Successful re-innervation of proximal limb peripheral nerve injuries is rare. Axons regenerate at ~1 mm/day, reaching hand muscles by 24 months, finding them atrophied and fibrosed. Peripheral nerve injury repair is often delayed waiting for spontaneous recovery. This waiting time should not be longer than 6 months as after 18 months reinnervation will not achieve effective muscular function. When spontaneous recovery is impossible, referral too late or damage too severe, other options like a transfer from a nearby healthy nerve to the injured one must be considered. They are very successful, and the deficit in the donor site is usually minimal. The most common nerve transfers are a branch of the spinal nerve to the trapezius muscle to the suprascapular nerve, a branch of the long head of the triceps to the axillary nerve, a fascicle of the ulnar nerve to the motor branch of the biceps muscle, two branches of the median nerve to the posterior interosseous nerve and the anterior interosseous nerve to the ulnar nerve. There are many more options that can suit particular cases. Introduced in brachial plexus injury repair, they are now also applied to lower limb, to stroke and to some spinal cord injuries.
- peripheral nerve injuries
- brachial plexus injuries
- nerve transfers
- nerve regeneration
- supercharge end-to-side
- nerve repair
- nerve graft
Peripheral nerve injuries can represent a serious problem, particularly when involving the brachial plexus. They usually induce devastating consequences and affect young people . The main cause is traffic accidents.
Motor endplate degeneration starts just after a motor nerve is injured. The growth speed of the regenerating axons is ~1 mm/day . The time needed for the regeneration will be proportional the distance between the injury site and the muscle endplates [3, 4]. Proximal limb peripheral nerve injuries pose severe difficulties to a successful re-innervation because of the long distance regenerating axons have to cover , taking up to 24 months to reach hands or feet [2, 5, 6], often finding them atrophied and substituted by fat and fibrous tissue [7–9].
Peripheral nerve injury repair is often delayed waiting for spontaneous recovery. This waiting time should be no longer than 6 months  as after 18 months successful re-innervation will not achieve effective muscular function [11–14].
Nerve grafts are often required [15, 16]. Unfortunately, their use is associated with worse results than direct repair , particularly in grafts longer than 7.2 cm [1, 18]. This occurs because the regenerating nerve fibres must cross two anastomoses instead of just one. The second anastomose site is reached much later with more fibrosis hindering the nerve fibre growth to cross it . Another reason for this is that only autologous sensory nerves are used as grafts to minimize donor site deficits . It has been shown that using sensory nerve grafts to repair motor nerve defects is associated with worse regeneration results than if motor nerves are repaired with motor nerve grafts .
Direct repair is not always possible: when there is no chance of spontaneous recovery (i.e. root avulsion), the referral is too late, the damage is too severe, the scarring at the injury site is significant, presence of large neuromas in continuity or in multilevel nerve injuries . In these cases, a nerve transfer from a nearby healthy nerve is a superior option. A healthy nerve is transected and coapted to a nearby injured one. This transforms a proximal nerve injury into a distal one near the motor endplates, reducing the time required for re-innervation [10, 13]. Unfortunately, the functional improvement is at the expense of reducing the number of functioning nerves . Obviously, the function lost must be less essential than the one we expect to recover . They yield better results than direct nerve repairs, particularly in proximal limb injuries and when a nerve graft is needed [9, 25, 26]. With good surgical planning the deficits induced on transecting the donor nerve are minimal [13, 24].
Distal nerve transfers in proximal nerve injuries reduce the time muscles are denervated, thus improving the outcomes [24, 27]. Nevertheless, the best results are obtained with simultaneous proximal nerve injury repair and distal nerve transfers  as this combination re-innervates more muscles .
Nerve transfers offer better results than tendon transfers . They preserve the original anatomical situation of muscles and tendons, allowing a much better physiological function [11, 12, 14, 22, 29, 30]. Moreover, nerve transfers can re-innervate more than one muscle and thus recover more than one function [11, 29, 31, 32] while tendon transfers are limited to a single one . Although initially introduced to repair peripheral nerve injuries, they are lately also being used in some cases of spinal cord injury (SCI) or stroke .
The mismatch between donor and recipient nerves is common (the first has fewer motor axons than the second). This is seldom a problem because a 20% of motor axons are enough to re-innervate the whole muscle [34, 35].
This means that each motor axon can increase up to five times the amount of muscle fibres it innervates .
Thus, it is possible to re-innervate a big nerve with a smaller branch but it comes at the price of courser movements . A reduced number of axons can successfully re-innervate a muscle provided it is done on time .
Initially, motor nerve transfers were the main concern. Over time it became obvious that sensory recovery is also essential as it allows a better motor control and avoids trophic ulcers [49–52]. This leads to the introduction of sensory nerve transfers [50, 52].
Nerve transfers were first used in the upper limbs but with time have also been applied to the lower limbs.
Balance in 1903 was the first to report a nerve transfer (SAN to facial nerve)  but it was Tuttle in 1913 the first to use them to repair brachial plexus injuries . Vulpius and Stoffel  in 1920 described the use of the MPN as donor nerve . Harris in 1921 reported the RAN to median nerve (MN) transfer . Förster  in 1929 transferred the thoracodorsal (TDN) and subscapular nerves to the axillary nerve (AXN). Lurje in 1948 transferred the pectoral and TDN nerves to the MCN . Seddon in 1963 described the use of the intercostal nerves (ICNs) as donor nerves . Samardzic et al. in 1980 performed the first double nerve transfer, pectoral to AXN and TDN to MCN . Bedeschi et al. in 1984 introduced the sensory nerve transfers . Novak and Mackinnon in 1991 reported the pronator
1.2. Types of nerve transfers
Attending to the nerves involved they can be classified as motor or sensory. The
2. Upper limb nerve transfers
2.1. Scapular nerve transfers
Long thoracic nerve (LTN) damage is associated with scapular winging. To correct it one of the two branches of the
2.2. Shoulder nerve transfers
Recovery of shoulder function is the second priority in brachial plexus injury. Shoulder abduction can be recovered with the
First described by Lurje  in 1948, the
Other donor nerves that have been used to re-innervate the SSN and AXN are the C3 and C4 anterior rami , ICNs [89–92], TDN , MPN [93, 94], LTN , PHN , subscapular nerve , rhomboid nerve , ipsilateral or contralateral C7 nerve root  and hypoglossal nerve . They can be used but only if the SAN to SSN and TLH to AXN transfers are not possible, as their clinical outcome is unsatisfactory [17, 22].
2.3. Elbow flexion nerve transfers
This is the priority in brachial plexus injuries. First reported in 1994 , the
2.4. Elbow extension nerve transfers
Although aided by gravity, there are many daily life activities that require active elbow extension (reaching overhead objects, changing from sitting to standing position, working over a table, throwing objects, changing from chair to bed in SCI patients, etc.) . Restoration of elbow extension is particularly important in tetraplegia. The recipient nerve is usually the nerve branch for the TLH. The best results have been obtained by transferring the TMN to the TLH [116, 117]. Other possibilities are to re-innervate the TLH with ICNs [24, 92, 118, 119], a UN fascicle , the MPN , TDN , PHN , contralateral C7 nerve root  and an RAN fascicle for the hand . The results have been poor, particularly the ICNs .
2.5. Intercostal nerve transfers
First used by Seddon  in 1963 in brachial plexus repair. Only recommended when there is no other choice (i.e. C5–T1 brachial plexus avulsion). Harvesting them is technically demanding, requiring arterial hypotension to control the bleeding as the cautery cannot be used until the ICN is fully harvested . Up to seven ICNs can be transferred. The first one was used by Durand et al.  in a single case. Harvesting the second one is not advised as it provides a large sensory contribution to the arm  (Figure 8). Additionally, it is technically very difficult to harvest and a nerve graft is always needed . Usually, the third to the fifth intercostal nerves are the ones used. In women, the fourth one should be preserved to retain the nipple’s area sensation. After harvesting the mean available, ICN length is 11–12 cm , so no nerve graft is usually needed. At least two of them per recipient nerve are needed [24, 124]. They have been used to re-innervate many nerves, like the AXN [89, 92], MCN [24, 105, 106, 124–126], TLH [92, 118, 119], TDN [89, 127] and SSN [90, 91]. Their sensory branches can be used to recover some limb sensation, ameliorating the neuropathic pain. Unfortunately, not being synergistic with the recipients nerves a long re-education must be expected . Usually their harvest is not associated with any pulmonary dysfunction [24, 128].
2.6. Phrenic nerve transfers
It has been used in C5–T1 nerve root brachial plexus avulsion to re-innervate the MCN , the median nerve (MN)  or the RAN . Unless its whole intra-thoracic segment is harvested, a nerve graft is needed . The clinical results are acceptable provided there is no other choice. Patients usually need to take a breath before starting the movement with the re-innervated muscle. Post-operatively patients show a decreased pulmonary capacity that improves after 2 years [114, 130]. It is not commonly used these days.
2.7. Contralateral C7 nerve transfer
It has been used in complete brachial plexus avulsions. It requires a long nerve graft or to shorten the humerus [122, 131], but this can be avoided crossing the donor C7 nerve root through the C6–C7 disc space . The targets are usually MN or MCN. Its use has been discouraged as its clinical results are poor and unreliable, the forearm and hand muscles do not get a good re-innervation and there is co-contraction of the donor and recipient limbs [24, 43]. In fact, initiating the movement often requires to start it in the contralateral normal side and there is co-contraction of the muscles of the donor and recipient sides . Its value is very much disputed.
2.8. Wrist and finger extension
In the case of proximal RAN damage with an intact MN, the best choice is the
Bertelli and Ghizoni reported successful restoration of wrist extension transferring the
In C7–T1 brachial plexus injuries, the shoulder and elbow mobility is preserved, but the finger movements are lost. The supinator muscle (SM) innervation is preserved as is comes from the C6 nerve root. Thus, it is possible to coapt one or both
2.9. Finger flexion and median nerve hand function
The primary goal of MN recovery is to provide first and second finger pincer as well as thumb opposition .
Reported by Palazzi et al.  in 2006 the
García-López et al.  reported a single case of
Thenar muscle re-innervation can be achieved coapting the
Finger flexion, particularly the thumb and index finger, can be recovered by coapting the
2.10. Pronation recovery
To restore active pronation, essential in many daily living activities, some have transferred the FCU nerve branch to the PT nerve . Others have transferred one of the branches of the FDS to the PT nerve . More recently, the nerve for the ECRB has been transferred to the PT branch . This last technique has a widespread acceptance.
2.11. Ulnar nerve hand function
When the UN is damaged in the arm or more proximally, the recovery of hand intrinsic muscles is dismal . The motor recovery can be improved by coapting the
Transfer of the
2.12. Nerve transfers for upper limb sensation recovery
Sensory nerve transfers sacrifice nerves that serve areas with non-critical sensation to recover it where this sense is vital (i.e. tip of the thumb and index fingers) [33, 49, 51, 61, 65]. They also help with neuropathic pain control [13, 29, 49, 156]. The donor nerve distal stump can be coapted end-to-side to a nearby sensory nerve to regain some protective sensation [14, 31, 66].
In the case of proximal MN damage, restoring the sensation in the ulnar aspect of the thumb and the radial side of the index finger is a priority to allow a useful pincer mechanism . The donors are the nerves supplying less essential areas like the third web space (MN branch) the forth web space (UN branch), the dorsal sensory branch of the UN and the radial sensory nerve (RSN) [22, 29, 49, 50, 65, 157, 158]. Ducic et al.  in 2006 recovered the sensation of the thumb and index fingers using the radial nerve branches as donors. Bertelli and Ghizoni  in 2011 reported the transfer of the distal superficial radial finger nerves of the thumb and index fingers to the ulnar aspect of the thumb and the radial aspect of the index finger. Flores et al.  transferred the superficial ulnar nerve to the third palmar digital nerve.
In the case of proximal RAN damage, the sensation in the dorsum of the hand can be recovered by coapting the lateral antebrachial cutaneous nerve (LABCN) to the RSN  (Figure 13). At the outer aspect of the elbow, both nerves run parallel to each other. The LABCN goes with the superficial radial vein and the RSN with the deep radial vessels. The LABCN is sectioned as distally as possible and coapted to the proximal part of the RSN .
In C7–T1 nerve root injuries the LABCN can be coapted with the sensory fascicles of the UN in the forearm to recover the sensation in the hand .
3. Nerve transfers in the lower extremity
Three areas have been explored. At the proximal level, nerve transfers between the femoral (FN) and obturator (OBN) nerves; at the knee, the nerve transfers between branches of the posterior tibial nerve (PTN) and the peroneal nerve (PN); and at the foot, some sensory nerve transfers for recovery of protective sensation. There have been some attempts to recover urinary continence in spinal injured patients.
FN injuries are the most disabling as they impair the capacity of standing and walking. The anterior branch of the OBN has been successful in re-innervating the FN [119, 161, 162]. The anterior branch of the OBN is selected to preserve the primary leg adductor muscle . The reverse transfer using an FN motor branch as donor to coapt it to the OBN has also been used with successful clinical outcomes .
Nerve transfer from an FN branch to the pudendal nerve to recover urinary continence has been achieved in a canine neurogenic bladder model  but its clinical application in the human being is still pending.
4. Transfers for spinal cord injured patients
Around a 50% of the SCI involves the cervical spinal cord . Tetraplegic patients suffer from a variable loss of arm and hand functions, usually asymmetrical . This creates serious difficulties to perform their daily activities (transfers back and forth from the wheelchair, feeding, computer handling, self-catheterization, etc.) . To recover any partial arm and/or hand function might mean an immense impact on their quality of life .
Nerve transfers used in SCI patients aim to recover elbow, wrist and finger extension, palmar grasp and thumb and index finger pinch and release. The nerve transfers mentioned above can also be used in these cases. The only difference is that in SCI there are three spinal cord areas [170–172]. The area above the injury will have normal spinal cord and nerves; the area of the injury will have neuronal loss and severe muscle atrophy. To recover function in this area, nerve transfers must be planned no later than 1 year after injury.
Below is the area of normal spinal cord disconnected from the rest of the central nervous system. The muscles depending from this area are not denervated, so nerve transfers can be done any time. The first area is the donor and second and third areas are the recipients. We aim to recover some functions of areas 2 and 3 transferring some nerve branches from area 1. In SCI, it is recommended to wait 12 months to give a chance for spontaneous recovery .
Elbow extension has been achieved by transferring the TM motor branch to the TLH .
Nerve transfers have become an essential way to repair irrecoverable peripheral nerve injuries. Mastering these techniques is essential for the peripheral nerve surgeon. The best results are obtained when patients are young; the procedure is not delayed more than 6 months after the injury, donor and recipient nerves are agonistic and when the donor nerve has no damage. Shoulder and elbow motor recovery is very successful in most patients. Hand recovery can also be achieved but results are not so good. The biggest experience is in upper limb nerve transfers. Lower limb nerve transfers have been attempted but the experience is limited and the choices few. In tetraplegic patients, we aim to recover some of the lost functions, simplifying their daily lives.
The authors thank the Department of Human Anatomy and Embryology of the Faculty of Medicine of the University of Valencia, particularly the laboratory curators Lucia and Carmina and Dr. Tomás Hernández Gil de Tejada and all personnel of the
Appendices and nomenclatures
|AIN||Anterior interosseous nerve.|
|BMN||Biceps muscle nerve.|
|ECRB||Extensor carpi radialis brevis.|
|ECU||Extensor carpi ulnaris.|
|EDC||Extensor digitorum communis.|
|EDM||Extensor digiti minimi.|
|EPL||Extensor pollicis longus.|
|FCR||Flexor carpi radialis.|
|FCU||Flexor carpi ulnaris.|
|FDS||Flexor digitorum superficialis.|
|FDP||Flexor digitorum profundus.|
|FPLN||Flexor pollicis longus.|
|LABCN||Lateral antebrachial cutaneous nerve.|
|LTN||Long thoracic nerve.|
|MPN||Medial pectoral nerve.|
|MRC||Medical Research Council.|
|PIN||Posterior interosseous nerve.|
|PTN||Posterior tibial nerve.|
|RSN||Radial sensory nerve.|
|SAM||Serratus anterior muscle.|
|SAN||Spinal accessory nerve.|
|SAM||Serratus anterior muscle.|
|SCI||Spinal cord injury.|
|TLH||Triceps long head.|
|TMN||Teres minor nerve.|
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