Fiber-type traps: revisiting common misconceptions about skeletal muscle fiber types with application to motor control, biomechanics, physiology, and biology.

Skeletal muscle is a highly complex tissue that is studied by scientists from a wide spectrum of disciplines, including motor control, biomechanics, exercise science, physiology, cell biology, genetics, regenerative medicine, orthopedics, and engineering. Although this diversity in perspectives has led to many important discoveries, historically, there has been limited overlap in discussions across fields. This has led to misconceptions and oversimplifications about muscle biology that can create confusion and potentially slow scientific progress across fields. The purpose of this synthesis paper is to bring together research perspectives across multiple muscle fields to identify common assumptions related to muscle fiber type that are points of concern to clarify. These assumptions include 1) classification by myosin isoform and fiber oxidative capacity is equivalent, 2) fiber cross-sectional area (CSA) is a surrogate marker for myosin isoform or oxidative capacity, and 3) muscle force-generating capacity can be inferred from myosin isoform. We address these three fiber-type traps and provide some context for how these misunderstandings can and do impact experimental design, computational modeling, and interpretations of findings, from the perspective of a range of fields. We stress the dangers of generalizing findings about "muscle fiber types" among muscles or across species or sex, and we note the importance for precise use of common terminology across the muscle fields.

Influence of Brachial Plexus Birth Injury Location on Glenohumeral Joint Morphology.

PURPOSE: Patient presentation after brachial plexus birth injury (BPBI) is influenced by nerve injury location; more contracture and bone deformity occur at the shoulder in postganglionic injuries. Although bone deformity after postganglionic injury is well-characterized, the extent of glenohumeral deformity after preganglionic BPBI is unclear. METHODS: Twenty Sprague-Dawley rat pups received preganglionic or postganglionic neurectomy on a single forelimb at postnatal days 3 to 4. Glenohumeral joints on affected and unaffected sides were analyzed using micro-computed tomography scans after death at 8 weeks after birth. Glenoid version, glenoid inclination, glenoid and humeral head radius of curvature, and humeral head thickness and width were measured bilaterally. RESULTS: The glenoid was significantly more declined in affected compared with unaffected shoulders after postganglionic (-17.7° ± 16.9°) but not preganglionic injury. Compared with the preganglionic group, the affected shoulder in the postganglionic group exhibited significantly greater declination and increased glenoid radius of curvature. In contrast, the humeral head was only affected after preganglionic but not postganglionic injury, with a significantly smaller humeral head radius of curvature (-0.2 ± 0.2 mm), thickness (-0.2 ± 0.3 mm), and width (-0.3 ± 0.4 mm) on the affected side compared with the unaffected side; changes in these metrics were significantly associated with each other. CONCLUSIONS: These findings suggest that glenoid deformities occur after postganglionic BPBI but not after preganglionic BPBI, whereas the humeral head is smaller after preganglionic injury, possibly suggesting an overall decreased biological growth rate in this group. CLINICAL RELEVANCE: This study expands understanding of the altered glenoid and humeral head morphologies after preganglionic BPBI and its comparisons with morphologies after postganglionic BPBI.

Preganglionic and Postganglionic Brachial Plexus Birth Injury Effects on Shoulder Muscle Growth.

PURPOSE: Brachial plexus birth injury can differ in presentation, depending on whether the nerve ruptures distal to, or avulses proximal to, the dorsal root ganglion. More substantial contracture and bone deformity at the shoulder is typical in postganglionic injuries. However, changes to the underlying muscle structure that drive these differences in presentation are unclear. METHODS: Seventeen Sprague-Dawley rats received preganglionic or postganglionic neurectomy on a single limb on postnatal days 3 and 4. Muscles crossing the shoulder were retrieved once the rats were sacrificed at 8 weeks after birth. External rotation range of motion, muscle mass, muscle length, muscle sarcomere length, and calculated optimal muscle length were measured bilaterally. RESULTS: Average shoulder range of motion in the postganglionic group was 61.8% and 56.2% more restricted at 4 and 8 weeks, respectively, compared with that in the preganglionic group, but affected muscles after preganglionic injury were altered more severely (compared with the unaffected limb) than after postganglionic injury. Optimal muscle length in preganglionic injury was shorter in the affected limb (compared with the unaffected limb: -18.2% ± 9.2%) and to a greater extent than in postganglionic injury (-5.1% ± 6.2%). Muscle mass in preganglionic injury was lower in the affected limb (relative to the unaffected limb: -57.2% ± 24.1%) and to a greater extent than in postganglionic injury (-28.1% ± 17.7%). CONCLUSIONS: The findings suggest that the presence of contracture does not derive from restricted longitudinal muscle growth alone, but also depends on the extent of muscle mass loss occurring simultaneously after the injury. CLINICAL RELEVANCE: This study expands our understanding of differences in muscle architecture and the role of muscle structure in contracture formation for preganglionic and postganglionic brachial plexus birth injury.

Assessments of Fatty Infiltration and Muscle Atrophy From a Single Magnetic Resonance Image Slice Are Not Predictive of 3-Dimensional Measurements.

PURPOSE: To (1) determine whether standard clinical muscle fatty infiltration and atrophy assessment techniques using a single image slice for patients with a rotator cuff tear (RCT) are correlated with 3-dimensional measures in older individuals (60+ years) and (2) to determine whether age-associated changes to muscle morphology and strength are compounded by an RCT. METHODS: Twenty older individuals were studied: 10 with an RCT of the supraspinatus (5 men and 5 women) and 10 matched controls. Clinical imaging assessments (Goutallier and Fuchs scores and cross-sectional area ratio) were performed for participants with RCTs. Three-dimensional measurements of rotator cuff muscle and fat tissues were obtained for all participants using magnetic resonance imaging (MRI). Isometric joint moment was measured at the shoulder. RESULTS: There were no significant associations between single-image assessments and 3-dimensional measurements of fatty infiltration for the supraspinatus and infraspinatus muscles. Compared with controls, participants with RCTs had significantly increased percentages of fatty infiltration for each rotator cuff muscle (all P ≤ .023); reduced whole muscle volume for the supraspinatus, infraspinatus, and subscapularis muscles (all P ≤ .038); and reduced fat-free muscle volume for the supraspinatus, infraspinatus, and subscapularis muscles (all P ≤ .027). Only the teres minor (P = .017) fatty infiltration volume was significantly greater for participants with RCTs. Adduction, flexion, and external rotation strength (all P ≤ .021) were significantly reduced for participants with RCTs, and muscle volume was a significant predictor of strength for all comparisons. CONCLUSIONS: Clinical scores using a single image slice do not represent 3-dimensional muscle measurements. Efficient methods are needed to more effectively capture 3-dimensional information for clinical applications. Participants with RCTs had increased fatty infiltration percentages that were likely driven by muscle atrophy rather than increased fat volume. The significant association of muscle volume with strength production suggests that treatments to preserve muscle volume should be pursued for older patients with RCTs. LEVEL OF EVIDENCE: Level II, diagnostic study, with development of diagnostic criteria on the basis of consecutive patients with universally applied reference gold standard.

Biomechanical Basis of Shoulder Osseous Deformity and Contracture in a Rat Model of Brachial Plexus Birth Palsy.

BACKGROUND: The purpose of this study was to investigate the relative contributions of two proposed mechanisms, strength imbalance and impaired longitudinal muscle growth, to osseous and postural deformity in a rat model of brachial plexus birth palsy (BPBP). METHODS: Thirty-two Sprague-Dawley rat pups were divided into four groups on the basis of surgical interventions to induce a strength imbalance, impaired growth, both a strength imbalance and impaired growth (a combined mechanism), and a sham condition in the left forelimb. Maximum passive external shoulder rotation angle (ERmax) was measured bilaterally at four and eight weeks postoperatively. After the rats were killed at eight weeks, the glenohumeral geometry (on microcomputed tomography) and shoulder muscle architecture properties were measured bilaterally. RESULTS: Bilateral muscle mass and optimal length differences were greatest in the impaired growth and combined mechanism groups, which also exhibited >15° lower ERmax (p < 0.05; four weeks postoperatively), 14° to 18° more glenoid declination (p < 0.10), and 0.76 to 0.94 mm more inferior humeral head translation (p < 0.10) on the affected side. Across all four groups, optimal muscle length was significantly correlated with at least one osseous deformity measure for six of fourteen muscle compartments crossing the shoulder on the affected side (p < 0.05). In the strength imbalance group, the glenoid was 5° more inclined and the humeral head was translated 7.5% more posteriorly on the affected side (p < 0.05). CONCLUSIONS: Impaired longitudinal muscle growth and shoulder deformity were most pronounced in the impaired growth and combined mechanism groups, which underwent neurectomy. Strength imbalance was associated with osseous deformity to a lesser extent. CLINICAL RELEVANCE: Treatments to alleviate shoulder deformity should address mechanical effects of both strength imbalance and impaired longitudinal muscle growth, with an emphasis on developing new treatments to promote growth in muscles affected by BPBP.

Age-related structural changes in upper extremity muscle tissue in a nonhuman primate model.

BACKGROUND: Longitudinal studies of upper extremity aging in humans include logistical concerns that animal models can overcome. The vervet is a promising species with which to study aging-related processes. However, age-related changes in upper extremity muscle structure have not been quantified in this species. This study measured age-related changes to muscle structure, examined relationships between muscle structure and measures of physical performance, and evaluated the presence of rotator cuff tears. METHODS: Muscle structure (volume, optimal fiber length, and physiologic cross-sectional area (PCSA)) of 10 upper extremity muscles was quantified from the right upper limb of 5 middle-aged and 6 older adult female vervets. RESULTS: Total measured PCSA was smaller (P = .001) in the older adult vervets than in the middle-aged vervets. Muscle volume reduction predominate the age-related reductions in PCSA. Total measured PCSA was not correlated to any measures of physical performance. No rotator cuff tears were observed. Supraspinatus volume was relatively larger and deltoid volume relatively smaller in the vervet compared with a human. CONCLUSIONS: The vervet is an appropriate translational model for age-related upper extremity muscle volume loss. Functional measures were not correlated to PCSA, suggesting the vervets may have enough strength for normal function despite loss of muscle tissue. Reduced relative demand on the supraspinatus may be responsible for the lack of naturally occurring rotator cuff tears.

Contributions of muscle imbalance and impaired growth to postural and osseous shoulder deformity following brachial plexus birth palsy: a computational simulation analysis.

PURPOSE: Two potential mechanisms leading to postural and osseous shoulder deformity after brachial plexus birth palsy are muscle imbalance between functioning internal rotators and paralyzed external rotators and impaired longitudinal growth of paralyzed muscles. Our goal was to evaluate the combined and isolated effects of these 2 mechanisms on transverse plane shoulder forces using a computational model of C5-6 brachial plexus injury. METHODS: We modeled a C5-6 injury using a computational musculoskeletal upper limb model. Muscles expected to be denervated by C5-6 injury were classified as affected, with the remaining shoulder muscles classified as unaffected. To model muscle imbalance, affected muscles were given no resting tone whereas unaffected muscles were given resting tone at 30% of maximal activation. To model impaired growth, affected muscles were reduced in length by 30% compared with normal whereas unaffected muscles remained normal in length. Four scenarios were simulated: normal, muscle imbalance only, impaired growth only, and both muscle imbalance and impaired growth. Passive shoulder rotation range of motion and glenohumeral joint reaction forces were evaluated to assess postural and osseous deformity. RESULTS: All impaired scenarios exhibited restricted range of motion and increased and posteriorly directed compressive glenohumeral joint forces. Individually, impaired muscle growth caused worse restriction in range of motion and higher and more posteriorly directed glenohumeral forces than did muscle imbalance. Combined muscle imbalance and impaired growth caused the most restricted joint range of motion and the highest joint reaction force of all scenarios. CONCLUSIONS: Both muscle imbalance and impaired longitudinal growth contributed to range of motion and force changes consistent with clinically observed deformity, although the most substantial effects resulted from impaired muscle growth. CLINICAL RELEVANCE: Simulations suggest that treatment strategies emphasizing treatment of impaired longitudinal growth are warranted for reducing deformity after brachial plexus birth palsy.

Computational sensitivity analysis to identify muscles that can mechanically contribute to shoulder deformity following brachial plexus birth palsy.

PURPOSE: Two mechanisms, strength imbalance or impaired longitudinal muscle growth, potentially cause osseous and postural shoulder deformity in children with brachial plexus birth palsy. Our objective was to determine which muscles, via either deformity mechanism, were mechanically capable of producing forces that could promote shoulder deformity. METHODS: In an upper limb computational musculoskeletal model, we simulated strength imbalance by allowing each muscle crossing the shoulder to produce 30% of its maximum force. To simulate impaired longitudinal muscle growth, the functional length of each muscle crossing the shoulder was reduced by 30%. We performed a sensitivity analysis to identify muscles that, through either simulated deformity mechanism, increased the posteriorly directed, compressive glenohumeral joint force consistent with osseous deformity or reduced the shoulder external rotation or abduction range of motion consistent with postural deformity. RESULTS: Most of the increase in the posterior glenohumeral joint force by the strength imbalance mechanism was caused by the subscapularis, latissimus dorsi, and infraspinatus. Posterior glenohumeral joint force increased the most owing to impaired growth of the infraspinatus, subscapularis, and long head of biceps. Through the strength imbalance mechanism, the subscapularis, anterior deltoid, and pectoralis major muscles reduced external shoulder rotation by 28°, 17°, and 10°, respectively. Shoulder motion was reduced by 40° to 56° owing to impaired growth of the anterior deltoid, subscapularis, and long head of triceps. CONCLUSIONS: The infraspinatus, subscapularis, latissimus dorsi, long head of biceps, anterior deltoid, pectoralis major, and long head of triceps were identified in this computational study as being the most capable of producing shoulder forces that may contribute to shoulder deformity following brachial plexus birth palsy. CLINICAL RELEVANCE: The muscles mechanically capable of producing deforming shoulder forces should be the focus of experimental studies investigating the musculoskeletal consequences of brachial plexus birth palsy and are potentially critical targets for treating shoulder deformity.

Biomechanical contributions of posterior deltoid and teres minor in the context of axillary nerve injury: a computational study.

PURPOSE: To determine whether transfer to only the anterior branch of the axillary nerve will restore useful function after axillary nerve injury with persistent posterior deltoid and teres minor paralysis. METHODS: We used a computational musculoskeletal model of the upper limb to determine the relative contributions of posterior deltoid and teres minor to maximum joint moment generated during a simulated static strength assessment and to joint moments during 3 submaximal shoulder movements. Movement simulations were performed with and without simulated posterior deltoid and teres minor paralysis to identify muscles that may compensate for their paralysis. RESULTS: In the unimpaired limb model, teres minor and posterior deltoid accounted for 16% and 14% of the total isometric shoulder extension and external rotation joint moments, respectively. During the 3 movement simulations, posterior deltoid produced as much as 20% of the mean shoulder extension moment, whereas teres minor accounted for less than 5% of the mean joint moment in all directions of movement. When we paralyzed posterior deltoid and teres minor, the mean extension moments generated by the supraspinatus, long head of triceps, latissimus dorsi, and middle deltoid increased to compensate. Compensatory muscles were not fully activated during movement simulations when posterior deltoid and teres minor were paralyzed. CONCLUSIONS: Reconstruction of the anterior branch of the axillary nerve only is an appropriate technique for restoring shoulder abduction strength after isolated axillary nerve injury. When shoulder extension strength is compromised by extensive neuromuscular shoulder injury, reconstruction of both the anterior and posterior branches of the axillary nerve should be considered. CLINICAL RELEVANCE: By quantifying the biomechanical role of muscles during submaximal movement, in addition to quantifying muscle contributions to maximal shoulder strength, we can inform preoperative planning and permit more accurate predictions of functional outcomes.

Age-related degenerative functional, radiographic, and histological changes of the shoulder in nonhuman primates.

BACKGROUND: Nonhuman primates have similar shoulder anatomy and physiology compared to humans, and may represent a previously underutilized model for shoulder research. This study sought to identify naturally occurring bony and muscular degeneration in the shoulder of nonhuman primates and to assess relationships between structural and functional aspects of the shoulder and measures of physical function of the animals. We hypothesized that age-related degenerative changes in the shoulders of nonhuman primates would resemble those observed in aging humans. METHODS: Middle-aged (n = 5; ages 9.4-11.8 years) and elderly (n = 6; ages 19.8-26.4 years) female vervet monkeys were studied for changes in mobility and shoulder function, and radiographic and histologic signs of age-related degeneration. RESULTS: Four out of 6 (4/6) elderly animals had degenerative changes of the glenoid compared to 0/5 of the middle-aged animals (P = .005). Elderly animals had glenoid retroversion, decreased joint space, walked slower, and spent less time climbing and hanging than middle-aged vervets (P < .05). Physical mobility and shoulder function correlated with glenoid version angle (P < .05). Supraspinatus muscles of elderly animals were less dense (P = .001), had decreased fiber cross-sectional area (P < .001), but similar amounts of nuclear material (P = .085). Degenerative rotator cuff tears were not observed in any of the eleven animals. DISCUSSION AND CONCLUSION: The vervet monkey naturally undergoes age-related functional, radiographic and histological changes of the shoulder, and may qualify as an animal model for selected translational research of shoulder osteoarthritis.

The science of rotator cuff tears: translating animal models to clinical recommendations using simulation analysis.

PURPOSE: The purpose of this article is to review basic science studies using various animal models for rotator cuff research and to describe structural, biomechanical, and functional changes to muscle following rotator cuff tears. The use of computational simulations to translate the findings from animal models to human scale is further detailed. METHODS: A comprehensive review was performed of the basic science literature describing the use of animal models and simulation analysis to examine muscle function following rotator cuff injury and repair in the ageing population. RESULTS: The findings from various studies of rotator cuff pathology emphasize the importance of preventing permanent muscular changes with detrimental results. In vivo muscle function, electromyography, and passive muscle-tendon unit properties were studied before and after supraspinatus tenotomy in a rodent rotator cuff injury model (acute vs chronic). Then, a series of simulation experiments were conducted using a validated computational human musculoskeletal shoulder model to assess both passive and active tension of rotator cuff repairs based on surgical positioning. CONCLUSION: Outcomes of rotator cuff repair may be improved by earlier surgical intervention, with lower surgical repair tensions and fewer electromyographic neuromuscular changes. An integrated approach of animal experiments, computer simulation analyses, and clinical studies may allow us to gain a fundamental understanding of the underlying pathology and interpret the results for clinical translation.

Computer simulation of nerve transfer strategies for restoring shoulder function after adult C5 and C6 root avulsion injuries.

PURPOSE: Functional ability after nerve transfer for upper brachial plexus injuries relies on both the function and magnitude of force recovery of targeted muscles. Following nerve transfers targeting either the axillary nerve, suprascapular nerve, or both, it is unclear whether functional ability is restored in the face of limited muscle force recovery. METHODS: We used a computer model to simulate flexing the elbow while maintaining a functional shoulder posture for 3 nerve transfer scenarios. We assessed the minimum restored force capacity necessary to perform the task, the associated compensations by neighboring muscles, and the effect of altered muscle coordination on movement effort. RESULTS: The minimum force restored by the axillary, suprascapular, and combined nerve transfers that was required for the model to simulate the desired movement was 25%, 40%, and 15% of the unimpaired muscle force capacity, respectively. When the deltoid was paralyzed, the infraspinatus and subscapularis muscles generated higher shoulder abduction moments to compensate for deltoid weakness. For all scenarios, movement effort increased as restored force capacity decreased. CONCLUSIONS: Combined axillary and suprascapular nerve transfer required the least restored force capacity to perform the desired elbow flexion task, whereas single suprascapular nerve transfer required the most restored force capacity to perform the same task. Although compensation mechanisms allowed all scenarios to perform the desired movement despite weakened shoulder muscles, compensation increased movement effort. Dynamic simulations allowed independent evaluation of the effect of restored force capacity on functional outcome in a way that is not possible experimentally. CLINICAL RELEVANCE: Simultaneous nerve transfer to suprascapular and axillary nerves yields the best simulated biomechanical outcome for lower magnitudes of muscle force recovery in this computer model. Axillary nerve transfer performs nearly as well as the combined transfer, whereas suprascapular nerve transfer is more sensitive to the magnitude of reinnervation and is therefore avoided.

Postural dependence of passive tension in the supraspinatus following rotator cuff repair: a simulation analysis.

BACKGROUND: Despite surgical advances, repair of rotator cuff tears is associated with 20-70% incidence of recurrent tearing. The tension required to repair the torn tendon influences surgical outcomes and may be dependent on the gap length from torn tendon that must be spanned by the repair. Detailed understanding of forces throughout the range of motion (ROM) may allow surgeons to make evidence-based recommendations for post-operative care. METHODS: We used a computational shoulder model to assess passive tension and total moment-generating capacity in supraspinatus for repairs of gaps up to 3 cm throughout the shoulder (ROM). FINDINGS: In 60° abduction, increased gap length from 0.5 cm to 3 cm caused increases in passive force from 3N to 58 N, consistent with those seen during clinical repair. For reduced abduction, passive forces increased substantially. For a 0.5 cm gap, tension throughout the ROM (elevation, plane of elevation, and rotation) is within reasonable limits, but larger gaps are associated with tensions that markedly exceed reported pull-out strength of sutures and anchors. Peak moment for a large 3 cm gap length was 5.09 Nm, a 53% reduction in moment-generating capacity compared to uninjured supraspinatus. INTERPRETATION: We conclude that shoulder posture is an important determinant of passive forces during rotator cuff repair surgery. Choosing postures that reduce forces intraoperatively to permit repair of larger gaps may lead to failure postoperatively when the shoulder is mobilized. For larger defects, loss of strength in supraspinatus may be substantial following repair even if retear is prevented.

Biomechanics of the Steindler flexorplasty surgery: a computer simulation study.

PURPOSE: Our goal was to investigate the capacity of a Steindler flexorplasty to restore elbow flexion to persons with C5-C6 brachial plexus palsy. In this procedure the origin of the flexor-pronator mass is moved proximally onto the humeral shaft. We examined how the choice of the proximal attachment site for the flexor-pronator mass affects elbow flexion restoration, especially considering possible side effects including limited wrist and forearm motion owing to passive restraint from stretched muscles. METHODS: A computer model of the upper extremity was used to simulate the biomechanical consequences of various surgical alterations. Unimpaired, preoperative, and postoperative conditions were simulated. Seven possible transfer locations were used to investigate the effects of choice of transfer location. RESULTS: Each transfer site produced a large increase in elbow flexion strength. Transfer to more proximal attachment sites also produced large increases in passive resistance to wrist extension and forearm supination. CONCLUSIONS: To reduce detrimental side effects while achieving clinical goals our theoretical analysis suggests a transfer to the distal limit of the traditional transfer region.