History

Smellie, a London obstetrician, is credited with the first medical description of a brachial plexus injury in 1768.¹⁴ In 1872, Duchenne in his book Traite de l’Eelectrisation Localisee et de son Application à la Pathologie et à la Thérapeutique described traction during birth as the mechanism of injury.¹⁵ Erb in 1874 reported that weakness of the deltoid, biceps, coracobrachialis, and brachioradialis muscles was caused by disruption of the C5 and C6 nerve roots.¹⁶ The location where the C5 and C6 nerve roots join to form the upper trunk is thus called Erb’s point. The much less common lower brachial plexus palsy (C8-T1) was described by Klumpke in 1885.¹⁷

Surgery for obstetric brachial plexus injury was introduced in 1903 by Kennedy, who reported on three patients. At 2 months of age, his patients underwent resection of C5-6 neuromas with direct suturing of the ends, and favorable results were achieved.¹⁸ Additional reports during the early 1900s resulted in many surgeons advocating early brachial plexus surgery in children who did not improve spontaneously.^19–21

In 1925, Sever concluded that there was no difference in outcome between surgically treated and conservatively managed patients after examining 1100 cases of obstetric brachial plexus palsy.¹² Sever’s results, coupled with the relatively high morbidity and mortality rates associated with surgery during the first part of the century, led to almost complete abandonment of brachial plexus surgery for nearly 5 decades.

With the advent of microsurgical techniques, the operating microscope, and modern pediatric anesthesia, resurgence of interest in the surgical treatment of brachial plexus injuries ensued in the 1970s. The reports of Gilbert and Tassin demonstrating favorable outcomes after direct repair of obstetric brachial plexus injury^22,23 are largely responsible for the increasing use of surgical treatment in the past 3 decades.

Pathophysiology

The traumatic origin of birth brachial plexus injury is considered to be a result of excessive traction applied to nerves secondary to shoulder dystocia, the use of extreme or improper traction, and hyperextension of the arms during breech delivery.⁷ Damage to the upper roots of the brachial plexus usually occurs during vertex delivery when shoulder dystocia necessitates excessive lateral flexion of the neck with the arm in adduction to free the shoulder from the pubic arch (Fig. 213-1). The right arm is involved more frequently because of the more common left occiput–anterior position of the descending fetus.²⁴ During breech deliveries, the upper roots are also more commonly affected.^25,26 One percent of obstetric palsies have occurred after cesarean section.²⁷

FIGURE 213-1 Most common mechanism of brachial plexus injury during vertex delivery. Lateral flexion of the neck is applied to free the shoulder from the pubic arch.

A number of studies have identified risk factors for these injuries, including high birth weight (>4 kg), shoulder dystocia, prolonged labor, primiparity, grand multiparity, instrument deliveries, breech presentation, siblings with obstetric palsy, maternal age (>35 years), maternal pelvic anatomy, and maternal gestational diabetes.^28–33 Although some patients with birth brachial plexus injury will have one or more risk factors, other will not have any. The last point has led many to raise questions regarding the etiology of this condition.

There appears to be a lack of evidence of identifiable risk factors for neonatal brachial plexus palsy.^34–38 Although shoulder dystocia is the most common risk factor identified, only 17% of patients with neonatal brachial plexus palsy in the largest series to date had this risk factor.⁶ The same study found that only 46% of infants with brachial plexus palsy had one or more identifiable risk factors.⁶ An example of patients born without risk factors include uncomplicated vaginal deliveries of infants with smaller than average birth weight.^39,40 These reports demonstrate that not all permanent brachial plexus injury is due to physician traction.³⁹ Some authors speculate that individual infants have inherent biologic variability in susceptibility to brachial plexus palsy.⁴¹

Bilateral injuries are rare (4%) and occur more commonly with breech presentation.^25,42 Neonatal brachial plexus injuries can be associated with clavicle and humerus fractures, facial nerve injury, cephalohematoma, and torticollis, but these conditions do not appear to portend a worse prognosis.

Natural History

As mentioned previously, recent studies indicate a good prognosis for patients, with 70% to 100% achieving complete spontaneous recovery (Table 213-1).^{3,5,9,43–46} Over the past 3 to 4 decades, the rate of recovery has been used to predict which patients will have full spontaneous recovery and which will have incomplete recovery, thus identifying patients who could benefit from surgical reconstruction of the brachial plexus. Poor prognostic features after obstetric brachial plexus injury include total plexopathy and lower plexus injury, typically characterized by Horner’s syndrome and increased root avulsion.^26,45,47,48 These injuries usually result in incomplete recovery. In general, injuries to the upper plexus are thought to be less severe and carry a better prognosis.

Infants who have complete recovery of motor function will show improvement in strength as early as 2 weeks of age, with normalization of strength complete by 12 to 18 months.⁴⁹ Assessment of strength in the biceps, triceps, and deltoid muscle groups by 6 months of age was an excellent predictor of outcome in our series of patients who experienced complete recovery.⁴⁶ Each child recovered to 3/5 strength in all three muscle groups by 5.5 months. Infants who show no signs of recovery and have a flaccid upper extremity at 2 months of age have suffered severe total brachial plexus palsy, and their long-term outcome is poor.^{21,22,50–52} Some investigators have noted that if an infant is to have functional use of an extremity, some recovery must be seen by 4 months of age.^8,9,26,49 We found that patients who experience persistent moderate weakness (less than antigravity strength of the biceps at 6 months of age) have unsatisfactory outcomes with observation.⁴⁶ This study and others have concluded that biceps muscle function at the end of the third month is the most important indicator of functional recovery of the affected limb.^45,46,53 Michelow and colleagues reported that favorable outcome was correctly predicted by biceps function at 3 months in 87% of patients.⁴⁵ The prediction rate was improved to 95% if biceps function along with extensor function of the elbow, wrist, thumb, or finger was used in the clinical assessment. Tassin’s study monitored 20 patients prospectively and found that if infants do not have biceps function by 3 months of age, limited shoulder movement is a probable consequence.⁵³ Recently, this particular finding has come into question inasmuch as Smith and coauthors reported good long-term shoulder function in patients with absent biceps function.⁵⁴ However, the prognostic value of absence of biceps function on improvement in shoulder function has yet to be determined.

Clinical Findings

Brachial plexus injury patterns vary and can be classified by two distinct schemes: anatomic localization and severity of pathology. Anatomic localization is used most by clinicians and allows surgical planning. Pathologic severity is difficult to apply clinically and is based on Seddon and colleagues’ original work, which defined the terms neurapraxia (stretch injury without axonal disruption), axonotmesis (physical disruption of axons or nerve fascicles), and neurotmesis (complete disruption of a nerve trunk or root).⁵⁵

Anatomic localization of perinatal brachial plexus palsy can be classified into three categories: upper, lower, and total brachial plexus palsy. The injury may be further localized to supraclavicular, involving the roots or trunks, or both, or infraclavicular, with injury distal to the level of the cords.

There are four major anatomic patterns of injury. The first is a purely upper brachial plexus lesion involving only C5 and C6; it results in weakness of the deltoid and biceps, with sparing of the triceps and distal musculature. It has been suggested that such patients typically demonstrate good spontaneous recovery.^56,57 The second and most common form is classic Erb’s palsy involving C5-7. This pattern is characterized by an extended arm, internally rotated shoulder, volar-flexed wrist, and extended fingers resulting in the “waiter’s tip” posture. The third type of injury is a total plexopathy involving C5-T1, which accounts for 20% of obstetric palsies.⁵⁷ Physical examination reveals a flaccid, insensate arm with marbled skin secondary to vasomotor disturbance. Damage to the spinal cord may have occurred. The last type of injury pattern seen is Klumpke’s palsy, which involves only the lower (C8-T1) brachial plexus. Clinically, it is manifested as an inability to pronate the forearm, hand paralysis with a “clawhand” posture, and Horner’s syndrome. Isolated lower brachial plexus injury is exceedingly rare and reportedly accounts for less than 1% of obstetric palsies.⁵⁶ We have not encountered such a case in our own patients. Patients with injury to the lower brachial plexus are less likely to recover useful function of the arm with conservative management than are those who suffer upper brachial plexus injury.

In general, postganglionic rupture of the roots and trunks is more common in the upper spinal roots, whereas preganglionic avulsion is more common in the lower spinal roots. Rupture-type injuries will demonstrate sensory conduction delay and paralysis of muscles receiving innervation from the trunk level and beyond. The only trunk branch that lends itself to clinical testing is the suprascapular nerve supplying the supraspinatus and infraspinatus muscles. In avulsion injuries, motor fibers are separated from the cell bodies, and all the musculature supplied by the injured root will be denervated, with resultant weakness. An elevated ipsilateral hemidiaphragm is present with C3-5 root injury. T1 root avulsion will produce Horner’s syndrome. Sensory fibers remain connected to cell bodies in the dorsal root ganglion, so nerve conduction will be normal. Injuries at or distal to the level of the cords are classified as infraclavicular. Cord-level branches include the lateral and medial pectoral, thoracodorsal, and subscapularis nerves. Therefore, if the most proximal weakness is noted in the pectoralis major, a lateral cord injury is suspected. Weakness of internal rotation driven by the latissimus dorsi denotes a posterior cord injury. Medial cord injury is clinically detectable only by forearm sensory loss.

Other causes of arm immobility or paralysis, both reversible and irreversible, should be considered in the differential diagnosis, including epiphyseal separation of the humeral head, fracture of the clavicle or humerus, septic arthritis of the upper limb, birth-related spinal cord injury, and congenital varicella of the upper limb.⁵⁸

Patient Evaluation

Since 1991, evaluation of patients with obstetric brachial plexus palsy at our institution has been performed in a multidisciplinary brachial plexus clinic by a team consisting of a pediatric neurosurgeon, pediatric neurologist, orthopedic surgeon, physical and occupational therapists, electrophysiologist, and nurse coordinator. A detailed obstetric and birth history is taken, with attention to the predisposing factors discussed previously. Associated injuries such as rib, spinal, clavicle, or humeral fractures are noted on plain radiographs. Clinically observed asymmetry of chest wall expansion and chest x-ray evidence of an elevated hemidiaphragm denote phrenic nerve injury. The patient is assessed for evidence of facial paresis or Horner’s syndrome. Passive range of motion of the involved arm, especially the shoulder, is evaluated. Motor strength is assessed with the simplified British Medical Council scale for muscle testing (0 to 5 scale). The Mallet score, which documents functional changes in the shoulder and arm, requires patient cooperation and is used additionally in patients older than 2 years.⁵⁹ Sensory examination is difficult, although reaction to pinch is helpful. Sensory loss is sometimes evidenced by self-mutilation (i.e., biting) of fingers.

Some palsies may resolve within days. It is not unusual for an arm to be entirely flaccid at birth, with rapid improvement revealing an upper palsy. After a few weeks when the initial traumatic neuritis has resolved, physical therapy can be instituted for persistent weakness. Physical therapy entails passive range-of-motion exercises performed by a family member under the guidance of a physical therapist.

The infant is re-examined at 4 weeks of age. Frequently, recovery is complete or nearly complete, which signifies a neurapraxic injury. At this point, if there is still total palsy associated with Horner’s sign, the outlook is poor, and parents are informed of the possible need for surgical intervention. If hand function is improving without evidence of shoulder recovery, the patient is managed conservatively because there is still opportunity for recovery.⁶⁰ Patients are examined on a monthly basis. Infants who make progressive recovery and have antigravity or greater than antigravity strength in the biceps, triceps, or deltoid muscles by 3 to 4 months of age continue to be monitored expectantly.⁴⁶ Infants displaying less than antigravity strength in each of these muscles are referred for neuroimaging and electrophysiologic studies in anticipation of surgery. If the deltoid, biceps, or triceps muscle still has less than antigravity strength at 6 months of age, we recommend brachial plexus surgery (Table 213-2). Braces are no longer advocated because of the propensity for contracture.²⁵

TABLE 213-2 Indications for Surgical Intervention

When surgery is being considered, electromyography (EMG) with nerve conduction studies is delayed until the third month. If an intrauterine lesion is suspected, EMG is performed within a week after delivery to document denervation.^61,62 EMG can provide useful information on the extent and distribution of brachial plexus injury and the recovery pattern. In addition, nerve root avulsion can be confirmed by normal sensory conduction in the presence of severe motor weakness. The usefulness of EMG in postoperative follow-up of patients is unclear. In infants, it takes only a small number of intact axons to provoke an electrical response that may not be associated with clinical recovery.

Preoperative cervical magnetic resonance imaging (MRI) evaluates nerve root avulsion.^63–65 The presence of pseudomeningoceles has been associated with nerve root avulsion; however, this finding is not pathognomonic and should instead be considered a sign of root damage inasmuch as 15% of pseudomeningoceles are not associated with complete nerve root avulsion.⁶⁶ In addition, 20% of avulsed nerve roots may not have an associated pseudomeningocele.⁶⁷ We use fast spin echo MRI for preoperative neuroimaging because it is less invasive and provides data comparable to that of computed tomographic myelography for operative planning (Fig. 213-2).⁴⁷ MRI does not clearly delineate nerve roots within the pseudomeningocele. In cases of total palsy, MRI allows imaging of the spinal cord.

FIGURE 213-2 Fast spin echo magnetic resonance image. Note the pseudomeningocele on the left.

Surgical Treatment

Exposure of the Brachial Plexus

Under general anesthesia with a short-acting neuromuscular agent, the patient is placed supine with a shoulder roll to elevate the clavicular region, and the head is turned to the contralateral side. The neck, chest, affected upper extremity, and both lower extremities are prepared, the incision marked, and drapes applied. In an infant, an arm board is not usually necessary. The entire affected upper extremity is kept available for visual inspection of muscle contraction in response to electrical stimulation during surgery. The supraclavicular portion of the incision begins a fingerbreadth beneath the mastoid tip and courses along the posterior border of the sternocleidomastoid muscle to the clavicle. For infraclavicular exposure, the incision then turns laterally along the superior border of the clavicle to reach the deltopectoral groove. At this point, it curves inferiorly along the groove and anterior axillary fold (Fig. 213-3). Repair of the upper roots is accomplished purely through a supraclavicular approach, whereas total palsy may require a combined approach.

FIGURE 213-3 Operating room positioning and incision for complete exposure of the brachial plexus.

Supraclavicular exposure is begun with an incision through the skin and platysma muscle along the posterior border of the sternocleidomastoid. The skin flaps are raised, followed by a second flap of fibrofatty tissue overlying the brachial plexus. The omohyoid muscle is divided. Dissection is extended down to expose the clavicle; the subclavius muscle and periosteum of the clavicle are divided. When neuroma extends beyond the divisions of the brachial plexus, it is necessary to free the clavicle off the clavicular portion of the pectoralis major muscle and expose the cords of the brachial plexus. A pectoral nerve arising from the anterior division of the upper trunk is identified and spared.

The initial dissection is directed to expose the C5 and C6 nerve roots and upper trunk. While exposing the upper trunk it is important to identify the phrenic nerve along the anterior scalene muscle and the spinal accessory nerve arising from C4. The accessory nerve emerges from the posterior part of the sternocleidomastoid muscle at the junction of its upper and middle thirds and continues toward the trapezius muscle. Direct electrical stimulation helps identify the phrenic and accessory nerves.

A neuroma involving the upper trunk is readily identified. The C5 nerve root is identified by following up the most superficial portion of the upper trunk toward the neural foramen. To expose the C6-T1 nerve roots, the anterior scalene muscle must be divided and partially removed. The T1 nerve root is adjacent to the pleura and subclavian vessels, and care is taken to avoid injury to these structures. One can recognize varying thickness of nerve roots. In cases of nerve root avulsion, the nerve root is replaced by thin fibrotic tissue; neuroma in the nerve roots thickens the affected roots. Soft Silastic vessel loops are placed around the roots for identification and traction. The three trunks are identified close to the clavicle. When neuroma at the level of the nerve roots and trunk is extensive, it is necessary to first identify the trunks and divisions of the brachial plexus and continue dissection toward the roots. One should keep in mind that the lower trunk is also immediately adjacent to the pleura and subclavian vessels. The upper trunk gives rise to the supraclavicular nerve, which is found above the clavicle. It is common to encounter the trunks surrounded by fibrotic tissue and scarred medial scalene muscle. To free the trunks, one should remove the fibrotic tissue. At this point, one should look for and spare the long thoracic, thoracodorsal, and subscapularis nerves, which are located under the upper trunk and above the medial scalene muscle. Infraclavicular exposure is obtained by extending the incision as previously described with dissection along the deltopectoral groove. The cephalic vein should be spared. Marking sutures are applied to the pectoralis major before dividing its insertion onto the humerus, and a cuff of tendon should be left at each end for later approximation. The pectoralis minor is divided, and repair is not essential at closure. Clavicular osteotomy is not needed. After division of the pectoralis muscles, the cords of the brachial plexus, median nerve, ulnar nerve, musculocutaneous nerve, and axillary nerve are identified.

Although the sural nerve is generally used for grafting, donor nerves may additionally be obtained from parts of the plexus where reconstruction is unlikely to succeed, such as the medial cord, ulnar nerve, or medial cutaneous nerve of the forearm. Sural nerve grafts are harvested via an open posterior lower leg incision.

Repair Procedures

Various grafting and neurotization procedures are needed to repair the brachial plexus. The main goal of surgery for primarily upper palsy is to restore shoulder and biceps muscle function. This goal can be achieved by nerve grafting to all or part of the upper trunk, supraclavicular nerve, or axillary nerve arising from the posterior cord. The accessory nerve, stumps of the C5 or C6 roots, or both, or the C7 nerve root can be used for grafting (Fig. 213-4). In patients with total plexus injury, various combinations of nerve grafting are needed. If two or three nerve root stumps are found, the nerve roots are divided and used for grafting all trunks or cords of the brachial plexus. If only one nerve root stump is available, it is grafted to the musculocutaneous nerve, and three to four intercostal nerves are connected to the ulnar nerve. Nerve grafts should be prepared 10% to 15% longer than the measured length to account for later contraction. Anastomosis can be completed with 9-0 Prolene epineural sutures or fibrin glue. We prefer to combine suture with fibrin glue because the results of repair with glue are equivalent or possibly slightly better than the use of suture alone. The pectoralis major is reinserted with nonabsorbable suture, and the wound is closed in layers, including the platysma muscle, in routine fashion. The shoulder is held in an adducted position over the trunk with a large elastic bandage.

FIGURE 213-4 Operative photographs of brachial plexus reconstruction and grafting in a 7-month-old girl who sustained a right-sided birth brachial plexus injury that failed to improve with conservative management. Magnetic resonance imaging revealed no evidence of nerve root avulsion. Electromyography revealed an incomplete brachial plexus injury with the most prominent findings involving the upper trunk. Preoperatively, the patient had 0/5 deltoid, 2/5 biceps, and 4/5 triceps strength. At surgery, a neuroma was found involving primarily C5 and extending into the upper trunk (A). Intraoperative nerve testing revealed poor conduction through C5 and C6 into the upper trunk. C7 was normal. The neuroma was excised and sural nerve interposition grafts placed from C5 and C6 to the upper trunk (B). At 7 months postoperatively (14 months of age), the patient has obtained a marked improvement in upper extremity function (deltoid, 3/5; biceps, 4/5; triceps, 4/5).

Neurotization is required in avulsion injuries. It involves nerve crossover or nerve transfer such that an uninjured neighboring donor nerve is connected directly or by grafts to a distal portion of a nonfunctioning nerve. The spinal accessory, phrenic, intercostal, medial pectoral, thoracodorsal, long thoracic, and subscapular nerves have been used for neurotization. When the spinal accessory nerve is used, one should use the nerve distal to the first branch to the trapezius muscle to avoid massive denervation of the trapezius. Partial denervation of the trapezius does not cause another deficit in the patient because it usually alleviates the elevated shoulder, which most adult patients consider an aesthetic benefit.^13,72 Although phrenic nerve transfer is safe in adult patients with normal diaphragmatic function, it is not recommended in infants because of their immature respiratory system and increased risk for fatal pulmonary complications. The efficacy of neurotization of the long thoracic nerve and the thoracodorsal, subscapularis, and pectoral nerves in infants is unknown.

Complications

Potential complications include loss of existing motor function, phrenic nerve injury, leakage of cerebrospinal fluid, pneumothorax, thoracic duct injury (left side), vascular injury to the carotid artery or the jugular or subclavian veins, pseudoarthrosis of the clavicle associated with osteotomy of the clavicle, and wound infection. Airway compromise secondary to hematoma or edema is a potential problem. The infant should be monitored for ability to clear secretions and maintain adequate airway exchange. The patient’s ability to swallow and the presence of a gag reflex should be checked preoperatively because vagal and laryngeal nerve function may be altered after surgical manipulation.⁷³

Postoperative Care

The average postoperative hospitalization is 2 to 3 days. The patient’s arm is immobilized in a sling for 3 weeks. Pain is generally well controlled with acetaminophen or ibuprofen. After wound healing and immobilization, patients are started on a rigorous physical therapy regimen to prevent joint stiffness or contractures and are examined in the clinic at regular intervals (i.e., every 3 months).

Surgical Outcome

Surgical reinnervation is advocated to avoid permanent changes in the denervated muscle and developing skeletal system that can result in long-term orthopedic sequelae.^74,75 Surgical treatment aims to achieve (1) stabilization of the shoulder by reactivation of the supraspinatus and deltoid, (2) establishment of elbow flexion with reactivation of the biceps, and (3) in patients with a nonfunctional hand, restoration of median nerve sensory function for future secondary reconstruction procedures.⁷⁶ Some surgeons believe that primary reinnervation should be considered up to 18 months of age, after which time secondary procedures should be performed.⁵⁷ For infants who are appropriate surgical candidates, surgery offers a chance for better long-term functional recovery. A number of authors have shown that neurologic improvement occurs in 75% to 95% of patients undergoing surgical reconstruction of the brachial plexus, with the majority attaining antigravity strength in the shoulder or elbow, or both.^{23,42,71,76,77} Boome and Kaye reported that greater than 95% of deltoid and 80% of biceps muscles attain antigravity strength after surgery.⁵⁰ Laurent and colleagues found that 85% to 95% of patients recover antigravity strength above the elbow, along with 50% to 70% recovery below the elbow.^42,57 In our most recent series, results after surgery for upper plexus lesion were better than those for lesions of the lower plexus (Table 213-3).^{42,50,71,78–82}

Recovery begins at approximately 2 to 10 months and continues until the age of 5 years. It is generally slower with grafted nerves than with sutured or directly repaired nerves.

Secondary Reconstruction

Secondary reconstructions are performed in patients with chronic obstetric brachial plexus lesions that are not amenable or fail to respond to microsurgical reconstruction. It is required because of the muscle imbalance secondary to unopposed contraction of innervated muscle groups. Abnormal stress placed on the bones and joints of the upper limb, with resultant progressive shoulder and elbow bony deformities, will result and require operative intervention to maximize upper extremity function. Frequently, patients will have an internally rotated and adducted shoulder after upper plexus lesions.⁸³ Joint contractures are common in patients after neonatal brachial plexus injury. Secondary procedures to treat the affected limb include arthrodesis, tenodesis, muscle releases, pedicled muscle/tendon transfers, and free neurovascular tissue transfer.

Conclusion

The incidence of birth brachial plexus injury has remained constant over the past several decades. Patients should be given a trial of conservative therapy with frequent and close follow-up. Motor strength examination at 3 months of age is predictive of good outcome if antigravity strength of the deltoid, biceps, and triceps is present. Strength testing at 6 months of age is predictive of poor outcome if antigravity strength in these muscles is not attained, and surgical treatment is recommended. Only careful clinical examination and detailed understanding of the anatomy of the brachial plexus will allow a carefully planned operation. MRI is recommended over computed tomographic myelography for preoperative evaluation. Intraoperative electrophysiology can help determine repair strategies, and knowledge of historically successful donor graft sites is important in determining surgical repair options. Each operation must be tailored to the individual patient’s needs. This approach avoids operating unnecessarily on patients who are destined to recover spontaneously, and yet it is early enough to avoid permanent changes, such as contractures, in denervated and developing skeletal muscle.^46,84,85

Brachial plexus repair for birth injury is effective in selected patients, with the majority of patients making functional gains. Outcome is determined after several years of recovery, and secondary orthopedic operations may be required in later childhood.