Acta Neurochirurgica
https://doi.org/10.1007/s00701-018-3671-0
CASE REPORT - PERIPHERAL NERVES
Double nerve transfer for restoration of hand grasp and release in C7
tetraplegia following complete cervical spinal cord injury
Mohammadreza Emamhadi 1 & Sasan Andalib 2,3
Received: 19 August 2018 / Accepted: 31 August 2018
# Springer-Verlag GmbH Austria, part of Springer Nature 2018
Abstract
Cervical spinal cord injury (SCI) can cause tetraplegia. Nerve transfer has been routinely utilized for reconstruction of hand in
brachial plexus injuries. Here, we report reconstruction of finger flexion (hand grasp) and extension (hand release) in a victim of
cervical spinal cord injury with tetraplegia. We also focus on importance of extension phase in restoration of hand function in the
tetraplegic case, in addition to provision of a detailed description of both operations including text, photographs, and a video. We
used double nerve transfer, namely brachialis branches of musculocutaneous nerve to anterior interosseous nerve (AIN) and
supinator branch of radial nerve to posterior interosseous nerve (PIN). We found that brachialis nerve transfer to AIN (for finger
flexion) and supinator branch nerve transfer to PIN (for finger extension) can provide finger flexion and extension simultaneously. Brachialis nerve transfer to AIN and supinator branch nerve transfer to PIN may be an acceptable surgical technique to restore
hand grasp and release in tetraplegia after SCI.
Keywords Tetraplegia . Nerve transfer . Neurotization
Introduction
Cervical spinal cord injury (SCI) may lead to tetraplegia. The
upper extremity dysfunctions in tetraplegic patients impair
daily living activities such as eating, personal hygiene, and
self-protection. Hand function is even of higher importance
than walking, bowel and bladder control, and sexual function
in these patients. Thus, restoration of some hand function can
indeed improve quality of the life of tetraplegic patients.
This article is part of the Topical Collection on Peripheral Nerves
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00701-018-3671-0) contains supplementary
material, which is available to authorized users.
* Mohammadreza Emamhadi
mr.emamhadi@gmail.com
1
Brachial Plexus and Peripheral Nerve Injury Center, Guilan
University of Medical Sciences, Rasht, Iran
2
Neuroscience Research Center, Poursina Hospital, Guilan University
of Medical Sciences, Rasht, Iran
3
Department of Neurosurgery, Poursina Hospital, School of Medicine,
Guilan University of Medical Sciences, Rasht, Iran
Surgical techniques such as tendon transfers, nerve grafts,
and nerve transfers may restore some motor functions [9].
Tendon transfers aiming to regain active wrist extension and
thumb flexion have yielded clear benefits in tetraplegia
resulting from cervical cord injury. Nerve transfers offer new
options of pain, motor, and sensory recoveries [7, 8, 10]. In
comparison with tendon transfers, nerve transfers provide a
better functional outcome as they are less invasive, maintain
the original anatomy and biomechanics of the upper limb, do
not require prolonged immobilization, and offer functional
improvement even when no tendon transfer options are available. Moreover, they may restore multiple functions with sacrifice of only one donor nerve.
Initially applied in cases of brachial plexus injuries, these
techniques have provided rewarding functional outcomes never hoped before [16].
The basic functional movements such as lateral thumb pinch
(key pinch), finger flexion (hand grasp), and finger extension
(hand release) are considered necessary for tetraplegic patients.
If the abovementioned movements in combination with elbow
extension are regained, the patient’s independency is remarkably increased. It should also be emphasized that in tetraplegia,
careful evaluation of the donors is an absolute prerequisite of
nerve transfer and this procedure is contraindicated when the
muscle is innervated by a donor nerve scoring less than M4.
Acta Neurochir
A few published reports have so far confirmed nerve transfer in tetraplegic upper extremity [1, 4–6, 15]; albeit, there
exists only one single report concerning hand reconstruction
for both grasp and release phases [17]. Here, we report a case
of complete cervical SCI with tetraplegia undergoing transfer
of brachialis branch of musculocutaneous nerve to anterior
interosseous nerve (AIN) for finger flexion and supinator
branch nerve to posterior interosseous nerve (PIN) for finger
extension. Cervical SCIs of C5 or below are normally candidates for the procedure since there are intact
musculocutaneous and axillary nerves to be used as donors.
Clinical presentation
A 30-year-old right-handed male patient was referred to our
center. The patient had a motorcycle accident with C6 burst fracture leading to tetraplegia and undergone C6 corpectomy and C5C7 stabilization 12 months before admission to our center. Our
aim was to provide functional improvement in his hand.
Preoperative clinical evaluation and electrodiagnostic
tests
According to the Medical Research Council (MRC) [14], on
motor examination, both trapezius muscles scored M5; biceps/brachialis, deltoid, and brachioradialis muscles were
M4 bilaterally. Triceps strength was M4 and M3 on the right
and left side, respectively, and pronation of forearms scored
M4. Wrist extension was M4 bilaterally and wrist flexion
scored M4 on the right side and M3 on the left side.
Supinator muscles scored M4. Finger and thumb extensors
and flexors were M0 and the right thumb was flexed into the
palm (Fig. 1). No spasticity was observed in the involved
muscles. According to the clinical examination, the patient
was classified in group 5 of the international classification of
surgery of the hand in tetraplegia [11] in the right side
(Video 1) and group 4 in the left side.
Fig. 1 Preoperative clinical examination showing that finger and thumb
extensors and flexors were completely paralyzed and right thumb was
flexed into the palm
Preoperative electromyography of brachialis and supinator
muscles showed a relatively normal recruitment. Fibrillations
were observed in the nerve transfer target muscles, but no
voluntary activity was confirmed.
Indication of surgery was given, planning to perform a
brachialis branch to AIN transfer to restore finger flexion
[6], and supinator branch to PIN transfer to regain finger extension [15] on the right upper limb.
Surgical technique
Double nerve transfer included tranbrachialis branch of
musculocutaneous nerve to AIN for finger flexion (Figs. 2
and 3) and supinator branch nerve to PIN for finger extension
(Fig. 4).
Nerve surgery was carried out under general anesthesia
without muscle relaxation agent aiming to restore function
on the right upper limb. The patient was supine with his right
arm abducted, supinated, and placed on an arm board.
A vertical incision on the medial surface of the arm allowed
exposure and identification of the musculocutaneous nerve and
its branches to the biceps and brachialis muscles. The brachialis
branch (donor nerve) was isolated with a vessel loop.
Exploration of the right median nerve was performed via an
S-shaped incision on the volar surface of forearm. The median
nerve was identified proximal to the lacertus fibrosus and its
course was followed between the two heads of the pronator teres.
Then, the AIN (recipient) was identified and its course was
followed proximally. A vessel loop was used to isolate it.
Response in flexor pollicis longus muscle was confirmed by
using intraoperative electrostimulation. The brachialis nerve
and AIN were sharply severed and under microscope, a
tension-free nerve coaptation between these nerves was made
by 9–0 epineural sutures (Fig. 2).
Then, the forearm was placed prone on the surgical
table. A 10-cm-long incision was made on the proximal
third dorsal side of the forearm and the supinator muscle exposed by laterally displacing the extensor carpi
radialis brevis muscle and extensor digitorum communis
muscle. The superficial portion of supinator muscle was
divided in order to expose the PIN and the motor
branches of the supinator muscle. The function of supinator muscle was confirmed by neurostimulatation.
Contraction of the extensor digitorum communis, extensor carpi ulnaris, extensors of the thumb, and index
muscles could be assessed on electric stimulation of
PIN. The contraction appeared as in upper motor neuron
paralyzed muscles, because the connection between
muscles and spinal cord is often intact; hence, the muscles below injury are kept alive. Then, supinator
branches were distally cut and the PIN was proximally
sectioned (Fig. 3). A tension-free coaptation was done
with 9–0 mononylon sutures under microscope. The
Acta Neurochir
Fig. 2 Intrafascicular dissection
of the median nerve at arm level
to explore AIN
subcutaneous tissue was finally approximated and the
skin was sutured.
Postoperative management
Immobilization of the forearm and the elbow (the wrist and the
forearm in neutral and the elbow flexed to 90°) in a splint was
done for 4 weeks. Once the splint was removed, the patient
was neurologically re-evaluated and no additional functional
deficit was detected. In particular, postoperative elbow flexion
force was unchanged. A month after the surgery, for motor
reeducation, a hand therapist commenced physiotherapy and
aided the patient with exercising passive flexion of the fingers
and the thumb coinciding with elbow flexion, and also passive
extension of the fingers and the thumb concurrently with forearm supination. Following motor reeducation (due to brain
neuroplasticity) and reinnervation of the target muscles, the
patient regained flexion and extension of the fingers and the
thumb as natural voluntary actions.
Follow-up and surgical outcome
Neurological follow-up was carried out every month lasting
for 20 months after surgery. Electrophysiological follow-up
was done every 2 months starting 6 months after surgery.
Postoperative electrodiagnostic tests showed early reinnervation of the extensors 6 months after surgery whereas the reinnervation was detected 8 months after the procedure in the
flexors. In the following 2 months, flexor pollicis longus and
flexor digitorum profundus also showed initial signs of
recovery.
Nine months after the surgery, finger extension was seen by
supination of the forearm. The patient recovered flexor
pollicis longus and first- and second-digit flexor digitorum
profundus scoring M3 15 months after the surgery.
The patient finally achieved M4 on thumb and finger
flexion, M3 on thumb extension, and M4 on finger extension and became able to pick up object and feed
himself with his right hand 20 months after surgery
(Video 1 and Figs. 4, 5 and 6).
Fig. 3 Transfer of brachialis branch of musculocutaneous nerve to AIN for finger flexion
Acta Neurochir
Fig. 6 Follow-up examination: the patient became able to feed himself
with his right hand
Fig. 4 Supinator branches were cut distally and the PIN was sectioned
proximally
Given the favorable results on the right upper extremity,
nerve transfers were then performed on the left upper extremity wherein follow-up is still in progress.
Discussion
In tetraplegic patients, the main goals of nerve reconstruction
are to restore elbow extension, wrist extension, finger flexion,
finger extension, and intrinsic hand function. A few published
reports have so far confirmed nerve transfer in tetraplegic
upper extremity [1, 4–6, 15]; albeit, there exists only one
Fig. 5 Right-hand grip reconstruction (a grasp phase, b release phase)
single report concerning hand reconstruction of both finger
flexion and extension [17].
Friden et al. [12] reported nerve transfer to regain wrist
extension in a subject with C5 tetraplegia. He transferred
brachialis muscle branch of the musculocutaneous nerve to
the extensor carpi radialis longus muscle branch of the radial
nerve, achieving active wrist extension. Bertelli et al. [5] could
restore only finger and thumb extension by transferring the
supinator motor branch to the PIN in a case of complete C6
SCI with preoperatively intact function in the brachioradialis,
radial wrist extensors, and supinator muscles and elsewhere,
Bertelli et al. [4] carried out a transfer of the teres minor nerve
branch of axillary nerve to long head of triceps nerve branch to
restore elbow extension in a C6 tetraplegic patient. Fourteen
months after the procedure, the patient achieved a M4 triceps.
In seven tetraplegic patients, Bertelli et al. [2] utilized one of
axillary nerve division to reinnervate the triceps long and upper medial head motor branches in 13 patients and transfer of
the nerve to the supinator to the PIN was carried out to reconstruct thumb and finger extension. Consequently, after followup of 19 months, elbow extension force scored M4 in most of
patients. Thumb extension scored M4 in 8 upper limbs and
finger extension scored M4 in 12 hands.
In the abovementioned papers, the authors did not perform a
nerve transfer to restore finger flexion. However, Bertelli et al.
[1] later reported a tetraplegic case undergoing nerve transfers
for elbow extension and thumb and finger extension, but they
carried out a tendon transfer for finger flexion. He transferred
tendon of brachioradialis to the flexor pollicis longus and flexor
digitorum superficialis for the index finger flexion.
On the other hand, there are reports of nerve transfer for
restoration of thumb and finger flexion without reconstruction
of finger extension. Bertelli et al. [3] attempted to restore only
finger flexion in a tetraplegic case by transferring nerve to the
brachialis or brachioradialis or extensor carpi radialis brevis
(ECRB) to AIN and concluded that nerve to ECRB is a better
donor than the other two nerves. Mackinnon et al. [15]
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reported a single case of C7 cervical SCI undergoing restoration of finger and thumb flexion following brachialis branch to
AIN transfer. The authors reported that flexor pollicis longus
and flexor digitorum profundus showed M3 muscle force
15 months after the surgery. Hawasli et al. [13] reported a
21-year-old male subject with complete C7 tetraplegia. The
patient underwent brachialis muscle branch to AIN transfer
and showed precocious reinnervation within 3 months after
the procedure with M2-M3 in the first- and second-digit flexor
digitorum profundus and flexor pollicis longus.
A few reports have been dedicated to both phases (flexion and
extension) of hand reconstruction. Brown [6] performed
brachialis branch of musculocutaneous transfer to the median
fascicle and restored wrist and finger flexion to allow pinch
and grasp and also transferred donor fascicles from the axillary
nerve to recipient fascicles of the radial nerve, one corresponding
to wrist and finger extension and the other corresponding to
elbow extension via triceps function. Although he did not report
any results, it appears that use of a recipient in proximal of radial
nerve, which has a marked distance from target muscles, takes a
longer time for reinnervation in contrast to the technique we used,
that is to say, transfer of supinator branch to PIN.
The report by Van Zyl et al. [17] pertained to restoring both
phases of hand function, along with elbow extension reconstruction by using nerve transfer in a man with C6 tetraplegia.
The authors transferred teres minor nerve branch to long head
of triceps nerve branch, brachialis nerve branch to anterior
interosseous nerve, and supinator nerve branch to posterior
interosseous nerve and achieved elbow extension, key pinch,
grasp, and release.
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the institutional and/or national research committee (Guilan University of Medical
Sciences) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent Informed consent was obtained.
References
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Conclusion
In tetraplegic patients, nerve transfers are safe and reliable
procedures for the reconstruction of elbow and wrist extension
and finger flexion and extension. Finger flexion and extension
should be simultaneously restored to achieve the best hand
function. It should be mentioned that finger extension is an
important phase of hand function because this function is required for object acquisition and release. In our case, we found
that brachialis nerve transfer to AIN (for finger flexion) and
supinator branch nerve transfer to PIN (for finger extension)
can provide a functional hand with grasp and release.
Inasmuch as most daily living activities could be performed
through hand grasp and release, such double nerve transfer
can be an acceptable surgical approach in tetraplegic patients
after cervical SCI.
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12.
13.
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Compliance ethical standards
17.
Conflict of interest The authors declare that they have no conflict of
interest.
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Acta Neurochir
Comments
A well planned, executed, documented, and described clinical case
report addressing a challenging spinal cord injury problem with very
good restoration of important and useful hand function.
Michel Kliot
California, USA
Doctors Emamhadi and Andalib report on a C7 quadriplegic patient
who benefited significantly from nerve transfers. As outlined in their
discussion section, there has been sparse literature on using nerve
transfers to improve the life of quadriplegic patients. The results
published thus far are very encouraging. Figures 5 and 6 demonstrate
the benefit the patient received from the procedure. Other nerve
transfers that have been reported in quadriplegic patients are a transfer
of the AIN to the ECRL for improvement of wrist extension and
stabilization of the hand. To improve wrist extension transfer of the
teres or deltoid branches on the axillary nerve to triceps branches of the
radial nerve to restore elbow extension. If this latter transfer proved to be
successful, quadriplegic patients that were wheel chair bound could use
their triceps to help transfer from their wheel chairs to the bed. I
congratulate the authors on their excellent results. I will be following
this literature to try to determine the optimal time for transfers and also
to judge the efficacy of these transfers. The alternate strategy for
improving hand grip in quadriplegic patients is spinal cord stimulation.
Both of these techniques open new doors for improving the lives of this
unfortunate group of patients.
Allan Friedman
North Carolina, USA