from in vitro studies focusing on cultured perivascular cells isolated from human supraspinatus tendon biopsies. The results suggest that the perivascular niche may be considered a source for tendon precursor cells. This study provides further information about the molecular nature and localization of tendon precursor cells, which is the basis for developing novel strategies towards tendon healing and facilitated regeneration. H. Tempfer and A. Wagner have contributed equally to this paper.     

Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration.

Degenerative tendon injury or "tendinopathy" is one of the most common disorders of the musculoskeletal system. We used a rat model (Soslowsky LJ, Thomopoulos S, Tun S, Flanagan CL, Keefer CC, Mastaw J, and Carpenter JE. J Shoulder Elbow Surg 9: 79-84, 2000) to identify novel gene expression in the exercised-induced degenerated supraspinatus tendon by microarray and real-time PCR analyses. We identified several novel groups of differentially expressed genes, including those involved in apoptosis and related stress responses, and also genes that appear to be involved in glutamate signaling in tendon tissue, similar to recent findings by us in a microarray study of healing in the transected Achilles tendon of the rat (24). Until recently this kind of cellular communication was thought only to exist in cells of the central nervous system (CNS), where it is vital for CNS function. We further show that glutamate appears to induce a proapoptotic response in cultured tendon cells, similar to the "excitotoxic" response of cells in the CNS that become overstimulated. This may prove to be at least a partial cause of degeneration in overused tendon tissue and allow the development of treatments or "prehibilitation" regimens for tendinopathy based on currently used non-toxic glutamate antagonists.     

Transglutaminases expression in human supraspinatus tendon ruptures and in mouse tendons

The ethiopathogenesis of rotator cuff disease remains poorly understood. Many studies advocate the importance of extra cellular matrix for the homeostasis of connective tissue. Transglutaminase enzymes family has been studied in the context of connective tissue formation and stabilisation. Here, we investigated transglutaminases expression pattern in biopsies of normal and injured supraspinatus tendons of human shoulders and in the Achilles tendons of transglutaminase 2 knock-out and wild-type mice. Our results show that different transglutaminase family members are differentially expressed in human and mouse tendons, and that transglutaminase 2 is down-regulated at mRNA and protein levels upon human supraspinatus tendon ruptures.     

Shear wave elastography of the supraspinatus muscle and tendon: Repeatability and preliminary findings

Shear wave elastography (SWE) is a promising tool for estimating musculoskeletal tissue properties, but few studies have rigorously assessed its repeatability and sources of error. The objectives of this study were to assess: (1) the extent to which probe positioning error and human user error influence measurement accuracy, (2) intra-user, inter-user, and day-to-day repeatability, and (3) the extent to which active and passive conditions affect shear wave speed (SWS) repeatability. Probe positioning and human usage errors were assessed by acquiring SWE images from custom ultrasound phantoms. Intra- and inter-user repeatability were assessed by two users acquiring five trials of supraspinatus muscle and tendon SWE images from ten human subjects. To assess day-to-day repeatability, five of the subjects were tested a second time, approximately 24 h later. Imaging of the phantoms indicated high inter-user repeatability, with intraclass correlation coefficient (ICC) values of 0.68–0.85, and RMS errors of no more than 4.1%. SWE imaging of the supraspinatus muscle and tendon had high repeatability, with intra- and inter-user ICC values of greater than 0.87 and 0.73, respectively. Day-to-day repeatability demonstrated ICC values greater than 0.33 for passive muscle, 0.48 for passive tendon, 0.65 for active muscle, and 0.94 for active tendon. This study indicates the technique has good to very good intra- and inter-user repeatability, and day-to-day repeatability is appreciably higher when SWE images are acquired under a low level of muscle activation. The findings from this study establish the feasibility and repeatability of SWE for acquiring data longitudinally in human subjects.     

Kinetic analysis of canine gait on the effect of failure tendon repair and tendon graft

Kinetic analysis of canine gait has been extensively studied, including normal and abnormal gait. However, no research has looked into how flexor tendon injury and further treatment would affect the walking pattern comparing to the uninjured state. Therefore, this study was aimed to utilize a portable pressure walkway system, which has been commonly used for pedobarographic and kinetic analysis in the veterinary field, to examine the effect of a failed tendon repair and tendon graft reconstruction on canine digit kinetics during gait. 12 mixed breed (mongrel) hound-type female dogs were included in this study and 2^nd and 5^th digits were chosen to undergo flexor tendon repair and graft surgeries. Kinetic parameters from the surgery leg in stance phase were calculated. From the results, after tendon failure repair, decrease of weight bearing was seen in the affected digits and weight bearing was shifted to the metacarpal pad. After tendon graft reconstruction, weight bearing returned to the affected digits and metacarpal pads. Slight alteration in peak pressure and instant of peak force were identified, but it was estimated to have little influence on post-reconstruction gait. This study could serve as a reference in evaluating canine digit function in flexor tendon injury for future studies.     

Biomimetic approaches to tendon repair

The linear organization of collagen fibers in tendons results in optimal stiffness and strength at low strains under tensile load. However, this organization makes repairing ruptured or lacerated tendons extremely difficult. Current suturing techniques to join split ends of tendons, while providing sufficient mechanical strength to prevent gapping, are inadequate to carry normal loads. Immobilization protocols necessary to restore tendon congruity result in scar formation at the repair site and peripheral adhesions that limit excursion. These problems are reviewed to emphasize the need for novel approaches to tendon repair, one of which is the development of biomimetic tendons. The objective of the empirical work described here was to produce biologically-based, biocompatible tendon replacements with appropriate mechanical properties to enable immediate mobilization following surgical repair. Nor-dihydroguaiaretic acid (NDGA), a di-catechol from creosote bush, caused a dose dependent increase in the material properties of reconstituted collagen fibers, achieving a 100-fold increase in strength and stiffness over untreated fibers. The maximum tensile strength of the optimized NDGA treated fibers averaged 90 MPa; the elastic modulus of these fibers averaged 580 MPa. These properties were independent of strain rates ranging from 0.60 to 600 mm/min. Fatigue tests established that neither strength nor stiffness were affected after 80 k cycles at 5% strain. Treated fibers were not cytotoxic to tendon fibroblasts. Fibroblasts attached and proliferated on NDGA treated collagen normally. NDGA-fibers did not elicit a foreign body response nor did they stimulate an immune reaction during six weeks in vivo. The fibers survived 6 weeks with little evidence of fragmentation or degradation. The polymerization scheme described here produces a fiber-reinforced NDGA-polymer with mechanical properties approaching an elastic solid. The strength, stiffness and fatigue properties of the NDGA-treated fibers are comparable to those of tendon. These fibers are biocompatible with tendon fibroblasts and elicit little rejection or antigenic response in vivo. These results indicate that NDGA polymerization may provide a viable approach for producing collagenous materials that can be used to bridge gaps in ruptured or lacerated tendons. The tendon-like properties of the NDGA-fiber would allow early mobilization after surgical repair. We predict that timely loading of parted tendons joined by this novel biomaterial will enhance mechanically driven production of neo-tendon by the colonizing fibroblasts and result in superior repair and rapid return to normal properties.     

Biomechanics of tendon injury and repair

Many clinical and experimental studies have investigated how tendons repair in response to an injury. This body of work has led to a greater understanding of tendon healing mechanisms and subsequently to an improvement in their treatment. In this review paper, characterization of normal and healing tendons is first covered. In addition, the debate between intrinsic and extrinsic healing is examined, and the cellular and extracellular matrix response following a tendon injury is detailed. Next, clinical and experimental injury and repair methods utilizing animal models are discussed. Animal models have been utilized to study the effect of various activity levels, motions, injury methods, and injury locations on tendon injury and repair. Finally, current and future treatment modalities for improving tendon healing, such as tissue engineering, cell therapy, and gene therapy, are reviewed.