0
Scientific Articles   |    
Structural Changes in Muscle and Glenohumeral Joint Deformity in Neonatal Brachial Plexus Palsy
Simone Hogendoorn, MD, MSc1; Karlijn L.J. van Overvest, MD, MSc1; Iain Watt, FRCP, FRCR1; AnneWil H.B. Duijsens, MD1; Rob G.H.H. Nelissen, MD, PhD1
1 Departments of Orthopaedics (S.H., K.L.J.v.O., A.H.B.D., and R.G.H.H.N.) and Radiology (I.W.), Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands. E-mail address for S. Hogendoorn: s.hogendoorn@lumc.nl. E-mail address for R.G.H.H. Nelissen: r.g.h.h.nelissen@lumc.nl
View Disclosures and Other Information
Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity.

Investigation performed at the Departments of Orthopaedics and Radiology, Leiden University Medical Center, Leiden, The Netherlands

Copyright ©2010 American Society for Journal of Bone and Joint Surgery, Inc.
J Bone Joint Surg Am, 2010 Apr 01;92(4):935-942. doi: 10.2106/JBJS.I.00193
5 Recommendations (Recommend) | 3 Comments | Saved by 3 Users Save Case

Abstract

Background: 

Internal rotation contracture of the shoulder is common in children with neonatal brachial plexus palsy. A long-standing contracture may cause osseous deformities in the developing shoulder. The purpose of the study was to evaluate the relationship between osseous deformities of the glenohumeral joint and structural differences due to muscle denervation in the rotator cuff muscles.

Methods: 

One hundred and two children with residual neonatal brachial plexus palsy underwent magnetic resonance imaging of both shoulders. The glenoid version and posterior, medial, and superior subluxation of the humeral head were measured. The shapes of the glenoid and the humeral head were categorized, and the infraspinatus, supraspinatus, subscapularis, and deltoid muscles were scored as being normal, atrophic, or atrophic with fatty degeneration.

Results: 

Muscle degeneration was most prominent in the subscapularis muscle. Glenoid version correlated with the structural differences in the subscapularis muscle. Posterior subluxation of the humeral head and the shape of the glenoid correlated with all abnormal rotator cuff muscles. Superior humeral subluxation correlated only with changes in the supraspinatus muscle. Medialization and the shape of the humeral head were not associated with atrophic changes of the rotator cuff. Regeneration of the rotator cuff muscles was not significantly different in patients with a C5-C6 (C7) or a complete brachial plexus lesion. However, the changes in glenoid version, the degree of posterior humeral subluxation, and the degree of medial humeral subluxation were significantly more severe in patients with a C5-C6 (C7) lesion compared with those in patients with a complete lesion of the brachial plexus.

Conclusions: 

Structural differences in the rotator cuff muscles alter the direction of the humeral head forces on the developing glenoid fossa and can lead to osseous deformities. Glenohumeral deformities are significantly greater with a C5-C6 (C7) lesion than with a complete brachial plexus lesion in which the large internal rotators are also affected. Reducing the muscular imbalance that occurs with a C5-C6 (C7) lesion could diminish glenohumeral joint incongruency and may improve the outcome of subsequent soft-tissue release or tendon transfer surgery.

Level of Evidence: 

Prognostic Level I. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article
    Sign In to Your Personal ProfileSign In To Access Full Content
    Not a Subscriber?
    Get online access for 30 days for $35
    New to JBJS?
    Sign up for a full subscription to both the print and online editions
    Register for a FREE limited account to get full access to all CME activities, to comment on public articles, or to sign up for alerts.
    Register for a FREE limited account to get full access to all CME activities
    Have a subscription to the print edition?
    Current subscribers to The Journal of Bone & Joint Surgery in either the print or quarterly DVD formats receive free online access to JBJS.org.
    Forgot your password?
    Enter your username and email address. We'll send you a reminder to the email address on record.

     
    Forgot your username or need assistance? Please contact customer service at subs@jbjs.org. If your access is provided
    by your institution, please contact you librarian or administrator for username and password information. Institutional
    administrators, to reset your institution's master username or password, please contact subs@jbjs.org

    References

    Accreditation Statement
    These activities have been planned and implemented in accordance with the Essential Areas and policies of the Accreditation Council for Continuing Medical Education (ACCME) through the joint sponsorship of the American Academy of Orthopaedic Surgeons and The Journal of Bone and Joint Surgery, Inc. The American Academy of Orthopaedic Surgeons is accredited by the ACCME to provide continuing medical education for physicians.
    CME Activities Associated with This Article
    Submit a Comment
    Please read the other comments before you post yours. Contributors must reveal any conflict of interest.
    Comments are moderated and will appear on the site at the discretion of JBJS editorial staff.

    * = Required Field
    (if multiple authors, separate names by comma)
    Example: John Doe





    Simone Hogendoorn, MD, MSc
    Posted on August 22, 2010
    Drs. Hogendoorn and Nelissen respond to Dr. Beckerman and colleagues
    Leiden University Medical Center, Leiden, The Netherlands

    We would like to thank Beckerman and colleagues for sending a Letter to the Editor concerning our article on the role of shoulder contractures on glenohumeral joint deformity in neonatal brachial plexus palsy (NBPP).

    In our study, an MRI was undertaken if, despite intensive physical therapy, a progressive deterioration of passive external rotation in adduction was observed or a Mallet function shoulder scale for hand-to-mouth and/or hand-to-head movement was scored <31 (1). We found no significant difference in the shape of the glenoid and humeral head between the older patient groups. The shape of the glenoid and the humeral head were scored on a visual scale (categorical variable) (2,3). The glenoid version, PHHA and the acromial beaking were continuous variables. Unfortunately, as compared to continuous variables, categorical variables have been generally shown to have less statistical power (4).

    In our study the majority of patients had a C5-C7 lesion (n = 91). The fact that the shape of the glenoid and humeral head were not significantly different between the patient groups can be explained by the small number of patients with a total brachial plexus lesion, creating selection by indication bias. Furthermore a second selection bias exists due to the fact that only patients eligible for tendon transfers had an MRI.

    Since tendon transfer surgery has the aim to improve functionality, only patients with a rather functional global hand function were included for this type of surgery at our institution. Thus, patients who had a C5-T1 lesion would only have a MRI of the shoulder (i.e. indication for secondary surgery at the shoulder joint), if some functional hand function existed or could be created after tendon transfers. This in contrast to primary nerve surgery where the aim is to gain any function.

    In analogy to developmental dysplasia of the hip, glenohumeral deformities in NBPP can be considered a continuous process starting with muscular imbalance with over pull of the internal rotators with the development of glenoid retroversion and a different anatomical position of the humeral head in relationship to the glenoid fossa followed by the formation of humeral and glenoid fossa deformities (5,6). Pearl et al. found a significant association between age and the severity of glenoid deformities (3). It will be interesting to evaluate the difference in glenoid and humeral head anatomy between older non-operated patients with a C5-C6 (C7) lesion versus a total lesion of the brachial plexus. In our study, the degree of glenoid retroversion, posterior humeral subluxation and medial subluxation was significantly more severe in patient with a C5-C6 lesion compared to those with a complete lesion of the brachial plexus. The fact that glenohumeral joint deformities are less severe in patients with a complete brachial plexus lesion might indicate that muscle paralysis is joint protective.

    Beckerman et al.questioned our theoretical reasoning. Contractures might be the reflection of an over pull of the internal rotator, but might also be a position created by co-contraction of both internal and external rotators. The latter has been discussed by van Dijk (7), who states that by aberrant nerve outgrowth may be an important contributor to disordered movement since it misleads central control. The child in NBPP might have apraxia of his affected arm with probable disturbance of the central program (7,8). In either case, over pull of the internal rotator or reducing activity in co-contraction would rebalance muscular action across the joint.

    We suggested that sequential injection of BoTN-A into the large internal rotators during the development of the glenohumeral joint could prevent glenohumeral joint deformities in children with a C5-C7 lesion. As describe by Goblets et al., BoTH-A has never been used in children without proven glenohumeral joint deformities to improve the muscular balance and development of a congruent glenohumeral joint before secondary orthopaedic surgery (9). The effect of BoTH-A on a denervated muscle with atrophy, fibrosis and fatty degeneration seems to be of no importance. However, BoTH-A injection into the less affected large internal rotators, like subscapularis (SC) or pectoralis major muscle might be beneficial. If BoTH-A is injected in a contracted SC muscle, it might open a time window for reducing the internal rotation contracture with physical therapy (i.e. elongation the muscle fibers).

    What the effect will be of botulin toxin A (BoTN-A) in C5-C6 (C7) lesions at the long run (at least one year) on recurrence of contractures remains to evaluated in at least an observational study, followed eventually by an RCT in preferably a single muscle. In literature, the use of BoTN-A has been used only once in the subscapularis muscle,as injection of the two parts of the subscapularis muscle is technically demanding. At our institution this is performed under general anesthesia in the lateral decubital position. The greater pectoral muscle is easier accessible, thus more papers might be published on this technique. Irrespective of this, the main contributor to the internal rotation contracture should be addressed, the subscapularis seems to important (10).

    We would like to thank Beckerman and colleagues for their discussion, which might give the unraveling of the cause-effect relationship between deformities and muscular changes in nerve injuries an extra impulse.

    References

    1. Hogendoorn S, van Overvest KL, Watt I, Duijsens AH, Nelissen RG. Structural changes in muscle and glenohumeral joint deformity in neonatal brachial plexus palsy. J Bone Joint Surg Am. 2010;92:935-42.

    2. Mallet J. [Obstetrical paralysis of the brachial plexus. II. Therapeutics. Treatment of sequelae. Priority for the treatment of the shoulder. Method for the expression of results]. Rev Chir Orthop Reparatrice Appar Mot. 1972;58:Suppl 1:166-8. French.

    3. Pearl ML, Edgerton BW. Glenoid deformity secondary to brachial plexus birth palsy. J Bone Joint Surg Am. 1998;80:659-67.

    4. Lazic SE. Why we should use simpler models if the data allow this: relevance for ANOVA design in experimental biology. BMC Physiol. 2008;8:16.

    5. Avisse C, Gomes H, Delvinquiere V, Ouedraogo T, Lallemand A, Delattre JF, Flament JB. Anatomic study of the pre- and neonatal hip. Physiopathologic considerations on dysplasia and congenital dislocation of the hip. Surg Radiol Anat. 1997;19:155-9.

    6. ter Steeg AM, Hoeksma AF, Dijkstra PF, Nelissen RG, De Jong BA. Orthopaedic sequelae in neurologically recovered obstetrical brachial plexus injury. Case study and literature review. Disabil Rehabil. 2003;25:1-8.

    7. van Dijk JG, Pondaag W, Malessy MJ. Obstetric lesions of the brachial plexus. Muscle Nerve. 2001;24:1451–61.

    8. DeMatteo C, Bain JR, Galea V, Gjertsen D. Botulinum toxin as an adjunct to motor learning therapy and surgery for obstetrical brachial plexus injury. Dev Med Child Neurol. 2006;48:245–52.

    9. Gobets D, Beckerman H, de Groot V, van Doorn-Loogman MH, Becher JG. Indication and effects of botulinum toxin A for obstetric brachial plexus injury: a systematic literature review. Dev Med Child Neurol. 2010;52:517-28.

    10. Carlioz H, Brahimi L. [Place of internal disinsertion of the subscapularis muscle in the treatment of obstetric paralysis of the upper limb in children]. Ann Chir Infant. 1971;12:159-67. French.

    Heleen Beckerman, PhD, PT
    Posted on July 28, 2010
    The Role of Shoulder Contractures in Neonatal Brachial Plexus Palsy
    Dept Rehabilitation Medicine VU University Medical Center, Amsterdam, The Netherlands

    To the Editor:

    We would like to compliment Hogendoorn and colleagues on their large correlational study on the relationship between glenohumeral joint deformity and muscular atrophy on average 5 years (sd 3.4 yr) after the onset of a neonatal brachial plexus injury (NBPI) (1). The 102 participating children were all eligible for orthopaedic surgery (1). Besides other deformities found, the shape of the glenoid was affected in 68% of the children, and the humeral head was affected in 47% of the children (1). Muscle degeneration was predominantly seen in the subscapularis muscle in 87% of the children, but was also present in the other rotator cuff muscles. These results correspond with results found in 24 younger children (2).

    In the Abstract, the authors conclude that reducing the muscular imbalance could diminish glenohumeral joint incongruency (1). We assume that these children indeed were operated on by the orthopaedic surgeons, and we are looking forward to the results of this orthopaedic intervention study and the effects on the glenohumeral joint deformities of these children.

    Although no significant differences in the shape of the glenoid and the humeral head and atrophic changes of the rotator cuff muscles were found between children with a total brachial plexus injury and children with a C5-C6 (C7) lesion, the authors remain within their conception that total muscle paralysis is joint protective. We are curious about the arguments they have to have. Moreover, the preventive use of botulinum toxin A (BoNT-A) to temporarily paralyze large internal rotator muscles is recommended (1). We wonder, however, whether there is really a role for BoNT- A injections in fatty, atrophic muscles to prevent shoulder joint deformity and to treat muscle contractures in NBPI. In a recently published review about indications and effects of BoNT-A in NBPI, internal rotation/adduction contracture of the shoulder muscles was one of four treatment indications identified (3). In 11 of the 12 reviewed studies, BoNT-A treatment included the pectoralis muscle and/or the latissimus dorsi muscle. Injections of the subscapularis muscle alone, was studied once. In most studies, BoNT-A treatment was given in combination with surgical reconstruction of an already structural joint deformity, or muscle transfer to improve muscle imbalance. Unfortunately, effects on glenohumeral joint deformity were not described (3).

    Shoulder deformities develop early in life (4). The developmental course of musculoskeletal deformities was recently studied in neonatal mice, denervated within 24h after birth (5,6). Shoulder contractures were observed from week two onwards, and other remarkable changes, such as hypoplasia of the humeral head, delayed mineralization, replacement of atrophic muscle tissue by fat, were also observed (5,6). These observations are in concordance with human studies. However, subscapularis muscle biopsies of 13 children with internal rotation contractures were essentially normal, and do support the theory of increased activity rather than denervation (7).

    In conclusion, to unravel the cause-effect relationship between glenohumeral joint deformities and muscular changes in neonatal children with a brachial plexus injury, and to differentiate primary joint lesions (i.e. not because of a trauma but because of denervation of the joint and muscles) (5,6,8) from secondary joint lesions (i.e. secondary to muscular imbalance and long-standing contractures) (1), a prospective, repeated-measures design in a large inception cohort of newborns, with a long-term follow-up of at least four years, is needed.

    The authors did not receive any outside funding or grants in support of this research for or preparation of this work. Neither they nor a member of their immediate family received payments or other benefits or a commitment or agreement to provide such benefit from a commercial entity

    References

    1. Hogendoorn S, van Overvest KL, Watt I, Duijsens AH, Nelissen RG. Structural changes in muscle and glenohumeral joint deformity in neonatal brachial plexus palsy. J Bone Joint Surg Am. 2010;92:935-42.

    2. van Gelein Vitringa VM, van Kooten EO, Jaspers RT, Mullender MG, van Doorn-Loogman MH, van der Sluijs JA. An MRI study on the relations between muscle atrophy, shoulder function and glenohumeral deformity in shoulders of children with obstetric brachial plexus injury. J Brachial Plex Peripher Nerve Inj. 2009;4:5. Erratum in: J Brachial Plex Peripher Nerve Inj. 2009;4:9.

    3. Gobets D, Beckerman H, de Groot V, Van Doorn-Loogman MH, Becher JG. Indications and effects of botulinum toxin A for obstetric brachial plexus injury: a systematic literature review. Dev Med Child Neurol. 2010;52:517-28.

    4. van der Sluijs JA, van Ouwerkerk WJ, de Gast A, Wuisman PI, Nollet F, Manoliu RA. Deformities of the shoulder in infants younger than 12 months with an obstetric lesion of the brachial plexus. J Bone Joint Surg Br. 2001;83:551-5.

    5. Kim HM, Galatz LM, Patel N, Das R, Thomopoulos S. Recovery potential after postnatal shoulder paralysis. An animal model of neonatal brachial plexus palsy. J Bone Joint Surg Am. 2009;91:879-91.

    6. Kim HM, Galatz LM, Das R, Patel N, Thomopoulos S. Musculoskeletal deformities secondary to neurotomy of the superior trunk of the brachial plexus in neonatal mice. J Orthop Res 2010 Mar 11. [Epub ahead of print]

    7. Hultgren T, Einarsson F, Runesson E, Hemlin C, Fridén J, Ljung BO. Structural characteristics of the subscapularis muscle in children with medial rotation contracture of the shoulder after obstetric brachial plexus injury. J Hand Surg Eur Vol. 2010;35:23-8.

    8. Midrio M. The denervated muscle: facts and hypotheses. A historical review. Eur J Appl Physiol. 2006;98:1-21.

    Related Content
    The Journal of Bone & Joint Surgery
    JBJS Case Connector
    Topic Collections
    Related Audio and Videos
    PubMed Articles
    Clinical Trials
    Readers of This Also Read...
    JBJS Jobs
    04/16/2014
    Georgia - Choice Care Occupational Medicine & Orthopaedics
    11/15/2013
    Louisiana - Ochsner Health System
    03/05/2014
    OK - The University of Oklahoma
    04/16/2014
    OH - OhioHealth Research and Innovation Institute (OHRI)