(10920684 - Neurosurgical Focus) Nerve Transfers For Severe Brachial Plexus Injuries - A Review
(10920684 - Neurosurgical Focus) Nerve Transfers For Severe Brachial Plexus Injuries - A Review
(10920684 - Neurosurgical Focus) Nerve Transfers For Severe Brachial Plexus Injuries - A Review
Nerve transfer procedures are increasingly performed for repair of severe brachial plexus injury (BPI), in which the
proximal spinal nerve roots have been avulsed from the spinal cord. The procedure essentially involves the coaption
of a proximal foreign nerve to the distal denervated nerve to reinnervate the latter by the donated axons. Cortical plas-
ticity appears to play an important physiological role in the functional recovery of the reinnervated muscles. The author
describes the general principles governing the successful use of nerve transfers. One major goal of this literature review
is to provide a comprehensive survey on the numerous intra- and extraplexal nerves that have been used in transfer
procedures to repair the brachial plexus. Thus, an emphasis on clinical outcomes is provided throughout. The second
major goal is to discuss the role of candidate nerves for transfers in the surgical management of the common severe
brachial plexus problems encountered clinically. It is hoped that this review will provide the treating surgeon with an
updated list, indications, and expected outcomes involving nerve transfer operations for severe BPIs.
Nerve transfers (so-called neurotization) involve the re- The anatomical and physiological principles that under-
pair of a distal denervated nerve element by using a prox- lie nerve transfers are relatively straightforward. Because
imal foreign nerve as the donor of neurons and their axons motor recovery has been the main goal, the choice of a
to reinnervate the distal targets. The concept is to sacrifice donor nerve element with a reasonable amount of motor
the function of a lesser-valued donor muscle to revive fibers is required.71 The loss of the muscle due to dener-
function in the recipient nerve and muscle that will under- vation when transferring the donor nerve must not repre-
go reinnervation.71 The first report of neurotization in an sent loss of important or critical function.55 Obviously, the
attempt to restore injured plexus function was published value of the neuromuscular element to be reinnervated
by Tuttle100 in 1913. A review of the historical precedents must greatly exceed the utility of the sacrificed one. An
as well as the anatomical basis and rationale for nerve excellent compromise is achieved if some function of the
transfers in brachial plexus surgery was most clearly pre- donor muscle can be retained, by using only a portion of
sented 20 years ago by Narakas.70 Since then, nerve trans- the nerve as the donor, which has been exemplified by the
fers have become increasingly popular and used for the use of half of the hypoglossal nerve (thus, not completely
repair of BPIs, especially in cases in which the proximal denervating ipsilateral tongue) for transfer to the facial
motor source of the denervated element is absent due to nerve for reanimation of the face.6,22,28,83
avulsion from the spinal cord.88 Increasingly advocated as There are several important principles to adopt to max-
well is the use of nerve transfers in cases in which the imize outcome in nerve transfers, the first of which is to
proximal motor source is available but the distance be- reinnervate the recipient nerve as close to the target mus-
tween removal and reimplantation is so long that the out- cle as possible.72 An outstanding example of the latter is
come would be poor;30,31 a nerve transfer into the dener- the transfer of an ulnar nerve fascicle directly to the biceps
vated distal nerve stump close to the motor end organ branch of the musculocutanoeus structure in close prox-
would then restore function, which otherwise would not be imity to its entry into the muscle.74 The second principle
possible.72 The use of nerve transfers has been a major involves performing a direct repair, without intervening
advance in the field of brachial plexus nerve reconstructive
surgery, with many different ingenious transfers associat- grafts; this tactic seems to be associated with improved
ed with improving results, as reported and reviewed re- outcomes, as reported convincingly after intercostal–mus-
cently.11,43, 64,88,98 culocutaneous transfers.45,58,69,76,103 The third principle is to
use combinations of similarly behaving neuromuscular
units, maximized when agonistic donor and recipient are
Abbreviations used in this paper: BPI = brachial plexus injury; chosen, as cortical readaptation is the physiological basis
MRC = Medical Research Council. for functional recovery.56,59 This may also be the physio-
logical underpinning that explains why intraplexal (for ex- the integrity of sensory roots but do not reflect the status
ample, medial pectoral–musculocutaneous) nerve donors of the motor (ventral) roots, which can be measured using
may yield superior results compared with extraplexal (for motor evoked potential and/or neck muscle potential mon-
example, intercostal–musculocutaneous) nerves.79 The itoring.15,73 The intraoperative electrical tests and operative
last principle, not so different from that in all nerve sur- findings are used in concert with the preoperative clinical,
gery (assuming that the nerve is irreparably damaged electromyography,9 and imaging16 findings to determine
and incapable of spontaneous functional regeneration)66 the extent of injury and presence of nerve root avulsion
in which prolonging axotomy and target denervation is as- and to guide operative decisions concerning the suitable
sociated with progressively poorer outcomes,30,31 is to per- nerve reconstructive procedure.
form the transfer surgery as early as possible to maximize The goal in the management of upper (C-5 and C-6)
outcomes.80,81 nerve root paralysis is complete repair. When the upper
two roots are avulsed from the spinal cord, the only repair
option is neurotization by a nerve transfer. The nature of
NERVE TRANSFER TECHNIQUES the reparative strategy is then dictated by the number of
root avulsions, including the consideration of whether C-
Surgical Approach 7 is also avulsed. On the other hand, even in complete
The surgical management of patients with a severe BPI severe palsy, the C-5 spinal nerve may be singularly
is first to determine preoperatively whether most or all the spared, thus allowing it to be used as the source of axons
nerve roots are truly avulsed.65 The second aspect of sur- for a plexus–plexus repair to distal elements.34,47 There are
gery is to perform nerve repair, which, in the severe cases some cases in which the proximal root stump may not be
with avulsion, incorporates appropriate nerve transfers to suitable for grafting. A very proximal intraforaminal dis-
reanimate the extremity.88 Surgical exploration therefore section of the nerve roots is invaluable for assessing the
warrants exposure of the entire supra- and infraclavicular nerve anatomically,48 and combined with the examination
plexus, with an appropriately made incision, as well as of frozen section of the very proximal stump to assess the
marking of incisions that will allow exposure of donor fascicular pattern and absence of ganglion cells, has been
nerves that may need to be transferred (Fig. 1). The upper useful in decision making. Other authors have assessed
extremity, extending to the anterior and lateral chest wall, the degree of myelin staining to predict the quality of the
and both legs being targeted for donor sural grafts, should stump;61 however, in uncertain circumstances, a nerve
be appropriately prepared. transfer is preferred to using a proximal stump of ques-
After complete and thorough exposure of the plexus, tionable integrity. The combinations for repair therefore
including intraforaminal dissection and external neuroly- include intraplexal grafts alone obtained from a single
sis of the nerve-in-continuity, intraoperative electrodiag- functioning root, intraplexal grafts, and selective transfers
nostic studies should be conducted.66 First, motor evoked (the usual scenario) or transfers alone for the devastating
stimulation is used to determine which roots are conduct- cases in which all nerve roots are avulsed (Fig. 1). The
ing by observing the distal muscles contraction, occasion- nerve transfer options available will be discussed further.
ally augmented by needle-based electromyography. Nerve
action potentials are measured across the neuroma or Accessory Nerve Transfer
in clinically nonfunctioning roots, with large fast-con-
ducting (preganglionic) nerve action potentials seen when In the earliest report of a nerve transfer by Tuttle100 in
the nerve root is avulsed.49,51,66,97 Somatosensory evoked 1913, the author mentioned using the accessory nerve (as
potentials produced in the contralateral cortex help gauge well as elements of the cervical plexus) as the donor.
Accessory (11th cranial) nerve transfers for otherwise
irreparable BPIs, however, were popularized independent-
ly in the early 1980s by Allieu, et al.,3,4 and others.5,71 In
the early series, a diverse number of recipient targets were
chosen, and, depending on the distal nerve element, inter-
posed grafts were often needed. Based on cadaveric stud-
ies,46 an improved appreciation of the extracranial acces-
sory nerve’s anatomy has led to the use of more distal
dissection of the nerve close to trapezius muscle inser-
tional points, where the very distal nerve is divided prior
to its transfer.41 This preserves some trapezius innerva-
tion and allows a direct transfer to the adjacent supras-
capular nerve, without the need for an interpositional graft
(Fig. 2).
For restoration of dynamic shoulder function, both the
suprascapular and axillary nerves have been chosen as tar-
gets. Whereas the former can be repaired directly by end-
Fig. 1. Photograph showing incisions to expose various plexal to-end suture with the distal accessory nerve, the latter
and extraplexal donor and recipient nerve elements. This patient requires planning an interposed nerve graft. The authors
suffered clinically complete Erb palsy and avulsion of C-5 and C- of recent series have confirmed Alnot’s bias5 that the
6 spinal nerves; he underwent surgery after a delayed referral (the suprascapular, compared with axillary, nerve is a superior
same patient is represented in Figs. 6 and 7). target for accessory nerve transfer, with generally good
lateral cord contribution to median nerve; they reported a however, noted that in their hands, a portion of the medi-
100% success rate with good sensory recovery.26 an nerve was a more reliable donor for achieving elbow
One of the main criticisms of this transfer technique flexion recovery than the phrenic nerve.43 When the
remains the long graft (and hence regeneration) distance. phrenic nerve is sacrificed, one important issue is the re-
The possibility of a prespinal retropharyngeal route for sulting respiratory compromise, in which decrease in vital
graft placement has been proposed.63 Nevertheless, the capacity has been measured to be a mean of approximate-
technique remains limited because of the rather modest ly 10%.55 Although not clinically important in the majori-
motor recovery, the fact that synchronous movement of ty of situations, this degree of respiratory loss will produce
the unaffected side is required, and the small but real risk symptoms in higher-demand situations and may be se-
that the donor site may be injured and a functional deficit verely detrimental to infants and children who develop
results.90,92 Perhaps a targeted approach to obtaining me- respiratory infections. This factor essentially precludes the
dian nerve distribution sensory recovery is warranted,26 use of the phrenic nerve as a donor in infants undergoing
although similar outcomes may be possible with a less nerve reconstruction for obstetric palsy. Moreover, it also
cumbersome transfer from the lower intercostal nerves to implies that the intercostal nerves should not be used as
the sensory (lateral cord) head of the median nerve.24 donors for transfer when phrenic nerve function is absent
preoperatively or when the phrenic nerve is transferred.
Cervical Plexus
The use of the anterior branches of the cervical plexus Medial Pectoral Nerves
(C-3 and C-4) for transfer to the distal elements usually The pectoralis major muscle has dual input from the
supplied by (the avulsed) upper spinal nerves was first medial and lateral pectoral nerves, arising from the medi-
advocated by Brunelli and Monini.14 Based on cadaveric al and lateral cords, respectively. Because C-5 and C-6
studies in which they observed present (but variable- avulsion interrupts the lateral cord supply, the muscle re-
sized) discernible sensory and motor branches, the authors mains innervated (and strong) as long a significant injury
reported modest results after selective transfer of motor is not incurred to the C-7 and C-8 elements. Although
branches to musculocutaneous, suprascapular, and axil- popularized recently for upper plexal injuries,13 using the
lary nerves and sensory branches to the median nerve. medial pectoral nerve as a donor for transfer was pre-
Earlier efforts to transfer the entire cervical plexus ele- viously considered and infrequently used, as indicated
ments to the avulsed C-5 and C-6 roots failed, likely be- by Narakas70 for adults and Gilbert33 for obstetric palsy.
cause of the great disparity between the number of axons Brandt and Mackinnon13 directed the medial pectoral to
in the donor cervical plexus elements and the recipient the musculocutaneous nerve, with the additional innova-
elements.14 Recently, however, Yamada and colleagues106 tion of turning the lateral antebrachial cutaneous nerve
performed surgery in three cases in which they transferred (the cutaneous derivative of the musculocutaneous nerve)
the anterior primary rami of C-3 and C-4, just distal to into the biceps muscle to avoid loss of motor axons into
phrenic nerve, via sural nerve grafts directly to the upper the cutaneous distribution. A resurgence of interest in this
trunk; the patients had suffered C-5 and C-6 avulsion transfer has been associated with reports of useful out-
injuries, and the authors reported good results postopera- comes (defined as MRC grade 3) in elbow flexion in
tively in shoulder girdle and biceps muscles, as well as approximately 84% of patients.78 Excellent results in ob-
improved sensation. In a larger series, they obtained even stetric palsy too have been published, with success in 68%
better results in cases involving upper plexus palsy and, of cases.12 Others have criticized the use of this transfer
surprisingly, in cases involving complete flail arm.105 Oth- strategy in obstetric palsy because of loss of arm adduc-
er investigators have been unable to validate these remark- tion, which can be useful for the infant, toddler, and child
able results, demonstrating more modest success when to hold objects against the trunk,59 especially because the
using the motor components (which are unfortunately intercostal transfer yields such favorable results in this set-
quite limited after phrenic nerve supply14) to branches ting.44 The results of various series vary, however, and
of the upper trunk when both C-5 and C-6 nerves are Samardzic, et al.,79 have noted that medial pectoral nerve
avulsed.25,47,50 transfers were associated with significantly improved out-
comes in elbow flexion compared with intercostal and ac-
Phrenic Nerve
cessory nerve transfers. These authors have also been one
Unlike the cervical plexus, which contains a variable of the few groups to demonstrate remarkably good results
number of motor fibers,14 the phrenic nerve contains a after axillary nerve transfer; they observed useful results
large number of pure motor axons that allow the possibil- in greater than 80% of patients.78
ity of entire or partial transfer with success.101 In the early With the increasing interest in the medial pectoral nerve
use of the phrenic nerve for transfer, investigators noted as a donor, the anatomy of the pectoral nerve complex has
good outcomes.17,101 Subsequently, transfers involving the been more clearly defined.8,39 The traditional concept of
phrenic nerve as the neurotizer have been performed with separate lateral and medial pectoral nerves innervating the
considerable success. 17,19,38,43,101,107 In one study of 12 pa- pectoralis minor and major muscles as discrete nerves has
tients, phrenic nerve transfer to musculocutaneous, supra- been replaced; in fact, these nerves run toward the pec-
scapular, or axillary nerves was successful in 75% of toralis minor and major muscles, exhibiting considerable
cases.88 Particularly, the transfer to the musculocutaneous branching and intermingling. Not infrequently, a plexus
nerve has been an excellent tactic, with 11 of 12 patients forms where branches from the medial and lateral pectoral
exhibiting better than antigravity function (MRC Grade 3) nerves, destined for the pectoralis major, merge and then
and 58% exhibited MRC Grade 4 function.55 One group, final branches move toward the muscle (Fig. 5A).8,39 Be-
cause only one or, at times, two of these terminal branch- eral authors.1,43,52,54,74,94 Most impressive have been the re-
es to the pectoralis are required (and quite distally) for the sults reported by Sungpet and associates94 who used a sin-
transfer, the practical implication is that some pectoralis gle ulnar nerve fascicle directed to the biceps muscle; they
major muscle supply can be preserved and a direct repair observed MRC Grade 3 or better outcome in 34 of 36 pa-
without intervening graft can be performed to the muscu- tients. They also noted that time to reinnervation began as
locutaneous nerve in the distal axilla (Fig. 5B).72 Caution early as 3.3 months postoperatively and that hand and
needs to be exercised if C-7 and C8 nerves are signifi- ulnar function, assessed using a series of tests and func-
cantly injured; in this case, the pectoralis major muscle tional tools, was not compromised during a long-term fol-
will be quite weak preoperatively, and this finding is a low-up period. The key aspect of the procedure is to rein-
contraindication to medial pectoral transfer. A similar so- nervate the biceps branch close to its motor entry into the
phisticated appreciation of the innervated anatomy to the muscle.93
biceps and brachialis muscles93 has prompted evolution in The authors of a recent report indicated that elbow flex-
transfer techniques so that both the biceps and brachialis ion function will be further augmented (especially in cases
muscles discretely become reinnervated.99 of delayed surgery) by also concomitantly reinnervating
brachialis muscle by using a graft from the medial pector-
Distal Interplexal Transfer al nerve.99 Another alternative to the ulnar fascicle is a fas-
An exciting development in neurotization has been the cicle of the adjacent median nerve to transfer to biceps
transfer of portions of functioning distal plexal elements muscle nerve; good results have been reported in 64%43 to
for the direct reinnervation of nerve branches going to 80% of patients.91
critical muscles that are paralyzed.72 This era really began An emerging transfer technique is the direct repair of
recently with anatomical studies of the fascicular patterns the anterior branch of the axillary nerve; in this procedure,
and their application in several patients in whom a single the nerve to the long head of triceps in the posterior arm is
redundant ulnar nerve fascicle was transferred to biceps used (Fig. 7).53,104 The anatomy involved in this transfer
branches in the medial arm to restore elbow flexion (Fig. operation104 as well as good-to-excellent results achieved
6).74 These initial excellent results were validated by sev- in seven cases,53 especially when combined with accesso-
ry–suprascapular nerve transfer, may herald improved dy-
namic shoulder function than previously possible with the
flail shoulder after C-5 and C-6 avulsions.53 Indeed, au-
thors of the most recent series have demonstrated the ben-
efit of several targeted transfers in patients with plexus
avulsions.11
Other Transfers
Although the hypoglossal nerve has been an excellent
donor for transfer to the facial nerve,75,82 it has an extreme-
ly limited value for neurotization of brachial plexus ele-
ments.28,57
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