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JNNP Online First, published on July 1, 2015 as 10.1136/jnnp-2015-310420
1
Division of Plastic Surgery,
Departments of Surgery,
University of Alberta
2
Co-directors Peripheral Nerve
Clinic, St. Josephs Health Care,
London, Ontario, Canada
3
Roth-McFarlane Hand and
Upper Limb Centre, St. Josephs
Health Care, Western
University, London, Ontario,
Canada
4
Department of Surgery,
Western University, (Hospital)
St Joseph’s Health Care,
London, Ontario, Canada
5
Department of Physical
Medicine and Rehabilitation,
Schulich School of Medicine
and Dentistry, Western
University, London, Canada
Correspondence to
Dr Thomas A Miller, 21
Grosvenor St. London,
Ontario, Canada N6A 1Y6;
tmiller@uwo.ca
Received 22 January 2015
Revised 19 May 2015
Accepted 4 June 2015
▸ http://dx.doi.org/10.1136/
jnnp-2014-310175
To cite: Korus L, Ross DC,
Doherty CD, et al. J Neurol
Neurosurg Psychiatry
Published Online First:
[please include Day Month
Year] doi:10.1136/jnnp-
2015-310420
Copyright Article author (or their employer) 2015. Produced by BMJ Publishing Group Ltd under licence.
Neurosurgery
REVIEW
Nerve transfers and neurotization in peripheral nerve
injury, from surgery to rehabilitation
Lisa Korus,1 Douglas C Ross,2,3,4 Christopher D Doherty,3,4 Thomas A Miller2,3,5
ABSTRACT
Peripheral nerve injury (PNI) and recent advances in
nerve reconstruction (such as neurotization with nerve
transfers) have improved outcomes for patients suffering
peripheral nerve trauma. The purpose of this paper is to
bridge the gap between the electromyographer/clinical
neurophysiologist and the peripheral nerve surgeon.
Whereas the preceding literature focuses on either the
basic science behind nerve injury and reconstruction, or
the surgical options and algorithms, this paper
demonstrates how electromyography is not just a
‘decision tool’ when deciding whether to operate but is
also essential to all phases of PNI management
including surgery and rehabilitation. The recent advances
in the reconstruction and rehabilitation of PNI is
demonstrated using case examples to assist the
electromyographer to understand modern surgical
techniques and the unique demands they ask from
electrodiagnostic testing.
BACKGROUND
Peripheral nerve injuries (PNI) are frequently
encountered by primary care physicians and specia-
lists alike. Despite their prevalence, management
and referral protocols are not always clear. Recent
advances in nerve reconstruction, particularly the
so-called nerve transfers, have improved the results
of surgical repair and can extend the time available
from injury to repair.1 2 Transfers such as those uti-
lised to restore elbow flexion have improved average
outcomes dramatically. Such transfers represent a
new paradigm in nerve reconstruction and utilise
adjacent uninjured nerves to reconstruct injured
ones. For the electromyographer, this introduces
another component to electrophysiological testing
because the functional status of potential donors has
become an important aspect of the assessment after
PNI. This paper will introduce the concept of, and
indications for, nerve transfers, give examples of
commonly utilised nerve transfers, outline import-
ant components of assessment by the electromyo-
grapher and introduce the key modifications
(relative to ‘conventional repair’) in the rehabilita-
tion of PNI after nerve transfer reconstruction.
A delay in diagnosis and repair or a very prox-
imal injury both result in the same adverse conse-
quence of prolonged denervation of the muscle
with loss of the motor endplate’s ability to ‘accept’
a regenerating axon. While assessing a group of
patients with radial nerve injury, Malikowski3 iden-
tified several factors on electrodiagnostic testing
which predict poor spontaneous outcome and are
most likely generalisable to other peripheral nerve
Korus L, et al. J Neurol Neurosurg Psychiatry 2015;0:1–10. doi:10.1136/jnnp-2015-310420
injuries; these include (1) compound muscle action
potential (CMAP) amplitude <10% of the contra-
lateral side, (2) Absent motor units on Needle elec-
tromyography (EMG) and (3) a marked reduction
in motor unit action potential (MUAP) recruitment
in the most proximal muscle expected to recover.
Knowledge of these factors may limit delays in the
surgical care of patients with PNI who are unlikely
to recover spontaneously.
Working with a rat hind limb model of nerve div-
ision and repair after various interval times from 0
to 52 weeks, Kuzon et al4 demonstrated a nearly
linear fall-off in muscle tetanic force as a function of
time to repair. It was noted that even a 2-week delay
in repair produced a 40% decrease in overall tetanic
power. In an elegant series of papers, Gordon et al
have demonstrated that poor function after a delay
in reinnervation of target muscles results from a
combination of decreased regenerative capacity in
chronically axonotmized proximal nerve stumps, a
decreasing capacity of distal nerve stumps to
support even freshly regenerating axons, and finally,
an inability of chronically denervated muscle to
recover from denervation atrophy5–7. Practically
speaking, it has become generally accepted that time
from injury to reinnervation beyond 18–24 months
will result in poor functional recovery; it is import-
ant to recall that this time includes the time from
injury to repair as well as the time from repair to
reinnervation at the motor endplate.
The roots of modern nerve repair began with
Seddon’s classic works arising from the World War
II.8 9 Millesi10 subsequently recognised the adverse
effects of nerve repair under tension and intro-
duced the widespread use of nerve grafts to over-
come gaps. Although the results of nerve repair
were improved using nerve grafts, outcomes were
frequently less than optimal. Factors that are asso-
ciated with a poor outcome after repair have been
recognised11 and are highlighted in the accompany-
ing paper in this journal by Simon et al.12
In summary, a delay in ‘delivering’ regenerating
axons to the motor endplate plays a key role in limit-
ing recovery after PNI. This emphasises the import-
ance of timely recognition of axonotmetic/
neurotmetic lesions and early referral to a peripheral
nerve surgeon where appropriate; surgical strategies
to minimise these effects include new reconstructive
techniques such as nerve transfers which bring the
‘live’ axons closer to the denervated muscle.
Assessment of PNI
Appropriate treatment of PNI is guided by history,
as well as serial physical and electrodiagnostic
1
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Neurosurgery
examinations. The key question is whether adequate, spontan-
eous recovery is likely to occur or is surgical exploration and
reconstruction warranted? In cases of acute, low-velocity (eg,
knife, glass) penetrating trauma with a concurrent motor or
sensory deficit, urgent referral for exploration and possible
repair is appropriate. It is optimal to complete primary neuror-
rhaphy as soon as possible, typically within 7–10 days, allowing
for easier technical coaptation. Often, irreversible retraction of
lacerated nerve ends occurs and repair after that time will
require nerve grafting and/or a nerve transfer with attendant
donor site morbidity as well as poorer average outcomes. Since
nerve deficits after gunshot wounds are commonly secondary to
the kinetic energy imparted by the missile (as opposed to nerve
laceration), they should be followed in the same fashion as
closed stretch injuries (outlined below).
Closed nerve injuries present a difficult and different chal-
lenge for the electromyographer and the peripheral nerve
surgeon. Many injuries will recover spontaneously,12–14 but for
the subgroup of patients with PNI, which will not, it is known
that outcomes are better the sooner the repair is per-
formed.3 11 12 Appropriate electrodiagnostic testing will assist in
determining which injuries are best observed and which should
be treated surgically.
Electrodiagnostic testing will detect nerve recovery 2–
3 months prior to clinical evidence of recovery and therefore is
critically important when following closed injuries. While diffi-
cult to generalise, most PNIs, which are destined to spontan-
eously recover with adequate function, will demonstrate this on
EMG/nerve conduction studies by 4–6 months postinjury. The
4–6 month time frame is dependent on many factors, and dis-
tance from the nerve lesion to the target muscle is crucial; there-
fore, for some injuries (eg, proximal sciatic nerve injuries), this
time frame may be too short. The practical take-home message
is to not continue to follow long term, hoping for a return of
motor units based solely on distance.13 The importance of serial
EMG/NCS (ie, q1–3 monthly) and the use of several comple-
mentary features on electrodiagnostic testing, such as CMAP
amplitude, motor unit recruitment in proximal muscles, the
presence of collateral reinnervation and the finding of nascent
units early, will assist in determining prognosis. Important signs
that can be useful to predict spontaneous recovery include both
a lessening degree of denervation, associated with an increase in
MUAPs and improvement in recruitment over time.3 13 14
While helpful in the assessment of compression neuropathies
and peripheral nerve tumours, at present, cross-sectional
imaging is often limited in terms of its clinical and diagnostic
usefulness in the investigation of traumatic nerve injuries,15
especially in the context of determining whether nerves in con-
tinuity are likely to spontaneously regenerate. One exception is
the assessment of the cervical spine in brachial plexus injuries,
when considering nerve root avulsion. CT myelography and
MRI have a diagnostic accuracy of 70% to 95%, when looking
for a pseudomeningocele and possible root avulsion.16 The sen-
sitivity of detection of cervical nerve root avulsion is reported
to be 93% for both MR and CT myelography.17 In a mixed
group of patients, Du et al18 found that MRI and EMG assess-
ment provided complementary information.
Surgical treatment of PNI
The ‘bridging’ of nerve gaps with nerve autografts has become
the gold standard in the delayed repair of nerve injuries.10 19
Recent modifications of this include the use of processed nerve
allografts20 and nerve conduits.21 Allografts appear to perform
better than nerve conduits, but there are insufficient data to
2 Korus L, et al. J Neurol Neurosurg Psychiatry 2015;0:1–10. doi:10.1136/jnnp-2015-310420
confirm that they are equivalent to nerve autografts, particularly
in major mixed motor nerves. Nerve grafts have been the long-
standing gold standard in delayed repair of nerve injuries;12
however, results from multiple studies comparing nerve grafts
with nerve transfers demonstrate that nerve transfers are com-
parable and in some references superior to nerve grafting for
PNI.22 23
In contrast to more traditional nerve grafting techniques,
intraoperative electrophysiological studies, which were a major
advance in the management of peripheral nerve trauma, are
often not needed nor indicated in nerve transfer surgery. The
generation of compound nerve action potentials (CNAPs) by
stimulating and recording electrodes applied directly to the
nerve trunk can be helpful in refining a surgical plan. The trad-
itional CNAP studies performed following surgical exposure of
the nerve are often helpful in brachial plexus surgery to deter-
mine nerves in continuity, and are outlined in the accompanying
paper and other reviews.12 19 24 25
Nerve transfers are a surgical technique in which an expend-
able or ‘redundant’ nerve (or fascicle contained within a nerve)
is divided and transferred to power an injured, more critical
muscle function. Although basic nerve transfers have been per-
formed for decades, they typically were a poorly functioning
‘last resort’ for severe injuries. An example of this is the use of
intercostal nerves to restore musculocutaneous nerve function
when all five roots were avulsed in a brachial plexus injury.26
Conversely, more recently described nerve transfers are com-
monly used instead of classic nerve graft procedures and utilise
richly innervated donor nerves and transfer them to specific
recipient motor nerves—frequently close to the neuromuscular
hilum.23 27–32
Nerve transfers ‘solve’ two of the common problems asso-
ciated with conventional nerve reconstruction. First, by utilising
donor nerves situated very close to the recipient nerve/muscle,
the problem of time to reinnervation (as in proximal injuries or
after a delay in diagnosis/referral) is significantly ameliorated.
Second, since such transfers typically use pure motor donor
nerves and transfer them to a ‘pure’ motor recipient nerve, the
problem of potentially mismatching proximal sensory fascicles
with distal motor recipient fascicles is avoided.
Since the publication of two key articles in 200427 and
2005,28 demonstrating improvement in elbow flexion, nerve
transfers have become established as a new paradigm in the
reconstruction of PNI. The transfers described in those two
papers can also serve as illustrative examples of the use of nerve
transfers. Until the advent of nerve transfers, a patient with an
injury to the upper trunk of the brachial plexus would be recon-
structed with nerve grafts spanning the injured segment.
Results of this type of reconstruction were reasonable, par-
ticularly in infants with birth-related Erb-type palsies, but fre-
quently useful function would not return to one or more of the
three key peripheral nerves formed by the C5 and C6 roots
(suprascapular, axillary and musculocutaneous).19 31–35 The
principal reasons for these unpredictable results were felt to be
secondary to (1) distance from injury to motor endplates and
(2) mismatching of proximal and distal fascicles across the seg-
mental injury.
Experience with nerve transfers in children remains limited,
although good outcomes have been reported.35 36 Whether
such transfers in children—and specifically birth-related brachial
plexus injuries—produce better outcomes is unclear. As noted in
a recent review by Tse et al,37 nerve transfers are indicated in
situations where conventional nerve grafting may not be pos-
sible or ideal: late presentations, failed primary reconstruction,
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Neurosurgery

multiple nerve root avulsions or isolated deficits. The authors
have found the latter to be particularly useful, such as in the
context of poor elbow flexion despite recovery of good shoulder
function in Erb-type palsies. At present, there has not been spe-
cific evaluation of nerve transfers compared to nerve grafting in
patients over the age of 65.
Oberlin29 and Mackinnon28 described nerve transfers to
restore elbow flexion which ‘ignored’ the injured area and
instead transferred nerve(s) close to the motor branches of
biceps and brachialis in the arm. In these reconstructions, a
microscopic, internal neurolysis of the ulnar nerve (Oberlin
single nerve transfer) or ulnar and median nerves (Mackinnon
double nerve transfer) adjacent to the motor branches of the
biceps and brachialis (figure 1) was performed to identify
‘redundant’ fascicles with the use of a portable nerve stimulator.
In the case of the ulnar nerve, such fascicles serve to innervate
the flexor carpi ulnaris (FCU) muscle and, in the case of the
median nerve, serve to innervate the flexor digitorum superficia-
lis (FDS) muscle. Once identified, the fascicles are divided and
transferred to the adjacent motor nerves of biceps (Oberlin) or
biceps and brachialis (Mackinnon). The nerve repair is typically
performed within 1–2 cm of the neuromuscular hilum, and
therefore times to reinnervation are very short. It is not uncom-
mon to achieve Medical Research Council (MRC) grade 3
recovery by 4–5 months postrepair, which is far sooner than
conventional upper trunk grafting would produce. Whereas it
was originally assumed that the loss of the donor muscle func-
tion was acceptable (flexor carpi radialis still present as the wrist
flexor, and flexor digitorum profundus still present as the finger
flexor), more experience has demonstrated that multiple fasci-
cles subserve these muscle functions and therefore the donor
nerve/muscle deficits are mild.
Over the past decade, multiple other nerve transfers have
been described and are being utilised with greater frequency.
Knowledge of these nerve transfers will allow the electromyo-
grapher to provide key information to the peripheral nerve
surgeon. With the advent of reconstruction with nerve transfers,
the reconstructive surgeon now wishes to know: (1) which
nerve(s) are injured, (2) is there any evidence of recovery and
(3) are nerve(s) which may act as potential donors for nerve
transfers functioning normally? The latter is a completely new
type of information being requested from the electromyogra-
pher. It is important to note that nerves in the proximity of the
injury may have been injured as well and muscle weakness on
clinical examination may not be seen until greater than 50% of
the axons innervating a muscle have been injured. Therefore,
EMG examination of potential donors provides critical informa-
tion to the surgeon attempting to assess which nerves to use.30
A list of commonly utilised nerve transfers is given in table 1.
Nerve transfers in the surgical management of PNI and a
review of the seminal papers are presented in table form and are
grouped to highlight the functional anatomic deficit.
Table 2 summarises the literature using median and ulnar
nerve fascicles and nerve transfers to the musculocutaneous
nerve to augment elbow flexion.
Reconstructing elbow flexion with nerve transfers produces
significantly better results than traditional sural nerve grafting of
neuromas in continuity of the upper trunk of the brachial plexus.
MRC grade 4/5 recovery is now a typical result for elbow flexion
power in brachial plexus injuries. This is seen both in the
authors’ clinical experience as well as in the greater than 180
patients in the published studies to date23 28 29 32–39 43 42
Tables 3 and 4 outline the surgical options to improve and
augment shoulder function. Table 3 summarises the

Figure 1 ‘Double Transfer’ to restore elbow flexion. Using microsurgical techniques, specific fascicles destined to innervate flexor carpi ulnaris
(FCU, within ulnar nerve) and flexor digitorum superficialis (FDS, within the median nerve) are identified and transferred to the motor branches of
the biceps and brachialis muscles, respectively. Redundancy of fascicles means some FCU and FDS function is maintained. Reconstruction may also
be performed using a single (aka ‘Oberlin’) transfer of the FCU fascicle to the biceps alone.

Korus L, et al. J Neurol Neurosurg Psychiatry 2015;0:1–10. doi:10.1136/jnnp-2015-310420 3

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Neurosurgery

nerve injury with no evidence of nerve recovery. Since the

Table 1 Commonly utilised neurotization procedures
results of axillary nerve reconstruction have been shown to be
Nerve injury Donor nerve Comments inferior if the repair is completed more than 6 months postin-
jury,46–48 51 the patient was referred to a peripheral nerve
Musculocutaneous/ Fascicle within ulnar nerve Transferred directly to
upper trunk brachial subserving FCU biceps motor branch
surgeon for possible exploration and reconstruction.
plexus Although conventional nerve grafting yields reasonable results
Musculocutaneous/ Fascicle within ulnar nerve Transferred directly to in isolated axillary nerve injuries, nerve transfers are increasingly
upper trunk brachial subserving FCU+fascicle biceps and brachialis utilised to reconstruct these injuries.46 48 51 Since the donor
plexus within median nerve motor branches nerve to reconstruct the axillary nerve is a branch from one of
subserving FDS, etc
the heads of the triceps, the importance of needle electrode
Ulnar nerve Distal AIN May be transferred
examination (NEE) EMG assessment of the triceps (2 of 3
end-to-end or
end-to-side to motor heads) is emphasised in this clinical scenario. In addition, clin-
component of ulnar ical and electrodiagnostic assessment of the posterior cord inner-
nerve vated latissimus dorsi, as well as of a distal radial innervated
Axillary nerve/upper Motor branches of radial May not be available in muscle (eg, extensor digitorum communis), is required.
trunk brachial plexus nerve to triceps (long or posterior cord injuries At 5 months postinjury, reconstruction was undertaken using
medial head)
the branch to the medial head of the triceps transferred to the
Suprascapular nerve Distal spinal accessory Proximal branches of
nerve CN XI retained to
anterior division of the axillary nerve. Electromyographic evi-
preserve trapezius dence of recovery of the posterior portion of the deltoid was
function evident at 2 months (8 weeks) postrepair. This illustrates that
Posterior interosseous Branches of median nerve May diminish options nerve recovery after nerve transfer is often surprisingly early
nerve (FDS, FCR) for later tendon postsurgery as well as the importance of EMG testing to detect
transfers
that early recovery. Such evidence of reinnervation marks the
Axillary nerve Medial pectoral nerve Difficulty with
time to begin rehabilitation focusing on enhancing cortical
relearning makes a
secondary choice reorganisation to utilise the transferred nerve.47 The patient
Long thoracic Thoracodorsal nerve – went on to have MRC grade 4 shoulder abduction and forward
nerve/C5 6, 7 injuries flexion.
Avulsion of multiple Intercostal nerves Challenging to relearn, The importance of using and initiating shoulder abduction
cervical roots elbow flexion power (deltoid) by beginning with elbow extension (thereby ‘firing’ the
modest donor nerve), both in therapy and in the EMG laboratory, is
Avulsion of all roots Contralateral C7 root Conflicting reports on crucial. The first nascent units are often recruited in the deltoid
extended with vascularised efficacy
nerve graft
by the kinesiological phenomena of elbow extension to start or
Peroneal nerve Branches of tibial nerve Very difficult to relearn
initiate shoulder abduction. Once reinnervation is detected,
(eg, lateral gastrocnemius). therapy on the injured muscle should begin with isolated iso-
May require nerve graft to metric contractions, so as not to overwork the recovering
extend muscle units. This peripheral and central neuroplasticity requires
AIN, anterior interosseous nerve; FCU, flexor carpi ulnaris; FCR, flexor carpi radialis; practice and the use of biofeedback, EMG and neuromuscular
FDS, flexor digitorum superficialis. stimulation, supervised in physiotherapy.40 52 The potential of
many nerve transfer procedures will not be fully realised
without specific physiotherapy, which we feel is best collabora-
suprascapular nerve function,33–35 42 43 and table 4 summarises tively supervised by the electromyographer and peripheral nerve
the importance of the deltoid in shoulder stability. surgeon. In other words, the patient requires relearning and
The majority of peripheral nerve surgeons now reconstruct neuroplasticity to initiate a contraction by first involving the
the suprascapular nerve by transferring the distal (leaving the nerve used to transfer (ie, elbow extension to abduct the arm;
important branches to the medial scapula portion of the trapez- figure 2).
ius muscle intact, ie, medial scapular stability) spinal accessory The following table (Table 4) focuses on shoulder stability with a
nerve. It obviates any questions of whether the proximal end of radial nerve to triceps transfer to the axillary nerve.40 46 47 49 50 52
a nerve graft sewn to the C5 nerve root is being sewn to a There are no trials comparing nerve transfer to traditional
sensory fascicle. Furthermore, results of this nerve transfer are nerve grafting.51 The current trend among peripheral nerve sur-
better when an interpositional nerve graft is not required and geons reconstructing an axillary nerve lesion is to utilise a nerve
when the time from injury to reconstruction is less than transfer from a branch of the radial nerve innervating the triceps.
6 months.37 44 45 It is a technically easier procedure than a nerve graft in the prox-
Three illustrative cases will outline the use of nerve transfers imal portion of the brachial plexus, particularly in larger patients,
as well as the important findings during electrodiagnostic assess- and has been shown to have excellent results.46–48
ment, including their use in follow-up and rehabilitation. When both the suprascapular and axillary nerves are injured,
there is good evidence that outcomes are better with traditional
reconstruction of both nerves. Several papers document better
Case example I: axillary nerve palsy outcomes when time from injury to reconstruction is less than
A middle-aged man suffered an anterior dislocation of his right 6–8 months.47 48
shoulder after a fall while skiing. The shoulder was reduced The studies looking at the surgical technique and functional
under conscious sedation 3 hours later. At 4 months postinjury, improvement in hand function are outlined in table 5.41 53–56
shoulder abduction remained poor. Imaging of the rotator cuff The results of using the anterior interosseous nerve for restor-
confirmed the cuff to be intact. Electrodiagnostic assessment at ation of hand function remain a promising tool in animal and
2 and 4 months postinjury documented an isolated axillary human modelling, but to date most series only have small
4 Korus L, et al. J Neurol Neurosurg Psychiatry 2015;0:1–10. doi:10.1136/jnnp-2015-310420
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Table 2 Surgical outcomes with nerve transfers to augment elbow flexion

Elbow flexion

Number of
cases Clinical outcome Surgery Commentary Commentary

Oberlin et al 29
4 85% M3 or better FCU(ulnar) to MCN Biceps Proof of concept Demonstrated it could be carried out
Leechavengvongs 32 93% M3 Oberlin Extension of original work Added numbers to data
et al38
Sungpet et al39 36 34/36 MRC 3 or Oberlin Single nerve transfer BP injury C5, 6, 7 avulsions did not do
better as well
Tung 200343 8 MRC 4 in 5; 4+ in 3 Oberlin plus med pectoral Attempt to improve the above Surgery performed a mean of 3.8=/−
nerve with a double transfer 1.6 months postBP injury
Mackinnon et al28 6 MRC 4+ in 4; and Oberlin plus FDS median to Clinical evidence of No weakness in hand function
grade 4 in 2 MCN to Biceps double transfer reinnervation by 5.5 months
(mean)
Terzis et al23 39 >M3+ in 53% Intercostal nerves to MCN Better results if operated on The literature reports 65–72% of pts
less than 4 months from injury greater than M3 with intercostal to
MCN40 41
Martins et al42 40 5 kg vs 5.6 kg; Randomised single vs double Outcome 12 months Strength measured with a push-pull
Flexion index O.2 transfer postsurgery dynamometer
±0.13
Tsai et al32 18 7/9 (78%) MRC >4 Oberlin and XI to SS in all Compared C5/6 injury with C5– Only 44% in the C5-C7 group achieved
patients 7 BPI MRC >4
MRC Medical research council Grades 0, no contraction; 3, active movement against gravity; 4, active movement against gravity and resistance.
Oberlin: Ulnar nerve to FCU transferred to MCN to Biceps.
XI to SS=spinal accessory to suprascapular nerve transfer.
Flexion index=injured side force/normal side force.
BP, brachial plexus; BPI, Brachial Plexus Injury; FCU, flexor carpi ulnaris; MCN, musculocutaneous nerve.

numbers. Further studies are required to better understand the

Table 3 Shoulder stability by augmenting the suprascapular nerve
outcomes of this procedure, including the difference between
with a spinal accessory nerve transfer
end-to-side and end-to-end coaptation.22 53 56–60 (see case 2 as
Number Clinical an illustrative example and figure 3).
Author of cases outcomes Surgery Commentary

Malessy 53 100% M4 Graft from C5 Only 15% Case example 2: ulnar nerve injury
et al44 in 24; Transfer gained A teenage right hand dominant female fell through a patio
from CN XI or abduction with door, lacerating the medial aspect of her arm 15 cm proximal to
XII in 29 a mean range
of 44°
the medial epicondyle. Unfortunately, an ulnar nerve injury was
Terzis et al45 102 >M3+ in 80% 80% with Results better
not recognised until 6 months later when electrodiagnostic
distal CN XI in patients with testing revealed no MUAPs and profuse denervation in the hand
time from injury intrinsics and flexor carpi ulnaris.
to surgery Isolated ulnar nerve injuries tend to have a poorer prognosis
<6 months, than median or radial injuries.11 61 This is in part due to the
with CN XI and
when direct large number of axons required to power the hand intrinsics as
repair (no graft) well as the distance required for axons to regenerate before
possible reaching their motor endplate targets. As such, ulnar nerve
Bertelli33 30 All patients Transfer of CN Patients with injuries proximal to the elbow have an especially poor progno-
with partial BP XI total BP palsies sis.55 61 To improve the results after such injuries, the anterior
palsies M3 or did not recover
better; only 3/ external
interosseous nerve (AIN) branch to the pronator quadratus (PQ)
16 with total rotation has been used to selectively innervate the motor branch of the
BP palsies >M3 ulnar nerve.41 53 54 56 In most cases, the ulnar nerve lesion will
Ruchelsman 25 Mean CN XI to Poorer results still be repaired proximally to restore proximal ulnar nerve func-
et al34 abduction >90° suprascapular when tion (FCU, FDP to ring and small fingers) as well as sensation.
transfer interpositional In this case, the ulnar nerve was explored proximal to the
nerve graft
required elbow and found to be transected with a 6 cm gap. Four cables
Tse et al35 177 Significant C5 to Obstetrical of a sural nerve graft were utilised to span the gap for reasons
improvements suprascapular upper trunk outlined above. Owing to the proximal nature of the injury as
in Active in 106, CN XI brachial plexus well as a delay in diagnosis, a distal nerve transfer was com-
Movement to injuries; final pleted. The motor component of the ulnar nerve was dissected
Scale suprascapular outcomes did
out beginning at Guyon’s canal for approximately 10 cm prox-
in 71 not favour
either treatment imal to the wrist. The terminal branch of the AIN was divided
as it entered PQ and transferred as an end-to-end repair to the
BP, brachial plexus.
motor component of the ulnar nerve. Electromyographic
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Table 4 Shoulder Stability by transferring the radial nerve to triceps to the axillary nerve
Author Number of cases Clinical outcomes Surgery Commentary

Leechavengvongs 7 100% M4 Long head of triceps branch Original paper describing triceps branch transferred to
et al46 of radial nerve transferred axillary nerve
to axillary
Bertelli (2004)31 21 30% M4, 70% M3 Long or lateral head of All C5, C6 avulsion injuries
triceps branch of radial to
axillary
Terzis et al47 176 >M3+ in 49.9% Multiple different donor Heterogeneous group with >30% having at least one root
nerves avulsed. Results better in patients <20 years, time from
injury to surgery <8 months, length of nerve grafts <6 cm
Lee et al48 36 16/21 MRC 3 or better Long head branch of radial Isolated axillary nerve injuries; poorer results if surgery
nerve to axillary >9 months postinjury, higher BMI and age >40
Ray et al49 8 MRC 4 or better in 50% Medial pectoral to axillary Upper trunk brachial plexus injuries
Estrella et al40 20 MRC >4 when CN XI to suprascapular and Shoulder function significantly better when both nerves
suprascapular and axillary radial to axillary reconstructed
nerves both reconstructed
Wolfe et al50 38 (14 grafts, 24 transfers) 100% graft patients >M3; Mean nerve graft length Mixed group of brachial plexus and isolated axillary nerve
86% transfer patients >M3 13.2 cm injuries. No difference in outcomes between groups.
Nearly all other papers note poorer outcomes with grafts
>6 cm
BMI, body mass index; MRC, Medical Research Council.

evidence of recovery in the abductor digiti minimi (ADM)
muscle was evident at 5 months postrepair with evidence of
clinical recovery 3 months later. The recruitment of new motor
units (nascent MUAPs) requires the forearm and wrist to be
pronated.
A different permutation of this transfer is illustrated in figure 3.
In this procedure, which may be used to augment the recovery of
an ulnar nerve lesion with a significant potential for recovery (eg,
after decompression of severe ulnar neuropathy at the elbow), the
donor AIN nerve is sutured to the motor component of the ulnar
nerve in an end-to-side manner,56 a ‘reverse’ end-to-side nerve
coaptation. The benefit of this transfer is that the motor compo-
nent of the ulnar nerve does not need to be cut as it does for an
end-to-end coaptation.
This transfer is more challenging for patients to relearn, and
therefore prolonged and focused rehabilitation is necessary to
maximise recovery, once reinnervation has occurred to the hand
intrinsics. The key for the electromyographer is to test both
ADM and FDI (and other dorsal interrossei from the fourth to
the first) with needle EMG while the forearm is in the supinated
and pronated positions. This is because the AIN that is used as
the motor to drive the ulnar nerve innervates PQ and therefore
is maximally firing when the forearm is actively pronated.
Typically, the electromyographer will see many more nascent
units in the ulnar innervated intrinsics while ‘firing’ the donor
AIN relative to asking the patient to contract the target muscles
alone. This is crucial not only in looking for early signs of rein-
nervation (ie, new nascent units), but also in the patient’s
rehabilitation. Once EMG signs of reinnervation occur, we insti-
tute a detailed protocol for our hand therapists, which includes
the use of neuromuscular stimulation, biofeedback and focused
isometric (on for 3–4 s holds) hand intrinsic use (abduction/
adduction of the interossei) with the forearm pronated. In our
experience, this is necessary to maximise function and concep-
tually improve neuroplasticity and ultimately hand intrinsic
function.57 In this case, the nerve transfer surgery and rehabili-
tation lead to grade 4+ MRC function of hand intrinsics at
18 months postoperatively.
The results of this procedure to date are summarised and out-
lined in table 5.
Reverse end-to-side transfer
Recently, nerve transfers have been described with a
‘Reverse-End-to-Side’ neurotisation as opposed to the typical

Figure 2 (A and B) Neuroplasticity

and the donor nerve. Needle recording
in the deltoid muscle with shoulder
abduction without, and with, elbow
extension (A and B). Note the fuller
interference pattern and the marked
increase in the number of new motor
units seen by initiating shoulder
abduction with elbow extension
(thereby ‘firing’ the donor nerve) in B.

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Neurosurgery

Table 5 Surgical outcomes to augment intrinsic hand function with nerve transfer
Number
Author of cases Clinical outcome Surgery Commentary Commentary

Battiston et al 53
7 86% M4 or greater AIN to motor branch One paediatric case (age 11)
of ulnar nerve achieving M5
Mackinnon et al41 8 Mean improvement in lateral AIN to motor branch All patients showed evidence of No MRC grade reported
pinch strength of 11.6 lb of ulnar nerve intrinsic reinnervation
Hasse et al54 2 Both patients had return of AIN to motor branch Objective strength measurements One patient required nerve graft
intrinsic hand function of ulnar nerve not reported from AIN to ulnar nerve
AIN, anterior interosseous nerve; BMI, body mass index; MRC, Medical Research Council.

‘End-to-End’ coaptation.58 In a reverse end-to-side neurotisa-
tion, the donor nerve is coapted to the side of a recipient nerve
through an epineurial window. This coaptation offers the advan-
tage of not completely downgrading the recipient nerve by
avoiding cutting the recipient nerve for an end-to-end coapta-
tion.56 This is beneficial if a proximal lesion exists in the recipi-
ent nerve and it is unclear whether regenerating axons will
eventually reinnervate motor end targets in a timely fashion,
thereby ‘supercharging’ the regenerating nerve. We have found
this type of nerve transfer particularly effective for severe com-
pression neuropathy of the ulnar nerve at the elbow where the
ulnar nerve is decompressed at this level and an AIN to ulnar
reverse end-to-side transfer is added to augment the recovery of
the motor axons. The results of this work will be published
shortly. There have been promising results in a rat model dem-
onstrating reinnervation comparable to an end-to-end coapta-
tion and one case report in humans.53 56–60
Case example 3: upper trunk brachial plexus palsy
A young, previously healthy male involved in a snowmobile
accident suffered a severe, right pan brachial plexopathy. Serial
physical examinations and EMG studies demonstrated recovery
in the muscles innervated by the middle and lower trunks. At
3 months postinjury, he had no clinical or EMG recovery of
shoulder abduction (deltoid), external rotation (infraspinatus) or
elbow flexion (biceps or brachialis). It is crucial to note that

Figure 3 Reconstruction of hand

intrinsic function with distal nerve
transfer. The distal anterior
interosseous nerve (AIN) is divided at
its entry into pronator quadratus at the
wrist and transferred to the motor
component of the ulnar nerve at the
level of take-off of the dorsal sensory
branch (DSB). Transfer may be
performed in an end-to-side
(illustrated) or end-to-end fashion.

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Neurosurgery

Table 6 C7 Contralateral transfer to augment upper limb function post-traumatic BP injury

Number Commentary
Author of cases Clinical outcome Surgical details (donor) (follow-up)

Gu et al62 50 70% Satisfactory results of 10 cases followed 2+ years 10 followed for 2+

years
Gu et al63 82 >M3 in 67% of musculocutaneous nerves, 63% of median Median, musculocutaneous, radial or 22 followed for 2+
nerves, 50% of radial nerves, 50% of thoracodorsal nerves thoracodorsal nerves years
Songcharoen et al64 111 >M3 in 48% Median nerve 21 followed for 2+
years
Gu et al65 224 > M3 in 80% of musculocutaneous nerves, 66% of radial Median, musculocutaneous, radial or 32 followed for 2+
nerves, 86% of Median nerves, 50% of thoracodorsal thoracodorsal nerves years
nerves
Terzis et al66 56 >M3 in 20% deltoid, 52% biceps, 24% triceps, 34% wrist Axillary, musculocutaneous, radial and median 6.1 years
and finger flexors, 20% wrist and finger extensors nerves
Chuang et al67 137 ≥M3 in 39–74% finger flexion Median, median and musculocutaneous nerves, 4 years
or median nerve followed by muscle transplant
Wang et al68 75 > M3 60% elbow flexion, 64% finger flexion, 53% thumb Direct coaptation to lower trunk (± humeral 57 months
flexion, 72% wrist flexion shortening osteotomy)
Tu et al69 40 >M3 30% of hemi transfer, 65% in total Total or hemitransfer to median nerve 6 years
BP, brachial plexus.

although being used as a diagnostic test, the EMG is also being nerve (fascicle subserving FDS) to the brachialis motor branch
used to plan the possible surgical reconstruction. The specific and ulnar nerve (fascicle subserving FCU) transferred to the
muscles of interest outside of the injured ones include those that biceps motor branch. At 5 months postsurgery, elbow flexion
may act as sources of donor nerves. These include the trapezius was 4−/5, and at 12 months elbow flexion was 4+/5 with shoul-
( possible cranial nerve XI to the suprascapular nerve), triceps der abduction and external rotation at 4−/5. Excellent power of
( possible radial to axillary nerve) and forearm finger and wrist elbow flexion is the norm with this type of reconstruction.
flexors ( possible FDS fascicle of the median to the brachialis A number of important outcomes are highlighted. Once
motor branch and FCU fascicle of the ulnar to the biceps motor again, these outcomes can be achieved, with focused rehabilita-
branch). tion including neuromuscular stimulation, once nascent units
At 4 months postinjury, he underwent brachial plexus recon- are detected in the target muscle. The key for the electromyo-
struction and the following nerve transfers: (1) distal CN XI to grapher relates to this early reinnervation, given the positive
the suprascapular nerve, (2) radial nerve (medial triceps branch) benefits of nerve transfer and remembering which function the
transferred to the axillary and (3) double transfer of the median donor transferred nerve formerly did. In this example, elbow
flexion is easily relearnt since we typically flex our fingers and
wrist while flexing our elbows (therefore, the donor nerve fires
without significant cortical reorganisation). Conversely, cortical
Table 7 Tibial nerve transfer to peroneal nerve to restore plasticity and relearning is enhanced by initiating external rota-
dorsiflexion tion with shoulder shrugging (to fire the donor CN XI (ie,
Number Clinical Commentary spinal accessory nerve) and shoulder abduction with elbow
Author of cases outcome Surgical details (follow-up) extension (to fire the donor triceps branch of the radial nerve).
The latter two ‘non-intuitive’ transfers require significantly
Gousheh 9 Foot drop Nerve to soleus 11 months8–14 more time, rehabilitation and repetition to recover fully.
et al72 resolved by and lateral head
1 year in the 6 of gastrocnemius
patients who to motor branch Other options in brachial plexus reconstruction in root
had palsy for of tibialis anterior avulsion with limited donor nerves available
<8 months muscle
In the case of a brachial plexus injury with nerve root avulsion,
Nath 14 ≥M3 in 86% Superficial Not given
table 6 outlines the findings when using a contralateral C7 trans-
et al73 peroneal or tibial
nerve to deep fer as the source of motor axons.62–69
peroneal Contralateral C7 transfer has shown successful results for
Strazar 1 M4 extensor Lateral 2 years reinnervation of a variety of muscle groups in the upper extrem-
et al74 hallicus, M2 gastrocnemius to ity. M3 strength or greater can be obtained in axillary, musculo-
peroneal motor branch of cutaneous, median and radially innervated muscles with
muscles tibialis anterior
muscle
minimal donor site morbidity, according to the published data
Giuffre 11 ≥M3 in 64% Tibial nerve to 17.7 months
to date.62–69 Drawbacks include the need for extensive or vascu-
et al75 motor branch of larised nerve grafts and the possible staging of reconstruction.
tibialis anterior Despite encouraging results, the majority of the data have come
muscle from a few centres, and the technique has not gained universal
Flores 13 ≥M3 in 20% Tibial nerve to 20.8 months popularity.65 67 70 71
et al76 ankle deep peroneal
dorsiflexion,
20% toe Foot drop secondary to severe peroneal injury
extension The following two patients had a severe peroneal nerve injury
requiring operative intervention. They were young males with a
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traumatic posterior dislocation of the knee. Both underwent
orthopaedic ligamentous reconstruction of the injured knee.
The mean time to subsequent nerve repair was 6.6 months.
Surgical nerve transfer was performed using a sural nerve graft
to connect two branches supplying the lateral gastrocnemius
with the tibialis anterior (TA) and peroneus longus. Only one
participant regained antigravity dorsiflexion at 2 years
follow-up. One patient went onto a posterior tibial tendon
transfer. Despite the fact that reinnervation to the tibialis anter-
ior could be demonstrated, this did not translate into functional
dorsiflexion of the ankle. EMG of TA at 1 year postsurgery
revealed volitional nascent motor units with dorsiflexion, acti-
vated only with plantar flexion.
Lower limb reconstruction to augment dorsiflexion
In the lower limb, the nerve transfer most commonly discussed
is the reconstruction of a severe peroneal nerve injury and the
goal is to improve foot drop with the tibial nerve transfer to the
peroneal nerve, which are summarised below in table 7.72–76
Although limited by a smaller number of small series, nerve
transfers to restore the function of the deep peroneal nerve have
demonstrated that it is technically possible and have shown some
limited success.72–76 Some series have shown restoration of M3
strength or greater in ankle dorsiflexion; however, these results are
not universal, and conceptually it has been difficult for patients to
relearn the antagonist/agonist relationship.75 Additionally, studies
tend to vary in the actual site of coaptation. More studies are
needed to determine the benefit of this operation, especially in the
context of the successful tendon transfers available to augment
dorsiflexion. In the authors’ opinion, the importance of neuroplas-
ticity in relearning this technique remains a major and important
factor to its lack of success to date.
CONCLUSIONS
Significant peripheral nerve injuries are best treated in a collab-
orative, multidisciplinary fashion involving the electromyogra-
pher and peripheral nerve surgeon. Such a model will optimise
decision-making when assessing patients and trying to decide
whether spontaneous recovery will occur or a better outcome is
expected from surgical reconstruction. A new paradigm of
relying on nerve transfers to reconstruct PNI has significantly
supplanted conventional repairs with nerve grafting. In turn,
this has changed the scope of preoperative assessment by the
electromyographer, as the reconstructive surgeon now requires
knowledge of the functional status of potential donor nerves. In
addition, early detection of reinnervation by serial, post-
operative EMG assessment will facilitate timely rehabilitation
after nerve transfers. Such reinnervation frequently occurs much
sooner than one would expect after conventional grafting.
Finally, rehabilitation protocols require maximising cortical plas-
ticity and recovery will be enhanced by occupational and phy-
siotherapists familiar with therapy after nerve transfer surgery.
Acknowledgements The authors wish to thank and acknowledge artist Christine
Zanutto for her contributions to the paper.
Contributors All authors have contributed to the outline, content and review of
this paper.
Competing interests None declared.
Provenance and peer review Commissioned; externally peer reviewed.
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Korus L, et al. J Neurol Neurosurg Psychiatry 2015;0:1–10. doi:10.1136/jnnp-2015-310420
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Nerve transfers and neurotization in

peripheral nerve injury, from surgery to
rehabilitation
Lisa Korus, Douglas C Ross, Christopher D Doherty and Thomas A Miller

J Neurol Neurosurg Psychiatry published online July 1, 2015

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