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

Crouch, Dustin L.; Hutchinson, Ian D.; Plate, Johannes F.; Antoniono, Jennifer; Gong, Hao; Cao, Guohua; Li, Zhongyu; Saul, Katherine R.

doi:10.2106/jbjs.n.01247

Cited by 29 publications

(43 citation statements)

References 32 publications

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“…In the control and forelimb suspension groups, no significant side-to-side differences were found for any of the metrics, apart from the pectoralis major muscle mass in the control group, which was lower in the sham limb (right) compared to the unimpaired limb (left) as previously reported 39 . This was expected, because the sham surgery involved a transverse infraclavicular incision through the pectoralis major to expose the brachial plexus.…”

Section: Resultssupporting

confidence: 81%

“…The torso was then fixed in 10% neutral buffered formalin for two days and stored in 70% ethanol at 4°C until muscle dissection. In 11 rats (5 control, 3 suspension, 3 amputation), 10 muscles surrounding the shoulder and upper forelimb were dissected bilaterally and stored in 70% ethanol at 4°C until architecture analysis: pectoralis major, acromiodeltoid, spinodeltoid, biceps long head, biceps short head, subscapularis, supraspinatus, infraspinatus, teres major, and triceps long head 39 . In the remaining 11 rats (3 control, 3 suspension, 5 amputation), four muscles (biceps long head, biceps short head, upper and lower subscapularis) were harvested bilaterally for composition analysis.…”

Section: Methodsmentioning

confidence: 99%

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Forelimb unloading impairs glenohumeral muscle development in growing rats

Merritt

2020

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1Proper joint loading is essential for healthy musculoskeletal development. Many pediatric 2 neuromuscular disorders cause irreversible muscle impairments resulting from both physiological 3 changes and mechanical unloading of the joint. While previous studies have examined the effects 4 of hindlimb unloading on musculoskeletal development in the lower limb, none have examined 5 solely forelimb unloading. Thus, a large deficit in knowledge of the effect of upper limb unloading 6 exists and must be addressed in order to better understand how the glenohumeral joint adapts 7 during development. Two forelimb unloading models were developed to study the effects of 8 varying degrees of unloading on the glenohumeral joint in growing rats: forelimb suspension (n=6, 9 intervention 21 days post-natal) with complete unloading of both limbs via a novel suspension 10 system and forearm amputation (n=8, intervention 3-6 days post-natal) with decreased loading and 11 limb use in one limb after below-elbow amputation. After 8 weeks of unloading, changes in muscle 12 architecture and composition were examined in ten muscles surrounding the shoulder. Results 13 were compared to control rats from a previous study (n=8). Both methods of altered loading 14 significantly affected muscle mass, sarcomere length, and optimal muscle length compared to 15 control rats, with the biceps long head and triceps long head observing the most marked 16 differences. Forearm amputation also significantly affected muscle mass, sarcomere length, and 17 optimal muscle length in the affected limb relative to the contralateral limb. Muscle composition, 18 assessed by collagen content, remained unchanged in all groups. This study demonstrated that 19 forearm amputation, which was administered closer to birth, had greater effects on muscle than 20 forelimb suspension, which was administered a few weeks later than amputation. 21 22 23Mechanical loading is critically important for healthy musculoskeletal development 1,2 and 24 maintenance 3,4 . In adult murine models, unloading via hindlimb suspension, microgravity during 25 spaceflight, and muscle paralysis causes changes in muscle architecture. For example, unloading 26 in adult murine animals caused substantial reductions of 41-66% in skeletal muscle size, mass, and 27 strength 6,8,9 , as well as up to 13% longer sarcomere lengths 8 . However, muscle composition 28 measured by collagen content was unaffected by unloading in adult rodents 7,11 . In growing 29 animals, unloading is particularly impactful, causing irreversible musculoskeletal changes 5,12,56 , 30 including altered joint morphology 12 , which influences surrounding muscle, and decreased muscle 31 mass by over 3 to 5-fold 5,56 . However, the effects of unloading on other muscle architecture metrics 32 (e.g., sarcomere length, optimal muscle length) and muscle composition (e.g., collagen content) 33 have not previously been examined in growing animals. 34Unloading models have traditionally focused on the hindlimbs 15 , resulting i...

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Section: Resultssupporting

confidence: 81%

Section: Methodsmentioning

confidence: 99%

Forelimb unloading impairs glenohumeral muscle development in growing rats

Merritt

2020

Preprint

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“…Multiple studies have attributed contractures and bony deformity to muscle imbalance due to weak extensors and external rotators [26][27][28]. However, recent murine and computational studies have found that impaired longitudinal muscle growth results in more pronounced osseous deformity than muscle imbalance [29,30].…”

Section: Natural Historymentioning

confidence: 99%

The natural history and management of brachial plexus birth palsy

Buterbaugh

Shah

2016

Curr Rev Musculoskelet Med

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Brachial plexus birth palsy (BPBP) is an upper extremity paralysis that occurs due to traction injury of the brachial plexus during childbirth. Approximately 20 % of children with brachial plexus birth palsy will have residual neurologic deficits. These permanent and significant impacts on upper limb function continue to spur interest in optimizing the management of a problem with a highly variable natural history. BPBP is generally diagnosed on clinical examination and does not typically require cross-sectional imaging. Physical examination is also the best modality to determine candidates for microsurgical reconstruction of the brachial plexus. The key finding on physical examination that determines need for microsurgery is recovery of antigravity elbow flexion by 3-6 months of age. When indicated, both microsurgery and secondary shoulder and elbow procedures are effective and can substantially improve functional outcomes. These procedures include nerve transfers and nerve grafting in infants and secondary procedures in children, such as botulinum toxin injection, shoulder tendon transfers, and humeral derotational osteotomy.

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“…This study was performed using humeri and scapulae obtained from a previous study (Crouch 2015). (19) All animal procedures were approved by the Institutional Animal Care and Use Committee at the Wake Forest School of Medicine. Sixteen Sprague Dawley rat pups (Harlan Laboratories, Indianapolis, Indiana) were grouped according to surgical intervention implemented five days after birth: neurectomy and sham ( n =8 each) (Figure 1).…”

Section: Methodsmentioning

confidence: 99%

“…These relationships were evaluated using both the microstructural metrics from this study and the macrostructural metrics from the previous study using these same bones (humeral head width, thickness, and curvature; glenoid inclination and curvature) (Crouch 2015). (5) For analysis 4, length-scale relationships between the glenohumeral joint macrostructure and underlying trabecular microstructure were assessed by stepwise multiple regression with forward selection, using Schwarz Bayesian information criterion to determine which trabecular microstructural properties (predictor variables) best explained the variability in the macrostructural measurements in the humeral head (width, thickness, and curvature) and glenoid fossa (inclination and curvature). Microstructural values from the humeral epiphysis and glenoid zone 3 (Z3) were used for the correlations and multiple regressions, since these regions were closest to, and thus most relevant to, the articulating glenohumeral joint.…”

Section: Methodsmentioning

confidence: 99%

Characterizing Trabecular Bone Properties near the Glenohumeral Joint Following Brachial Plexus Birth Injury

Eb¹,

Cm²,

Af³

et al. 2020

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1Brachial plexus birth injury (BPBI) causes functional arm impairment in 30-40% of those affected 2 due to altered loading on the glenohumeral joint. While gross morphological osseous deformities 3 have been seen in the humerus and scapula, alterations in the underlying trabecular bone 4 microstructure and mineralization are not clear. Using a murine model of BPBI, trabecular bone 5 alterations were explored in the proximal humerus and distal scapula, which surround the 6 articulating surface of the joint. Samples were scanned using micro-CT, reoriented, and analyzed 7 for standard trabecular metrics. The regions of interest closest to the articulating surface showed 8 the greatest detriments. In the scapula, the scapular neck region showed less robust trabecular bone 9 in the neurectomy group with decreased BV/TV (p=0.001), BMD (p=0.001), Conn.D (p=0.006), 10 Tb.N (p<0.0001), and DA (p=0.033), and increased Tb.Sp (p<0.0001) compared to sham. In the 11 humerus, the epiphysis showed less robust trabecular bone in neurectomy group, but to a much 12 lesser extent than the scapular neck. The neurectomy group showed reduced BMD (p=0.007) and 13 Tb.N (p=0.029) compared to sham. Data suggest deformities are worse near the articulating 14 surface, likely due to the greater amount of mechanical loading. The reduction in trabecular 15 microstructure and mineralization may compromise bone strength of the affected limb following 16 BPBI. Further investigation of the underlying trabecular bone deformities following injury are 17 necessary to eventually inform better treatments to limit the development of deformities. 18 19 Keywords 20 brachial plexus birth injury, trabecular microstructure, bone mineral density, glenohumeral joint 21 25the mechanical loading of the joint, which is critical for normal bone and joint development. 26Regions in the glenohumeral joint experience abnormal growth and macrostructural deformities are comprised primarily of cancellous bone, which plays an integral role in transferring joint 29 loading along the bone and is known to adapt to altered loads (Wolff, 1892(Wolff, /1986 Frost, 1994). 30Trabecular bone loss has been observed in many reduced loading scenarios, such as 31 spaceflight (7) (Vico et al., 2000), prolonged bedrest (8) (Kazakia et al., 2014), and spinal cord injury 32 (Eser et al., 2004). (9) However, the nature and extent of trabecular bone changes after BPBI are 33 not well understood. While no human BPBI study has examined bone microstructural properties, 34 several studies using murine BPBI models have reported trabecular bone detriments in the humeral 35 head, with fewer and thinner trabeculae and greater separation compared to contralateral limb and 36 sham control groups (10)(11)(12) (Kim, 2009; Kim, 2010; Potter, , 2014). These trabecular changes were 37 observed in conjunction with global musculoskeletal changes, including humeral anteversion and 38 glenoid retroversion (10,11) (Kim et al., 2009; Kim et al., 2010), as well as decreased supraspinatus 39 muscle volum...

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

Abstract: 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.

Cited by 29 publications

References 32 publications

Forelimb unloading impairs glenohumeral muscle development in growing rats

Forelimb unloading impairs glenohumeral muscle development in growing rats

The natural history and management of brachial plexus birth palsy

Characterizing Trabecular Bone Properties near the Glenohumeral Joint Following Brachial Plexus Birth Injury

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