magnetic resonance imaging and ultrasonography in brachial ... · months of age in infants with...
TRANSCRIPT
Department of Diagnostic Radiology
Helsinki University Central Hospital University of Helsinki, Finland
Department of Surgery
Hospital for Children and Adolescents Helsinki University Central Hospital
University of Helsinki, Finland
MAGNETIC RESONANCE IMAGING AND ULTRASONOGRAPHY
IN BRACHIAL PLEXUS BIRTH INJURY
Tiina Pöyhiä
Academic Dissertation To be presented with the permission of
The Faculty of Medicine of the University of Helsinki, For public discussion in Small Hall, Main building of the University of Helsinki,
On 20th of May 2011 at 12 noon.
Helsinki 2011
Supervised by Docent Antti Lamminen
Helsinki Medical Imaging Center Helsinki University Central Hospital
Department of Diagnostic Radiology, University of Helsinki Helsinki, Finland
Docent Jari Peltonen Department of Orthopaedics
Hospital for Children and Adolescents
Helsinki University Central Hospital Helsinki, Finland
Reviewed by Docent Kimmo Mattila
Medical Imaging Centre of Southwest Finland Turku University Hospital
Department of Diagnostic Radiology, University of Turku Turku, Finland
Docent Timo HurmeDepartment of Pediatric Surgery
Turku University Hospital
University of Turku Turku, Finland
To be discussed with Professor Osmo Tervonen
Department of Diagnostic Radiology Oulu University Hospital
University of Oulu Oulu, Finland
ISBN 978-952-92-8894-6 (pbk.)ISBN 978-952-10-6939-0 (PDF)
Unigrafia Oy, YliopistopainoHelsinki 2011
To Reino
CONTENTS
LIST OF ORIGINAL PUBLICATIONS….....………………………………………………. 7
ABBREVIATIONS……………………………………………………………………………. 8
ABSTRACT …...…………………………………………………………………………........ 9
INTRODUCTION ……….....……………………………………………………………….... 11
REVIEW OF THE LITERATURE …………………………………………………………. 12
ETIOLOGY OF BRACHIAL PLEXUS BIRTH INJURY……………………………… 12
EPIDEMIOLOGY OF BPBI……...……………………………………………………... 13
ANATOMY OF THE BRACHIAL PLEXUS…………………………………………... 14
PATHOMECHANICS OF BPBI……...………………………………………………… 14
PROGNOSIS OF BPBI……...…………………………………………………………... 17
DIAGNOSIS OF BPBI……...…………………………………………………………… 18 Clinical findings……...…………………………………………………………... 18 Electromyography ……...…………………….…………………………..……… 21 Somatosensory evoked potential ……...…………………………………………. 21 Radiography……...……………………………………………………………….. 21 Conventional arthrography……...………………………………………………... 24 Ultrasonography ……...…………......…………………………………………… 24 Conventional myelography and Computed tomography myelography…………... 25 Computed tomography ……...…………………………………………….……... 27 Magnetic resonance imaging ……...……………………………………...…….... Imaging of the nerves……...……………………………………………… Imaging of the muscles……...…………………………………………….. Imaging of the bony structures……...……………………………………..
27283031
Magnetic resonance arthrography……...………………………………………… 31
TREATMENT OPTIONS IN BPBI……………………………………………………... Conservative treatment……...…………………………………………………….
3232
Brachial plexus reconstruction……...……………………………………………. 32 Botulinum toxin treatment……...……………………………………………….... 34 Secondary operative treatment……...……………………………………………. 35 Tendon surgery……...……………………………………………………... 35 Relocation…………………………………………………………….……. 37 Osteotomy of the humerus…………………………………………………. 38
AIMS OF THE STUDY ………………………………………………………………………... 39
I US screening for GH join instability in BPBI……...…………………………………..... 39 II MRI of rotator cuff muscle changes related to GH joint pathology in BPBI………….. 39 III Muscle changes in BPBI with elbow flexion contracture …………………………...... 39 IV MRI evaluation of surgically treated shoulder girdle in BPBI ……...……………….... 39
MATERIALS AND METHODS ……...………………………………………………………. 40
PATIENTS……...…………………………………………………………………………. 40 US screening for GH joint instability in BPBI (I) ……...……………………………. 40 MRI of rotator cuff muscle changes related to GH joint pathology in BPBI (II) …… 40 Muscle changes in BPBI with elbow flexion contracture (III) ……...………………. 40 MRI evaluation of surgically treated shoulder girdle in BPBI (IV) ……...………….. 41
HEALTHY CHILDREN……...…………………………………………………………... 41
METHODS ……...………………………………………………………………………... 41 US screening for GH joint instability in BPBI (I) ……...…………………………… 41
MRI of rotator cuff muscle changes related to GH joint pathology in BPBI (II) …... 43 Muscle changes in BPBI with elbow flexion contracture (III) ……...……………… 46 MRI evaluation of surgically treated shoulder girdle in BPBI (IV) ……...…………. 47
STATISTICAL ANALYSIS ……...…………………………………………………….... 50
RESULTS ………………………………………………...…………………………………….. 51
US screening for GH joint instability in BPBI (I) ……...…………………………… 51 MRI of rotator cuff muscle changes related to GH joint pathology in BPBI (II) …... 59 Muscle changes in BPBI with elbow flexion contracture (III) ……...……………… 61 MRI evaluation of surgically treated shoulder girdle in BPBI (IV) ……...…………. 64
DISCUSSION …………………………………………...……………………………………... 67
Early detection of posterior subluxation of the humeral head……...…………..……. 67 MRI of muscle and articular changes in late sequlae in permanent BPBI……...…… 70 Imaging findings after treatment of BPBI……...……………………………………. Role of imaging in BPBI……...………………………………………………….…...
7576
Methodological considerations……...……………………………………………….. 77Implications for possible future studies……...………………………………………. 78
CONCLUSIONS……...………………………………………………………………………… 79
ACKNOWLEDGEMENTS ……...…………………………………………………………… 80
APPENDIX ……….....…………………………………………………………………….…... 82
REFERENCES ………………………………………………………………………………... 88
7
LIST OF ORIGINAL PUBLICATIONS
This thesis is based on the original articles, which are referred to in the text by their Roman
numerals I-IV:
I Pöyhiä T, Lamminen A, Peltonen J, Kirjavainen M, Willamo P, Nietosvaara Y.
Brachial Plexus Birth injury: US screening for glenohumeral joint instability. Radiology
2010;254(1):253-260.
II Pöyhiä T, Nietosvaara Y, Remes V, Kirjavainen M, Peltonen J, Lamminen A.
MRI of rotator cuff muscle atrophy in relation to glenohumeral joint incongruence in
brachial plexus birth injury. Pediatr Radiol 2005;35:402-409.
III Pöyhiä T, Koivikko M, Peltonen J, Kirjavainen M, Lamminen A, Nietosvaara Y.
Muscle changes in brachial plexus birth injury with elbow flexion contracture: an MRI
study. Pediatr Radiol 2007;37:173-179.
IV Pöyhiä T, Lamminen A, Peltonen J, Willamo P, Nietosvaara Y.
Treatment of shoulder sequelae in brachial plexus birth injury. Acta Orthopaedica.
Accepted for publication.
The publishers of original publications kindly granted their permission to reproduce the articles in
this thesis.
8
ABBREVIATIONS
BPBI brachial plexus birth injury
CT computed tomography
DW diffusion-weighted
EMG electromyography
ENMG electroneuromyography
FCU flexor carpi ulnaris
F0-F3 degree of fatty infiltration 0-3
GH glenohumeral
GHJ glenohumeral joint
GSA glenoscapular angle
MR magnetic resonance
MRI magnetic resonance imaging
PD proton density
PER passive external rotation
PHHA percentage of humeral head anterior to the middle of the glenoid fossa
ROM range of motion
SR0-SR2 size reduction 0-2
SE spin echo
SEP somatosensory evoked potential
STIR short time to inversion recovery; short tau inversion recovery
T tesla
TA time of aquisition
TAM total active motion
TE time to echo
TM teres major
TR time of repetition
T1 longitudinal relaxation
T2 transverse relaxation
T2* transverse relaxation obtained using gradient echo sequences
US ultrasonography/ ultrasound
9
ABSTRACT
Brachial plexus birth injury (BPBI) is caused by traction of the head during delivery. The upper
brachial plexus (C5-C6) is most commonly affected. Despite advances in obstetrics the incidence of
BPBI varies from 1 to 4 per 1000 living births in western countries. Mild injuries, in which the
nerve has only been stretched, will heal and patients will recovery completely, but in permanent
palsy patients may require operative treatment. Diagnostic imaging is needed to determine the
correct surgical treatment. Delayed diagnosis can lead to deterioration of the glenohumeral joint and
poor patient outcome.
This study is focused on imaging findings in permanent brachial plexus birth injury. Such findings
include ultrasound screening for posterior shoulder subluxation, and MRI evaluation of rotator cuff
muscle changes in relation to glenohumeral joint pathology and muscle changes in BPBI with
elbow flexion contracture. Additionally the outcome of surgical treatment of glenohumeral joint
deformity was evaluated.
The results of the present population-based study show that in Helsinki during years 2003-2006,
among 132 BPBI patients out of 41980 born neonates (3.1 per 1000), 27 (0.64 per 1000) of the
BPBI cases did not heal during the first year of life and the palsy was considered permanent. One-
third of these permanent BPBI patients developed posterior subluxation of the humerus during the
first year of life. The rate of posterior subluxation was even higher among BPBI patients sent from
the tertiary catchment area (I). All rotator cuff muscles, especially the subscapular muscle were
atrophic in patients with internal rotation contracture (II). Every studied BPBI patient with elbow
flexion contracture had fatty infiltration and size reduction of the supinator muscle, and pathological
changes also occurred in the brachialis muscle (III). In all patients for whom the relocation
operation was successful (10/13 of these undergoing the surgery) congruency of the glenohumeral
joint improved, with mean glenoid version improvement of 33º (IV).
In conclusion, ultrasound (US) screening of the glenohumeral joint should be performed at 3 and 6
months of age in infants with persisting symptoms of BPBI, because the risk for shoulder instability
is high during the first year of life (I). Imbalance of the shoulder muscles leads to progressive
glenoid retroversion, subluxation of the humeral head and internal rotation contracture (II).
Brachialis muscle pathology seems to be the main cause of elbow flexion contracture. The more
severely affected the pronator teres muscle, the more restricted the prosupination movement (III).
10
Glenohumeral joint deformity in BPBI can be treated by shoulder relocation in young patients.
Among patients younger than 5 years, successful relocation of the humeral head results in
remodeling of the glenohumeral joint (IV).
11
INTRODUCTION
Brachial plexus birth palsy was described in 1779 by Smellie (Smellie 1779). Nearly one hundred
years later Duchenne presented a case report of four neonates with upper plexus injuries (Duchenne
1872). Erb gave his name to typical upper root injury by localising the lesion at the junction of the
C5 and C6 roots by electrical stimulation (Erb 1874). Klumpke, the first female medical intern in
Paris, added to the medical knowledge of her day with a report of a lower plexus lesion with
possible involvement of sympathetic fibres causing Horner´s syndrome (Klumpke 1885).
Maternal diabetes is the main etiologic risk factor for macrosomia, which predisposes a fetus to
shoulder dystocia (Acker et al. 1985, Bradley et al. 1988). Despite the increased glucose balance
during pregnancies of diabetic mothers, macrosomia has not decreased during the last 25 years
(Teramo 1998). It has been shown that shoulder dystocia leads to brachial plexus birth injury
(BPBI) in 26% of deliveries of babies with a birth weight over 4500g (Rouse et al. 1996). In
addition to macrosomic children (+ 2 SD) in vertex presentation, small children in breech
presentation are also in danger of BPBI. The severity of the injury varies from mild nerve stretching
of the brachial plexus, to rupture of the nerves or to total avulsion of the nerve roots from the spinal
cord. The majority of children with BPBI recover within the first year of life, but 25% develop
permanent palsy (Andersen et al. 2006). Muscle imbalance as a result of nerve injury may lead to
internal rotation contraction of the shoulder, and retroversion of the glenoid with subluxation of the
humeral head. If elbow flexion has not recovered at all within 3-9 months, a primary plexus
reconstruction operation is performed (Clarke and Curtis 1995). In spite of possible primary
operations, continued restriction of total active movement of the hand or secondary bony
deformities may require additional surgical corrections (Leffert 1998).
In addition to clinical findings and electromyography (EMG), diagnostic imaging will help to
evaluate the need for and type of treatment required. Magnetic resonance imaging (MRI) allows
non-invasive visualisation of possible root avulsion without contrast agent, which is needed in
myelography and computer tomography (CT) -myelography studies (Gasparotti et al. 1997). Plain
radiographs demonstrate fractures and deformities of the bones. With ultrasonography (US),
possible posterior subluxation of the humeral head can be detected without sedation of the patient
(Saifuddin et al. 2002). MRI allows evaluation of the muscles, cartilage and unossified bony
structures. In this study possible pathological shoulder and elbow joint changes in BPBI were
analyzed using ultrasound or magnetic resonance imaging.
12
REVIEW OF THE LITERATURE
ETIOLOGY OF BRACHIAL PLEXUS BIRTH INJURY
Since 1779, when Smellie ascribed paralysis of the arm of neonate to delivery, the discussion about
etiologic factors has been vigorous. Poliomyelitis, toxin agents, congenital syphilis and infective or
ischemic factors have been suggested as reasons for brachial plexus palsy. Despite the colorful
discussion in the past, the obstetric origin of brachial plexus injury among newborns has been
widely accepted. Sever emphasized the role of traction of the brachial plexus during delivery as a
cause of BPBI (Sever 1916). Diabetes, macrosomy, shoulder dystocia and operative vaginal
delivery (forceps or vacuum extraction) have been accepted as important risk factors for BPBI.
When birthweigth increased from less than 3500g to more than 4500 g, the incidence of BPBI was
45 times higher in a Swedish study (Bager 1997). A previous child with obstetric brachial palsy and
multiparity are regarded as additional risk factors (Gherman et al. 2003). Also, excessive maternal
weight gain during pregnancy has been reported to predispose the mother to delivery problems and
the infant to BPBI (Lewis et al. 1998). In a recent retrospective study based on the Swedish Medical
Birth Registry, the rates of BPBI increased significantly during the period 1987-1997 (Mollberg et
al. 2005). Thus maternal obesity in western countries seems to increase brachial plexus birth
injuries. The incidence of BPBI increased from 0.1 % to 0.5 % when body mass index registered at
first visit at the maternal center increased from under 19 to over 30 in the above mentioned study
(ibid.). The majority of BPBI babies are delivered from vertex presentation (Wolf et al. 2000).
Breech presentation along with high birth weight results in a higher risk of BPBI (Soni et al. 1985).
McFarland et al. were the first to report BPBI after cesarean section (McFarland et al. 1986).
Despite the known risk factors, shoulder dystocia remains partly unpredictable, besides after
cesarean section (Backe et al. 2008). BPBI has also been reported after breech presentation of a
child with 830g birth weight (McFarland et al. 1986).
13
EPIDEMIOLOGY OF BPBI
The reported incidence of BPBI varies over ten-fold in western countries (Adler and Patterson
1967, Hoeksma et al. 2000) (Table 1).
Table 1. Incidence of BPBI
Author and year Area Incidence per 1000Adler and Pattersson 1967 New York/ USA 0.38Hardy 1981 Auckland/ New Zealand 0.87Levine et al. 1984 Ohio/ USA 2.6Jackson et al. 1988 California/ USA 2.5Sjöberg et al.1988 Malmö/ Sweden 1.9Alanen 1989 Turku/ Finland 1.8Walle and Hartikainen-Sorri 1993 Oulu/ Finland 2Bhat et al. 1995 Pondicherry/ India 1.0Gilbert et al. 1999 California/ USA 1.5Hoeksma et al. 2000 Amsterdam/ Holland 4.6Donelly et al. 2002 Dublin/ Ireland 1.5Evans-Jones et al. 2003 United Kingdom, Ireland 0.42Dahlin et al. 2007 Malmö/ Sweden 3.8Backe et al. 2008 Trondheim/ Norway 3
The number of permanent cases among BPBI has been estimated to vary from 14% to 20% (Rust
2000, Noetzel et al. 2001), while in the population-based study 25% of children with BPBI in
Sweden had persistent functional and cosmetic abnormalities of the upper limb (Sjöberg et al.
1988). Andersen et al. also concluded that in 25% of cases of BPBI, symptoms remain permanent
(Andersen et al. 2006). Although risk for shoulder subluxation associated with BPBI was reported
at the beginning of the last century (Whitman 1905, Fairbank 1913, Sever 1925), few subsequent
reports have been published. Babitt and Cassidy considered the shoulder instability to be rare
(Babitt and Cassidy 1968). Polloc and Reed reported 4 posterior subluxations out of 11 patients
with BPBI (Polloc and Reed 1989). 62% (26/42) of patients imaged with either CT or MRI in order
to evaluate associations between functional limitations, muscular deformity and persistent palsy had
posterior subluxation in a study performed by Waters et al. (Waters et al. 1998). In the population-
based study from Malmö, Sweden, the incidence of posterior dislocation of the shoulder has been
calculated as being 0.28 per 1000, (7.3%, 6/82) of all BPBI patients during a 6-year study period
(Dahlin et al. 2007). In the North American study Moukoko et al. reported posterior shoulder
instability in eleven (8%) out of 134 neonates with BPBI (Moukoko et al. 2004).
14
ANATOMY OF THE BRACHIAL PLEXUS
The brachial plexus is a complicated cable network which is formed by the ventral rami of the
lowest four cervical and first thoracic spinal nerve roots (C5-T1) (Appendix, Fig.1). These roots
fuse to three trunks: upper (C5-C6), middle (C7) and lower (C8-T1). Each trunk divides into two
parts, resulting altogether in six divisions: anterior and posterior, each having upper, middle and
lower trunks. These six divisions further form three cords: posterior, lateral and medial. Anterior
divisions of the upper and middle trunks (C5-C7) unite to form the lateral cord. Posterior divisions
of all three trunks (C5-T1) join to form the posterior cord, while the anterior division of the lower
trunk (C8-T1) continues as the medial cord. The cords are then divided into 5 nerves: the ulnar
nerve originates from the medial cord, the median nerve from the medial and lateral cords, the
musculocutaneus nerve from the lateral cord, and the axillary and radial nerves from the posterior
cord. Through this network creation every nerve gets fibers from several spinal roots, which
minimizes the risk of possible damage for example in the case of root avulsion. According to the
microscopic study, the adult brachial plexus consists of an average of 118 047 myelinated nerve
fibers (range 85 566-166 214) (Bonnel 1984). Roughly, C5 and C6 innervate the muscles of the
shoulder region, arm and elbow, and C7 muscles of the forearm and partly of the wrist. C8 and T1,
in turn, innervate muscles of the hand and fingers. The brachial plexus is located under the
sternocleidomastoid muscle, between the anterior and medial scalene muscles (Appendix, Fig.2).
The clavicle protects the brachial plexus at the level of plexus divisions (Kawai 2000).
PATHOMECHANICS OF BPBI
Fetomaternal disproportion may lead to lateral traction of the head away from the shoulder causing
nerve injury during labor. This is confirmed in the study of Walle and Hartikainen-Sorri, who found
that two-thirds of shoulder injuries involved the anterior shoulder after strong traction of the head in
order to liberate the shoulder behind the symphysis in delivery. The posterior shoulder, which was
affected in one-third of cases, was most probably compressed against the sacral promontory of the
mother (Walle and Hartikainen-Sorri 1993). In breech presentation, if the body is pulled out
strongly during delivery while the arm has been slipped up over the bent head, the pulling forces
over-stretch or even tear the nerves. C8-T1 roots are especially vulnerable to avulsions, because
there is poor connective tissue support around these nerves. On the other hand C5 and C6 roots
seldom avulse, because they are fixed with ligaments to the osseus margins of the foraminas
15
(Bonnard and Anastakis 2001). Nonetheless, when rare upper root avulsions appear, they have been
strongly associated with breech presentation (Geutjens et al. 1996).
Depending on the degree of damage, the conductivity of the nerves may be diminished or
completely destroyed. At the neural level the injury may lead to demyelination, axonal degeneration
or avulsion of the nerve root from the spinal cord. The clinical consequences of the nerve injury
include disruption of the motor and possibly also sensory function. Seddon classified nerve injury
into three types: neurapraxia lesions, axonotmesis and neurotmesis (Seddon 1942). The mildest type
of injury is neuropraxia (the myelin sheath is damaged around the intact axon), where stretching of
the nerve resolves completely (remyelination) within the first months of life. In the more severe
injury, called axonotmesis, Wallerian degeneration of the axon takes place distal to the site of
injury. While the endoneural tube remains intact, the axon regenerates at a rate of 1 to 2 mm per day
(Brushart 1999). This axonal regeneration usually results in recovery. In the most severe type of
neural injury, neurotmesis, the axon as well as the surrounding connective tissue are damaged. In
the case of total nerve rupture or avulsion spontaneous recovery does not occur (Hentz and James
1999).
Already at the beginning of the last century, Whitman classified shoulder dislocation in young
children as belonging to three categories: 1. True congenital displacement of the humeral head,
which he regarded as very rare; 2. traumatic dislocations occurring during delivery; and 3. aquired
subluxation resulting from injury to the brachial plexus (Whitman 1905). Intrauterine or congenital
dislocation of the humeral head is very rare (Heilbonner 1990). Zancolli and Zancolli regarded
humeral epiphyseolysis to be due to obstetric trauma, and is often present in the case of internal
rotation contracture of the shoulder, joint deformity and posterior subluxation of the humeral head
(Zancolli and Zancolli 1993). They also presumed that during labor a direct muscle lesion occurs
at the same time as the plexus injury, which is followed by fibrosis of the muscles and scar
contractions (Zancolli and Zancolli 2000). The above theory is not widely accepted. Only a few
studies support the theory that the humeral head dislocates during delivery at the same time as
brachial plexus injury occurs (Thomas 1914) and is maintained by the muscle imbalance
(Dunkerton 1989, Troum et al. 1993). Most authors think that the posterior subluxation of the
humeral head develops gradually as a result of the muscle imbalance (Fairbank 1913, Gilbert
1993, Waters et al. 1998). In most BPBI patients, the strength of the internal rotators dominate,
leading to an internally rotated position of the arm and to a reduced range of motion (Gilbert
1993). Bone and cartilage remodel according to the mechanical relation to the muscle action and
16
joint reaction forces (Johnstone and Foster 2001). During prolonged internal rotation the pressure
of the humeral head is directed to the posterior corner of the glenoid, resulting in a more posterior
position of the humeral head and increased retroversion of the glenoid (Pearl et al. 2003).
Pathomechanics in the elbow is analogous to that in the shoulder region: muscle imbalance leads to
a decreased range of motion, which results in soft tissue contractures, bony deformities and possibly
dislocations (Waters 2005). The initial muscle imbalance leading to pronation of the forearm may
change in the long-term depending on the recovery process. Normal prosupination movement
requires functioning of the biceps brachii, brachioradialis, pronator teres, pronator quadratus and
supinator. Pronation or supination contracture may develop with or without interosseus membrane
contraction and subluxation/dislocation of the radius or the ulna (Zancolli and Zancolli 2000).
Aitken reported 27 (25.2%) posterior dislocations of the radial head with bowing of the ulna out of
107 patients with BPBI. An additional 6 (5.6%) patients had anterior dislocation of the humeral
head in the same study, resulting in an incidence of 30.8% for bony deformity in the elbow region
(Aitken 1952). The first signs of bony malformation and incipient posterior subluxation of the radial
head were seen radiographically as early as two months of age in the above mentioned study (ibid).
Ballinger and Hoffer followed 121 patients with Erb´s C5-6 palsies for at least 2 years (average
follow-up was over 6 years). Patients with elbow surgery, radial head dislocations, elbow
subluxations or mixed palsy with affision of the lower roots were excluded from the series giving
38 patients with classic C5-6 palsy for follow-up. 34 of these 38 patients had elbow flexion
contracture (Ballinger and Hoffer 1994). Elbow extension deficit has been reported in 90% of
permanent BPBI patients in Sweden (Strömbeck et al. 2007). Patients with permanent BPBI have
frequently limitations of forearm rotation. 86% patients with permanent BPBI symptoms had active
pronation beneath normal values and 64% had active supination below normal values in the study
of Sibinski et al. (Sibinski et al. 2007).
Delayed maturation of the bony structures has been reported in association with BPBI (Polloc and
Reed 1989). Bae et al. measured size differences in the affected and uninvolved upper extremities
(Bae et al. 2008). Their study demonstrated that the affected upper extremity was approximately
95% of the length and girth of the contralateral upper limb. The difference was statistically
significant (p<0.01). The nerve injury and weakened power of the muscles may be reasons for the
decreased growth potential (ibid.).
17
PROGNOSIS OF BPBI
According to the study of Gherman et al. the outcome of BPBI is difficult to predict on the basis of
ante-or intrapartum characteristics (Gherman et al. 2003). Patients with permanent brachial plexus
injury had a higher mean birth weight, but otherwise there were not significant differences in ante-
or intrapartum characteristics between temporary (transient) and permanent brachial plexus injuries
(ibid.). Hoeksma et al. concluded that a complete neurological recovery occurs in 66 % of patients,
and the extent of recovery seemed not to be predictable on the basis of direct initial post partum
symptoms (Hoeksma et al. 2004). In other studies the rate of full recovery in BPBI has been
reported to be between 13%-80% (Wickström et al. 1955, Gordon et al. 1973, Lindell-Iwan et al.
1995, Evans-Jones et al. 2003). Bennet and Harrold reported permanent palsy in 25% of patients;
the higher the number of affected roots, the worse the recovery rate (Bennet and Harrold 1976). In
the case of full recovery, which occurred among three out of every four of their patients, the
symptoms disappeared within the first five months. Also, patients with persistent symptoms showed
partial recovery (ibid.).
In a population-based retrospective study with a mean follow-up time of 13.3 years, the extent of
the brachial plexus birth injury was the most important prognostic factor for predicting the final
outcome in 112 patients who had undergone brachial plexus surgery (Kirjavainen et al. 2007).
ROM and strength of the affected upper limb was better preserved in patients with C5-C6 injury
than in those with C5-T1 injury in a 12 year follow-up study (Kirjavainen et al. 2011).
If symptoms persist, any developing internal rotation contracture is commonly followed by glenoid
deformity. Pearl and Edgerton recommend early imaging with a modality that will visualize the
skeletally immature glenohumeral joint. According to their experience, the passive external rotation
may become restricted as early as in the first six months of life (Pearl and Edgerton 1998).
Hoeksma et al. detected a strong association (P=0.004) between shoulder contracture and osseus
deformity in a retrospective study done in Amsterdam evaluating the outcomes for 52 children with
BPBI at a mean age of 3.7 years, born between years 1991 and 1998 (Hoeksma et al. 2003). In this
study, the prevalence of a shoulder contracture (>10º) was 56% (29/52) and osseus deformity 33%
(16/48 patients with complete radiographic follow-up) (ibid.).
18
DIAGNOSIS OF BPBI
Clinical findings
It is important to have a thorough patient history. Type of delivery, presentation, possible use of
forceps or suction cup, shoulder dystocia, birth weight and Apgar scores give valuable information
needed to evaluate neonates. The strength of all muscles, possible contractures, range of motion and
especially shoulder abduction and external rotation are assessed. Palpation gives information
regarding possible clavicle or humeral fractures. Among older children who can play or follow
instructions, range of motion is graded with the Mallet scale (Figure 1) in order to evaluate shoulder
function. In this assessment, shoulder function is evaluated in 5 different movements: abduction,
external rotation, hand to neck, hand to back and hand to mouth. Each movement is then graded for
1 to 5 points, where 1 indicates no function and 5 normal function (Mallet 1972). A goniometer is
used for measurements of both active and passive ranges of motion of the forearm (Americal
Academy of Orthopaedic Surgeons 1988). Sensibility may be assessed for each dermatomy using
filament tests and stereognosis when needed.
Table 2. Sequels of BPBI
Main symptoms Main muscles affected Extent of root injuryFunctional deficit* inexternal rotation of the shoulder,abduction, elbow flexion,supination,(±) wrist extension
deltoid, supraspinous, infraspinous,biceps, brachial, coracobrachial,brachioradial, supinator,(±) radial wrist extensors
C5-C6
all above movements andextension of the elbow, wrist,and fingers
all above muscles and teres major,triceps, extensors/ flexors of wrist,extensors of the fingers
C5-C7
flexion of the fingers flexor digitorum superficiale/profundus, flexor pollicis longus,interossei and lumbrical muscles
C8, T1#
all above movements � flail hand all the above muscles C5-T1
* Degree of the functional deficit vary from mild to severe. # Horner´s syndome may follow.(Leffert 1998). (±) may or may not be present.
19
The strength of the unaffected muscles dominates the clinical findings, resulting in the so-called
“waiter`s tip” position, characteristic for upper plexus lesions in BPBI. This typical posture is due to
the injury in the upper trunk (C5 and C6), which results in weakness of the abductors and external
rotators of the shoulder, flexors and supinators of the elbow and extensors of the wrist (Table 2). At
the same time unaffected internal rotators and adductors, elbow extensors and wrist flexors
(Appendix, Figs. 3-6) remain powerful by innervation received from the middle trunk and C7. As a
result of this muscle imbalance, the shoulder is adducted and internally rotated, elbow extended
with forearm pronated and the wrist and fingers are flexed. If the upper plexus injury is extended to
root C7, the involvement of the radial nerve may cause a sight flexion of the elbow. In the case of
injury to the entire plexus, all the muscles may be affected, resulting in flail arm with no movement.
An isolated lower plexus lesion with decreased grip power of the hand is very rare (Sever 1916).
Horner syndrome (ptosis, miosis, enophtalmos, anhidrosis) may be associated with avulsion of T1.
Clavicle fracture has to be taken into account as a differential diagnostic possibility in cases where
there is a lack of shoulder movements of the newborn baby. Neonates with BPBI findings also have
to be evaluated for possible associated injuries such as facial or phrenic nerve palsy.
20
Figure 1. Mallet´s classification of function in brachial plexus birth injury (From Gilbert 1993,
with permission).
21
Electromyography (EMG)Terzis et al. has recommended electromyography (EMG) for assessing brachial plexus injury
(Terzis et al. 1986). EMG measures the function of the motor unit, which includes the anterior horn
cell in the spinal cord, the axon, neuromuscular synapse, and muscle connected with it. Function of
peripheral sensory fibres can be assessed with EMG. EMG may be used to assess the extent of the
injury, possible need for surgery and progression of recovery (Smith 1996). In the case of
denervation, the nerve does not conduct electrical signals any more, and muscle cells develop
fibrillation as a sign of denervation activity. Due to gradual Wallerian degeneration it takes 2 to 3
weeks before the fibrillation appears. This spontaneous muscle activity disappears when muscle
fibres either degenerate or innervate. It may be challenging to insert EMG needles into neonates,
because EMG diagnosis requires measurements of several muscles. Denervation appears and
disappears earlier among neonates than adults (Vredeveld 2001) and can lead to underestimation of
the severity of the nerve injury (Vredeveld et al. 2000). Recovery can be observed earlier among
neonates using EMG, because distances are shorter although the axons grow at the same speed as in
adults (Vredeveld 2001).
Somatosensory evoked potential (SEP)With somatosensory evoked potentials, the electrical stimulation of the peripheral nerve is
measured from the cortex. If there is a lesion in the somatosensory pathway, the stimulation does
not reach the cortex. Using SEP the proximal root damage can beneficially be detected and the
conductivity of nerve stumps assessed prior to grafting (Landi et al. 1980). Intraoperatively the
functional continuity between proximal stump of the ruptured root and cortex can be assessed
(ibid.). Jones reported that surgical findings were in good agreement with those seen on SEP (Jones
1979).
RadiographyDuring the neonatal period, radiographs are obtained to identify fractures and dislocations.
Discontinuity of the cortex can be seen in cases of nondislocated clavicle fractures. The hump-like
elevation of the bone contour is evident in 8 or 9 days after fracture as a sign of callus formation
(Silverman and Kuhn 1993). Fractures of the clavicle or humerus usually heal without
complications, but they may sometimes hide the symptoms of BPBI.
22
The position of the unossified humeral head and possible posterior subluxation are difficult to
depict on plain radiographs in neonates. Odgen et al. studied the radiologic development of the
humerus among 23 children, from newborn to 14 years old. A proximal humeral ossification center
was radiographically invisible in all three of the studied full-term stillborn babies, but it had
appeared by 3 months of age among the other three studied children (Odgen et al. 1978). Goddard
states that the humeral ossification center is visible on plain radiographs in approximately 20% of
newborns during the first week of life, and the ossification center of the greater tuberosity appears
between 6 to 8 months of age (Goddard 1993). The main ossification center is always located
medially with respect to the line going along the long axis of the humerus. True epiphyseolysis of
the humeral head may be challenging to diagnose among young children because capital epiphysis
may imitate epiphyseolysis due to internal rotation associated with BPBI (ibid.). Posterior
dislocation of the ossified humeral head can be verified with axial radiographs (Figure 2), which
will show the humeral head lying posterior to the glenoid (Dunkerton 1989). BPBI-associated bony
anomalies including hypoplastic humeral head, an inferiorly directed coracoid and tapered acromion
can additionally be visualized with plain radiographs (Sever 1925). BPBI patients may present
delayed ossification of the epiphyseal centers on the affected side (Pollock and Reed 1989). The
findings for acquired glenoid deformity resulting from BPBI may be similar to those for congenital
glenoid deformity seen, for example, in Apert syndrome, Hurler syndrome, mucopolysaccharidosis
VI, oculo-mandibulo-melic dysplasia, Pierre Robin syndrome, and TAR syndrome (Lachman
2007). The glenoid deformity seen in BPBI is usually unilateral, while underdevelopment of the
glenoid is bilateral in most of the above-mentioned syndromes (Currarino et al. 1998). BPBI may
result in up to 6-8 cm growth retardation of the arm (Narakas 1987). McDaid et al. used plain
radiographs to evaluate the length discrepancy of the affected upper limb compared to the
unaffected side in 22 children with BPBI. The length of the affected upper limb was on average
92% of that of the upper limb on the healthy uninvolved side. The retardation in size is most
probably due to the lack of biomechanical function and stress that is needed for optimal
development (McDaid et al. 2002).
If there is concern about possible diaphragmatic paralysis, conventional chest films may provide
useful information. This information is especially important before anesthesia for surgical
procedures and also medico-legally.
Intraoperative fluoroscopy or plain radiographs are used to verify the position of the bones as well
as fixation material needed in humeral rotation osteotomy (Bae and Waters 2007).
23
Figure 2. Radiograph demonstrates posterior dislocation of the humeral head on the left side in AP
(B) and axial (D) views compared to the right healthy side (A,C). Patient has C5-7 injury, no
previous surgical procedures performed.
right left
right left
A B
C D
24
Conventional arthrographyConventional arthrography has been used in evaluation of birth injuries of the shoulder (White et al.
1987). Pearl and Edgerton performed intraoperative arthrograms to assess BPBI-associated
pathological changes of the glenohumeral joint and they classified the shape of the glenoid as being
normal, flat, biconcave or pseudoglenoid (Pearl and Edgerton 1998). The glenoid surface was
regarded as pseudoglenoid when the posterior aspect of the glenoid was clearly retroverted both in
relation to the unoccupied anterior concavity and to the plane of the scapula (ibid.). A few years
later they compared MRI, intraoperative arthrography and arthroscopic findings with each other and
concluded that if MRI is not available, arthrography at the time of the surgery is informative (Pearl
et al. 2003). Kon et al. correlated intraoperative arthrography findings with the degree of passive
external rotation among 64 children with internal rotation contracture secondary to BPBI. They
concluded that intraoperative arthography correlated with the degree of internal rotation contracture
(Kon et al. 2004). Nowadays invasive arthrography has been replaced with preoperative MRI.
Ultrasonography (US)Musculoskeletal ultrasound is a widely used, non-invasive and inexpensive imaging modality,
which can be used without sedation for neonates and infants (Keller 2005). Ultrasonography (US)
has proved to be useful in detecting glenohumeral effusion in septic arthritis (ibid.), slipped
humeral epiphyses (Zieger et al. 1987, Broker and Burbach 1990), posterior displacement of the
humeral head in BPBI (Hunter et al. 1998, Saifuddin et al. 2002) and rotator cuff pathology
(Daenen et al. 2007). US is therefore a good method in making differential diagnosis and
assessment of shoulder joint pathology in patients with BPBI. The accuracy of US in clavicular
fractures has been assessed by Graif et al. 1988, and Grissom and Harcke 2001. In the case of new
clavicle fractures, soft tissue swelling and discontinuity of the cortex may be seen. After a couple
of weeks a healing fracture with callus is seen as a hump-like elevation of the bone contour, while
the normal clavicle has a mildly s-shaped structure on US (Katz et al. 1988).
US of the plexus area
A few studies have reported the use of US in assessment of the brachial plexus. Nerve bundles are
seen as hypoechoic structures (Sheppard and Lyer 1998, Shafighi et al. 2003). Haber et al.
demonstrated the use of US in detection of brachial plexus traction injuries among adults (Haber et
al. 2006). US succeeded in visualizing scar tissue seen as a hyperechoic area, but could not
distinguish the nerve from the scar and failed to follow the continuity of the nerve. Furthermore,
25
US was unsuccessful in the detection of the neuroma, later found during operation. Visualization
of C5-C7 levels was possible using US, but not nerve roots C8 and T1, which are located too deep
and caudally. The attachments of the nerve roots to the spinal cord were also hidden behind bone
shadows (ibid.). With these limitations, US is a challenging tool even in experienced hands for
detection of brachial plexus nerve lesions among neonates, who have thinner nerve structures than
adults.
US of the shoulder girdle
US enables dynamic investigation of shoulder instability (Bianchi et al. 1994, Schydlowsky et al.
1998). US is therefore a suitable method for differential diagnosis and assessment of shoulder joint
pathology in patients with BPBI. Although US is a widely-used method for assessing hip dysplasia
and instability screening (Harcke and Grissom 1990, Holen et al. 1994 , Holen et al. 1999), it is
infrequently used as a screening method for BPBI-associated posterior subluxation of the humeral
head. Hunter et al. presented the use of a posterior approach with US to detect posterior
subluxation of the humeral head (Hunter et al. 1998). Moukoko et al. tried to verify posterior
shoulder dislocation with a lateral approach, and noticed that the growing ossification center
obscures visibility of the glenoid area (Moukoko et al. 2004). In their study, posterior shoulder
instability was detected visually with US at a mean age of 6 months. In the case of posterior
displacement, the center of the humeral head was located posterior to the axis of the scapula
(Moukoko et al. 2004). Vathana et al. described measurement of the �-angle to assess the posterior
subluxation of the humeral head. The �-angle is measured between the line along the posterior
margin of the scapulae and the line tangent to the humeral head. Normally the �-angle is 30º or
less, while posterior subluxation increases the angle value (Vathana et al. 2007).
Conventional myelography and computed tomography myelographyConventional myelograms with intrathecal contrast medium were previously used to verify root
avulsions (Murphey et al. 1947). In the case of root avulsion, a dural covered diverticulum
containing cerebrospinal fluid may be formed (Figure 3), even extending through the intervertebral
foramen and this can be seen on a myelogram (Petras et al. 1985). However, nerve root avulsions
have also been reported without dural abnormalities (Davies et al. 1966). Nagano et al. have even
reported normal roots despite a meningocele configuration on myelogram, most probably due to
dural rupture without discontinuity of the nerve rootlets (Nagano et al. 1989). That is why
visualization of the nerve root itself is necessary when interpreting scans. Since Sir Godfrey
26
Hounsfield invented CT in the early 1970s, CT has little by little become a diagnostic tool for nerve
root injuries (Marshall and De Silva 1986, Cobby et al. 1988). However, even in the beginning of
the 1990s Hashimoto et al. concluded in their study that myelography is necessary for preoperative
evaluation of cervical nerve root avulsion associated with birth palsy, because using CT
myelography it was difficult to verify nerve root avulsions with no associated traumatic
meningocele (Hashimoto et al. 1991). The possible reason for these difficulties with CT diagnostics
was that their CT-study was performed using 5 mm thick sections and only axial images were
available. Since that time the CT-technique has developed considerably (Volle et al. 1992). CT
myelography images were obtained by performing scanning 90 to 120 minutes after intrathecal
injection of a water-soluble contrast agent into the lumbar spinal canal (Carvalho et al. 1997).
Walker et al. obtained 95% sensitivity and 98% specificity for complete nerve root avulsions with
CT myelography using 1 mm contiguous axial images in infants and 3 mm slice thickness in adults
(Walker et al. 1996). Nowadays, conventional myelography has been replaced by cross-sectional
imaging techniques. Three-dimensional rotational CT-myelography has been successfully used
especially among adults following cervical puncture at C1/C2 level (Kufeld et al. 2003). The
possible risk related to allergic reactions, radiation, sedation and the time needed to complete the
imaging procedure are limitations for CT myelography in small children (Birchansky and Altman
2000).
Figure 3. Radiographs demonstrate meningocele at the level of C7 root on the left side in
myelogram obtained with intrathecal contrast medium.
ap lateral
C7C7
27
Computed tomography (CT)Computed tomography has been used to evaluate the brachial plexus from its origin to the axillary
area (Fishman et al. 1986, Armington et al. 1987, Cooke et al. 1988). CT does not reveal detailed
information of the thin nerves of the plexus area, although it can delineate the surrounding
landmarks: anterior and middle scalene muscles, subclavian and axillary arteries and veins, clavicle
and neural foramina.
The bony structures of the shoulder girdle and possible dislocation of the humeral head can be
visualized easily with CT (Hernandez and Dias 1988, Beischer et al. 1999). Friedman et al. first
described of technique to measure the glenoid version of the shoulders in the axial plane (Friedman
et al. 1992). Mintzer et al. demonstrated that the glenoid is normally most retroverted in the first
two years of life and after that the retroversion diminishes gradually, reaching adult glenoid
orientation (-1.7º±6.4º) during the 10 first years of life (Mintzer et al. 1996). Waters et al. assessed
the amount of posterior subluxation using CT or MRI by measuring the percent of the humeral head
situated anterior to the line drawn through the medial tip of the scapula and the midpoint of the
glenoid (Waters et al. 1998). Terzis et al. were the first to demonstrate on CT that glenohumeral
joint congruency can be restored by palliative surgery for shoulder deformities in BPBI. Their study
included pre-and postoperative CT scans of 28 patients treated in their clinic over 18 years (Terzis
et al. 2003). Due to radiation exposure, CT has nowadays often been replaced with MRI, which
additionally allows visualization of the cartilage and soft tissues.
Magnetic resonance imaging (MRI)After Sir Peter Mansfield and Paul C. Lauterbur developed magnetic resonance for medical imaging
in the 1970s, MRI has added imaging capabilities with multiplanar images and good tissue contrast
(Mansfield and Maudsley 1977, Lauterbur 1980). With a strong magnet, using radiofrequency
transmit and receiver coil system images are obtained without ionizing radiation. The potential of
MRI in the musculoskeletal system imaging aroused great interest already in the beginning of the
1980s (Pettersson et al. 1985).
Magnetic resonance imaging is a non-invasive imaging modality for both traumatic and
nontraumatic brachial plexopathies (Miller et al. 1993, Sureka et al. 2009) and gives good soft
tissue contrast (Flanders et al. 1990). T1-weighted images with a short echo time (TE) and short
repetition time (TR) allow good resolution of anatomical details due to a relatively high signal-to-
28
noise ratio. T2-weighted images (long TE, long TR) demonstrate water content in various tissues,
while the signal-to-noise ratio is usually lower than in T1-weighted images. Fat-supression
techniques are used to reduce or null the signal from fat, which is often utilized in the detection of
increased fluid concentration in tissues. T1-weighted fat-supression techniques are utilized in
contrast enhanced studies (Tanttu and Sepponen 1996).
Imaging of the nervesIf a lesion of the central nervous system is suspected, evaluation with MRI is warranted. MRI has
proven superior in the detection of small extra-axial fluid collections, and white matter and
brainstem injuries associated with birth trauma (Barkovich 2005). MRI can visualize intradural
lesions, for example intra-medullary odema and haemorrhage, without radiation and contrast agents
(Flanders et al. 1990). Cerebrospinal fluid (CSF) acts as a natural contrast agent around affected
nerve roots (Rapoport et al. 1988 Popovich et al. 1989, Posniak et al. 1993, Yilmaz et al. 1999).
Nerve roots are clearly visualized in the axial plane as they exit the foramina (de Verdier et al.
1993). Doi et al. reported in their study 92.9% sensitivity and 81.3% specificity for detecting root
avulsions with MRI among adults (Doi et al. 2002). However, some studies have shown a low
accuracy for MRI. The study by Ochi et al. in adults reported accuracies of 73% for C5 and 64% for
C6 root avulsions using MRI (Ochi et al. 1994). Medina et al. reported only 50% sensitivity but
100% specificity for nerve root avulsions in cases of pseudomeningocele among children less than
18 months of age. In the above mentioned study they used FSE T2- and FSE T1-weighted
sequences with slice thicknesses of 1.5 to 4 mm. (Medina et al. 2006). Due to the small dimensions
of newborns, imaging of the nerves is very challenging. MR images are sensitive to motion
artefacts, which may interfere with the interpretation of the images (Carvalho et al. 1997). Sedation
or general anesthesia is needed to guarantee that the little child does not move during the
examination procedure. Imaging protocols vary depending upon the facilities in different
institutions. Recently, the technology has developed considerably. 3 D MR myelography has been
recommended as an imaging modality of first choice, because it showed in traumatic brachial
plexus injuries 92% diagnostic accuracy, 89% sensitivity and 95% specificity (Gasparotti et al.
1997). CT myelography can then be reserved as an imaging possibility in cases where there are
discrepancies between clinical, electromyographic and 3D MR myelographic findings (ibid.). With
3D heavily T2-weighted MR myelography sequences (CISS 3 D, True FISP 3D, BFFE and
FIESTA) root avulsions and nerve retraction balls are better assessed (Vargas et al. 2010). Modern
29
technology can allow 0.5 mm slice thickness, which allows good visualization of the preganglionic
roots and possible avulsions (Figure 4).
Figure 4. Coronal BFFE-image with 0.5 mm slice thickness showing an avulsion of the right C8-
root with a meningocele of a 4-month old girl with BPBI on the right side.
MR neurography has been used to evaluate peripheral nerves of the brachial plexus (van Es 2001,
Filler et al. 2004, Smith et al. 2008). The brachial plexus is difficult to visualize because it runs
obliquely to all of the three standard orthogonal planes. Trunks are best visualized in an oblique
coronal plane and the cords in either an oblique coronal or sagittal plane (Panasci et al. 1995). Blair
et al. described in 1987 the anatomic details of the brachial plexus assessed with MRI for the first
time. The brachial plexus was seen best in the sagittal plane, and signal intensity was similar to that
of the muscle: low in both T1- and T2- weighted images (Blair 1987). The neurovascular bundle is
surrounded by fat, which gives a good contrast to the nerves (Sherrier and Sostman 1993). Gupta el
al. reported that operative findings confirmed focal fibrosis, neuromas and scarring in complete MR
evaluation of the brachial plexus (Gupta et al. 1989). The sensitivity and specificity of MRI have
been reported to be 97% and 100% respectively in BPBI-associated post-traumatic neuroma.
BFFE cor 0.5 mm
C 8
30
Neuroma can be seen as a high signal intensity mass on T2-weighted and STIR images (Medina et
al. 2006).
Imaging of the musclesMRI is the only imaging method that shows the early phase of muscle denervation before fatty
infiltration develops (Shabas et al. 1987). MRI shows muscle edema as a high signal intensity on
T2-weighted images highlighted by the fat-suppression technique. The short tau inversion recovery
(STIR) sequence is ideal for detecting skeletal muscle edema because increased edema is additive
with signal intesity (Fleckenstein et al. 1991). MRI can detect the signal intensity changes in
denervated muscles earlier than EMG, i.e. already 4 days after injury (West et al. 1994). MRI of the
muscle has been suggested to be particularly useful among children who may be difficult to assess
by clinical and electrodiagnostic examination (ibid). In chronically denervated muscles, fatty
infiltration is seen on T1-weighted images as high signal intensity in addition to muscle atrophy
(Fleckenstein et al. 1993). Hence MRI is a suitable method for grading muscle pathology, as shown
in the study of Mahjneh et al. (Mahjneh et al. 2004). Nakagaki et al. used the largest width of the
supraspinatus muscle belly and the length of the muscle measured from coronal oblique MRI
images to estimate size and atrophy of the muscle atrophy after rotator cuff tear (Nakagaki et al.
1995). Thomazeau et al. measured supraspinatus belly atrophy by calculating the ratio between the
cross-section of the supraspinatus muscle and the largest bony limits for supraspinatus fossa in a Y-
shaped position (Thomazeau et al. 1996). A Y-shaped view in the oblique-sagittal plane is obtained
at the most lateral point where the scapular spine is in contact with the rest of the scapula. Zanetti et
al. extended the quantification of the muscles to the cross-sectional areas of the subscapular and
infraspinous/teres minor muscles in the same Y position (Zanetti et al. 1998). Rotator cuff muscle
volumes were assessed using shoulder MRI in the study performed by Lehtinen et al. (Lehtinen et
al. 2003).
Bredella et al. correlated MRI findings with electrophysiologic findings and concluded that MRI
can supplement information obtained from EMG by allowing the age (acute/chronic) of the muscle
lesion to be approximated, possibly showing the morphologic cause of the lesion (Bredella et al.
1999). Nerve entrapment syndromes, such as posterior interosseus nerve and radial tunnel
syndromes, have to be taken into account as different diagnostic possibilities in the evaluation of
muscle edema or atrophy of the supinator and extensor muscles (Rosengren et al. 1997, Bordalo-
Rodriques and Rosenberg 2004). The posterior interosseus nerve arises from the radial nerve and
penetrates the supinator muscle. The nerve is most commonly compressed at the arcade of Frohse,
31
at the level of the cranial part of the supinator muscle resulting in muscle weakness (Bayramoglu
2004) and muscle denervation patterns in MRI (Andreisek et al. 2006). The compression of the
median nerve in pronator syndrome and the ulnar nerve in cubital tunnel syndrome as well as
anterior interosseus nerve entrapment may lead to high signal intensity changes in T2-weighted
images and further to atrophy and intramuscular fatty degeneration (bright on T1 and T2) in the
affected muscles (ibid.).
Imaging of the bony structuresMRI allows the evaluation of glenoid retroversion, possible subluxation/dislocation of the humeral
head and cartilaginous structures in the younger child (van der Sluijs et al. 2001). Gudinchet et al.
reported MRI findings of five children with BPBI-associated internal rotation contracture: a blunt
posterior glenoid surface was visualized in all patients (Gudinchet et al. 1995). Gradient echo
sequence allowed a good visualization of posterior thinning of the hyaline cartilage and
fibrocartilage of the labrum both anteriorly and posteriorly (ibid.). Waters et al. evaluated in a
prospective study the severity of the glenohumeral deformity associated with BPBI (Waters et al.
1998). They performed either MRI or computed tomography for 42 BPBI patients. The
glenoscapular angle was measured according the technique described by Friedman et al. (Friedman
et al. 1992). The degree of subluxation was graded by measuring the percentage of the humeral
head located anterior to the line going through the medial tip of the scapula and middle of the
glenoid fossa (Waters et al. 1998). They found progressive glenoscapular retroversion and posterior
subluxation of the humeral head with increasing age (ibid.). Kozin stated that failure to maintain
passive external rotation above the neutral position should be regarded as a probable sign of
underlying joint deformity (Kozin 2004). MRI gives better evaluation of the glenoid cartilage and
labrum and may be more sensitive in the early detection of glenoid deformity than arthrography
(Pearl et al. 2003). Clarification of the shape of the posterior glenoid is essential for the planning of
surgical interventions and for subsequent evaluation of postoperative outcome (Kon et al. 2004).
Magnetic resonance (MR) arthrography
MR arthrography with intra-articular contrast agent gives information especially about rotator cuff
lesions (de Jesus et al. 2009), ligament, hyaline cartilage and labral structures (Chiavaras et al.
2010). The technique is invasive and is seldom needed in children with brachial plexus birth injury.
32
TREATMENT OF BPBI
Conservative treatmentPhysical and occupational therapy is important in the treatment of brachial plexus birth injury.
Exercises to maintain the passive range of motion of the affected upper limb are teached already to
the parents of a newborn with BPBI. Active and passive range of motion exercises are useful in
preventing development of contractures. Splints and orthoses are used in cases of contractures in
order to prevent further deformity. Sensory training is recommended if sensory deficits exist.
Children are encouraged to use the weak extremity in play, age appropriate hobbies and activities
(Ramos and Zell 2000).
Brachial plexus reconstructionIn 1903 Kennedy first reported primary plexus reconstruction, done by resection of the proximal
plexus neuroma and making primary suture repair (Kennedy 1903). Tassin regarded plexus surgery
to be necessary if the biceps function had not appeared by three months of age (Tassin 1983). In
Finland, Solonen et al. and Alanen et al. reported a few decades ago successful early primary
reconstructions of the partially torn brachial plexus by either nerve grafting or direct neuroraphy
(Solonen et al. 1981, Alanen et al. 1990).
Early primary exploration and microsurgical repair may improve long-term outcome. Gilbert and
Tassin recommend make the decision about possible early brachial plexus surgery by evaluating
biceps muscle function. They recognized that if the deltoid and biceps have not started functioning
by at the age of 3 months, the outcome is poor without plexus reconstruction (Gilbert and Tassin
1984). Thus Gilbert et al. recommend plexus surgery if biceps function is completely absent at three
months of age in C5-C6 palsies. They extended the criteria for operation to complete palsies with a
flail arm and Horner syndrome after one month of age. After breech delivery, complete C5-C6
palsy with flail hand and a negative EMG without any signs of regeneration, are regarded as reason
for surgery as well (Gilbert et al. 1988). Haerle and Gilbert got encouraging results in 75% of
patients who underwent early exploration and repair of lower roots. They recommended early repair
of the avulsed lower roots with nerve transfers in cases of extensive paralysis of the hand at 3
months of age with Horner´s syndrome (Haerle and Gilbert 2004). Some authors would prefer a
longer follow-up time to select candidates for plexus surgery (Clarke and Curtis 1995). According
to the thesis of Tassin, some recovery may occur spontaneously, but the surgical results are better
33
(Tassin 1983). This was confirmed by Waters, who also followed outcome of patients who had
some recovery between the 4th and 6th months. Those patients who had plexus reconstruction done
at six months of age because of absent biceps function had a better outcome than those who had
some spontaneous recovery at the age of 5 months (Waters 1999). When biceps function is lacking
at the age of three months, some recovery may occur spontaneously, but it is less satisfactory than
that achieved with surgery, as found after a minimum two year follow-up (ibid.). When no recovery
of the muscles occurs, possible cervical avulsions should be verified before plexus surgery.
Surgical planning demands appropriate differentiation between preganglionic lesions of the nerve
rootlets and postganglionic injury. Preoperative myelography, EMG, the use of intraoperative SEP
and advanced microsurgical techniques facilitate early surgical treatment (Alanen et al. 1990).
Repair of upper roots is performed through a supraclavicular approach, while a transclavicular
approach is needed to repair a complete lesion (Gilbert 1993). A nerve stimulator is needed during
the operation. Depending on the type of injury, excision of the neuroma, end to end suture, grafting
or neurotization are performed.
Surgical treatment of a preganglionic lesion usually consists of neurotization. In neurotization, an
intact donor nerve is released from its end organ and attached to the distal part of the damaged
nerve. For example, intercostal nerves, the hypoglossal nerve or the contralateral C7 nerve are
possible candidates for nerve transfers in neurotization reconstruction (Bonnard and Anastakis
2001). When the phrenic nerve is used as an axon donor for neurotization of the musculocutaneus
nerve, there is a danger of decreased diaphragm function and vital capacity (Luedemann et al.
2002). Recently Hsu et al. reported a new technique for repairing cervical root avulsions with a
sural nerve graft (Hsu et al. 2004). They operated on eight patients, including one newborn baby
with brachial plexus birth injury. In the first part of the two stage surgery, they implanted the sural
nerve graft into the spinal cord using a posterior approach. The dura mater was incised
longitudinally and a tiny hole was made to the pia mater, thereafter the graft was fixed with fibrin
glue. The distal end of the nerve graft was protected with a Foley tube with a radiopaque clip and
placed in the supraclavicular region. After one week, the distal anastomosis was made using an
anterior approach. After a mean follow-up period of 8.87 months, they reported improvement in
electrophysiological function and muscle power grading postoperatively. Due to laminectomy, this
technique includes the risk of possible development of cervical spine deformity (Hsu et al. 2004).
34
In the case of a postganglionic lesion, the surgical planning is based on the possible continuity of
the nerve or distance between the damaged nerve ends. Neurolysis and release of adhesions may be
needed. The neuroma is excised if it decreases the nerve conductivity more than 50%. The sural
nerve is the most commonly used graft. Boome and Kaye reported good recovery with effectively
normal deltoid strength in 80% of the patients operated on using sural grafts (Boome and Kaye
1988). Nowadays, nerve grafts are glued instead of conventional suturing which minimizes damage
to the nerve ends. Either end-to-end or end-to-side anastomoses are made with fibrin glue
(Grossman 2000, Grossman et al. 2003).
Botulinum toxin treatmentPhysiotherapy should be used to prevent or minimize the development of muscle and joint
contractures. In addition to physiotherapy, botulinum toxin treatment may be used to diminish the
dominating power of unaffected muscles while waiting for nerve regeneration (Rollnik et al. 2000).
Especially the treatment of subscapular (Alfonso et al. 1998) and pectoralis major (Jellicoe and
Parsons 2008, Price et al. 2007) muscles is performed with botulinum toxin. Botulinum toxin is the
neurotoxin obtained from the anaerobic bacterium Clostridium botulinum in laboratory conditions.
Botulinum toxin prevents nerve endings from releasing acetylcholine, which is needed as a neuro
transmitter to reach the endplates of the muscle in order to cause muscle contraction. Botulinum
toxin is injected into internal rotators to allow the weak antagonist muscles to strengthen. EMG
guidance can be used but when palpation is used to identify muscles, injection into either the mid-
belly or several sites of the muscle is recommended (Childers and Markert 2007). In the study
performed by Hogendoorn et al., glenohumeral deformities were significantly greater with a C5-C6
(C7) lesion than with a total palsy in which the internal rotators were affected as well (Hogendoorn
et al. 2010). The balance between agonist and antagonist muscles is needed to prevent the
development of joint contractures and bony deformities. Early treatment with botulinum toxin may
prevent retroversion of the glenoid and development of bony deformities by balancing the effect of
the dominating muscle on immature bones (Ramachandran and Eastwood 2006). After botulinum
boxin injection immobilization of the shoulder in a spica cast in external rotation has been used in
treatment of subluxation of the humeral head (Ezaki et al. 2010). The effect of botulinum toxin lasts
approximately 3-4 months, allowing the function of the affected muscles to be restored.
35
Secondary operative treatmentIn spite of possible primary reconstruction surgery, incomplete recovery or residual dysfunction
may occur, leading to secondary deformities, which need additional operative treatment. The
surgical operation is tailored to the individual based on clinical and radiological findings. The goal
of the operation is to restore the function of the shoulder, most commonly to improve the limited
abduction and external rotation. Due to typical internal rotation contracture of the humeral head,
patients lack the ability to place the hand on the neck and they need to put the hand in the so-called
“trumpet position” (the arm is abducted as in blowing a trumpet) when lifting the hand to the
mouth. Prior to the operation the status of the glenohumeral joint has to been assessed in order to
make a choice between different types of operative treatment.
Secondary correction operations were performed already at the beginning of the last century by
Fairbank with the technique of open exploration and reduction of the glenohumeral joint after
liberation of the subscapularis tendon (Fairbank 1913). Sever developed the technique, and adviced
that opening the joint capsel should be avoided (Sever 1916). This technique was further developed
by L`Episcopo, who carried out muscle transplantation of the teres major and later on also the
latissimus dorsi muscle from the role as of internal rotators to assist weak external rotation
(L`Episcopo 1939). Wickström et al. reported excellent results using the above mentioned combined
technique in 10 out of 16 patients (Wickström et al. 1955). In a modification by Phipps and Hoffer
the pectoralis major is released, teres major and latissimus dorsi are transferred near to the insertion
of the infraspinatus into the rotator cuff (Phipps and Hoffer 1995).
Tendon surgeryShoulder
When there is internal rotation contracture with a congruent glenohumeral joint, a soft-tissue
operation alone should improve external rotation (Jellicoe and Parsons 2008). Release of tight
anterior structures, tendon lengthening and muscle transfers have been used to improve poor
external rotation (Narakas 1993). As part of the corrections, z-lengthening of the tendon of the
subscapular muscle has in particular been advocated (van der Sluijs et al. 2004, Bertelli 2009). It
has also been proposed that tendon transfers might halt the development of glenohumeral deformity
(Waters and Bae 2005).
36
If retroversion of the glenoid, humeral head flattening and possible dislocation are already present,
tendon transfers or other soft-tissue operations are not sufficient alone (Waters and Peljovich 1999,
Waters and Bae 2006). Kozin et al. assessed MRI findings in a one year follow-up study after
tendon transfers and detected no improvements in glenoid version or humeral head subluxation
(Kozin et al. 2006). To prevent deterioration of the glenohumeral joint, Gilbert et al. regarded early
release important if external rotation is less than 20 to 30 degrees (Gilbert et al. 1988). They
propose trapezius transfer to improve abduction and latissimus dorsi transfer to restore abduction
and external rotation (ibid). Many studies prefer latissimus dorsi and teres major transposition to
the infraspinatus position in order to improve weak external rotation (Waters and Bae 2005) with a
possible concomitant release of subscapular muscle (Aydin et al. 2004, Nath and Paizi 2007).
In a long-term follow-up study Pagnotta et al. reported that after latissimus dorsi transfer active
external rotation was better preserved than shoulder abduction. The function of the muscle transfers
was better maintained in patients who took part in a physiotherapy program or engaged in physical
activities, especially swimming (Pagnotta et al. 2004). Kirkos et al. published a report on a follow-
up study, conducted a mean of 30 years (range 25 to 42) after anterior release, teres major and
latissimus dorsi transfers of 10 patients with BPBI (Kirkos et al. 2005). They observed a
deterioration in early successful results by the end of the long follow-up period. This may be due to
degeneration of the glenohumeral joint, transferred muscles and surrounding soft tissues (ibid).
Elbow and forearm
To decrease limitations in forearm rotation, Zancolli has developed Z-lengthening of the biceps
tendon. The technique includes rerouting of the biceps tendon around the radius to produce
pronation. Interosseus membrane is also released if needed (Zancolli 1967). Surgical procedures are
tailored on the basis of different elbow problems including elbow flexion contracture, possible
dislocations of the radius or ulna, weak flexion and supination contracture (Hoffer and Phipps
2000). When there is elbow flexor deficiency, Steindler flexorplasty may be performed for elbow
flexion reconstruction. In this technique, described by Arthur Steindler in 1918, increased flexion is
achieved by transferring the pronator teres, flexor carpi radialis, palmaris longus, flexor carpi
ulnaris and flexor digitorum superficialis arising from the medial epicondyle of the humerus to a
more proximal position (Leffert 1998). With the above-mentioned technique, Carrol and Cartland
achieved good results in 56%, fair results in 25% and poor results in 19% of 28 cases operated on
because of poliomyelitis, or BPBI or other trauma to the brachial plexus (Carrol and Cartland
37
1953). In a series described by Al–Qattan, good results were obtained in 89% of BPBI cases (8 out
of 9) operated on using Steindler flexorplasty (Al-Qattan 2005).
Relocation of the humeral headIf muscle imbalance leads to posterior subluxation or dislocation of the glenohumeral joint,
relocation of the humeral head is needed. The glenoid surface will be better preserved if the patient
is operated on before 4 year of age (El Gammal et al. 2006). Goddard in turn stated that deformity
of the humeral head is detected increasingly among children operated on after 4 years of age
(Goddard 1993). Thus, prolonged conservative treatment may lead to a failed outcome after a
relocation operation, because the remodeling capacity of the growth area diminishes after 4 years of
age. In a prospective study by Birch et al. 100 children underwent primary plexus surgery at a
median age of 4 months (Birch et al. 2005)..Posterior dislocation of the shoulder was observed in
30 of these children and the shoulders were relocated successfully in all of them after the age of one
year. Dislocation of the shoulder had an adverse effect on functional outcome. Even patients with
successful relocation of the humeral head had lower Mallet scores than those without dislocation
(ibid.). Torode and Donnan presented results of 12 children with BPBI-associated posterior
dislocation of the humeral head who had undergone open reduction via an anterior approach at a
mean age of 2 years and 3 months. Postoperative immobilization was carried out with a shoulder
spica for 6 weeks and an additional 6 weeks in an orthosis. The dislocation and relocation of the
humeral head was confirmed using CT. No redislocations were detected over a minimal follow-up
of 12 months (Torode and Donnan 1998). Hui and Torode reported that open reduction with tendon
lengthening decreased glenoid version by a mean of 31% over a mean follow-up period of 3 years
and 7 months for 23 operated patients (mean age at surgery 2 years 5 months) (Hui and Torode
2003).
Kambhampati et al. performed a relocation operation for 183 patients with posterior subluxation or
dislocation of the numeral head (Kambhampati et al. 2006). The anterior capsule was preserved as
much as possible. For 70 patients, the degree of retroversion was over 40° or the humeral head was
particularly unstable after relocation, and so an additional derotation osteotomy was done. The
majority of the patients maintained a reduction during the 5 year follow-up period. There were only
20 failures with recurrent malpositioning of the humeral head. The mean Mallet score improved
from 9.4 to 13. Remodeling of the humeral head was evident in most cases after successful
relocation. Remodeling of the glenoid was difficult to measure because only plain radiographs were
38
taken in most cases. The successful relocation was done at a median age of 2 years 2 months,
whereas patients with recurrent relocation were operated on a median age of 4 years 5 months
(ibid).
Osteotomy of the humerus
In cases of internal rotation contracture with advanced glenohumeral deformity and an already
flattened humeral head, Wickström et al. recommended rotation osteotomy of the humerus above
the insertion of the deltoid. The goal of the external rotation osteotomy is to improve the functional
arc of the shoulder rotation. An amount of external rotation sufficient to allow the hand to be
brought to the mouth with the elbow in flexion and the arm adducted was selected during the
operation (Wickström 1955). Goddard and Fixen performed rotation osteotomy using the above
mentioned technique for 10 patients with good results. According to their experience sufficient
lateral rotation of the distal part of the humerus is 30º beyond the neutral position. This correction
improves the supination enough to allow the palm to be brought to the mouth instead the dorsum of
the hand (Goddard and Fixen 1984). Bae and Waters propose 60º to 90º as a desirable external
rotation. During the operation the hand has to be placed at the midline in order to avoid
overcorrection before fixation with plate and screws (Bae and Waters 2007). Kirkos and
Papadopoulos performed rotational osteotomy of the proximal part of the humerus on 22 patients
with an average age of 10 years and 3 months because of internal rotation contracture or limited
active external rotation of the shoulder. The average increase of 25 degrees external rotation and 27
degrees in active abduction allowed the patients to better wash themselves and eat. Given this good
result, they recommended rotational osteotomy for late treatment of deformity in BPBI (Kirkos and
Papadopoulos 1988). Several reports support rotational osteotomy as a late deformity correction
method in BPBI (Al-Qattan 2002, Waters and Bae 2006). Al-Qattan performed derotational
osteotomy of the humerus in 15 children, whose hand-to-neck Mallet score values increased from
2.2 to 4 after an average three years follow-up (Al-Qattan 2002).
39
AIMS OF THE STUDY
I: US screening for GH joint instability in BPBI
To assess prospectively the use and optimal timing of routine ultrasound (US) screening in
order to detect shoulder subluxation in brachial plexus birth injury (BPBI) among infants.
II: MRI for detecting rotator cuff muscle changes related to GH joint pathology in
BPBITo assess rotator cuff muscles and the glenohumeral (GH) joint in brachial plexus birth injury
(BPBI) with MRI and to investigate whether or not any correlation exists between muscular
pathology and the deformity of the glenohumeral joint.
III: Muscle changes in BPBI with elbow flexion contracture
To investigate whether there is a correlation between specific patterns of muscular pathology and
limited range of motion of the elbow in brachial plexus birth injury.
IV: MRI in evaluation of the surgically treated shoulder girdle in BPBI
To evaluate the outcome of shoulder operations in BPBI by MRI and to define the
indications for different shoulder operations in correcting GH-subluxation and improving the
range of motion of the joint.
40
MATERIALS AND METHODS
PatientsThe study was approved by the ethics committee of the Hospital for Children and Adolescents,
Helsinki University Hospital. When clinically indicated, MR imaging was performed under
anesthesia in young patients.
US screening for GH joint instability in BPBI (I)All neonates born in Women´s Hospital, Helsinki from 2003 to 2006 with evident or suspected
BPBI as diagnosed by a pediatrician in a routine examination performed on all infants at 2 days of
age were included in the prospective study. All BPBI patients born during the same 4-year-long
study period who were referred to Children´s Hospital, Helsinki University Hospital maximum of 1
year of age from 8 other obstetric hospitals within the catchment area were also enrolled in the
study. Neonates who had only a birth fracture of the clavicle without sufficient findings to support a
diagnosis of BPBI during clinical examinations at 2-days, 2-weeks, and 1-month of age were
excluded from the study. Patients that had a full recovery were also excluded from further follow-up
and from the study.
MRI of rotator cuff muscle changes related to GH joint pathology in BPBI (II)
Of the 42 consecutive BPBI patients who were referred to the Hospital for Children and
Adolescents, Helsinki University Central Hospital, 22 were boys and 20 girls. In the period March
2002 through April 2003, all patients underwent MRI because of internal rotation contracture, lack
of active external rotation of the glenohumeral joint or possible posterior subluxation of the humeral
head. Three patients (2 boys, 1 girl) were excluded from the study because MRI could not be
completed for technical reasons, leaving 39 patients younger than 16 years in the prospective study.
The mean age of the patients was 7.7 years (range 2.0-15.7 years). The right shoulder was affected
in 23 patients (59%) and the left shoulder in 16 (41%). Seven patients (18%) had undergone
brachial plexus reconstruction and 6 (15%) a subscapular release operation.
Muscle changes in BPBI with elbow flexion contracture (III)Study III included 15 consecutive BPBI patients (9 boys, 6 girls) with elbow flexion contracture
who were referred to Children´s Hospital, Helsinki. The mean age of the patients was 11 years
(range 3-18 years). The injury involved the upper roots (C5-C6) in six (40%), the C5-C7 roots in
five (33%) and the entire plexus (C5-T1) in four patients (27%) according clinical and ENMG
41
findings. The right side was affected in 10 patients (67%) and the left in five (33%). Two patients
had had obstetric brachial plexus surgery at 3 and 5 months of age.
MRI evaluation of surgically treated shoulder girdle in BPBI (IV)
During the period March 2002 through December 2005, 34 permanent BPBI patients (14 girls, 20
boys) underwent surgery of the shoulder region in the Hospital for Children and Adolescents,
Helsinki University Central Hospital. The final study group consisted of 31 patients. Three patients
were excluded from the study because two of the patients failed to participate in the preoperative
MRI study and one patient underwent a subscapular release operation by a surgeon not participated
in the study. BPBI extended to the upper plexus (C5-C6) in 7 patients, to roots C5-C7 in 15 and to
the entire plexus (C5-Th1) in 9 patients. Primary plexus reconstruction had been performed for 9
patients (29%).
Healthy childrenThree healthy neonates (1 girl, 2 boys) participated in three ultrasound examinations for both
shoulders performed by three pediatric radiologists at 2-day intervals over the course of one week
for intra- and interobserver measurements in study I.
MethodsUS screening for GH joint instability in BPBI (I)
Clinical protocol
A physiotherapist performed the examination at 2 weeks of age. Individualized passive range of
motion exercises, which patients were unable to do actively, were taught to the parents. Repeat
examinations were performed by a pediatric orthopedic surgeon or a hand surgeon at 1, 3, 6, and 12
months of age or until function of the upper extremities was clinically normal and symmetrical.
Stability of the shoulders and range of motion of the upper limb joints were recorded during all
examinations. Possible other birth injuries and stability and range of motion of all joints were
assessed during the clinical examination at 1 month of age. The extent of the injury was assessed
clinically according to the following scheme: C5, weak shoulder; C5-6, weak shoulder and elbow;
C5-7, weak shoulder, elbow, and wrist; C5-8, weak shoulder, elbow, wrist, and hand; C5-T1, flail
hand. The prevalence of permanent palsy at 1 year of age was calculated for all neonates with BPBI
born in Helsinki during the 2003-2006 period. After the 1 year follow-up period, classification as
42
temporary or permanent BPBI was made. Patients with temporary BPBI had a full recovery over the
1 year follow-up period, whereas patients with permanent BPBI had persisting pathological findings.
Ultrasound study
A pediatric radiologist performed the scheduled US of both shoulders for all patients at 1, 3, 6,
and 12 months of age. When there was full clinical recovery, the patient was removed from the US
study.
The US study was carried out using an 8 MHz linear transducer (Acuson, Sequoia 512, Acuson
Corporation, Mountain View, CA, USA or ATL HDI 5000, ATL Ultrasound, Bothell, WA, USA)
and stability of the glenohumeral joint was assessed according to the modified method of Hunter et
al. (Hunter et al. 1998). Sizes of the humeral head and the humeral ossification center were
measured in transverse and longitudinal views. Possible humeral fractures or physeal injuries were
recorded. A posterior axial approach with the upper arm of the patient adducted and the elbow
flexed to 90° was used both in the static evaluation of joint congruency in maximal internal and
external rotation and in the dynamic part of the study. In dynamic evaluation, the shoulder was
scanned during the full range of internal to external rotation and the possible posterior subluxation
of the humeral head was assessed visually. Posterior scanning also revealed the shape of the
posterior glenoid. During the US examination young infants were lying on their side, and 1-year-
olds were seated. A parent supported the child and held the studied hand in the proper position.
Figure 5.
US image of the left affected glenohumeral joint of a 1- month old girl with BPBI. a) Withouttracing. b) With tracing. c) �-angle (20º) is within normal limits at the age of 1 month andossified nucleus of the humeral head is located ventral to posterior scapular line. CG=cartilaginous glenoid, OC= ossification center of humeral head.
SCAPULA
CGSCAPULA
HUMERALHEAD
�-angle20°
oc
a b c
43
Ultrasound measurements
Measurement of the �-angle was performed as described by Vathana et al. in order to evaluate
possible posterior subluxation in addition to the visual assessment (Vathana et al. 2007). The angle
between the posterior margin of the scapula and the line drawn tangentially to the humeral head and
posterior edge of the glenoid is called the �-angle (the normal value is � 30°, Figure 5). Normally the
humeral ossification center is located anterior to the posterior margin of the scapula (the posterior
scapular line). In subluxation the posterior displacement of the humeral head gradually increases
relative to the above described line.
Intra-and interobserver variations were evaluated by doing the measurements on healthy children.
Three pediatric radiologists independently performed a total of 18 US examinations each. Both
shoulders of 3 newborns were examined by all three observers three times at two-day intervals over
the course of one week.
MRI of rotator cuff muscle changes related to GH joint pathology in BPBI (II)
Physical examination
A senior orthopaedic surgeon assessed the range of motion of the shoulder, glenohumeral (GH)
congruence and possible subluxation of the GH joint by inspection and palpation during passive
movements of the arm. The degree of internal contracture was measured by passive external
rotation (PER) with the arm in adduction. PER and GH joint subluxation were used to appraise
degree of internal rotation contracture and GH joint incongruence.
Magnetic resonance imaging
Both shoulders were imaged using a surface coil in a 1.5 T MR imager (Siemens, Erlangen,
Germany). T1-weighted spin echo images (TR 817 ms, TE 20 ms, TA 6 min 2 sec, matrix 220 x
256) in axial, oblique coronal, and oblique sagittal planes were obtained. In addition T2*-weighted
2 D gradient echo (MEDIC) images (TR 944.3 ms, TE 25.8 ms, flip angle 30 º, TA 4 min 2 sec,
matrix 256 x 256) were obtained in the axial plane. The field of view was 160 mm x 138 mm in T1-
weighted images and 220 mm x 220 mm in 2 D gradient echo images. A 4.0 mm slice thickness
was used in all sequences and the scans were archived in PACS (IMPAX, Agva-Gaevert N.V.,
Mortsel, Belgium).
A senior radiologist, blinded to the clinical situation, evaluated all MR images using the IMPAX
4.5 for Orthopedics software tool. The glenoscapular angle (GSA; degree of version of the glenoid)
44
was measured by drawing two bisecting lines according to the technique described by Friedman et
al. (Friedman et al.1992). The first line was drawn between anterior and posterior corners of the
glenoid cartilage. A second, bisecting line was drawn from the medial tip of the scapula to the
middle point of the glenoid. The angle between the first line going through the posterior margin of
the glenoid and the line along the axis of the scapular (posteromedial quadrant) was measured. The
GSA was obtained by subtracting 90° from the posteromedial quadrant angle (Figure 6). The
glenoid configuration was classified using the scheme of Pearl et al., as concentric (the humeral
head centered in a glenoid with a matching curve), flat, biconcave (the humeral head articulated
with a posterior surface of the glenoid), or pseudoglenoid (the posterior articular surface of the
glenoid retroverted in relationship to the original glenoid). In the pseudoglenoid case, the angle of
version was measured along the posteriorly retroverted glenoid (Pearl et al. 2003).
The percentage of humeral head anterior to the middle of the glenoid fossa (PHHA) was measured
as described in Waters et al. (Waters et al. 1998): The anterior aspect of the humeral head (anterior
to the scapular line described above) is divided by the transverse diameter of the humeral head, and
then multiplied by 100 (Figure 6). Normally, half of the humeral head is located anterior to the
scapular line and the PHHA value is around 50%. The more severe is the posterior subluxation, the
lower is the PHHA value.
In order to evaluate the degree of rotator cuff muscle atrophy, the greatest thicknesses of the
subscapular, infraspinous, and supraspinous muscles were measured from the oblique sagittal plane
in millimeters (Figure 7). To exclude the effect of age variation, the muscle ratio between the
affected side and the normal contralateral side was calculated for every muscle. Muscle atrophy was
considered mild for a ratio of 0.9 – 0.75, moderate for a ratio of 0.75 – 0.5, and severe for a ratio of
< 0.5. The amount of fatty infiltration was assessed visually from the deltoid muscle without
measurements in diameters.
45
Figure 6.
Measurements of the glenoscapular angle (GSA) and the percentage of humeral head anterior to
the middle of the glenoid fossa (PHHA). Reprinted with permission from the Pediatric Radiology
from Tiina H. Pöyhiä, Yrjänä A. Nietosvaara, Ville O.Remes, Mikko O. Kirjavainen, Jari I.
Peltonen, Antti E. Lamminen: MRI of rotator cuff muscle atrophy in relation to glenohumeral joint
incongruence in brachial plexus birth injury. Pediatr Radiol 35: 402-409, 2005.
Figure 7.
Schematic drawing show the greatest thickness measurements of the rotator cuff muscles from
oblicque sagittal plane (ss= supraspinous muscle, is= intraspinous muscle, sc= subscapular
muscle). Reprinted with permission from the Pediatric Radiology from Tiina H. Pöyhiä, Yrjänä A.
Nietosvaara, Ville O.Remes, Mikko O. Kirjavainen, Jari I. Peltonen, Antti E. Lamminen: MRI of
rotator cuff muscle atrophy in relation to glenohumeral joint incongruence in brachial plexus birth
injury. Pediatr Radiol 35: 402-409, 2005.
GSA= Angle measured - 90°PHHA= (AB:AC)x100Anterior
Posterior
is
ss
sc AP
46
Muscle changes in BPBI with elbow flexion contracture (III)
Physical examination
An experienced orthopedic surgeon measured both passive and active range of motion of the elbow
and of the forearm using a goniometer in order to assess the congruency of the elbow joint. Normal
range of motion of the elbow is rated from 0� (full extension) to 150� (full flexion). Pronation and
supination were measured with the upper arm in adduction and the elbow at 90� flexion, with
normal values measuring 90�–0�–90� (total active motion, TAM, 180�).
Magnetic resonance imaging
The prospective MRI studies were performed with a 1.5-T Siemens Sonata or a Siemens Vision
imager (Siemens, Erlangen, Germany) using a surface coil, with the patient supine. Imaging studies
were carried out between April 2004 and September 2005. T1-weighted axial spin echo (SE)
images (TR 760 ms, TE 20 ms, matrix 256 x 256, field of view 160 x 138 mm, 3.0-mm slice
thickness, an approximate acquisition time of 6 minutes) were obtained. The interslice gap and the
number of slices were adjusted to cover the arm, elbow, and forearm. Congruency of the elbow
joint was assessed with following MR sequences: sagittal T1-weighted flash 2 D (TR 500 ms, TE10
ms, flip angle 90°, matrix 256 x 256, field of view 150 x 138 mm, and 3.0 mm slice thickness with
an approximate acquisition time of 4 minutes), coronal T2-weighted (TR 3000 ms, TE 90 ms,
matrix 256 x 256, field of view 150 x 138 mm), and PD-weighted (TR 3000 ms, TE16 ms, matrix
256 x 256, field of view 150 x 138 mm) with 3.0-mm slice thickness and an approximate
acquisition time of 5 minutes. Both the affected and the contralateral upper limb were imaged with
the same protocol. For technical reasons, one patient underwent the MR study only for the elbow
region. All the remaining 14 patients underwent the entire MR study.
The images were interpreted by consensus, by two radiologists with 3 and 5 years experiences in
musculoskeletal radiology blinded to both clinical history and findings, using ordinary clinical
workstations (Agfa Impax DS3000, Agfa-Gevaert Group, Mortsel, Belgium). The congruency of
the elbow joint was evaluated. The degree of muscle atrophy was assessed visually based on the
presence of an abnormal amount of fatty infiltration or reduction in size of the muscle compared to
the healthy contralateral side. The amount of muscle fat content was semi-quantitatively graded on
a four-point scale (F0-F3), and the reduction in muscle size was assessed using a three-grade scale
(SR 0-SR 2), both adapted from Mahjneh et al. in the following way: (F0) normal muscle signal
intensity: homogenous hypointense signal, contrasting sharply with subcutaneous and intermuscular
fat; (F1) hyperintense: patchy but not confluent intramuscular signal; (F2) hyperintense; patchy and
47
confluent intramuscular signal, involving <50% of individual muscle volume; (F3) homogenously
hyperintense: confluent intramuscular signal, involving >50% of individual muscle volume; (SR 0)
normal size; (SR 1) moderate atrophy corresponding to a slight (<50%) reduction in muscle size;
(SR 2) severe atrophy (>50%) of the muscle (Mahjneh et al. 2004).
MRI evaluation of surgically treated shoulder girdle in BPBI (IV)
Clinical examination
A physiotherapist measured with a goniometer external rotation in adduction and abduction as well
as elevation of the arm pre- and postoperatively. Range of motion of the upper limb was assessed
and Mallet classification (Figure 1) was used for functional assessment of the shoulder (Mallet
1972).
The most important denominator in selection of the operation method was congruency of the GHJ.
The relocation operation (n=13) was performed for young patients (age 0.9–7.7 years) with posterior
shoulder subluxation and deformity (GSA -60º to -20º, PHHA 4-40%). An additional operation had
been performed for four relocation patients: teres major transposition for three patients and internal
rotation osteotomy of the humerus for one patient. The coracoid process was shortened in addition to
subscapular tendon lengthening and coracohumeral ligament recession in 10 of these 13 patients.
Two of the patients had a biconcave glenoid and eleven a pseudoglenoid.
Older patients (age 5.7–14 years) with a deformed GHJ (GSA -60º to -35º, PHHA range -10% to
21%) were operated on using external rotation osteotomy (n=5) above the deltoid tuberosity. In this
operation the distal humerus was externally rotated (30º –40º) and osteosynthesis was performed
with a plate.
Children (n=5) without significant shoulder joint deformity (internal rotation contracture: limited
passive external rotation, range -20º to 0º) were treated by subscapular tendon lengthening.
Children (n=8) with poor active elevation without significant shoulder joint deformity (limited active
abduction, range 90º to 180º) were treated by teres major transposition; for 3 of these patients
(internal rotation contracture with limited active abduction) subscapular lengthening was also done.
The algorithm of the treatment protocol is shown in Figure 8.
48
After relocation surgery the upper extremity was immobilized with a thoracobrachial cast or soft
cast for 3 to 7 weeks (mean 5 weeks). The immobilization time was 3 to 4 weeks after humeral
osteotomy, 3 to 4 weeks after subscapular tendon lengthening and 4 to 5 weeks after teres major
transposition. Possible postoperative complications were registered and the opinion of the patient
(above 7 years) or parents (children under 7 years of age) was obtained regarding the usefulness of
the operation.
Magnetic resonance imaging
Pre- and postoperative MRI of the affected shoulder was performed for all patients at a mean MRI
follow-up time of 3.8 (SD1.2) years (range 1.7–6.8 years). Imaging studies were done with a 1.5 T
MRI imager (Magnetom Vision, Siemens, Erlangen, Germany or Achieva, Philips Medical
Systems, Best, the Netherlands) with a surface coil. During the MR examination the patient was in
the supine position on the table with the arm along the side of the body. The MR imaging protocol
consisted of the following sequences for the Siemens imager: T1-weighted spin echo images in
axial, oblique coronal, and oblique sagittal planes (TR 817 ms , TE 20 ms, TA 6 min 2 sec, matrix
220 x 256, FoV 160 x 138 mm) and T2*-weighted 2 D gradient echo images in the axial plane (TR
944.3 ms, TE 25.8 ms, flip angle 30 º, TA 4 min 2 sec, matrix 256 x 256, FoV 220 x 220 mm). For
the Philips MRI imager, the corresponding parameters were: T1-weighted spin echo images in
axial, oblique coronal, and oblique sagittal planes (TR 500 ms, TE 15 ms, TA 4 min, matrix 240 x
240, FoV 160 x 144 mm) and 3D WATSc sequence in the axial plane (TR 20 ms, TE 7.7 ms, flip
angle 25 º, TA 5 min 47 sec, matrix 288 x 232, FoV 160 x 129 mm). Slice thickness was 4.0 mm in
all the sequences, except 2mm in the Philips 3 D WATSc- sequence. The measurements were
performed using the IMPAX for Orthopedics (Agfa-Gevaert Group, Mortsel, Belgium) software
tool.
The glenoscapular angle (GSA), according to the method defined by Friedman et al. (Friedman et
al. 1992), and PHHA, according Waters et al., were measured as described in the methods section
of study II (Waters et al. 1998). The shape of the glenoid was classified as either normal concentric,
flat, biconcave or pseudoglenoid according Pearl el al. (Pearl et al. 2003). The glenohumeral joint
was classified as congruent, subluxated, or badly deformed pseudoglenoid when the humeral head
was articulating to the deformed posteriorly retroverted glenoid which was located in a different
plane than the normal glenoid.
49
50
Statistical analysis
Study I: US screening for GH joint instability in BPBIAnalysis of variance (NCSS and PASS; Number Cruncher Statistical Systems, Kaysville, Utah) was
used for statistical analysis. A difference with P=0.05 was considered significant, and 95%
confidence intervals were calculated for the measurements (Figures 10,11) using spreadsheet
software (Microsoft Office Excel 2003 for Windows; Microsoft, Redmond, Wash).
Study II: MRI of rotator cuff muscle changes related to GH joint pathology in BPBI
The Mann-Whitney test and Spearman´s rank correlation test were used for statistical analysis
(SPSS for Windows, version 13.0, SPSS, Chicago, IL, USA). A P-value < 0.05 was considered
statistically significant.
Study III: Muscle changes in BPBI with elbow flexion contracture
The Wilcoxon signed-rank test was used, as appropriate, for statistical analysis. P-values of < 0.05,
<0.01 and < 0.001 were considered to indicate significant, very significant and highly significant
differences, respectively. Correlations were calculated using Spearman´s two-tailed correlation test
(SPSS for Windows, version 13.0, SPSS, Chicago, IL, USA), where a P-value < 0.05 was
considered statistically significant.
Study IV: MRI evaluation of surgically treated shoulder girdle in BPBI
Values of ROM are presented as medians (range) with SE. Mallet score sums were expressed with
mean values and standard deviations. The Wilcoxon test was used to compare pre- and
postoperative Mallet and GSA- values in different operation groups. P< 0.05 was considered
significant.
51
RESULTS
US screening for GH join instability in BPBI (I)Of the 41 980 live births during the years 2003-2006 at Women´s Hospital 187 neonates with
suspected BPBI were referred to Children´s Hospital. A clavicle fracture was diagnosed in 75 of
these neonates, of whom 55 were excluded from the study because they had insufficient clinical
findings to support BPBI, leaving 132 patients with BPBI (73 girls, 59 boys; right side 73, left side
59). The incidence of BPBI in Helsinki during the study period was 3.1 BPBI per 1000 live births.
There were 131 cephalic and 1 breech presentation, all vaginally delivered with a mean birth weight
of 4172g (range 2930 – 5850g). In 31 cases (23%) vacuum cup assistance was needed during
delivery.
Additionally 21 BPBI patients from eight different obstetric hospitals within the tertiary catchment
area from among 48 994 births were also referred to Children´s Hospital. These BPBI patients (11
girls, 10 boys; right side 14, left side 6, bilateral 1) were referred at 1-12 months of age. All of these
patients were vaginally delivered; vacuum cup assistance was needed in 8 cases with cephalic
presentation. The mean birth weight was 4389 g (range 3605 – 5310 g).
Clinical findings. The extension of affected roots are presented in Table 3. BPBI healed during the
first year of life in 105 cases (80%) out of 132 palsies, leaving 27 cases for whom BPBI was
considered to be permanent (incidence 0.64 per 1000 live births). Primary brachial plexus surgery
was performed for one (0.76%) of 132 BPBI patients and one (4%) of 27 permanent palsies. Only
two of the referred patients from the tertiary catchment area had temporary palsy and two (9.5%) of
these referred 21 patients had had obstetric brachial plexus surgery.
Tabl
e 3.
Affe
cted
root
s in
BPBI
.
W
omen
´s H
ospi
tal
Ref
erre
d pa
tient
s fro
m te
rtiar
y ca
tchm
ent
area
Exte
nt o
f BPB
I at 2
day
s Ex
tent
of B
PBI
at 1
yea
r of a
geR
isk fo
r per
man
ent
palsy
Exte
nt o
f roo
t inj
ury
Exte
nt o
f BPB
Iat
1 y
ear o
f age
Roo
ts
Tem
pora
ryPe
rman
ent
Tem
pora
ry
Perm
anen
t0
--
105
--
21
(C5)
17-
10%
--
-2
(C5-
6)51
822
14%
23
143
(C5-
7)30
91
23%
-9
34
(C5-
8)7
7-
50%
-2
-5
(C5-
Th1)
-
33
100%
-5
2Su
m10
527
132
219
21
Tabl
e 4.
Pri
mar
y di
agno
sis o
f pos
terio
r sub
luxa
tion.
Wom
en´s
Hos
pita
l
Ref
erre
d pa
tient
s
fro
m te
rtiar
y ca
tchm
ent a
rea
All
patie
nts c
ombi
ned
Mon
ths
Clin
ical
lyU
S�-
angl
eC
linic
ally
U
S�-
angl
eC
linic
ally
US
�-an
gle
1-
--
--
--
--
35
547
º (40
º-62º
) 6
648
º (36
º-65º
) 11
1148
º (36
º -65
º)6
23
47º (
40º-6
0º)
12*
65º (
53º-7
8º)
35
54º (
40º -
78º)
121
1*50
º1
2 #
42º (
38º-4
5º)
23
44º (
38º -
50º)
Sum
89
810
1619
Mea
n �-
angl
e m
easu
rem
ents
are
giv
en w
ith ra
nges
. * N
o ea
rlie
r US
stud
ies d
one.
# 6
-mon
th U
S st
udy
was n
orm
al fo
r one
pat
ient
, 12-
mon
th U
Sst
udy
was t
he fi
rst f
or a
noth
er p
atie
nt.
52
Eighteen of the 27 patients with permanent palsy from Women´s Hospital had restricted passive
external rotation of the shoulder at a mean age of 2.5 months (median 1 month, range 0.5-12
months). Clinically evident instability of the shoulder was recorded at a mean age of 6 months
(median 3 months, range 3 months to 3 years) in 9 (50%) of these 18 patients. At the time of
diagnosis of posterior subluxation of the humeral head the mean passive external rotation was 52°
(range 0°-80°). None of the patients with temporary palsy developed shoulder instability.
Thirteen of the 19 patients with permanent palsy from the tertiary catchment area had restricted
passive external rotation of the shoulder at a mean age of six months (median 6.5 months, range 3-11
months). Nine (69%) of these 13 patients had clinically diagnosed posterior subluxation of the
humerus at a mean age of four months (median 3 months, range 2-9 months). At the time of
diagnosis of posterior subluxation of the humeral head the mean passive external rotation was 48°
(range 0°-80°).
Ultrasound findings. A total of 194 US studies were performed for 96 BPBI patients during the
study period (Figure 9). Twenty-four children were examined at 1, 3, 6, and 12 months of age.
Growth of the cartilaginous humeral head and ossification center during the first year of life is
presented in Figure 10, where error bars show 95% confidence intervals. On the affected side the
widths of the cartilaginous humeral head and the ossified nucleus were smaller than on the healthy
side in all patients with permanent palsy. Patients with posterior subluxation of the humeral head had
the largest discrepancy (Figure 11). A conjoint fracture of the humerus was detected in two patients,
but no physeal injuries were seen. At 1 month of age glenohumeral congruency and shape of the
glenoid were symmetrical in all scanned children. Nine (6.8%) of the 132 BPBI patients born at
Womens´s Hospital and 10 (48%) of the 21 BPBI patients referred from the tertiary catchment area
developed US-verified posterior subluxation of the humeral head (Table 4). US study was not done
for two patients with clinically detected posterior subluxation. 15 patients with clinically and
ultrasonographically verified posterior subluxation had rounded posterior margins of the glenoid.
Posterior subluxation (�-angles 38°-53°) was detected on US in three patients who were clinically
estimated to have a congruent glenohumeral joint. The results for the subgroup of patients who
participated in the complete US follow-up program are presented in Figure 10b and Figure 11b. In
this group there were 10 posterior subluxations, all of which were permanent palsies. Seven of these
subluxations were diagnosed by US at 3 months of age (Figure 12) and three at 6 month.
53
54
Neonates referred to Children´s Hospital (n=187)from primary catchment area (Women’s Hospital)
Ultrasound study (n=75)
Patients excluded (n=55) • clavicular birth fracture without BPBI
BPBI patients (n = 132)
Ultrasound study not done (n=54)• full recovery before 1 month of age (n=50)• refused (n=4)
Ultrasound study not done (n=43)• full recovery before 3 months of age
Ultrasound study (n=26)
Ultrasound study (n=23)
Ultrasound study(n=20) (n=2) (n=0) (n=4) (n=0) (n=1)• not done (n=2) • not done (n=1) • not done (n=2) • not done (n=2)
Ultrasound study (n=2) Ultrasound study (n=2)
1 month
3 months
6 months
12months
Ultrasound study notdone (n=1)• full recovery before 12months of age
Figure 9. Flowchart providing information about the number and timing of US studies conducted onneonates referred to Children`s Hospital from a) Women´s Hospital of Helsinki.
55
BPBI patients referred to Children´s Hospital from tertiary catchment area outside of Helsinki (n=21)
Ultrasound study (n=7)
Ultrasound study (n=6) Ultrasound study (n=7)
Ultrasound study (n=3)Ultrasound study (n=5)
Ultrasound study (n=3) (n=1) (n=1) (n=1) (n=1) (n=1)• not done n=1 • not done n=2 • not done n=3 • not done n=2 • not done n=3
Ultrasound study (n=3)
1months
3months
6months
12months
Ultrasound study not done (n=1)• full recovery before 3 months of age
Ultrasound studynot done (n=1)• full recovery before
12 months of age
Figure 9. Flowchart providing information about the number and timing of US studies conductedon neonates referred to Children`s Hospital from b) tertiary catchment area outside Helsinki.
56
Size of the humeral head (mm) on the healthy size
0 5 10 15 20 25 30
1
2
3
4
mm
1 month
3 months
6 months
12 months
cw
ch
ow
oh
Figure 10 a. Ultrasound (US) findings of a healthy humeral head performed on 82 patients withbrachial plexus birth injury (BPBI) at 1 month of age. Thirty-nine US examinations were done at 3months of age, 38 at 6 months of age, and 35 at 1 year of age. Error bars show 95% confidenceintervals. cw=cartilage width, ch=cartilage height, ow=osseus width, oh=osseus height.
Figure 10 b. Ultrasound (US) findings of a healthy humeral head in the 24 BPBI patients whoparticipated in US studies at all time points. Error bars show 95% confidence intervals.cw=cartilage width, ch=cartilage height, ow=osseus width, oh=osseus height.
Size of the humeral head (mm) on the healthy side (n=24)
0 5 10 15 20 25 30
1
2
3
4
mm
1 month
3 months
6 months
12 months
cw
ch
ow
oh
57
Figure 11. Effect BPBI on humeral head growth analyzed by calculating the ratio of the humeralhead width between the affected and the healthy side. Error bars show 95% confidence intervals.ct= cartilage temporary palsy, cpc= cartilage permanent BPBI congruent GHJ, cps=cartilagepermanent BPBI subluxation of the humeral head, ot= osseus temporary palsy, opc= osseuspermanent BPBI congruent GHJ, ops= osseus permanent BPBI subluxation of the humeral head.a)Ultrasound measurements were performed on 51 patients with temporary BPBI at 1 month ofage, on 9 patients at 3 months of age, and on 8 patients at both 6 and 12 months of age. Nineteen ofthe 44 patients with permanent BPBI had posterior subluxation of the humeral head (top graph).
Figure 11 b) Ultrasound measurements of the 24 patients in the subgroup who participated in USexaminations at all time points. Among these patients BPBI was permanent in 20 patients, of whom10 had posterior subluxation of the humeral head (bottom graph).
Humeral head width% (affected/healthy) in BPBI
70 80 90 100 110
1
2
3
4
5
6
%
1 month
3 months
6 months
12 months
ct
cpc
cps
ot
opc
ops
Humeral head width% (affected/healthy) in BPBI (n=24)
70 80 90 100 110
1
2
3
4
5
6
%
ct
cpc
cps
ot
opc
ops
1 month
3 months
6 months
12 months
58
Figure 12.
US images of a 3-month-old girl with permanent brachial plexus birth injury on right side.
a) Both glenohumeral joints: normal finding on the left unaffected side and posterior
subluxation of the right humeral head (�-angle 40º)(upper images). b) Posterior subluxation
of the right humeral head in internal rotation (IR) and relocation in external rotation (ER)
(lower images).
LEFT IR RIGHT IR
RIGHT IR RIGHT ER
59
MRI of rotator cuff muscle atrophy related to GH joint incongruence in BPBI (II)
Posterior subluxation of the humeral head was clinically detected in ten (25%) patients and the
mean PER was 34° (range 20° to 85°) in physical examination. In MRI the shape of the glenoid was
concentric in 18, flat in six, biconcave in two and pseudoglenoid in 13 children. The mean GSA was
-20.1º ± 18.2º (range -60º to 0º) and the average PHHA was 30.2% (range -36% to 54%) on the
affected side (Figure 13). Mean values of GSA and PHHA measurements are presented in Table 5.
Figure 13. Axial T1-W images of a) normal right shoulder and b) the affected left shoulder of a
8-year-old boy with BPBI (C5-7). Retroversion of the left glenoid with an abnormal GSA of -45º,
PHHA 18%. On the normal right side GSA is -2º and PHHA 47%.
Table 5. Mean values of glenoscapular angle (GSA) and percentage of humeral head anterior to themiddle of glenoid fossa (PHHA) measurements in affected (BPBI) and contralateral (normal) side.GSA=Glenoscapular angle, PHHA=Percentage of humeral head anterior to the middle of glenoidfossa. N=number of patients.
Age (years) N GSA BPBI GSA normal PHHA BPBI PHHA normal2.0-4.0 11 -29.7 -2.9 29.5 46.74.1-8.0 12 -19.6 -2.3 31 46.38.1-12.0 6 -10.3 -2 41.7 45.712.1-14 10 -16.1 -2.4 23 46.4
GSA -2°PHHA 47%
A
BC A
B
C
GSA -45°PHHA 18%
a b
60
Muscle atrophy was noted in all rotator cuff muscles (Figure 14); affected/healthy muscle ratios are
presented in Table 6 and correlations in Table 7. Muscle atrophy of the supraspinous muscle was
classified as mild in 17, moderate in 11 and severe in one patients. The corresponding values for
infraspinous and subscapular muscles were 5, 26, 5 and 13, 16 , 7, respectively. The difference
between the affected side and the healthy side was statistically significant for all three muscles:
supraspinous (p=0.01), infraspinous (p<0.001), and subscapular (p<0.001). On the affected side
every patient had also intramuscular fatty degeneration of the deltoid muscle.
Table 6. Affected/healthy muscle ratio showing muscle atrophy.
Muscle No prior subscapular release (n=33) Prior subscapular release (n=6)Supraspinous 81.9 % (range 49-100%) 73.15% (range 49-100%)Infraspinous 69.1% (range 38-100%) 56.96% (range 29-71%)Subscapular 69.4% (range 15-100%) 60.8% (range 32-96%)
Figure 14. Oblique sagittal T1-W images of the a) affected right shoulder and b) the normal left
shoulder of a 6-year-old girl with BPBI (C5-7). Muscle atrophy was observed in the supraspinous,
infraspinous and subscapular muscles.
a b
61
Table 7. Correlations of various anatomical and functional measurements.
Correlations rs P rs (ratio) P
GSA/PHHA 0.80 0.01supras/infras 0.81 0.01 0.54 0.01supras/subsc 0.67 0.01 0.36 0.05infra/subsc 0.66 0.01 0.35 0.05GSA/supras 0.32 0.05GSA/infras 0.37 0.05GSA/subsc 0.56 0.01 0.47 0.01PHHA/suprasPHHA/infras 0.35 0.05PHHA/subsc 0.45 0.01 0.51 0.01PER/GSA 0.41 0.01PER/PHHA 0.48 0.01PER/supras 0.32 0.05PER/infras 0.38 0.05 0.41 0.01PER/subsc 0.53 0.01 0.43 0.01
Note: GSA= glenoscapular angle, PHHA= the percentage of humeral head anterior to the middleof the glenoid fossa, supras= supraspinous musle, infras= infraspinous muscle, subsc= subscapularmuscle, PER= passive external rotation, rs= correlation coefficient, rs (ratio) = correlation of thediameters of the affected muscle/ the contralateral healthy muscle, P= statistical significance.
Muscle changes in BPBI with elbow flexion contracture (III)TAM and passive motion of the elbow ranged between 50º and 140º (mean 113º) resulting in a
mean elbow extension deficit of 31° (10º to 90º). Mean active pronation was 57º (5º to 90º) and
mean active supination 34º (range 0º to 80º). Passive pronation was better than active in five
children (mean 14º, range 10º to 30º) and passive supination better than active in eight children
(mean 39º, range 10º to 75º). Radial head dislocation occurred in one patient (patient 7), and
subluxation of the humeroulnar joint in one (patient 14) both detected in physical examination and
in MR imaging. In MR imaging, congruency of the elbow joint was found to be normal in 12
patients and the radiohumeral joint was subluxated in one additional patient (patient 9) without
clinically evident instability. Atrophy was visible especially in the supinator, brachial, and
brachioradial muscles (Table 8). The summary of clinical and MR imaging findings is presented in
Table 9.
TAM of the elbow correlated with TAM of the forearm (rs=0.67, p=0.01). Elbow TAM correlated
negatively with size reduction in the brachioradial muscle (rs= �0.62, p=0.05), with wrist and finger
flexors (rs= �0.74, p=0.01), and with patient age (rs= �0.52, p=0.05). Forearm TAM correlated
62
negatively with the extent of injury (C5–6 vs. C5–7 vs. total) (rs= �0.72, p=0.01), with fatty
infiltration (rs= �0.66, p=0.01) and size reduction (rs= �0.62, p=0.05) in the pronator teres muscle.
The extent of injury correlated with the summed grades of fatty atrophy and size reduction in the
muscles (rs=0.52, p=0.05) and with the extent of pathological findings on MRI in the ten muscles
examined (rs=0.76, p=0.01).
Table 8. Changes of the muscles in BPBI.
Muscle (root) F SR F/SRDeltoid (C5-6) 0 (0-2)* 1 (0-1) * 7Biceps (C5-6) 0 (0-1) * 0 (0-1) 7Brachial (C5-6) 1 (0-2) *** 1 (0-2) *** 15Brachioradial (C5-6) 1 (0-2) ** 1 (0-1)** 11Supinator (C5-6) 2 (1-3) *** 1 (1-2)*** 15Protanor teres (C6-8) 0 (0-1) * 0 (0-1)** 7Anconeus (C7-8) 0 (0-3) 0 (0-2)* 7Triceps (C6-Th1) 0 (0-2) 1 (0-2)** 10Extensors (C6-Th1) 0 (0-1) 1 (0-1)** 11Flexors (C6-Th1) 0 (0-2) 0 (0-1)** 7
Median (range) amount of fatty infiltration (F, 0-3) of affected side and median (range) reduction
in size of muscle (SR, 0-2) are given. Numbers of the patients who have fatty infiltration and/or size
reduction (F/SR) of the studied muscles are provided. Extensors =extensor muscles of wrist and
fingers, Flexors = flexor muscles of wrist and fingers. The nerve roots innervating studied muscles
are also given in the parentheses. Statistically significant differences between the affected and
healthy muscles are marked as follows: * p < 0.05, ** p < 0.01, *** p < 0.001.
Tabl
e 9.
Tot
al a
ctiv
e m
otio
n (T
AM) o
f the
elb
ow a
nd fo
rear
m a
nd m
uscl
e at
roph
y.
Patie
nt1
23
45
67
89
1011
1213
1415
Age
(yea
rs)
69
86
168
312
1218
813
1316
12Ex
tent
of i
njur
y C
5-6
C5-
7 C
5-7
C5-
6 C
5-6
Tota
l C5
-7
C5-
6 C
5-6
C5-
7 C
5-6
Tota
l To
tal
Tota
l C5
-7TA
M
of
elb
ow
14
0º
135º
13
5º
130º
13
0º
125º
12
0º
120º
11
5º
110º
10
5º
105º
90
º85
º50
ºFl
exio
n-ex
tens
ion
15-1
55
10-1
4510
-145
25-1
5515
-145
20-1
4525
-145
20-1
4030
-145
30-1
4040
-145
35-1
4050
-140
50-1
3590
-140
F0
11
00
0N
/A 1
00
10
00
1B
icep
sSR
10
00
00
N/A
00
01
01
00
F1
11
11
01
11
12
11
02
Bra
chia
lSR
11
01
11
00
11
21
12
1F
01
10
00
01
11
11
20
1B
rach
io-
radi
alSR
01
00
00
10
10
11
11
1F
01
00
00
N/A
00
00
00
20
Tric
eps
SR1
10
10
1N
/A 0
01
11
12
1F
22
22
11
12
22
32
12
2Su
pina
tor
SR1
22
21
11
12
12
11
22
F0
00
00
00
00
00
11
11
Pron
ator
SR0
00
01
10
00
10
11
11
TAM
of f
orea
rm
160º
75
º15
0º
125º
11
0º
100º
60
º10
0º
165º
60
º11
0º
70º
15º
10º
60º
Pros
upin
atio
n ac
t.80
-0-8
075
-0-5
70-0
-80
65-0
-60
70-0
-40
60-0
-40
60-0
-070
-0-3
090
-0-7
520
-0-4
050
-0-6
070
-0-0
15-0
-05-
0-5
60-0
-0
Add
ition
al d
ata
�+
#+
��•
F=fa
t, SR
=si
ze re
duct
ion
in m
uscl
e. F
lexi
on-e
xten
sion
and
act
ive
pros
upin
atio
n m
ovem
ents
are
giv
en in
deg
rees
. Exp
lana
tions
of t
he a
dditi
onal
data
: �=
flex
or c
arpi
uln
aris
(FC
U) p
ro e
xten
sor d
igito
rum
com
mun
is tr
ansp
ositi
on, +
= p
lexu
s rec
onstr
uctio
n, #
= ra
dioh
umer
al in
cong
ruen
ce,
*= h
umer
ouln
ar in
cong
ruen
ce, •
= a
nter
ior e
lbow
flex
or re
leas
e, N
/A n
ot a
vaila
ble.
63
MRI evaluation of surgically treated shoulder girdle in BPBI (IV)
All patients or parents were satisfied to the result of the operation except one patient who found no
improvement from a subscapular tendon lengthening operation. Table 10 presents the data on
number of patients with different operation types, age at the time of surgery, postoperative GSA,
PHHA, type of glenoid, congruency of the GH joint, external rotation in adduction, and elevation
measurements. Pre- and postoperative mean values and standard deviations of Mallet score sums are
shown in Figure 15. The only complication was a deep wound infection in one patient who had
undergone a relocation operation.
A relocation operation of the humeral head was performed for 13 patients. After successful
relocation (10/13) the postoperative median value for passive external rotation was 48° (range 10° to
80°, SE 8). The improved postoperative measurements were as follows: active external rotation
among 10 patients in adduction (median increase 38°, range 10° to 100°, SE 9) and in abduction
(median 48°, range 15° to 80°), and in elevation among 6 patients (median 40°, range 30° to 70°).
After the successful relocation operation the mean increase in Mallet score sum (Figure 15) was 5.5
(SD 3.0). The postoperative mean improvement in GSA was 33° (SD 14) and PHHA 25% (SD 10)
among 10 patients. In the relocation group the difference between pre-and postoperative GSA values
was statistically significant (p<0.05). Postoperatively the shape of the glenoid improved in 10
patients (flat 9, concentric 1). Three failed procedures resulted in resubluxation of the humeral head.
Two of these patients were over 6 years old at the time of the relocation operation and the third
patient had an immobilization time that was too short (4 weeks).
Humeral osteotomy was performed for five patients at a mean age of 9.4 (SD 3.2) years. The
postoperative median passive external rotation was 30° (range 0° to 60°, SE 10). In this group the
median increase in active external rotation in adduction was 25° (range 20° to 40°, SE 3.7) and in
abduction 30° (range 25° to 45°). Elevation improved in two patients postoperatively. One patient
had an increased PHHA of 16%. GSA values or the shape of the glenoid did not change after
humeral osteotomy.
The median passive external rotation was 45º (range -20º to 80º, SE 17) after subscapular tendon
lengthening operation. For four patients the subscapular tendon lengthening operation resulted in
better active external rotation in adduction (median increase 20°, range 20° to 35°, SE 3.7) and in
abduction (median 55°, range 45° to 75°, SE 6.6). For three patients elevation improved (median
20°, range 20° to 40°, SE 6.6) as well. In retrospect, one of these five patients should have been
64
65
treated with osteotomy. GSA, PHHA, and the shape of the glenoid did not improve after subscapular
tendon lengthening.
A teres major to infraspinatus transposition operation was done for eight patients, three of whom
also had subscapular tendon lengthening. The median active external rotation in abduction was 73°
(range 45° to 80°, SE 6.0). Postoperatively, five of these eight patients showed improved active
external rotation in adduction (median 40°, range 10° to 45°, SE 6.8), whereas elevation (median
25°, range 10° to 90°, SE 13) improved in six patients. This operation type did not improve GSA,
PHHA, or shape of the glenoid.
5 10 15 20 25
1
Relocation preop
Relocation postop
Osteotomy preop
Osteotomy postop
Subscapular tendon lengthening preop
Subscapular tendon lenghtening postop
Teres major to infraspinatus transposition preop
Teres major to infraspinatus transposition postop
p < 0.05
p < 0.05
Figure 15. Pre- and postoperative mean values and standard deviations of Mallet score sums fordifferent operation types.
Mallet score
66
Table 10. Patient data before and after surgery
Relocation(n = 13)
Osteotomy(n = 5)
ST lengthening (n =5)
TM transposition(n = 8)
Age 4 (0,9-7.7) 8,3 (5,7-14) 11 (5.3-15) 5.4 (3.8-11)Roots injured 3 (2-5) 3 (2-5) 3 (2-5) 3 (2-5)Plex. rec. (n) 4 - 1 4Add. oper (n) * (3), (1) # (3)
pre post pre post pre post pre postGSA (º) -40
(-60 to -20)-10(-47 to -1)
-45(-60 to -35)
-45(-60 to -35)
-9(-27 to -7)
-7(-27 to -2)
-8.5(-21 to -3)
-6(-14 to -1)
PHHA (%) 15(4 to 40)
40(5 to 47)
14(-10 to 21)
10(-10 to 34)
38(20 to 48)
45(10 to 48)
45,5(37 to 54)
46,5(37 to 53)
ER (º) -20(-45 to 0)
10(-30 to 80)
-20(-30 to -10)
0(0 to 20)
-20(-20 to -10)
0(-20 to 15)
0(-30 to 0)
5(-20 to 45)
Elevation (º) 110(70 to 180)
130(45 to 180)
110(95 to 160)
110(95 to 170)
160(140 to 170)
180(160 to 180)
105(90 to 180)
165(100 to 180)
Glenoid (n) concentric - 1 - - 3 3 5 5 flat - 9 1 1 1 1 3 3 biconcave 2 - - - - - - - pseudoglenoid 11 3 4 4 1 1 - -Congruency(n) congruent - 9 - - 4 4 8 8 sublux 4 2 1 2 1 1 - - deformed 9 2 4 3 - - - -
Median (range) values of age, number of roots injured, degrees of GSA, ER and elevation,
percentage of PHHA are given for all operated patients. ST lengthening = subscapular tendon
lengthening, TM transposition= teres major transposition, Plex. rec.=plexus reconstruction,
GSA=glenoscapular angle, PHHA=percentage of humeral head anterior to the middle of the
glenoid fossa, ER=active external rotation in adduction, Glenoid=type of glenoid,
Congruency=congruency of the glenohumeral joint, Additional operations performed later:
*= teres major transposition, �= osteotomy , #= subscapular lengthening, n= number of patients.
67
DISCUSSION
Fetal macrosomia, shoulder dystocia, breech extraction and instrumental deliveries are known to be
risk factors for BPBI (Soni et al. 1985). Nerve root injury most often affects the upper roots but may
affect the entire plexus. The majority of patients have temporary palsy and recover within the first
years of life (Jackson et al. 1988). In permanent palsy nerve injury results in a limited range of
motion of the shoulder, elbow and hand as well as anatomical changes of the affected upper limb.
Most authors believe that BPBI-associated shoulder pathology develops gradually after birth and is
not caused by direct joint trauma (Gilbert 1993, Waters et al. 1998). The discussion has been quite
extensive in the literature concerning BPBI-associated bony deformities imaged with plain
radiographs (Polloc and Reed 1989), CT (Hernandez and Dias 1988, Friedman et al. 1992, Waters
and Peljovich 1999, Hui and Torode 2003) and MRI (Gudinchet et al. 1995, Waters et al. 1998,
Pearl et al. 2003, Kozin 2004). Discussion concerning imaging findings of the pathological muscle
changes in BPBI has intensified lately.
This prospective study included a population-based section where the incidence and early detection
of posterior subluxation were defined. Further, the prospective part also included studies on MRI
findings of muscle and articular changes in the shoulder and elbow areas in late sequelae of
permanent BPBI and additionally imaging findings after operative treatment of shoulder sequelae in
BPBI.
The incidence of BPBI has been reported to vary between 0.42 and 3.8 per 1000 in different studies
(Hardy 1981, Levine et al. 1984, Jackson et al. 1988, Bhat et al. 1995, Evans-Jones et al. 2003,
Dahlin et al. 2007). Previously full recovery in BPBI has been reported in 13-80% of cases
(Wickström et al. 1955, Gordon et al. 1973, Evans-Jones et al. 2003). In our population-based data,
the incidence of BPBI was found to be 3.1 per 1000 births, which is in line with previous
Scandinavian studies (Sjöberg et al. 1988, Walle and Hartikainen-Sorri 1993, Dahlin et al. 2007).
Full clinical recovery took place within the first year of life in 80% of our patients. Thus, the
incidence of permanent BPBI in Helsinki is 0.64 per 1000.
Early detection of posterior subluxation of the humeral head
In brachial plexus birth injury, the imbalance of the developing muscle leads to progressive posterior
subluxation. A humeral head that is too dorsally located further limits external rotation and reduces
68
the function of the glenohumeral joint. The glenoid surface becomes first flat and then slopes
posteriorly, resulting in progressive glenohumeral deformity (Pearl and Edgerton 1998). However,
the exact timing of this process has not been studied in depth and the age at which pathological
changes of the shoulder occur is unknown.
In evaluating and screening instability of the hips, US is a commonly used method (Holen et al.
1994, Holen et al. 1999, Harcke and Grissom 1990). Despite shoulder problems being the most
common permanent sequelae in BPBI, US screening of shoulder joints in BPBI patients is
infrequently performed.
Hunter et al. used the posterior approach with US to detect posterior instability in BPBI patients
(Hunter et al. 1998). Moukoko et al. changed their technique to a posterior US approach after
realizing that the ossification center obscured the view of the glenoid in the lateral US approach
technique (Moukoko et al. 2004). We studied in a 4-year prospective study the time frame of
development of shoulder pathology in BPBI using posterior approach US in the City of Helsinki
and in BPBI patients referred from the tertiary catchment area.
In a North American study, posterior shoulder dislocation was detected by US at a mean age of 6
months (range 3-10 months) (Moukoko et al. 2004). Among Swedish BPBI children posterior
shoulder dislocation was clinically observed between 4 and 12 months of age (median 6.5 months)
(Dahlin et al. 2007). We believe, that shoulder instability can be detected earlier using US than by
clinical means only. Shoulder instability can be detected earlier with ultrasound since over half of
our patients with posterior subluxation were diagnosed already at 3 months of age.
Moukoko et al. calculated the risk of posterior dislocation of the humeral head during the first year
of life in patients born with BPBI to be 8% in North America (Moukoko et al. 2004). In a
population-based study Dahlin et al. found a 7.3% early incidence of posterior shoulder dislocation
in BPBI in Sweden (Dahlin et al. 2007). Our population-based study in Helsinki gave very similar
findings: 6.8% of all neonates born with BPBI had sonographically-verified posterior subluxation
of the humeral head during the first year of age. Shoulder instability developed only in patients
with permanent BPBI, affecting one-third of these children. Among patients referred from the
tertiary catchment area to our hospital, the rate of posterior subluxation was even higher. 19 of 21
referred patients still had BPBI symptoms at the age of 1 year; in other words, they had permanent
BPBI. 10 patients of these 19 (53%) had posterior subluxation, but this is because only the severe
69
cases were sent to our hospital. The referred patients were not included in the incidence
calculation, so they did not bias the result.
The best clinical indicator for posterior shoulder subluxation is the loss of external rotation of the
shoulder (Moukoko et al. 2004). External rotation of the GH joint was restricted in all our patients
with posterior subluxation of the humeral head. 10 of the 31 patients with restricted passive
external rotation maintained glenohumeral congruency during the study period. US was a useful
screening method that allowed detection of subluxation of the humeral head in 3 out of 19 patients,
not depicted clinically. Based on our results US should be performed only if BPBI symptoms
persist because patients with temporary palsy did not develop shoulder instability.
Hypoplasia of the humeral head and shoulder deformities result from permanent BPBI due to
growth disturbances (Pollock and Reed 1989). In our study, the size of the affected humeral head
was smaller in all patients with permanent BPBI. Mean size difference was most marked in
patients with instability of the shoulder. The size of the humeral head was 7% smaller and the size
of the ossification center 18% smaller on the affected side at an age of 1 year. The bar graphs
(Figures 10b and 11b) for the patients who, participated in all the scheduled US studies show that
the excluded patients did not bias the results because the bar graphs do not differ substantially
from the graphs with all the studied patients included. Most common cause not participate in all
US studies was exclusion due to full clinical recovery (= 93 patients).
The etiology of displacement of the humeral head in BPBI has been widely discussed. The theory
that the humeral head dislocates during delivery at the time that the brachial plexus injury occurs,
and then muscle imbalance maintains the dislocation is supported by Dunkerton (Dunkerton 1989).
Gilbert and Waters et al. presented that the muscle imbalance after BPBI leads to posterior
subluxation or dislocation of the humeral head (Gilbert 1993, Waters et al. 1998). According to
our findings, US examination of the glenohumeral joint was normal at the age of 1 month in all
patients evaluated. This supports the hypothesis that muscle imbalance instead of birth trauma
underlies glenoid retroversion and posterior subluxation.
US is a fast and reliable tool for diagnosing posterior subluxation of the humeral head. In
permanent BPBI there is a high risk for shoulder instability during the first year of life. Over half
of the posterior subluxations were detected at 3 months of age and 89% were detected at 6 months
of age in our population-based study. In our whole data set, 58% of posterior subluxations were
70
diagnosed with US by 3 months of age and 84% by 6 months. The timing of these screening exams
resembles recommendations for US screening for hip dysplasia. Early detection of posterior
subluxation allows the possibility of early treatment with botulinum toxin and planning of
operative shoulder relocation if needed.
MRI of muscle and articular changes in late sequelae in permanent BPBIIn permanent BPBI neural damage causes changes in the affected muscle anatomy and function
(Zancolli and Zancolli 2000). Muscle dysfunction and imbalance results in progressive loss of
external rotation and abduction and allows malformation of the bony structures. Bony deformities
with increased glenoid retroversion allow posterior subluxation of the humeral head (Waters et al.
1998). However, the underlying muscle pathology in BPBI has not been properly evaluated using
modern imaging. MRI is the method of choice for evaluating denervated muscles (Fleckenstein et
al. 1993), it can provide precious information about the type and distribution of the primary neural
injury. So far reports of imaging findings have concentrated on the injury in osseus and
cartilaginous structures in the shoulder girdle. To our knowledge, BPBI retarded muscle pathology
of the arm or forearm has not been elucidated previously with MRI.
Shoulder girdle
In a study of a healthy pediatric population Mintzer et al. imaged 111 normal shoulders in order to
verify the values for normal glenoid version. The retroversion of the glenoid was biggest during the
first 2 years of life (-6.3° ± 6.5°), and decresed to 2.1° ± 5.9° among children after 2 years and to
–1.7° ± 6.4° among children older than 8 years (Minzer et al 1996).
Insufficient recovery of the damaged nerves results in permanent muscle changes including
increased muscle atrophy and intramuscular fatty degeneration (Fleckenstein et al. 1993). To our
knowledge, our study was the first to show that atrophy of the subscapular muscle was most evident
and correlated with increased posterior subluxation of the GH joint. After a subscapular release
operation, these changes became more evident, obviously due to permanent damage to the muscle.
Degeneration of the subscapular muscle seems to contribute to the development of glenoscapular
deformity. Distinct atrophy of the infraspinous muscle was also seen. Kozin emphasized the
denervation of infraspinous and teres minor muscles (Kozin 2004). However, our study shows that
all the rotator cuff muscles were affected. The normal function of the subscapular and infraspinous
muscles as agonist/antagonist is disturbed due to muscle imbalance, resulting in a restricted range of
motion of the GH joint. Additionally atrophy of the deltoid muscle was observed. It could not be
71
quantified in the present study because the greatest cross-sectional area of the muscle was not
visualized on the images focused on the GH joint.
In our study, there was also a correlation between GSA and thickness of the studied muscles. The
correlation was most obvious between GSA and subscapular muscle and its ratio (Table 7). Our
results are confirmed in a recent study by Hogendoorn et al. who reported that BPBI-associated
muscle degeneration was most prominent in subscapular muscle. They measured diameters of the
affected muscle and compared them to the unaffected side (Hogendoorn et al. 2010). Additionally
they scored the deltoid, infraspinous, supraspinous and subscapular muscle atrophy with a 3-point
visual scale. In 55% of their 102 patients subscapular muscle was atrophic with fatty degeneration
or fibrosis, and in 87% of the studied children the subscapular muscle was either atrophic or
atrophic with fatty degeneration (ibid).
In the present study the thickness of the affected subscapular muscle was 69.4% of the unaffected
muscles among patients without prior subscapular release. In all studied patients the subscapular
muscle atrophy was most often classified as severe. A clear correlation was seen between the GSA
and PHHA, showing the degree of subluxation. GSA ranged widely on the affected side (-60º to 0º )
while little variability was seen (-9º to 1º) at the healthy side. An accurate level for the image
positioning is essential in order to obtain exact measurements of the glenoscapular angle.
Our results are in line with newly published study by van Gelein Vitringa et al. (van Gelein Vitringa
et al. 2010). In a retrospective study they reported MRI findings of 36 infants with BPBI at less
than 12 months of age (mean age 4.8 months). They measured the thicknesses and segmental
volumes of subscapular, infraspinous and deltoid muscles and analysed the relation between muscle
ratios and GSA, subluxation and PER. They expected to find atrophy especially in the infraspinous
muscle and to a lesser extent in the subscapular muscle, but the study found the most severe atrophy
for the subscapular muscle. The volume of the affected subscapular muscle was only 64% and its
thickness only 79% of the corresponding values on the unaffected muscle. For the infraspinatus
muscle the corresponding values were 74% and 83%, respectively. They observed subluxation to
correlate to and GSA as well as PER (van Gelein Vitringa et al. 2010).
Our results are interesting, because subscapular muscle is, at first clinically thought to be the least
affected muscle, while paralyzed external rotators keep the arm internally rotated. Einarsson et al.
have recently reported increased mechanical stiffness and a reduction in a sarcomere length in
72
muscle biopsies they took during open surgery of BPBI children with internal rotation contracture
(Einarsson et al. 2008). They concluded that insufficient passive streching of the muscle probably
leads to changes in the extracellular matrix resulting in a dynamic feedback system to the sarcomere
level (ibid).
In our study PER correlated with ratios of all the studied muscle thicknesses. In contrast to our
study, van Gelein Vitringa et al. found no relation between muscle atrophy and external rotation
(van Gelein Vitringa et al. 2010). They suggested that inaccurate measurement of the PER for the
non-sedated infants in their study could be explanation. A more probable explanation is that
contractures need time to develop and in their study all the children were younger than 12 months,
while in our study the average age of the patients was 7.7 years.
In an earlier prospective study van Gelein Viringa et al. confirmed our findings that glenoid
deformity was related to severe infraspinatus atrophy and subluxation of the humeral head was
related to both infraspinatus and subscapularis atrophy (van Gelein Vitringa et al. 2009). Our study
was the first to show the relation between imaging findings of muscle atrophy and glenohumeral
deformity associated with BPBI in children with a mean age of 7.7 years. Van Gelein Vitringa et al.
showed that that this relation already existed at a mean age of 3.3 years in 24 studied children. In
this study they measured the thickness and segmental volume of subscapular, infraspinous and
deltoid muscles. They did not find any relation between PER and muscle atrophy either (ibid). In
the study performed by Kozin, progressive loss of external rotation beyond neutral correlated both
with increased glenoid retroversion and posterior subluxation of the humeral head (Kozin 2004).
In the two studies published by van Gelein Vitringa et al. both shoulders were imaged at the same
time in axial plane, there after thickness and the segmental volume of the studied muscles were
measured from axial images (van Gelein Vitringa et al. 2009 and 2010). In our study both shoulders
were imaged separately with a surface coil and the thickness measurements were performed from
oblique sagittal images. When shoulders are imaged separately, the imaging planes can be adjusted
to the possible three dimensional rotation of the scapula allowing more precise measurements. It is
not possible when both shoulders are imaged simultaneously. On the other hand, among our
patients the fatty infiltration of the muscles made the margins of the muscle very lacy, so thickness
measurement was chosen to simplify the measurement. Although measurement of the area and
calculation of the segmental volume gives a more precise approximation of the muscles it does not
73
completely characterize whole muscle either. Further studies are needed to get a complete
assessment of muscle atrophy and related features.
Glenoid deformity with increased retroversion leads to posterior subluxation of the humeral head,
followed by a diminished range of motion of the GH joint because of abnormal momentum of the
muscles of the rotator cuff. The multiplanar imaging capability of MRI allowed evaluation of both
GH joint deformity and atrophy of the muscles around the shoulder joint. The present study
provides new information about the degree of muscle atrophy in BPBI and verified its correlation
with the development of secondary deformation of the GH joint. Defining muscle changes
associated with shoulder deformation will help to understand pathogenesis. A thorough assessment
of the shoulder joint is mandatory preoperatively before any operative treatment aimed to improve
shoulder function in BPBI. Correctly timed operative treatment may prevent development of more
severe sequelae.
Elbow and forearm
Elbow flexion contracture may be caused by deformation of the elbow joint or muscle imbalance or
combination of these two. It is a common finding in permanent BPBI (Hoffer and Phipps 2000).
One obvious reason for extension deficit of elbow in our study was elbow joint incongruency
detected clinically or on MRI in 4 patients out of 15. There was a discrepancy between clinical
findings and interpretation of the MRI in two patients with radial head subluxation. A possible
explanation for MR to miss subluxation is that MR imaging captures a static view of the joint while
clinical diagnosis of the subluxation of the radial head is made when moving the elbow. Elbow
flexion contracture is most probably caused by atrophy of brachial muscle. Brachial and supinator
muscles were affected in all our patients. The biceps brachii was better preserved, only seven
patients showed degenerative changes in MRI. The further distally situated motor points for
supinator and brachial muscles may demand longer time for reinnervation than for biceps brachii
(Kawai 2000). Hoeksma et al. had similar results and reported that supination was the last
movement to recover (Hoeksma et al. 2004).
Permanent injury of the entire plexus results in significant deterioration of forearm function.
However, in our study fatty degeneration and size reduction of the supinator muscle were also seen
in all patients with upper plexus lesions and extension deficits of the elbow. This may suggest that
the supinator muscle, which is the most distal target muscle receiving innervation from C5 and C6
roots, is substantially affected in all patients with permanent BPBI. The longer the reinnervation
74
time of the muscle is, the worse the pathological changes are in the muscle. Irreversible atrophy of
the supinator muscle seems to take place before the muscle is reinnervated. An unaffected pronator
teres warranted better preserved TAM of the forearm. This underlines the significance of the
balanced function of agonist and antagonist muscles in maintaining an optimal range of motion.
The supinator function of the biceps brachii can probably compensate for the deficient supinator
muscle in BPBI patients with an unaffected pronator teres, and thus preserve a sufficient range of
prosupination.
Supinator atrophy is rarely seen in the pediatric population. In the present study every BPBI patient
with elbow flexion contracture had significant atrophy of the supinator muscle. TAM did not
correlate with supinator pathology or brachial pathology, because all patients had changes in the
above-mentioned muscles innervated by C5-6 roots. Swelling and edema of the supinator muscle
detected by MRI has been reported in radial tunnel syndrome (Bordalo-Rodriques and Rosenberg
2004). In cases of early or subacute denervation, hyperintensity is seen on STIR images due to
increased water content of the muscle (Fleckenstein et al. 1993). These findings may disappear, in
contrast to our irreversible findings when end-stage muscle changes have already occurred. When
there is chronic denervation of the muscles, fatty infiltration and size reduction are visible on T1-
weighted images.
Based on our findings we present a suggested pathomechanism for BPBI. The neural injury
launches the cascade: changes in target muscles lead to diminished muscle amplitude followed by
muscle function imbalance of the upper limb, resulting in permanent joint deformity with
incongruence and instability. In this suggested pathomechanism, there can be a feedback cycle in
which diminished muscle amplitude increases changes in target muscle structure and the already
developed permanent joint deformity and joint incongruence/instability enhance each other.
Previously, upper limb pathology in BPBI have been characterized principally by clinical and
radiographic methods. In addition to the anatomy of the growing joints, MRI can be used to reliably
visualize muscular pathology. Permanent muscular changes are often found behind diminished
range of elbow and forearm motion in BPBI. MR imaging can visualize these muscle changes
which lead to functional impairment of the elbow and forearm in permanent BPBI. MRI is a good
diagnostic tool for revealing fatty infiltration and atrophy of the supinator muscle in permanent
BPBI patients. MRI studies could thus serve as objective medicolegal tools.
75
Imaging findings after treatment of BPBI
Patients in this study have great variability in the extent of their injuries (C5-C6, C5-C7, C5-T1)
and they have undergone various secondary surgical treatments. We wanted to examine this
complex field to help to choose the best of the different operation techniques for future patients.
Maintenance or restoration of glenohumeral congruency is the goal of the shoulder sequelae
treatment in BPBI. The remodeling capacity of the growth plates has an influence on the final
outcome after the relocation operation. In a recent study El Gammal et al. have suggested that
glenohumeral remodeling capacity decreases after 4 years of age (El Gammal et al. 2006). This
observation is in line with the correction of acetabular dysplasia. After 4 years of age, the
remodeling capacity of the treated congenital dislocation of the hip is clearly diminished (Kasser et
al. 1985, Lalonde et al. 2002). The above suggestion is supported by our study. Two of our patients
who were at age of 6.9 and 7.7 years at the time of their operations, failed to preserve the relocation
and developed resubluxation without glenohumeral remodeling. These patients should have been
treated by osteotomy, evaluating the situation retrospectively. The immobilization time for our third
patient with resubluxation was too short.
For a congruent glenohumeral joint with an internal rotation contracture of the shoulder, soft-tissue
procedures alone should be sufficient to improve external rotation (Jellicoe and Parsons 2008). We
reached the same conclusion: in our study, absent passive external rotation of the shoulder was
treated with subscapular tendon lengthening in congruent joints. Poor active external rotation in
shoulder abduction or poor active abduction were indications for TM transposition in order to
improve hand to neck movement in patients with a congruent glenohumeral joint.
Tendon transfers have been suggested for preventing the development of shoulder deformity. After
latissimus dorsi and teres major tendon transfers to the rotator cuff combined with appropriate
extra-articular musculotendinous lengthenings, Waters et al. have shown scarce improvement in
glenoid version and glenohumeral congruency (Waters et al. 2005). Mintzer et al concluded that
glenoid version may diminish about 6° in childhood during the 10 first years (Mintzer et al. 1996).
Thus minor changes in glenoid version in patients who have undergone corrective soft-tissue
procedures may be due to normal growth. In a 1-year follow-up study performed by Kozin et al.
functional outcome improved without improvement of glenoid version or congruency of the GHJ in
23 children after latissimus dorsi and teres major tendon transfers, determined both clinically and
76
with MRI study (Kozin et al. 2006). Our results are in line with these findings; retroversion of the
glenoid improved only after relocation of the humeral head.
Clinically it is not easy to determine when decreased external rotation is a result of muscle-related
internal rotation contracture or GHJ incongruence. In the study of Kon et al. internal rotation
contracture correlated with intraoperative arthrography findings of consistent patterns of deformity
of the GHJ in BPBI (Kon et al. 2004). They proposed arthrography or MRI for the assessment of
glenoid deformity in order to help in surgical planning. Torode and Donnan recommend CT
scanning to detect potential posterior dislocation for all children with BPBI and restricted external
rotation (Torode and Donnan 1998). The preoperative investigations are essential in planning an
optimal surgical strategy, but we advocate MRI instead of CT; MRI has an exceptional capacity to
visualize cartilage, muscle, and bony structures without radiation. Waters et al. emphasize the role
of MRI assessment in determination of the need for and timing of surgical treatment, because no
significant correlation existed between physical examination and glenohumeral deformity in their
study of 74 BPBI children with an age range of 0.6 to 6.2 years (Waters et al. 2009).
The choice of the surgical technique is based on the congruency of the shoulder joint, age of the
patient, presence of internal rotation contracture and strength of external rotators and abductors of
the shoulder. According to our results, glenohumeral congruence can be improved only after a
properly performed and timed relocation of the humeral head.
Role of imaging in BPBIIn the diagnosis and follow-up of BPBI and its sequelae, several imaging methods have proved to be
important. US reveals the posterior subluxation of the humeral head at an early stage before
permanent deformities have developed and enables early treatment. MRI using 3D heavily T2
weighted sequences is superior in detecting preganglionic root avulsions, valuable information
needed for surgical planning (Vargas et al. 2010). Furthermore, MRI is needed for preoperative
planning of the shoulder girdle. Selection of different surgical operation types is based on the
congruence of the glenohumeral joint, degree of glenoid version and the condition of the muscles.
This information is often difficult to obtain clinically. MR can differentiate glenoid retroversion,
posterior subluxation of the humeral head, joint deformity, or muscle atrophy as possible factors
resulting in decreased external rotation. Elbow joint incongruence, muscle atrophy and intramuscular
fatty infiltration are detectable with MRI when clarifying the reason for elbow flexion contracture.
77
Possible remodelation of the glenoid can be visualized with MRI during postoperative follow up.
MRI has definite potential in the evaluation of brachial plexus injuries in the future. Diffusion-
weighted (DW) neurography and fiber tracking (tractography) have shown promise in imaging of the
brachial plexus (Vargas et al. 2010, Tagliafico et al. 2011).
Methodological considerationsAs this was a clinical study, a prospective observational approach was chosen. Due to the clinical
setting it was impossible to use a double-blind study design in the dynamic US study. The clinical
setting resulted in other limitations to this prospective study as well. Some neonates missed the
scheduled US study either because of infections or insufficient co-operation of the guardians,
especially patients with a long journey from the tertiary catchment area. However, patients were
excluded mostly because of full recovery.
The study design also included patients referred from the tertiary catchment area for US analysis.
Although this patient group was not included in the incidence calculation, they did not disturb the
diagnostic methodology or the primary goal of determining the usefulness of US as a diagnostic
tool. These patients were included because they did not influence to diagnostic accuracy of the US.
In the US study the healthy humeral head served as a healthy control, decreasing the influence of
interindividual variation.
The two-day interval between US studies was regarded to be sufficient to exclude growth of the
ossification center between measurements done in order to calculate intra- and interobserver
variation.
The same pediatric radiologist performed most of the US studies, but because of the slow learning
curve in this relatively rare disorder, this is probably not a disadvantage. US findings were not
confirmed with any other imaging modality. However, it would have been unethical to expose
children to the radiation of CT study, or the sedation necessary for MRI.
In our study concerning muscle pathology of the arm and forearm the group size was very small.
Operative procedures on the elbow region in BPBI are relatively seldom performed and as this was
a clinical study the patients were referred to imaging in order to assess the need for possible
78
surgical treatment. Although the group was small, it gives a good understanding of the imaging
findings of 15 consecutive patients with extension deficit of the elbow. Two radiologists with
extensive experience in musculoskeletal radiology blinded to clinical history and findings
interpreted the MRI images by consensus.
There are relatively small numbers of patients in different groups in our prospective follow-up
study after surgical treatment. Nevertheless, several secondary surgical approaches are necessary
in this complex field of late sequelae after nerve injury. We believe that all possible evidence on
sequelae is valuable for the care of the patients with BPBI.
Implications for possibly future studiesDuring recent years MRI sequences have advanced a lot, reaching 0.5 mm slice thickness with a
good visualization of nerve roots. Further studies are needed to establish the role of MRI in the
imaging of the nerve roots.
When the US studies were carried out, information about botulinum toxin treatment was also
collected. The aim of the botulinum toxin treatment is to achieve equilibrium between the power of
affected and unaffected muscles while waiting for recovery of the affected muscles (Rollnik et al.
2000) and thus inhibit the development of the posterior subluxation of the humeral head. Further
research is warranted to determine the outcome for BPBI patients with botulinum toxin-treated
posterior subluxation.
The mean follow-up time of 3.8 years after operational treatment is relatively short. There is
concern about the loss of clinical improvements during a longer follow-up: loss of abduction in a
longer term follow-up after latissimus dorsi transfer was reported by Pagnotta et al. (Pagnotta et al.
2004). Kirkos et al. reported in a mean 30 year-long follow-up study loss of operatively-gained
active external rotation, which had been achieved with anterior release and tendon transfer of teres
major and latissimus dorsi (Kirkos et al. 2005). A long term follow-up of our patients, at least to the
end of the growing period, could provide more information to scientific data to test their results.
79
CONCLUSIONS
I: US screening for GH joint instability in BPBIIn permanent BPBI the risk for shoulder instability is 30% during the first year of life. US of the
glenohumeral joint should be performed at 3 and 6 months of age in infants with persisting
symptoms of BPBI.
II: MRI of rotator cuff muscle changes related to GH joint pathology in BPBI
All rotator cuff muscles, especially the subscapular muscle were atrophic in BPBI patients with
internal rotation contracture or a lack of active external rotation of the shoulder joint. Muscle
imbalance of the shoulder muscles results in progressive glenoid retroversion, subluxation of the
humeral head and internal rotation contracture.
III: Muscle changes in BPBI with elbow flexion contractureElbow flexion contracture is mainly caused by brachialis muscle pathology. Fatty infiltration and
size reduction of the supinator muscle occurred in all of the studied patients. Prosupination of the
forearm is better preserved when the pronator teres is not severely affected.
IV: MRI evaluation of surgically treated shoulder girdle in BPBIRemodelling of the glenohumeral joint can be achieved after successful relocation of the humeral
head in patients younger than 5 years. Functional improvement of the shoulder was also achieved
with rotation ostetomy of the humerus, subscapular tendon lengthening and teres major
transposition operations.
80
ACKNOWLEDGEMENTS
This study was carried out during the years 2002-2010 in the Department of Pediatric Radiology, at
Helsinki Medical Imaging Center, University of Helsinki, in cooperation with the Department of
Surgery, Hospital for Children and Adolescents, Helsinki University Central Hospital.
I would like to express my gratitude to Professor Emerita Leena Kivisaari, acting Professor Taina
Autti, acting Professor Nina Lundbom, Professor Risto Rintala, Docent Pekka Tervahartiala,
Medical Director of the Helsinki Medical Imaging Center, Jyrki Putkonen, CEO of Helsinki
Medical Imaging Center, Docent Jari Petäjä, Head of the Hospital for Children and Adolescents for
providing excellent research facilities.
I am most grateful to my supervisor Docent Antti Lamminen for sharing his extensive knowledge in
the field of musculoskeletal radiology and for gentle guidance and encouragement during this
project. I owe my warm gratitude to my supervisor Docent Jari Peltonen for enthusiastic and
constant support during the years of research.
My deepest thanks go to Docent Yrjänä Nietosvaara, who taught me the principles of hand surgery
in BPBI and contributed to all levels of this study: study design, clinical studies, data acquisition
and interpretation, manuscript drafting and revision for intellectual content as well as surgical
procedures performed. This study would not have started nor would it have ever been finished
without him. It has been a privilege and a great pleasure to work with him.
I am sincerely grateful to all my co-authors: PhD Mikko Kirjavainen, Docent Mika Koivikko,
Docent Ville Remes and PT Patrick Willamo.
I wish to thank the official reviewers, Docent Kimmo Mattila and Docent Timo Hurme for their
valuable comments and constructive advice after their thorough evaluation of the manuscript.
I have the honor to work with the best pediatric radiologists. I wish to express my warm thanks to
my nearest chief, Docent Kirsi Lauerma, for creating a positive atmosphere and allowing the
opportunity to take the time necessary to do the research. I thank my colleagues Anna Föhr, Miia
Holmström, Teija Kalajoki-Helmiö, Reetta Kivisaari, Laura Martelius, Liisa Mäkinen, Kaija
81
Niskanen, Sakari Mikkola, Raija Seuri and Sanna Toiviainen-Salo from the Department of Pediatric
Radiology for their kind collaboration. Kirsi and Kaija are also acknowledged for kindly taking part
in the intra-and interobserver measurements.
I wish to extend my warm thanks to Eila Syrjänen and Birgitta Palomäki-Salminen from the
Department of Surgery for their excellent collaboration, Raija Åkerblom from the library of the
Hospital for Children and Adolescents for help in searching for old articles, Helena Lustig for
advice with computer problems, and the staff of the Pediatric Radiology Department for their
positive attitude towards the present work.
Mothers who voluntarily brought their newborns for repeated ultrasound measurements for the sake
of science are greatly acknowledged.
I thank all my friends for their friendship, sharing and refreshing moments: those who have been
there for decades, and those whom I have come to know during the recent busy years. I am also
delighted with the companionship of all the gorgeous women in Women-web.
My whole-hearted thanks go to my mother and late father for lifelong love and caring and to my
precious brother and his family for being there.
I owe this book to Docent Reino Pöyhiä, my Love and Best Friend. As a husband you have always
encouraged and supported me. With your energy, sense of humour, music and gourmet food you
have kept my spirits high. I am also grateful for your help with the computer and statistics whenever
needed. We are blessed with two brilliant children: Aino-Maria and Sakari – my beloved ones– you
are my joy, you brighten my days!
Financial support by the Pehr Oscar Klingendahl Foundation, the Maud Kuistila Foundation, the
Radiological Society of Finland, the Foundation for Pediatric Research, Päivikki and Sakari
Sohlberg Foundation, The Finnish Medical Society Duodecim, HUS Röntgen EVO and EVO of the
Hospital District (HUS) is greatly appreciated.
Helsinki, April 2011, SDG
88
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