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Double Motor Nerve Transfer for All Finger Flexion in Cervical Spinal Cord Injury: An Anatomical Study and a Clinical Report

      Purpose

      To explore the feasibility of restoring all finger flexion after a cervical spinal cord injury.

      Methods

      Double nerve transfer was conducted in 22 cadaver upper extremities. Donor nerves were the brachialis branch of the musculocutaneous nerve and the extensor carpi radialis brevis (ECRB) branches of the radial nerve. Recipient nerves were the anterior interosseous nerve (AIN) and the flexor digitorum profundus (FDP) branch of ulnar nerve (ulnar-FDP). Nerve transfers were evaluated on 3 parameters: surgical feasibility, donor-to-recipient axon count ratio, and distance from the coaptation site to the muscle entry of recipient nerve. A complete C6 spinal cord injury reconstruction was accomplished in a patient using a double nerve transfer of ECRB to ulnar-FDP and brachialis to AIN.

      Results

      In the cadaver study, nerve transfers from ECRB to AIN, brachialis to AIN, and ECRB to ulnar-FDP were all feasible. The transfer from the brachialis to ulnar-FDP was not possible. Mean myelinated axon counts of AIN, brachialis, ulnar-FDP, and ECRB were 2,903 ± 1049, 1,497 ± 606, 753 ± 364, and 567 ± 175, respectively. The donor-to-recipient axon count ratios of ECRB to AIN, brachialis to AIN, and ECRB to ulnar-FDP were 0.24 ± 0.15, 0.55 ± 0.38, and 0.98 ± 0.60, respectively. The distance from coaptation of the ECRB to the ulnar-FDP muscle entry was shorter than for the other nerve transfers (54 ± 14.29 mm). At 18 months, there was restoration of flexion in all fingers and functional improvement from double nerve transfer of the brachialis to the AIN and the ECRB to the ulnar-FDP.

      Conclusions

      Restoration of all finger flexion may be feasible by the ECRB to ulnar-FDP and brachialis to AIN double nerve transfer.

      Clinical relevance

      Double nerve transfer can be used in C6-C7 spinal cord injury and patients with lower arm–type brachial plexus injury who have no finger flexion but have good brachialis and ECRB.

      Key words

      Traumatic spinal cord injury (TSCI) is a devastating occurrence. Restoration of arm and hand movement in tetraplegia appears to be the highest priority in TSCI cases.
      • Anderson K.D.
      Targeting recovery: priorities of the spinal cord-injured population.
      The recent development of distal nerve transfers has provided new options for tetraplegia treatment. Nerve transfer, including multiple nerve transfers in a single stage,
      • Bertelli J.A.
      • Ghizoni M.F.
      Single-stage surgery combining nerve and tendon transfers for bilateral upper limb reconstruction in a tetraplegic patient: case report.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      • van Zyl N.
      • Hahn J.B.
      • Cooper C.A.
      • Weymouth M.D.
      • Flood S.J.
      • Galea M.P.
      Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.
      offers several benefits such as preserving biomechanical muscle function and obviating the need for prolonged immobilization.
      Among nerve transfers for finger flexion restoration, common donor nerves are the brachialis branch (C5-C6)
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      • Mackinnon S.E.
      • Yee A.
      • Ray W.Z.
      Nerve transfers for the restoration of hand function after spinal cord injury.
      and the extensor carpi radialis brevis (ECRB) branch (C6).
      • Bertelli J.A.
      • Mendes Lehm V.L.
      • Tacca C.P.
      • Winkelmann Duarte E.C.
      • Ghizoni M.F.
      • Duarte H.
      Transfer of the distal terminal motor branch of the extensor carpi radialis brevis to the nerve of the flexor pollicis longus: an anatomic study and clinical application in a tetraplegic patient.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      The anterior interosseous nerve (AIN) (C8-T1)
      • Mackinnon S.E.
      • Yee A.
      • Ray W.Z.
      Nerve transfers for the restoration of hand function after spinal cord injury.
      • Bertelli J.A.
      • Mendes Lehm V.L.
      • Tacca C.P.
      • Winkelmann Duarte E.C.
      • Ghizoni M.F.
      • Duarte H.
      Transfer of the distal terminal motor branch of the extensor carpi radialis brevis to the nerve of the flexor pollicis longus: an anatomic study and clinical application in a tetraplegic patient.
      is the recipient nerve for finger flexion and can restore the flexor of the thumb and flexor digitorum profundus (FDP) of the index and middle fingers (AIN-FDP). Another potential recipient nerve that has not received attention for finger flexion is the FDP branch of the ulnar nerve (C8-T1), which supplies the ulnar-FDP.
      Previous research
      • Schreiber J.J.
      • Byun D.J.
      • Khair M.M.
      • Rosenblatt L.
      • Lee S.K.
      • Wolfe S.W.
      Optimal axon counts for brachial plexus nerve transfers to restore elbow flexion.
      showed that the success of a nerve transfer depends on having a donor-to-recipient axon count ratio of more than 0.7:1, a short distance from the coaptation site to the target structure
      • Brown J.M.
      • Shah M.N.
      • Mackinnon S.E.
      Distal nerve transfers: a biology-based rationale.
      and a relatively easy, tensionless nerve repair.
      • Mackinnon S.E.
      • Colbert S.H.
      Nerve transfers in the hand and upper extremity surgery.
      We performed a study to explore the feasibility of restoring all finger flexion after a cervical spinal cord injury using the AIN and ulnar-FDP branches as recipient nerves and the brachialis and ECRB branches as donor nerves. We also report on the outcome of conducting 4 nerve transfers bilaterally, including double nerve transfer of the brachialis to the AIN and the ECRB to the ulnar-FDP in a patient with a complete C6 TSCI.

      Materials and Methods

      Anatomical study

      The protocol of this research was approved by the ethics committee of our institution. We dissected 22 upper extremities under ×3.3 magnification in 4 areas including the ECRB at the elbow (Fig. 1A), the brachialis branch in the upper arm, the AIN from the wrist to the upper arm (Fig. 1B), and the ulnar-FDP at the elbow (Fig. 1C). After identifying these nerve branches, the ECRB branch was transferred to the AIN and the ulnar-FDP branch below the elbow. The brachialis branch was transferred to the AIN portion of the median nerve and the ulnar-FDP portion of the ulnar nerve above the elbow (Fig. 2). The distance between the nerve coaptation site and the recipient nerve entry into the target muscle was measured using a Vernier digital caliper. A total of 80 nerve specimens, each 20 mm long, were embedded in paraffin, sectioned transversely, and stained with a combination of hematoxylin-eosin and Luxol fast blue.
      • Clasen R.A.
      • Simon G.R.
      • Ayer J.P.
      • Pandolfi S.
      • Laing I.R.
      A chemical basis for the staining of myelin sheaths by luxol dye techniques; further observations.
      Myelinated axons were counted and the cross-sectional fascicular area of each nerve was measured.
      Figure thumbnail gr1
      Figure 1Anatomical study. Dissection of right upper limb. A Anterolateral aspect, ECRB branch (purple background) arises distal to the extensor carpi radialis longus (ECRL) and brachioradialis. B Anterior aspect. The AIN (pink background) arises from the median nerve at the cubital fossa, extending proximally inside the median nerve. C Medial aspect of the elbow. The ulnar-FDP (orange background) arises from deep in the ulnar nerve dissected between two heads of the flexor carpi ulnaris (FCU). SRN, superficial radial nerve.
      Figure thumbnail gr2
      Figure 2Anatomical study. Schematic diagram of the study. Before nerve transfer and measurement of distance from coaptation site to muscle entry (black dashed line) after nerve transfer.

      Clinical study

      An 18-year-old patient had experienced a cervical spine fracture dislocation in a motor vehicle accident 8 months before undergoing nerve transfers to restore elbow extension and hand motion. The patient was diagnosed as complete cervical TSCI, scored as C6A according to the International Standards for Neurological Classification of Spinal Cord Injury (revised 2011)
      • Kirshblum S.C.
      • Burns S.P.
      • Biering-Sorensen F.
      • et al.
      International standards for neurological classification of spinal cord injury (revised 2011).
      and group 3 according to the International Classification for Surgery of the Hand in Tetraplegia.
      • Friden J.
      • Gohritz A.
      Tetraplegia management update.
      Motor power was recorded bilaterally using the Medical Research Council system. Results were M5 shoulder abduction, M5 elbow flexion, M0 elbow extension, M4 wrist extension, and M0 finger and thumb motion (Video 1, available on the Journal’s Web site at www.jhandsurg.org). Using electromyography, the extensor digitorum communis, FDP, and triceps showed fibrillation potentials and positive sharp waves, which indicated lower motor neuron injury. Those findings are considered time-dependent and indicate a need for early rescue by nerve transfer.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      The patient and her family were informed of the investigational nature of the protocol approved by the ethic committee of our institution and signed an informed consent before participation, in accordance with the Declaration of Helsinki guiding biomedical research involving human subjects.
      The operation was performed in the supine position by 2 surgical teams (led by K.S. and J.K.); it was completed in one session lasting 5.5 hours (Fig. 3). An electric stimulator was used to identify the motor branch of donor and recipient nerves during transfer.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      Four nerve transfers were carried out in each limb: (1) the posterior deltoid branch to the triceps branch via a transaxillary approach; (2) the supinator nerve branch to the posterior interosseous nerve (PIN) as described by Bertelli et al
      • Bertelli J.A.
      • Tacca C.P.
      • Winkelmann Duarte E.C.
      • Ghizoni M.F.
      • Duarte H.
      Transfer of axillary nerve branches to reconstruct elbow extension in tetraplegics: a laboratory investigation of surgical feasibility.
      • Bertelli J.A.
      • Tacca C.P.
      • Ghizoni M.F.
      • Kechele P.R.
      • Santos M.A.
      Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report.
      ; (3) the brachialis branch to the AIN portion on the posteromedial aspect of the median nerve as described by Mackinnon et al
      • Mackinnon S.E.
      • Yee A.
      • Ray W.Z.
      Nerve transfers for the restoration of hand function after spinal cord injury.
      ; and (4) the ECRB branch to the ulnar-FDP branch using the technique described subsequently.
      Figure thumbnail gr3
      Figure 3Clinical study. Four nerve transfers on the left upper extremity. The patient received 4 nerve transfers (circle diagrams) bilaterally in a single stage.
      The ECRB branch was identified at the same area as the nerve transfer from the supinator to the PIN on the lateral side of the cubital fossa. The distal end of the ECRB branch was transposed medially to the cubital fossa area. The ulnar-FDP branch was approached via a separate straight-line incision along the proximal forearm between the medial epicondyle and the olecranon process, dividing the fascia between the 2 heads of the flexor carpi ulnaris to identify the branch arising from the deep aspect of the ulnar nerve. The proximal part of the ulnar-FDP branch was dissected out from the main ulnar nerve and was cut proximally close to the medial epicondyle. A tunnel was created between the flexor digitorum superficialis and the FDP muscle to pass the ulnar-FDP branch to the cubital fossa. The ECRB motor branch was approximated to the ulnar-FDP branch without tension. Arm slings were used after surgery, allowing some degree of arm motion but avoiding strong direct pressure on the surgical wounds. The patient followed up regularly at 3-month intervals.

      Results

      Anatomical study

      The nerve transfer from the ECRB to the AIN, the brachialis to the AIN, and the ECRB to the ulnar-FDP were found to be feasible. The one exception was the brachialis branch transfer to the ulnar-FDP owing to the difficulty in isolating the ulnar-FDP portion within the ulnar nerve above the medial epicondyle. Dissection of the AIN from the other fascicles of the median nerve above the elbow was 30.6 ± 13.0 mm below where the brachialis branch entered the muscle. In 7 of 22 specimens (32%), the AIN also had branches to the ulnar-FDP of the fingers.
      We achieved an approximation of tensionless ECRB branch transfers to the AIN and ulnar-FDP in all specimens. The distance from the transfer site to the muscle entry point of the FDP averaged 54.03 ± 14.29 mm. This was less than the distance to the muscle entry of the pronator quadratus (PQ) and FPL branches of the AIN but similar to the distance between the ECRB and the FDP muscle entry of the AIN. For the brachialis to AIN nerve transfer, the AIN portion needed to overlap at least 1.5 cm above the muscle entry of the brachialis branch. When this overlap could not be achieved with the isolated AIN, other more proximal fascicles of the median nerve were included in the transfer. The distances between the brachialis coaptation site and the muscle entry of the 3 branches of the AIN were substantially longer than the corresponding distances between the ECRB and the muscle entry of the AIN (Fig. 4).
      Figure thumbnail gr4
      Figure 4Anatomical study. Box plot of distance from the nerve coaptation site to the entrance of the recipient nerve into muscle. The distance in nerve transfer from the ECRB branch to the ulnar-FDP branch is the shortest.
      The number of myelinated axons and the fascicular cross-sectional area of the AIN branch were significantly higher than those of the other nerve branches (P < .05). These parameters were similar when the ECRB branch was compared to the ulnar-FDP branch (Table 1). The donor-to-recipient axon count ratio of the ECRB branch to the AIN, the brachialis branch to the AIN, and the ECRB branch to the ulnar-FDP branch was 0.24 ± 0.15, 0.55 ± 0.38, and 0.98 ± 0.60, respectively.
      Table 1Number of Myelinated Axons and Cross-Sectional Fascicular Area of Nerve Branches (Mean ± SD)
      NerveMyelinated Axons, nCross-Sectional Fascicular Area, mm2
      AIN2,903 ± 10490.925 ± 0.420
      Brachialis1,497 ± 6060.446 ± 0.229
      Ulnar-FDP753 ± 3640.279 ± 0.159
      ECRB576 ± 1750.198 ± 0.077

      Clinical case

      At 10 months after surgery, the patient had regained M3 elbow extension, M4 finger and thumb extension, M4 finger flexion, and M2 thumb flexion. At 18 months, thumb flexion had improved to M4. In terms of functional improvement, the patient was able to pinch and place small objects, hold a spoon, knit, and write (Fig. 5, Video 1).
      Figure thumbnail gr5
      Figure 5Clinical study. Appearance of the left hand after the operation. A, B Finger extension and flexion at 18 months. C Holding a spoon and D pinching and placing small objects at 1 year.

      Discussion

      Restoration of arm and hand function with cervical TSCI is critical for independence and improved quality of life. Traditional treatments to restore functionality include tendon transfers and tenodesis. However, those tendon surgeries usually require prolonged periods of using an orthosis and multistage operations. Brachialis muscle transfer across the elbow joint for finger flexor
      • Bertelli J.A.
      • Ghizoni M.F.
      Brachialis muscle transfer to reconstruct finger flexion or wrist extension in brachial plexus palsy.
      has been found to be useful but has not been universally successful.
      • DeGeorge Jr., B.R.
      • Becker H.A.
      • Faryna J.H.
      • Spinner R.J.
      • Bishop A.T.
      • Shin A.Y.
      Outcomes of muscle brachialis transfer to restore finger flexion in brachial plexus palsy.
      Single-stage tendon and joint operations, proposed by Fridén et al,
      • Fridén J.
      • Reinholdt C.
      • Turcsanyii I.
      • Gohritz A.
      A single-stage operation for reconstruction of hand flexion, extension, and intrinsic function in tetraplegia: the alphabet procedure.
      offer improved treatment outcomes. However, the extensor tenodesis depends on wrist motion, and excursion after tendon transfer may be limited. Recently, distal nerve transfers were introduced for tetraplegia. Conducting several nerve transfers in a single operation can restore function to multiple muscle groups. In this case, the patient received 4 nerve transfers bilaterally without the need for a prolonged rigid orthosis.
      Several authors have described nerve transfers to restore elbow and finger extension in tetraplegia using both the axillary nerve branch to the triceps branch
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      • van Zyl N.
      • Hahn J.B.
      • Cooper C.A.
      • Weymouth M.D.
      • Flood S.J.
      • Galea M.P.
      Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.
      • Bertelli J.A.
      • Tacca C.P.
      • Winkelmann Duarte E.C.
      • Ghizoni M.F.
      • Duarte H.
      Transfer of axillary nerve branches to reconstruct elbow extension in tetraplegics: a laboratory investigation of surgical feasibility.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for elbow and finger extension reconstruction in midcervical spinal cord injuries.
      and the supinator branch to the PIN.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      • van Zyl N.
      • Hahn J.B.
      • Cooper C.A.
      • Weymouth M.D.
      • Flood S.J.
      • Galea M.P.
      Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for elbow and finger extension reconstruction in midcervical spinal cord injuries.
      There has been less agreement, however, about nerve transfers to restore digit flexion. In 2017, Bertelli et al
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      reported 17 upper-limb operations to restore finger flexion in tetraplegia patients using 3 different nerve donors to the AIN, including a nerve branch of the ECRB, the brachialis, or the brachioradialis. Superior outcomes with the ECRB donor were most likely a result of the shorter distance for nerve regeneration, direct motor to target transfer, and synergistic finger flexion benefits of ECRB.
      This anatomic study suggests that the ECRB can serve as a donor to both the AIN and the ulnar-FDP below the elbow, but that the brachialis branch can serve as a donor only to the AIN above the elbow. Isolation of the AIN on the posteromedial portion of the median nerve at the brachialis branch level cannot be achieved universally. In most cases, a brachialis to AIN transfer involves several nerve fascicles, some of which may not be directly involved with finger and thumb flexion. However, inclusion of the flexor digitorum superficialis portion of the median nerve increases the power of finger flexion. These differences may explain the mixed results observed in clinical series using brachialis to AIN nerve transfer.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      Our study found that the donor-to-recipient axon count ratio of the brachialis to AIN transfer was 0.55:1 and that the distance to entry in AIN-innervated muscles was significantly longer than when the transfer was below the elbow with ECRB as the donor nerve, which suggests that a brachialis to AIN transfer requires a longer time for muscle recovery.
      The anatomical study suggests that ECRB to AIN or ulnar-FDP nerve transfer is the preferred option for restoring finger flexion in tetraplegic patients because of the shorter axon regeneration distance. However, the AIN myelinated axon count is considerably higher than with the other nerve branches studied. The donor-to-recipient axon count ratio for ECRB to AIN branch transfers is only 0.24:1. The different myelinated axon counts reported in other articles
      • Ray W.Z.
      • Chang J.
      • Hawasli A.
      • Wilson T.J.
      • Yang L.
      Motor nerve transfers: a comprehensive review.
      may have resulted from differences in histological technique. For most researchers, the reference standard of peripheral nerve histology is toluidine blue staining of resin-embedded semi-thin sections. This methodology is time-consuming and expensive and requires special equipment; however, histological images that can be observed using ordinary hematoxylin-eosin staining are often poor. In our study, a neuropathologist (S.K.) used the technique of combining hematoxylin-eosin and Luxol fast blue
      • Carriel V.
      • Garzon I.
      • Alaminos M.
      • Campos A.
      Evaluation of myelin sheath and collagen reorganization pattern in a model of peripheral nerve regeneration using an integrated histochemical approach.
      to verify the myelinated axon count (Figures in data set). The anterior interosseous nerve provides motor axons to the FPL, AIN-FDP, and PQ. When the trunk of the AIN is the recipient nerve, some axons may regenerate into the PQ branch. The terminal motor FPL branch of the AIN may be used when the ECRB is the donor.
      • Bertelli J.A.
      • Mendes Lehm V.L.
      • Tacca C.P.
      • Winkelmann Duarte E.C.
      • Ghizoni M.F.
      • Duarte H.
      Transfer of the distal terminal motor branch of the extensor carpi radialis brevis to the nerve of the flexor pollicis longus: an anatomic study and clinical application in a tetraplegic patient.
      Bertelli et al
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      observed all finger flexion using a single AIN recipient nerve in 4 of 5 upper-limb cases. In our study, the AIN included branches to the ulnar-FDP in 7 of 22 upper limbs, which could explain the results of Bertelli et al.
      Finally, the anatomic study noted the relatively short distance and favorable donor-to-recipient axon count ratio of 0.98:1 for nerve transfers below the elbow for the ECRB branch to the ulnar-FDP branch and for the restoration of finger flexion. Tubbs et al
      • Tubbs R.S.
      • Custis J.W.
      • Salter E.G.
      • Blount J.P.
      • Oakes W.J.
      • Wellons III, J.C.
      Quantitation of and landmarks for the muscular branches of the ulnar nerve to the forearm for application in peripheral nerve neurotization procedures.
      reported that ulnar nerve branches to the forearm muscles can easily be localized and used for nerve transfer. The clinical case in which that nerve transfer was applied along with other nerve transfers is a further demonstration of the potential of this technique for restoring finger flexion in patients with C6 and C7 spinal cord injury and in those with lower-arm brachial plexus injury who have no finger flexion but who have good brachialis and ECRB nerves.
      There are 2 reasons for preserving the brachioradialis nerve. One is for a potential future tendon transfer procedure in patients in whom there is no motor recovery after nerve transfer. The other is that previous studies reported poor results in nerve transfers from the brachioradialis to the AIN.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      Double nerve transfer has limitations. For example, in C6 SCI, the ECRB often includes a C6 contribution that could render this nerve unusable. Rigorous ongoing assessment and long-term follow-up are necessary before double nerve transfer can be widely applied to this rare but complex patient population.

      Acknowledgments

      The authors gratefully acknowledge Faculty of Medicine, Chiang Mai University, the primary funders (grant ID ORT 2558-03559); Dr G. Lamar Robert, who reviewed English language; Professor Dan Y. Sherman, who helped planning the research, and Mrs Areerak Phanphaisarn, who conducted the statistical analysis of the data.

      Supplementary Data

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