Neonatal brachial plexus palsy—Management and prognostic factors

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Available online at www.sciencedirect.com

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Neonatal brachial plexus palsy—Management and prognostic factors Lynda J.-S. Yang, MD, PhD Department of Neurosurgery, University of Michigan, 1500 E. Medical Center Dr, Room 3552 TC, Ann Arbor, MI 48109-5338

article info

abstract

Keywords:

Successful treatment of patients with neonatal brachial plexus palsy (NBPP) begins with a

Brachial plexus

thorough understanding of the anatomy of the brachial plexus and of the pathophysiology

Obstetric

of nerve injury via which the brachial plexus nerves stretched in the perinatal period

Neonatal

manifest as a weak or paralyzed upper extremity in the newborn. NBPP can be classified by

Surgery

systems that can guide the prognosis and the management as these systems are based on

Rehabilitation

the extent and severity of nerve injury, anatomy of nerve injury, and clinical presentation.

Outcomes

Serial physical examinations, supplemented by a thorough maternal and perinatal history, are critical to the formulation of the treatment plan that relies upon occupational/physical therapy and rehabilitation management but may include nerve reconstruction and secondary musculoskeletal surgeries. Adjunctive imaging and electrodiagnostic studies provide additional information to guide prognosis and treatment. As research improves not only the technical aspects of NBPP treatment but also the ability to assess the activity and participation as well as body structure and function of NBPP patients, the functional outcomes for affected infants have an overall optimistic prognosis, with the majority recovering adequate functional use of the affected arm. Of importance are (i) early referral to interdisciplinary specialty clinics that can provide up-to-date advances in clinical care and (ii) increasing research/awareness of the psychosocial and patient-reported quality-oflife issues that surround the chronic disablement of NBPP. & 2014 Elsevier Inc. All rights reserved.

Introduction The management of patients with neonatal brachial plexus palsy (NBPP) begins with the understanding that stretching the nerves of the brachial plexus in the perinatal period manifests as a weak or paralyzed upper extremity, with the passive range of motion greater than the active, in a newborn.

Classification The most useful classification scheme for the management and the prognosis of NBPP was proposed by Gilbert and E-mail address: [email protected] http://dx.doi.org/10.1053/j.semperi.2014.04.009 0146-0005/& 2014 Elsevier Inc. All rights reserved.

Tassin,1 refined by Narakas2,3 (Table 1), and supported by Birch et al.4 Group I represents the clinical findings resulting from injury to the nerve roots C5 and C6—characterized by paresis/ paralysis of the deltoid and biceps but active function in the limb extensors, wrist, and hand. The clinical findings in Group II are related to injury of the nerve roots C5, C6, and C7; therefore, in addition to paresis/paralysis of the deltoid and the biceps, paresis/paralysis of the triceps and the wrist extensors is also present, but the long flexors and the intrinsic muscles of the hand are relatively unaffected. Group III represents paresis/ paralysis of the muscles of the entire arm (flail arm), consistent with injury of all the nerve roots of the brachial plexus (the C5,

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Table 1 – The Gilbert and Tassin/Narakas classification scheme used for grading the severity of NBPP and for prognosis.

Group

Affected nerve roots

I II III IV

C5 and C6 C5, C6, and C7 C5, C6, C7, C8, and T1 C5, C6, C7, C8, and T1 with Horner's syndrome

Rate of full spontaneous recovery (%)
90
65 o50
0

C6, C7, C8, and T1). Group IV manifests as a flail arm with the additional presence of Horner's syndrome (ptosis, meiosis, and anhydrosis) of the ipsilateral eye and face, presuming injury to all the nerve roots of the brachial plexus with a very proximal injury to the lower nerve roots. When this classification system is used between 2 and 4 weeks after birth, it facilitates determination of the extent of injury to guide prognosis and subsequent management. Other classification schemes that guide the prognosis and the management rely upon the anatomy and physiology of the nerve injury. Sunderland reported a physiologic scheme comprising five types of pathology in increasing severity: (1) neurapraxia (transient nerve injury that may result from a brief ischemic episode or from any form of compression, demyelination, or axonal constriction or stretch); (2) axonotmesis (transient or permanent nerve injury in which the majority of the supporting structures of the nerve, endoneurium, perineurium, and epineurium are preserved, but disruption of the axonal nerve fibers is present); (3) lesion of the axon and the endoneurium (likely resulting in permanent nerve injury); (4) lesion of the axon, endoneurium, and perineurium (likely resulting in permanent nerve injury); and (5) complete transection of the entire nerve (permanent nerve injury).5 For example, most nerve reconstruction surgeons manage patients

Fig. 1 – Waiter's-tip posture of the right arm.

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conservatively before proposing surgical intervention to ensure that they do not operate on neurapraxic lesions. There is also an anatomical scheme comprising four categories based on the anatomical location: upper, lower, and total plexus palsy.6,7 The concept of an “upper” plexus palsy involving the C5, C6, and sometimes C7 was initially defined anatomically by Erb8 in 1874 after Duchenne9 described four cases of complete paralysis of shoulder movement and elbow flexion in 1872. The upper palsy, also commonly referred to as Erb's palsy, is the most common type of NBPP.4,10 Erb's palsy is visually recognized by the stereotyped “waiter's-tip posture” with the arm adducted, shoulder internally rotated, wrist flexed, and fingers extended (Fig. 1). Similarly, Klumpke's palsy is visually recognized by a flaccid hand in an otherwise active arm, characterizing “lower” plexus palsy,11,12 this type of NBPP is extremely rare13 (e.g., 1 in 350 patients in the author's practice). “Pan”plexopathy is characterized by total plexus palsy, as described by Narakas Groups III and IV, with total loss of function of the arm (flail arm).

Assessment of the neonate with NBPP Physical examination Obstetric providers may suspect NBPP on the basis of initial observations of the infant in the perinatal period. However, physical examination and ultimate diagnosis are best achieved by the combined efforts of neonatologists, neurologists, pediatricians, physiatrists, and occupational/physical therapists. The basic premise of the brachial plexus examination relies on an understanding of the complex anatomy of the nerves of the brachial plexus (the complete description of the brachial plexus is outside the scope of this article but can be found in the published literature14). Many of the maneuvers in the physical examination are best evaluated by seeking a patient's voluntary cooperation, which neonates are unable to provide. Therefore, different strategies must be used to assess NBPP in neonates compared with older individuals, although the basic principles remain constant. These strategies will also vary substantially based on the normal development of the infant during the first 2 years of life as motor and sensory function mature. To provide the appropriate context for the physical examination, a thorough family, maternal, and perinatal history must be obtained. Soon after birth, the treating physician should assess the infant for skeletal injuries or bony fractures by clinical and/or radiographic examination because some musculoskeletal injuries preclude early occupational/physical therapy for NBPP. Note that no substantial evidence exists to support further injury of the nervous elements with gentle handling of the neck and the affected limb (during exercises to ensure passive range of motion), and immobilization is not recommended except when associated with skeletal injuries. Surveillance of spontaneous movements and normal reflexes should be performed as part of the observational examination as global neurologic deficits may indicate other neurologic disorders that can occur concurrently with NBPP.15 Similarly, keen observation of ptosis and meiosis, consistent

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with Horner's syndrome, indicates lower trunk involvement (panplexopathy or Klumpke's palsy). A noticeable asymmetric expansion of the chest cavity and difficulty with oxygenation or feeding can indicate diaphragmatic palsy resulting from phrenic nerve injury (the phrenic nerve derives from the C3, C4, and C5), which can be confirmed with plain radiographs, ultrasonography, or fluoroscopy in the intubated patient. Diaphragmatic palsy can be a dangerous condition resulting in respiratory embarrassment and early failure to thrive, and this should be addressed promptly.16 Likewise, observation of classic postures (e.g., waiter's tip) implies particular NBPP lesions. To focus management paradigms, localization of the NBPP lesion is critical, and neurologic examination is the mainstay of lesion localization. With regard to specific motor function, the treating physician should assess the passive and the active range of motion of the affected arm. Since contractures and joint subluxations do not develop until several months after birth, early limitations of passive range of motion imply other musculoskeletal disorders.17,18 Active range of motion and muscle power can be difficult to assess because infants do not follow commands, but engaging the neonate with simulation or with irritating stimuli can be instructive. Significant motor and sensory function can be gleaned from both spontaneous and stimulated responses, so adequate time should be devoted to sheer observation. Sensory function is similarly difficult to assess in detail, but an overall impression can be inferred by judging the infant's response to particular stimuli (e.g., pinprick, pinch, heat, or cold) in the respective dermatomes. Indications of chewing or biting of the arm or the hand imply sensory alterations in the affected area.19 Similarly, presence of skin rashes in dermatomal distributions can also indicate sensory alterations. As the infant grows, measurements of the circumference and the length of the arm can be tracked as indicators of musculoskeletal dysfunction.20

Assessment scales Assessment of motor function Assessment scales in NBPP are used to gauge the extent of injury, prognosticate potential recovery, and determine treatment. Commonly used scales primarily focus on joint angles or muscle activation. Muscle power is generally expressed via the U.K. Medical Research Council scale for muscle movement (MRC scale) (Table 2). This scale provides structured grading of individual muscle groups, but it does not provide any information about the overall function of the limb or the child. Because the MRC scale requires voluntary cooperation, it is difficult to apply in newborns but can be inferred from Table 2 – The UK Medical Research Council scale for muscle movement (MRC scale) for muscle power. M0—No detectable muscle contraction M1—Palpable muscle contraction without movement M2—Movement in a horizontal plane (gravity eliminated) M3—Movement overcoming the pull of gravity M4—Movement overcoming resistance beyond the pull of gravity M5—Normal strength

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Table 3 – The Active Movement scale (AMS) for assessing motor function in newborns. Observation

Muscle grade

Gravity eliminated No contraction Contraction, no motion Motion r1/2 range Motion 41/2 range Full motion

0 1 2 3 4

Against gravity Motion r1/2 range Motion 41/2 range Full motion

5 6 7

observation of the infant's responses to stimulation or play. To overcome these difficulties in assessing the motor function in newborns, Curtis et al.21 proposed the Active Movement scale (AMS) (Table 3). As the infant grows, the function of the whole limb becomes critical, and the Mallet scale provides a quantifiable assessment for shoulder and elbow or upper plexus function (Table 4).22 To augment the practitioner's assessment of the limb, the Mallet scale can be used in conjunction with Gilbert's classification of shoulder paralysis (Table 5), with some consistency reported between the two systems.4 For elbow function, an elbow recovery scale has been suggested by Gilbert and Raimondi23 (Table 6). Similarly, Raimondi24 has

Table 4 – The Mallet scale.

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Table 5 – The Gilbert scale for assessing shoulder function.

Table 7 – The Raimondi scale for assessing hand function.

Shoulder function

Stage

Flail shoulder Abduction or flexion to 451; no active external Abduction o901; external rotation to neutral Abduction ¼ 901; weak external rotation Abduction o1201; incomplete external rotation Abduction 41201; active external rotation Normal

0 I II III IV V VI

proposed a hand evaluation scale (Table 7) that has been used to assess hand function after nerve repair/reconstruction and found to correlate with the preoperative Gilbert and Tassin/ Narakas group.25

Assessment of overall function Although the above assessment scales have been the mainstay of outcomes reported by surgeons as a measure of technical success or for preoperative evaluation,26–28 they do little to address the overall function of the child.29 A scheme based on five dimensions of disablement was proposed by the National Center for Medical Rehabilitation Research comprised of pathophysiology, impairment, functional limitation (activity), disability (participation), and societal limitation.30 It well demonstrates the shortcomings of the assessment scales described above, especially regarding the functional limitation (activity), disability (participation), and societal limitation in patients with NBPP. Likewise, the International Classification of Functioning, Disability, and Health defines function based on body functions, activities, and participation.31 Speech dominance32 and limb preference33 have also been studied in the context of NBPP. Sundholm et al.34 contend that NBPP should be described in terms of impairment and disability; they reported that many children had difficulty with activities of daily living. With further regard to self-care and activities of daily living in a child with NBPP, the Pediatric Evaluation of Disability Inventory (PEDI) is a tool used to determine a child's ability to perform self-care activities in relation to developmental ageexpected performance.35 The PEDI was unable to discriminate Table 6 – The Gilbert–Raimondi scale for assessing elbow function recovery. Elbow function

Score

Flexion Nil or some contraction Incomplete flexion Complete flexion

1 2 3

Extension No extension Weak extension Good extension

0 1 2

Extension deficit 01–301 301–501 4501

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0 1 2

Description

Grade

Complete paralysis or slight finger flexion of no use; useless thumb—no pinch; and some or no sensation Limited active flexion of the fingers; no extension of the wrist or the fingers; and possibility of thumb lateral pinch Active flexion of the wrist, with passive flexion of the fingers (tenodesis), and passive lateral pinch of the thumb Active complete flexion of the wrist and the fingers and mobile thumb with partial abduction—opposition. Intrinsic balance; no active supination; and good possibilities for palliative surgery Active complete flexion of the wrist and the fingers; active wrist extension; and weak or absent finger extension. Good thumb opposition, with active ulnar intrinsics, and partial pronation/supination Hand IV, with finger extension and almost complete pronation/supination

0 I

II

III

IV

V

between the self-care ability of children with NBPP versus their peers but was effective in distinguishing between the different levels of NBPP severity.36 Application of functional outcomes measures such as PEDI or creation of new patient-/ parent-reported quality-of-life outcomes measures are important steps toward functional assessments for determining later childhood treatment and for evaluating treatment efficacy in patients with NBPP.

Supplementary studies Electrodiagnostic examination Supplementing the physical examination with electrodiagnostic (EDX) findings is helpful to determine whether spontaneous recovery is occurring or whether nerve repair/ reconstruction will be beneficial, and a thorough discussion of EDX in NBPP has been published.37 Early referral of neonates with NBPP and extensive nerve injury may improve outcomes; e.g., the early presence or absence of elbow extension or elbow flexion on clinical examination and of motor unit potentials on electrodiagnostic examination in the biceps muscle correctly predicted whether lesions were mild or severe with respect to long-term involvement in 85–94% of infants.38 EDX findings can provide information regarding the location, severity, and extent of NBPP. For example, identification of an avulsed nerve root is critical to NBPP management; avulsion injuries are considered neurotmetic, spontaneous recovery does not occur, and surgical nerve reconstruction is recommended early. Nerve root avulsions are preganglionic injuries (the motor cell body is detached from its axon, but the sensory cell body is continuous with its distal axon, Fig. 2) and generally do not lend themselves to nerve graft repair but are amenable to nerve transfers if appropriate donors exist. In contrast, ruptured (Fig. 3) nerve roots/trunks (postganglionic neurotmetic or rarely axonotmetic injuries; EDX studies can identify but cannot distinguish axonotmesis from

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Fig. 2 – Avulsion (preganglionic) lesion.

neurotmesis) are more amenable to nerve graft repair or rarely spontaneous functional recovery, so conservative management is initially recommended. In either circumstance, preoperative identification of an avulsed nerve root allows better development of the intraoperative surgical strategy. EDX studies can also identify neurapraxic lesions, leading to the sole recommendation of conservative management. Neurapraxia is characterized by normal motor and sensory nerve conduction distal to the site of injury without denervation on needle electromyography (EMG) of the relevant muscles. However, reduced or absent voluntary motor units may be seen in the muscles. Neurapraxic lesions generally resolve spontaneously within a period of weeks to a few months. If neurological recovery does not progress as expected, further evaluation is warranted.

Nerve conduction studies (NCS) The principles of performing NCS in an infant and a young child are similar to that for an adult patient. However, due to the infant's age and size, appropriate modifications must be made to accommodate the developing nervous system. It is commonly accepted that the normal values in NCS vary with age, and motor conduction velocities in newborns are

Fig. 3 – Rupture (postganglionic) lesion.

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approximately half that of adults. NCS in infants is important but has significant challenges with quantifying axonal loss and with correlating the extent of axonal loss with future recovery. Using NCS to diagnose avulsion (preganglionic lesions) in NBPP relies on an understanding of the spinal nerve roots. The sensory nerve action potential (SNAP) is preserved, but loss of compound motor action potential (CMAP) coupled with denervation potentials and loss of voluntary motor unit action potential (MUAP) recruitment are consistent with the diagnosis of nerve root avulsion.39 Identification of a preganglionic lesion by EDX studies may be confounded by the simultaneous presence of both preganglionic and postganglionic lesions. Contrastingly, EDX studies that demonstrate both motor and sensory axon loss and loss of SNAP and CMAP are consistent with nerve root/trunk rupture (a postganglionic lesion). Therefore, the presence or the absence of SNAPs in the context of an absent CMAP from the respective muscles is the EDX feature that differentiates the avulsion injury from rupture of the nerve roots. The axonal viability index has been used to study the outcomes of infants affected by NBPP,40 and it is defined as the ratio of the amplitude of the CMAP of the involved side to that of the unaffected limb. Motor conduction study results were used to distinguish children with poor outcomes at 1 year of age from those with partial or complete recovery: those with poor outcomes had an axonal viability index of o10% for the axillary nerve, o20% for the proximal radial nerve (triceps), and o50% for the distal radial nerve. Generally, an absent CMAP was associated with a poor outcome.

Electromyography (EMG) EMG comprises assessment of the muscle at rest and then during voluntary movement. At rest, the muscle is evaluated for signs of abnormal spontaneous activity, which is consistent with lack of nervous input. The presence of fibrillation potentials and positive sharp waves indicates that nerve degeneration is occurring. MUAPs are evaluated by assessing the amplitude, phase, duration, and firing rate-related to force. Theoretical and animal studies suggest that neonates likely develop denervation potentials earlier than the adult time period of 14–21 days.41,42 The quality and the quantity of MUAPs in infants and children are also different from the standard definition with adult norms. A normal adult MUAP is triphasic, infant MUAPs are often biphasic, and the amplitude of MUAPs in children aged 0–3 years ranges between 200 and 700 μV.43,44 The recruitment pattern is difficult to elicit as voluntary activity is not easily controlled or graded since infants cannot follow commands. When assessing voluntary muscle activation, EDX focuses on the presence and the number of voluntary motor units present and characterizes their morphology recruitment patterns. Nerve regeneration and reinnervation of muscles is indicated by collateral sprouting from surviving axons, appearing as polyphasia, large amplitude units, or increased duration potentials. Evidence of axonal regeneration is suggested by the presence of “nascent units,” which are small in amplitude, highly polyphasic, and have prolonged duration.

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Utility of EDX in NBPP The practical utility of EDX in NBPP is controversial. Many contend that needle EMG is overly optimistic when compared to the patient's clinical presentation and ultimate outcome.45–48 The phenomenon of synkinesis (aberrant reinnervation) further confounds EDX findings and may be the practical phenomenon underlying the clinical issue of cocontractions45: synkinesis may allow innervation of antagonist muscles that preclude the desired movement. Motor unit interference pattern was also found to consistently overestimate future clinical recovery, and no correlation was seen between this particular EMG finding and recovery of clinical strength.44 Although EDX must be interpreted with caution and in the context of other clinical information, the sensitivity of EDX for detecting a postganglionic rupture was 92.8% but only 27.8% for preganglionic avulsion injuries,49 indicating that EDX can be useful in the appropriate situation.

Radiologic examination In the immediate postnatal period, radiographic imaging may be indicated urgently to assess for the presence of clavicular or humeral fractures or diaphragmatic asymmetry, but the focus of this section will be imaging of the nervous brachial plexus elements. Keep in mind that neurological deficits in NBPP may mask symptoms due to coincidental, but more distal, nerve lesions resulting from fractures of the long bones in the arm,50 and ignoring these coincidental lesions can lead to decreased outcomes after intervention. Traditionally, imaging studies of the brachial plexus in NBPP are performed only when microsurgical nerve repair/reconstruction is indicated due to the potential complications from the imaging procedure. However, with modern magnetic resonance imaging (MRI) techniques, imaging may be taking its place in the management arena. Like EDX, radiologic investigations supplement the clinical presentation by attempting to provide information on the type, location, and extent of nerve injury. Ideally, radiographic studies of the brachial plexus should delineate the course of the pathoanatomy of the cervical spinal roots, from their origin as dorsal and ventral rootlets at the spinal cord through the vertebral foramina, the extraforaminal spinal nerve roots, the trunks, the divisions, and the cords of the brachial plexus down to the terminal branches innervating the muscles of the arm. At present, this remains an unrealistic ideal as does the functional imaging of central connections of the brachial plexus in babies. However, the reported sensitivity of computerized tomography/myelography (CTM) for detecting a postganglionic rupture was 58.3% and 72.2% for preganglionic nerve root avulsion.49 Consequently, radiographic imaging is concentrated on these injury types, but more specifically on nerve root avulsions. Later, a child fails to recover as predicted or new neurological symptoms develop, radiographic examination can reveal arachnoid cysts compressing the spinal cord or herniation of the spinal cord into a large pseudomeningocele51 and superficial siderosis.52

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for diaphragmatic paralysis consequent to a phrenic nerve lesion, for which plication may be necessary.16 The integrity of the diaphragm is essential when the phrenic nerve is being considered as a possible donor in a nerve transfer in babies with suspected multiple root avulsions.

Ultrasonography Few, if any, reports exist regarding the use of ultrasonography (US) in NBPP. We have had some experience applying US preoperatively and comparing the preoperative CTM or MRI and intraoperative pathology with the US results. In our experience, the utility of US is complementary to that of CTM or MRI as US can give information on the muscles and the location of the brachial plexus neuroma to facilitate the formation of strategies for nerve reconstruction. Furthermore, to avoid radiation from x-rays, US can be used to assess for diaphragmatic movement (phrenic nerve function).

Computed tomography/myelography CTM has been the long-preferred NBPP diagnostic tool at most specialty brachial plexus centers. Many investigators reported high sensitivity in the assessment of intradural root avulsions,53–55 and it permits separate evaluation of the ventral and the dorsal nerve roots in the intradural space (Fig. 4). However, the disadvantages of CT-myelography are the need for general anesthesia and lumbar puncture for intrathecal contrast introduction, as well as radiation exposure. Other difficulties include the inability to determine the correct spinal level,56 but the absence of hypodense root shadows with or without a pseudomeningocele is suggestive for nerve root avulsion/preganglionic injury. Note that the presence of a pseudomeningocele is not an absolute proof of root avulsion. CT-myelography cannot assess for ruptures (postganglionic injury) or other types of lesions of nerve roots within the foramen or in their extraforaminal course.

Magnetic resonance imaging MRI is becoming the preferred modality for imaging the brachial plexus in infants and yields similar information to CTM with regard to the proximal nerve roots (Fig. 5). MRI avoids the use of ionizing radiation, does not require lumbar puncture, can be performed with mild sedation in babies, and may be more costeffective despite the different MRI techniques applied at different institutions.57 Intact, avulsed, compressed, or scarred intradural spinal nerves are all possible to detect by MRI, as the methodology continues to improve. Furthermore, using differential techniques, imaging of extraforaminal roots, trunks, divisions, cords, and terminal branches is possible.56 In contrast, although magnetic resonance neurography (MRN) is an imaging technique that is highly sensitive in detecting lesions of the peripheral nerves in adults, it has not been applied successfully in NBPP due to the small size of the nerves.

Treatment Conservative management/rehabilitation and therapy

Plain radiographs X-ray examinations can show fractures of the cervical spine, humerus, or clavicle in the newborn. A chest x-ray can assess

The severity of neonatal brachial plexus palsy (NBPP) ranges from mild nerve stretch injuries with rapid recovery to nerve

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Fig. 4 – A CTM image of an avulsion lesion (A) coronal (B) axial.

root avulsions with no spontaneous recovery. Correspondingly, a significant percentage of NBPP patients do not regain full arm function, so the principles of rehabilitation remain constant: maintain range of motion (ROM) at all relevant joints to avoid contracture formation, encourage muscle strengthening, prevent compensatory movement patterns, and, most importantly, promote normal childhood development.

Overall rehabilitation management Rehabilitation management includes the development of treatment plans that address both short- and long-term goals. Regardless of whether nerve repair/reconstruction occurs, occupational and/or physical therapy should be initiated to optimize outcomes; e.g., the infant who develops early contractures as well as the child who has no contractures will not recover function. The therapist must formulate

Fig. 5 – A MR image of an avulsion lesion (A) coronal (B) axial.

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treatment strategies by considering the upper extremity in the context of the motor power of each muscle, potential safety precautions, functional recovery, and the long-term psychosocial effects of NBPP; this can only be accomplished if the therapist understands the anatomy of the brachial plexus intimately. Proximal stability and core strength are critical and underlie the distal mobility and fine/gross motor coordination. Therapy evaluation and treatment can and should begin as early as day 1 of life, particularly in cases where the infant is otherwise medically stable. The most important goal of early therapy for NBPP patients is maintenance of soft tissue and joint flexibility. Passive range-of-motion exercises are critical and must be taught to the parents/caregivers to be performed routinely at home.58 These exercises can be performed safely and effectively to gently stretch the relevant muscles and joint structures to avoid development of contractures (resulting from excessive contraction of the functioning muscles that are not counterbalanced by the paretic muscles). As formal therapy appointments wane, the need for parent-initiated home exercises arises, and multimedia formats have been reported effective.59 Children with NBPP risk developing skeletal deformities of the trunk and the affected extremity due to poor bone growth associated with weakness of certain muscles, unopposed activities of other muscles, or muscle imbalance.60

Infants Motor training should begin as early as possible to stimulate activity in denervated muscles, to enable muscles to be activated as soon as nerve regeneration has taken place, to prevent or minimize soft tissue contractures, and to minimize ineffective substitution movements. Motor training should continue for as long as nerve recovery is still occurring (potentially for years). In addition to range-of-motion home exercises, parents should be educated regarding the need for “tummy time” at each diaper change to promote symmetrical head rotation and positioning. Torticollis is an abnormal head posture, including ipsilateral tilt, contralateral rotation, and translation, and has been associated with NBPP.61 Persistent torticollis can lead to plagiocephaly and facial asymmetry; deformational plagiocephaly can be appreciated as early as 6 weeks of age with a preexisting diagnosis of torticollis.62 For infants with torticollis, parents should be encouraged to vary the position of the infant's head during play, feeding, and sleeping. Use of positioning wedges may be helpful. Home programs using neck stretches to address tightness of the sternocleidomastoid muscle may be required for some infants and should be taught to families by appropriately trained therapists, and aggressive intervention is rarely required. In some instances, a newborn will require a hand/elbow splint prior to discharge from the hospital (e.g., tightness of the finger joints and/or significant atrophy of the thenar eminence, especially when associated with Horner's syndrome). An elbow flexion splint may be indicated if subluxation is present. Extreme hyperextension of the elbow reflects absent biceps muscle activity in the context of intact triceps muscle activity, causing severe muscle imbalance. Passive

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range-of-motion exercises for elbow flexion should be performed with careful attention to position of the forearm in supination or pronation (whichever position prevents subluxation from occurring). Pain should be absent during newborn range-of-motion exercises. If pain is present, re-evaluate for skeletal injury. Sensory alterations can be present and manifest as the absence of or impaired sensation in all or part of the extremity, based upon the pathoanatomy of the nerve injury. With altered sensation, hyperesthesia and allodynia are expressed in the newborn with “fussiness” or chewing of the affected part of the arm. Desensitization can relieve the symptoms and can be achieved by the use of a firm touch versus a light touch, the use of infant massage, a variety of texture inputs from fabrics, or vibratory input from infant toys. If a skeletal fracture is present, the arm should be immobilized using a sling, with the shoulder adducted and internally rotated and the elbow flexed at 901 so that the arm rests upon the infant's chest for the first few weeks. The newborn should be lifted by scooping the newborn under the buttocks with one hand and under the head with the other versus lifting the infant under the axillae. Teaching families to dress the involved extremity first and undress it last can reduce unnecessary movement of the involved extremity during the healing phase of the fractured area(s). Once the infant's muscles are stretched and prepared for activity, elicitation of active (versus passive) range-of-motion exercises can be encouraged by stroking, tapping, or vibrating the muscle belly. Elicitation can occur in gravity-eliminated positions, progressing to antigravity positions, and ultimately in weight-bearing positions that are developmentally appropriate for the patient. Vibration/stroking can be used to elicit biceps contraction or elbow flexion to achieve movement patterns of the hand to the face or the mouth, elbow extension such as batting at toys overhead, and wrist extension patterns to facilitate reaching for toys. The therapy sessions should include interventions that facilitate the patient's current level of generalized development. The impact of the weak arm upon developmental milestones should be a major focus of every therapy session. Infants with NBPP learn quickly to adapt to their development with a unilateral bias since there is generally no accompanying cognitive deficit. For example, to preclude the bias, progression toward symmetrical development begins with learning to roll to both the right and the left sides. Some infants master the “commando crawl,” while others will not learn to crawl and will progress directly from sitting to walking. Protective reactions in the affected extremity are often delayed or weak, yet they must be a focus of therapy. A small therapy ball can be used to develop forward protective reactions in the prone and the sitting positions. Similarly, with the increasing popularity of the “back-tosleep” campaign, prone activities and bilateral neck rotation must be encouraged to promote maximal function of the recovering muscles and to prevent plagiocephaly. Use of inhibitory or facilitative Kinesio-taping (KMS, LLC, Albuquerque, NM) and dynamic weight-shifting activities can maximize the development of proximal stability within the trunk and the shoulder area. Flexibility throughout the neck and the trunk is imperative for optimal shoulder range of motion.

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Symmetrical movement patterns facilitate motor planning and proper development. A motor pattern program should be initiated to avoid the inadvertent establishment of compensatory motor patterns. Neglect of the affected extremity can occur, so the affected arm should be brought into the child's visual field as much as possible. Encourage the child to explore the involved hand at midline with the other hand and, if appropriate, encourage mouthing of the involved hand. Toys such as play mats, overhead play gyms, wrist rattles, toys that make noise or vibrate, and lightweight rattles with small-diameter handles may be used at home to encourage bilateral integration. Additionally, rehabilitation management of the toddler, older children, and teenagers has been discussed in detail elsewhere.63

Botulinum toxin injections In children with NBPP, botulinum toxin has been used in the treatment of contractures.64 In a study of 22 children who still had contractures after serial casting, application of botulinum toxin type-A (Dysports) to the biceps brachii, brachialis, pronator teres, and pectoralis major muscles combined with serial casting of the elbow for 30 days resulted in significantly increased elbow extension and nine-hole peg test scores but no change in the Mallet scale or the muscle power after 12 months. Botulinum toxin injections to the triceps muscles have been utilized to promote elbow flexion by temporarily relaxing the antagonist muscle, but no formal studies support this use.

Pain management Pain in NBPP, if it occurs, usually does so as the infant matures, but its presence is difficult to detect in infants and in young children. In those with chronic disablement, discomfort results from overuse movements, such as keyboarding or performing a task at home or at school. Treatment goals for the child with pain include the following: (1) reducing the pain with oral or cutaneous medications, (2) determining the substituted movement patterns that are causing the pain, and then (3) teaching the patient to move more effectively (e.g., use of adaptive equipment)—in such a way that minimizes pain as well as overuse of the adjacent joints during that particular task.

Education and communication Education of the families regarding the anatomy, clinical presentation, and treatment options for brachial plexus palsy is critical for optimal outcomes for the patient and the practitioner. NBPP is a complex disorder with acute and chronic ramifications; therefore, it can be overwhelming and difficult to comprehend. The emotional response may be similar to those of families who are grieving a loss and may have significant effects upon the mother's postpartum recovery. Fathers tend to react differently than mothers, and their feelings cannot be discounted. Appropriate communication with pediatricians and other medical care providers of the patient (such as social workers and neuropsychologists) can facilitate comprehensive care for the patient and the family and can reduce the approximately 50% incidence of pursuit of malpractice by affected families presenting to a specialty clinic (unpublished data). Therefore, early referral to an interdisciplinary brachial plexus clinic is often beneficial.

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A systematic approach aids in the education of parents/ caregivers. One paradigm consists of identifying the patient with a chronic disablement, introducing the patient to an appropriate clinic, assessing the physical/developmental progress, assessing for biological risks, establishing the cost and the ability of the parents to cover the cost, and, most importantly, setting and managing expectations.65

Nerve reconstruction The appropriate selection of NBPP patients who may benefit from surgical intervention remains controversial, and several different paradigms have been reported.66–68 Most NBPP surgeons agree that all patients with neurotmetic lesions or nerve root avulsions are reasonable surgical candidates. Some consider absent or significantly impaired hand function, in the context of a flail arm at birth, to be an absolute indication for nerve surgery as soon as the infant reaches the age of 3 months69 and/or by 3–4 months of age for those patients who demonstrate no spontaneous recovery of shoulder external rotation and elbow flexion/forearm supination at that time. Some surgeons proceed with surgical exploration if the true shoulder and elbow movement is absent by 6 months of age, since they feel that the potential benefits from repairing neurotmetic lesions generally outweigh the risks of negative exploration.70 Surgery for NBPP is rarely performed before 3 months of age and is almost always performed before 9 months of age. Early assessment by a specialty center allows institution of conservative management options, determination of the severity of the brachial plexus lesion(s), addressing of social and psychosocial issues, and appropriate time needed to consider the recommended treatment options for the parents/caretakers.

Nerve reconstruction strategies The goal of nerve reconstruction in patients with NBPP is the restoration of hand grasp function, elbow flexion, shoulder movements, and the extension of the elbow, wrist, and fingers, in order of priority. The surgical repair/reconstruction strategy depends upon the number of available viable proximal spinal nerve stumps for grafting (i.e., for ruptures/ postganglionic lesions), the cross-sectional area of the stumps, and the availability of donor nerves for neurotization or nerve transfer operations (i.e., for avulsion/preganglionic lesions). The resultant functional outcome is determined by integrity of the specific surgical connections made between proximal and distal stumps and/or between donors and recipients. A thorough discussion of surgical strategies is outside the scope of this review.70

Post-operative care After nerve repair/reconstruction, some surgeons place the infant's upper body in a prefabricated cast to limit movement of the head and the affected arm for 2 weeks, whereas other surgeons do not immobilize. Patients undergo clinical examinations at our outpatient clinic initially at frequent intervals and then at 6-month intervals. Recovery of function can occur up to 4–5 years after nerve reconstruction.

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Outcomes Natural history The natural history of NBPP, around which the management and the prognosis revolve, remains the subject of speculation and controversy in the literature. The complete potential scope of NBPP is difficult to define because of the variety of theoretical combinations of lesions within the elements of the brachial plexus; e.g., because the brachial plexus is comprised of five roots, three trunks, six divisions, three cords, and five terminal branches, thousands of theoretically different brachial plexus lesions are possible for the nerves alone, even without regard to additional musculoskeletal issues, although the most common form of NBPP is the supraclavicular upper trunk lesion. Further difficulties with the sheer determination of the natural history include the definition of recovery and the potential bias introduced by the referral patterns of reporting physicians71,72 since many patients with Erb's palsy recover spontaneously and are not referred to the specialists who publish most reports. With these caveats in mind, some authors provide an encouraging view of the natural history of NBPP with over 80% occurrence of a favorable functional outcome or complete recovery,73–78 whereas other authors provide a opposing view, with less than 50% with good recovery or freedom from persisting disabilities.72,79–83 As the absence of spontaneous clinical improvement persists over increasing time, the potential for recovery diminishes,74,84,85 and early recovery (clinical improvement within weeks with functional recovery by 3–4 months) is generally associated with favorable outcomes.74,86 The predictors of recovery described above use simple clinical muscle assessments (e.g., Narakas Classification). Other authors have constructed paradigms based on more complicated statistical analyses of multiple independent clinical variables.38,75,87 Regardless, a number of children appear normal and seem to have recovered function, but the affected extremity is not equally functional, when measured by more appropriate sensitive tests.

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strategies, and varied assessment techniques) preclude direct comparison of surgical results among studies. Therefore, the following describes the results from representative studies and reviews.92 Clarke et al. reported that early improvements in neurologic function were produced by neurolysis but were unsustained over time, whereas nerve grafting after resection of the neuroma-in-continuity produced significant improvements in function with a mean follow-up of 4 years.93 Shenaq et al.94 reported that in 282 NBPP infants with a mean followup of 5 years, 75% had good to excellent results after primary and secondary reconstructive surgery. Gilbert et al.91,95 reported the results of 436 patients who underwent nerve reconstruction and secondary reconstructive procedures for NBPP: 80% with Group I palsy and 61% with Group II palsy had “good” or “excellent” shoulder function after 4 years. For elbow function, the study reported “good” results in all of the Group I and II patients and “good” results in 81% of Group III and IV patients. In general, hand function after C8-T1 injury is difficult to recover, and secondary shoulder reconstructive procedures improve the overall outcome. These results reflect the complex nature of the surgical strategy and the need to evaluate the treatment course longitudinally, even after a primary surgery is completed. Additionally, neurotizations or nerve transfers are often undertaken as part of the nerve reconstruction or alone as an isolated procedure. The spinal accessory nerve has been used widely to neurotize the suprascapular nerve to improve shoulder function by reinnervating the supraspinatus and infraspinatus muscles (part of the rotator cuff). The results of this transfer are difficult to assess because it is often done in conjunction with other nerve transfers to restore deltoid muscle function and conflicting reports exist.96,97 In contrast, nerve transfers to restore elbow flexion generally yield good to excellent results.98–102 Regardless of the neurologic recovery, functional recovery also can be compromised by musculoskeletal defects (e.g., contractures and joint subluxation), even with appropriate therapy. When spontaneous recovery and/or primary nerve reconstruction does not yield adequate functional recovery, addressing the consequent shoulder difficulties103 and the lack of hand function104 can significantly improve the outcomes of patients with NBPP.

Surgical outcomes Primary nerve reconstruction The indications for surgical nerve reconstruction in NBPP vary among different practitioners, with the exception of Narakas Group III and IV lesions, for which nerve reconstruction is generally recommended. For example, some feel that the inability to pass the “cookie test” at 9 months is a reasonable indication for surgery,88,89 whereas others rely upon the “towel test” (inability to remove a towel covering the faces at 6 months with the affected arm)90 or the lack of biceps function at 3 months of age.91 Many practitioners use a combination of these clinical observations supplemented by ancillary studies to guide their practice, standard guidelines or critical pathways have been developed. Similarly, many challenges (including the variability of anatomical lesions in the complex brachial plexus structure and adjacent musculoskeletal elements, differing surgical

Conclusion In the 21st century, infants who sustain NBPP have an overall optimistic prognosis, with the majority recovering adequate functional use of the affected arm. However, of utmost importance are (i) early referral to interdisciplinary specialty clinics that can provide up-to-date advances in clinical care and (ii) increasing research/awareness of the psychosocial and patient-reported quality-of-life issues that surround the chronic disablement of NBPP.

refere nces

1. Gilbert A, Tassin JL. Surgical repair of the brachial plexus in obstetric paralysis. Chirurgie. 1984;110(1):70–75.

232

SE

M I N A R S I N

P

E R I N A T O L O G Y

2. Narakas AO. Obstetrical brachial plexus injuries. In: Lamb DW, ed, The Paralysed Hand. The Hand and Upper Limb. Edinburgh [Lothian]; New York, NY: Churchill Livingstone; 1987. 116–135. 3. Narakas AO. Injuries to the brachial plexus. In: Bora FWJ, ed, The Pediatric Upper Extremity: Diagnosis and Management. Philadelphia, PA: Saunders; 1986. 247–258. 4. Birch R, Bonney G, Wynn Parry CB. Birth Lesions of the Brachial Plexus. Surgical Disorders of the Peripheral Nerves. London: Churchill Livingstone; 1998;209–233. 5. Sunderland S. Nerves and nerve injuries. In: Green DP, Hotchkiss RN, Pederson WC, et al., eds. Green's Operative Hand Surgery, 4th ed. New York, NY: Churchill Livingstone; 1999. 750–779. 6. Sunderland S. A classification of peripheral nerve injuries producing loss of function. Brain. 1951;74(4):491–516. 7. Dodds SD, Wolfe SW. Perinatal brachial plexus palsy. Curr Opin Pediatr. 2000;12(1):40–47. 8. Erb W. Uber eine eigentumliche Lokalisation von Lahmungen im Plexusbrachialis. Verh Naturhistorisch Med Ver Heidelberg. 1874;2:130–136. 9. Duchenne GBA. De l'electrisation localisee et de son application a la pathologie et a la therapeutique, 2nd ed. Paris: J. B. Balliere; 1872. 10. Gilbert A. Long-term evaluation of brachial plexus surgery in obstetrical palsy. Hand Clin. 1995;11(4):583–594 [discussion 94-5]. 11. Dejerine-Klumpke A. Contribution a l'etude des paralysies radiculaires du plexus brachial. Paralysies radiculaires totales. Paralysies radiculaires inferieures. De la participation de filets sumpathiques oculo-pupillaires dans ces paralysies. Rev Med Paris. 1885;5:591–616. 12. Ulgen BO, Brumblay H, Yang LJ, Doyle SM, Chung KC. Augusta Dejerine-Klumpke, M.D. (1859-1927): a historical perspective on Klumpke's palsy. Neurosurgery. 2008;63 (2):359–366 [discussion 66-7]. 13. al-Qattan MM, Clarke HM, Curtis CG. Klumpke's birth palsy. Does it really exist? J Hand Surg Br. 1995;20(1):19–23. 14. Medical Research Council of UK. AIDS to Examination of the Peripheral Nervous System, 4th ed. London: Saunders (Guarantors of Brain); 2000. 15. Alfonso I, Alfonso DT, Price AE, Grossman JA. Cortical dysplasia and obstetrical brachial plexus palsy. J Child Neurol. 2008;23(12):1477–1480. 16. Bowerson M, Nelson VS, Yang LJ. Diaphragmatic paralysis associated with neonatal brachial plexus palsy. Pediatr Neurol. 2010;42(3):234–236. 17. Hoeksma AF, Wolf H, Oei SL. Obstetrical brachial plexus injuries: incidence, natural course and shoulder contracture. Clin Rehabil. 2000;14(5):523–526. 18. Steeg AM, Hoeksma AF, Dijkstra PF, Nelissen RG, De Jong BA. Orthopaedic sequelae in neurologically recovered obstetrical brachial plexus injury. Case study and literature review. Disabil Rehabil. 2003;25(1):1–8. 19. McCann ME, Waters P, Goumnerova LC, Berde C. Selfmutilation in young children following brachial plexus birth injury. Pain. 2004;110(1-2):123–129. 20. Uysal H, Demir SO, Oktay F, Selcuk B, Akyuz M. Extremity shortness in obstetric brachial plexus lesion and its relationship to root avulsion. J Child Neurol. 2007;22(12):1377–1383. 21. Curtis C, Stephens D, Clarke HM, Andrews D. The active movement scale: an evaluative tool for infants with obstetrical brachial plexus palsy. J Hand Surg Am. 2002;27 (3):470–478. 22. Mallet J. Obstetrical paralysis of the brachial plexus. II. Therapeutics. Treatment of sequelae. Priority for the treatment of the shoulder. Method for the expression of results. Rev Chir Orthop Reparatrice Appar Mot. 1972;58(suppl 1):166–168.

38 (2014) 222–234

23. Gilbert A, Raimondi P. Evaluation of results in obstetric brachial plexus palsy. The elbow. International meeting on obstetric brachial plexus palsy. Heerlen, NL; 1996. 24. Raimondi P. Evaluation of results in obstetric brachial plexus palsy. The hand. International meeting on obstetric brachial plexus palsy. Heerlen, NL; 1993. 25. Kirjavainen M, Remes V, Peltonen J, Rautakorpi S, Helenius I, Nietosvaara Y. The function of the hand after operations for obstetric injuries to the brachial plexus. J Bone Joint Surg Br. 2008;90(3):349–355. 26. Gilbert A, Tassin J-L. Obstetrical palsy: a clinical, pathologic, and surgical review. In: Terzis JK, ed, Microreconstruction of Nerve Injuries. Philadelphia, PA: WB Saunders; 1987. 529–553. 27. Waters PM. Comparison of the natural history, the outcome of microsurgical repair, and the outcome of operative reconstruction in brachial plexus birth palsy. J Bone Joint Surg Am. 1999;81(5):649–659. 28. Gilbert A, Khouri N, Carlioz H. Birth palsy of the brachial plexus—surgical exploration and attempted repair in twenty one cases. Rev Chir Orthop Reparatrice Appar Mot. 1980;66 (1):33–42 [author's transl]. 29. Piatt JH Jr. Birth injuries of the brachial plexus. Pediatr Clin North Am. 2004;51(2):421–440. 30. Butler C, Chambers H, Goldstein M, et al. Evaluating research in developmental disabilities: a conceptual framework for reviewing treatment outcomes. Dev Med Child Neurol. 1999;41 (1):55–59. 31. World Health Organization. International classification of functioning, disability, and health. Geneva: World Health Organization; 2001;1–25 (11). 32. Auer T, Pinter S, Kovacs N, et al. Does obstetric brachial plexus injury influence speech dominance? Ann Neurol. 2009;65(1):57–66. 33. Yang LJ, Anand P, Birch R. Limb preference in children with obstetric brachial plexus palsy. Pediatr Neurol. 2005;33 (1):46–49. 34. Sundholm LK, Eliasson AC, Forssberg H. Obstetric brachial plexus injuries: assessment protocol and functional outcome at age 5 years. Dev Med Child Neurol. 1998;40(1):4–11. 35. Dumas HM, Fragala-Pinkham MA, Haley SM, et al. Computer adaptive test performance in children with and without disabilities: prospective field study of the PEDI-CAT. Disabil Rehabil. 2012;34(5):393–401. 36. Ho ES, Curtis CG, Clarke HM. Pediatric Evaluation of Disability Inventory: its application to children with obstetric brachial plexus palsy. J Hand Surg Am. 2006 Feb;31(2):197–202. 37. Spires MC, Leonard JA, Wolfe J. The role of electrodiagnosis in infants with brachial plexus palsies. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011. 38. Malessy MJA, Pondaag W, Yang LJS, Hofstede-Buitenhuis SM, le Cessie S, van Dijk JG. Severe obstetric brachial plexus palsies can be identified at one month of age. PLoS One. 2011;6(10):e26193. 39. Smith SJ. The role of neurophysiological investigation in traumatic brachial plexus lesions in adults and children. J Hand Surg Br. 1996;21:145–147. 40. Heise CO, Siqueira MG, Martins RS, et al. Motor nerve conduction studies in obstetric brachial plexopathy for a selection of patients with a poor outcome. J Bone Joint Surg Am. 2009;91:1729–1737. 41. Van Dijk JG, Pondaag W, Malessy MJ. Obstetric lesions of the brachial plexus. Muscle Nerve. 2001;24:1451–1461. 42. Gonik B, McCormick EM, Verweji BH, et al. The timing of congenital brachial plexus injury: a study of electromyographic findings in the newborn piglet. Am J Obstet Gynecol. 1998;178:688–695.

S

E M I N A R S I N

P

E R I N A T O L O G Y

43. Carmo RJ. Motor unit action potential parameters in human newborn infants. Arch Neurol. 1960;3:136–140. 44. Sacco G, Buchthal F, Rosenfalck P. Motor unit patterns at different ages. Arch Neurol. 1962;6:366–373. 45. Heise CO, Siqueira MG, Martins RS, et al. Clinicalelectromyography correlation in infants with obstetric brachial plexopathy. J Hand Surg Am. 2007;32:999–1004. 46. Sherburn EW, Kaplan SS, Kaufman BA, et al. Outcome of surgically treated birth-related brachial plexus injuries in twenty cases. Pediatr Neurosurg. 1997;27:19–27. 47. Clarke HM, Curtis CG. An approach to obstetrical brachial plexus injuries. Hand Clin. 1995;4:563–581. 48. Gilbert A, Razaboni R, Amar-Khodja S. Indications and results of brachial plexus surgery in obstetrical palsy. Orthop Clin North Am. 1998;19:91–105. 49. VanderHave KL, Bovid K, Alpert H, et al. Utility of electrodiagnostic testing and CT myelography in the preoperative evaluation of neonatal brachial plexus birth palsy. J Neurosurg Pediatr. 2012;9(3):283–289. 50. Bodner G, Buchberger W, Schocke M, et al. Radial nerve palsy associated with humeral shaft fracture: evaluation with US —initial experience. Radiology. 2001;219:811–816. 51. Miravet E, Sinisterra S, Birchansky S, et al. Cervicothoracic extradural arachnoid cyst: possible association with obstetric brachial plexus palsy. J Child Neurol. 2002;17:770–772. 52. Aquilina K, Kumar R, Lu J, et al. Superficial siderosis of the central nervous system following cervical nerve root avulsion: the importance of early diagnosis and surgery. Acta Neurochir (Wien). 2005;147:291–297. 53. Slooff ACJ, Versteege CWM, Blaauw G, et al. Radiological and related investigations. In: Gilbert A, ed, Brachial Plexus Injuries. London: Martin Dunitz Ltd.; 2001. 31–37. 54. Hashimoto T, Mitomo M, Hirbuki N. Nerve root avulsion of birth palsy: comparison of myelography with CT myelography and somatosensory evoked potentials. Radiology. 1991;178:841–845. 55. Walker AT, Chaloupka JC, de Lotbiniere AC, et al. Detection of nerve rootlet avulsion on CT myelography in patients with birth palsy and brachial plexus injury after trauma. Am J Roentgenol. 1996;167:1283–1287. 56. Birchansky S, Altman N. Imaging the brachial plexus and peripheral nerves in infants and children. Semin Pediatr Neurol. 2000;7:15–25. 57. van Ouwerkerk WJR, van der Sluijs JA. Radiographic assessment in pediatric brachial plexus palsies. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011. 58. University of Michigan Brachial Plexus Program. Home Exercise Therapy Program for Brachial Plexus Palsy. Ann Arbor, MI: Evolution Media; 2007. 59. Murphy KM, Rasmussen L, Hervey-Jumper SL, et al. Assessment of a home exercise DVD for children with brachial plexus palsy. PM R. 2011;4(3):190–197. 60. Shepherd RB. Brachial plexus injury. In: Campbell SK, ed, Decision Making in Pediatric Neurologic Physical Therapy. Philadelphia, PA: Churchill Livingstone; 1999. 235–259. 61. Hervey-Jumper SL, Justice D, Vanaman M, Nelson VS, Yang L J-S. Torticollis associated with neonatal brachial plexus palsy. Pediatr Neurol. 2011;45(5):305–310. 62. Oh AK, Hoy EA, Rogers GF. Predictors of severity in deformational plagiocephaly. J Craniofac Surg. 2009;20:1629–1630. 63. Nelson VS, Justice D, Rasmussen L, Popadich MG. Rehabilitation concepts for pediatric brachial plexus palsies. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011.

38 (2014) 222–234

233

64. Basciani M, Intiso D. Botulinum toxin type-A and plaster cast treatment in children with upper brachial plexus palsy. Pediatr Rehabil. 2006;9:165–170. 65. Godfrey MM, Nelson EC, Wasson JH, et al. Microsystems in health care: planning patient-centered services. Jt Comm J Qual Saf. 2003;29:159–170. 66. Borschel GH, Clarke HM. Obstetrical brachial plexus palsy. Plast Reconstr Surg. 2009;124:144e–155e. 67. Bertelli JA, Ghizoni MF. The towel test: a useful technique for the clinical and electromyographic evaluation of obstetric brachial plexus palsy. J Hand Surg Br. 2004;29:155–158. 68. Haerle M, Gilbert A. Management of complete obstetric brachial plexus lesions. J Pediatr Orthop. 2004;24:194–200. 69. Pondaag W, Malessy MJ. Recovery of hand function following nerve grafting and transfer in obstetric brachial plexus lesions. J Neurosurg. 2006;105:33–40. 70. Malessy MJA, Pondaag W. Nerve repair/reconstruction strategies for neonatal brachial plexus palsies. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011. 71. Jahnke AH Jr, Bovill DF, McCarroll HR Jr, James P, Ashley RK. Persistent brachial plexus birth palsies. J Pediatr Orthop. 1991;11(4):533–537. 72. Wickstrom J. Birth injuries of the brachial plexus. Treatment of defects in the shoulder. Clin Orthop. 1962;23:187–196. 73. Bennet GC, Harrold AJ. Prognosis and early management of birth injuries to the brachial plexus. Br Med J. 1976;1 (6024):1520–1521. 74. Gordon M, Rich H, Deutschberger J, Green M. The immediate and long-term outcome of obstetric birth trauma. I. Brachial plexus paralysis. Am J Obstet Gynecol. 1973;117(1):51–56. 75. Michelow BJ, Clarke HM, Curtis CG, Zuker RM, Seifu Y, Andrews DF. The natural history of obstetrical brachial plexus palsy. Plast Reconstr Surg. 1994;93(4):675–680 [discussion 81]. 76. Donn SM, Faix RG. Long-term prognosis for the infant with severe birth trauma. Clin Perinatol. 1983;10(2):507–520. 77. Brown KL. Review of obstetrical palsies. Nonoperative treatment. Clin Plast Surg. 1984;11(1):181–187. 78. Bisinella GL, Birch R. Obstetric brachial plexus lesions: a study of 74 children registered with the British Paediatric Surveillance Unit (March 1998-March 1999). J Hand Surg Br. 2003;28(1):40–45. 79. Adler JB, Patterson RL Jr. Erb's palsy. Long-term results of treatment in eighty-eight cases. J Bone Joint Surg Am. 1967;49 (6):1052–1064. 80. Gjorup L. Obstetrical lesion of the brachial plexus. Acta Neurol Scand. 1966;42(suppl 18):1–80. 81. Rossi LN, Vassella F, Mumenthaler M. Obstetrical lesions of the brachial plexus. Natural history in 34 personal cases. Eur Neurol. 1982;21(1):1–7. 82. Eng GD. Brachial plexus palsy in newborn infants. Pediatrics. 1971;48(1):18–28. 83. Eng GD, Koch B, Smokvina MD. Brachial plexus palsy in neonates and children. Arch Phys Med Rehabil. 1978;59 (10):458–464. 84. Sever JW. Obstetric paralysis: its etiology, pathology, clinical aspects and treatment, with report of four hundred and seventy cases. Am J Dis Child. 1916;12:541–578. 85. Gilbert A, Brockman R, Carlioz H. Surgical treatment of brachial plexus birth palsy. Clin Orthop Relat Res. 1991;264: 39–47. 86. Pondaag W, Malessy MJ, van Dijk JG, Thomeer RT. Natural history of obstetric brachial plexus palsy: a systematic review. Dev Med Child Neurol. 2004;46(2):138–144. 87. Nehme A, Kany J, Sales-De-Gauzy J, Charlet JP, Dautel G, Cahuzac JP. Obstetrical brachial plexus palsy. Prediction of

234

88.

89.

90.

91.

92.

93.

94.

95.

96.

97.

SE

M I N A R S I N

P

E R I N A T O L O G Y

outcome in upper root injuries. J Hand Surg Br. 2002;27 (1):9–12. Marcus JR, Clarke HM. Management of obstetrical brachial plexus palsy: evaluation, prognosis, and primary surgical treatment. Clin Plast Surg. 2003;30(2):289–306. Curtis C, Stephens D, Clarke HM, Andrews D. The active movement scale: an evaluative tool for infants with obstetrical brachial plexus palsy. J Hand Surg Am. 2002;27(3):470–478. Bertelli JA, Ghizoni MF. The towel test: a useful technique for the clinical and electromyographic evaluation of obstetric brachial plexus palsy. J Hand Surg Br. 2004;29(2):155–158. Gilbert A. Long-term evaluation of brachial plexus surgery in obstetrical palsy. Hand Clin. 1995;11(4):583–594 [discussion 594-585]. Alhodaib NI, Clarke HM. Outcomes of treatment for neonatal brachial plexus palsy. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011. Lin JC, Schwentker-Colizza A, Curtis CG, Clarke HM. Final results of grafting versus neurolysis in obstetrical brachial plexus palsy. Plast Reconstr Surg. 2009;123(3):939–948. Shenaq SM, Bullocks JM, Dhillon G, Lee RT, Laurent JP. Management of infant brachial plexus injuries. Clin Plast Surg. 2005;32(1):79–98 (ix). Gilbert A, Pivato G, Kheiralla T. Long-term results of primary repair of brachial plexus lesions in children. Microsurgery. 2006;26(4):334–342. Terzis JK, Kostas I. Outcomes with suprascapular nerve reconstruction in obstetrical brachial plexus patients. Plast Reconstr Surg. 2008;121(4):1267–1278. Pondaag W, de Boer R, van Wijlen-Hempel MS, HofstedeBuitenhuis SM, Malessy MJ. External rotation as a result of

38 (2014) 222–234

98.

99.

100.

101.

102.

103.

104.

suprascapular nerve neurotization in obstetric brachial plexus lesions. Neurosurgery. 2005;57(3):530–537 [discussion 530-537]. Chuang DC-C, Mardini S, Ma H-S. Surgical strategy for infant obstetrical brachial plexus palsy: experiences at Chang Gung Memorial Hospital. Plast Reconstr Surg. 2005;116(1):132–142. Kawabata H, Shibata T, Matsui Y, Yasui N. Use of intercostal nerves for neurotization of the musculocutaneous nerve in infants with birth-related brachial plexus palsy. J Neurosurg. 2001;94(3):386–391. El-Gammal TA, Abdel-Latif MM, Kotb MM, et al. Intercostal nerve transfer in infants with obstetric brachial plexus palsy. Microsurgery. 2008;28(7):499–504. Noaman HH, Shiha AE, Bahm J. Oberlin's ulnar nerve transfer to the biceps motor nerve in obstetric brachial plexus palsy: indications, and good and bad results. Microsurgery. 2004;24(3):182–187. Wellons JC, Tubbs RS, Pugh JA, et al. Medial pectoral nerve to musculocutaneous nerve neurotization for the treatment of persistent birth-related brachial plexus palsy: an 11-year institutional experience. J Neurosurg Pediatr. 2009;3(5): 348–353. VanderHave KL, Kozin SH. Shoulder sequelae in children with brachial plexus palsy. In: Chung KC, McGillicuddy JE, Yang L J-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011. Sebastin SJ, Chung KC. Reconstructive strategies for recovery of hand function. In: Chung KC, McGillicuddy JE, Yang LJ-S, et al., eds. Practical Management of Adult and Pediatric Brachial Plexus Palsy. London: Elsevier; 2011.