Nerve and tendon transfers in tetraplegia: A new narrative


List of abbreviations

SCI

spinal cord injury

ICSHT

international classification of surgery for the hand in tetraplegia

PIN

posterior interosseous nerve

AIN

anterior interosseous nerve

ECRL

extensor carpi radialis longus

ECRB

extensor carpi radialis brevis

BR

brachioradialis

FDS

flexor digitorum superficialis

FDP

flexor digitorum profundus

FLP

flexor pollicis longus

EPL

extensor pollicis longus

ECD

extensor communis digitorum

PT

pronator teres

CMC

carpometacarpal

IP

interphalangeal

EPI

extensor proprius indicis

EDM

extensor digitorum minimi

FCU

flexor carpi ulnaris

FP

flexor pollicis

MP

metacarpophalangeal

Introduction

The most common causes of spinal cord injury (SCI) are road accidents and falls from a height, with a prevalence for male patients between 16 and 30 years old ( ) and an incidence between 10 and 80 new cases per millions of people annually worldwide ( ).

More than 50% of all spinal cord injuries involve cervical spine leading tetraplegia as main clinical feature, with loss of effective upper-limb function.

The lack of hand function is the sequela which mostly affected the quality of life in patients with tetraplegia and always requires support in their daily-life activities and mobility from other people ( ; ; ). Furthermore, it is reported as more desired than bowel, bladder and sexual function, standing and pain control ( ; ). In this scenario, tendon transposition is a reliable surgical technique able to restore active movement and strength of a damaged anatomical segment; however, the shortage of functional muscles above the segment lesion available for transfer is the main problem treating cervical SCI ( ). Similarly, nerve transfer required the adjustment of a healthy donor nerve to a denervated anatomical district to restore function nerve-target, but this means to sacrifice a potential useful nervous structure ( ).

In our review, we are going to illustrate the current available techniques of tendon and nervous transfer in order to restore hand and forearm function combining nerve and tendon transfer in patients with tetraplegia.

Classifications

The most useful and accepted classification for upper-limb lesion in tetraplegia is the:

The Classification for Surgery of the Hand in Tetraplegia (ICSHT), where, the most common patterns of injuries are classified following the number of functional muscles existing below the elbow.

A functional muscle is described as muscle graded 4 or more according to the Muscle Grading System ( ) ( Table 1 ), and the ICSHT principles are reported in the literature as the “gold standard” to choose the most appropriate reconstructive technique mainly based on tendon transfer and tenodesis procedure ( Table 2 ).

Table 1
International Classification for Surgery of the Hand in Tetraplegia (ICSHT).
Motor GROUP Characteristics Function
0 No muscle below elbow suitable for transfer
1 BR Flexion and supination of the elbow
2 ECRL Extension of the wrist
3 ECRB Extension of the wrist
4 PT Pronation of the wrist
5 FCR Flexion of the wrist
6 Finger extensors Extrinsic extension of the fingers
7 Thumb extensor Extrinsic extension of the thumb
8 Partial digital flexors Extrinsic flexion of the fingers
9 Lacks only intrinsics
10 Exceptions
BR brachioradialis, ECRL extensor carpi radialis longus, ECRB extensor carpi radialis brevis, PT pronator teres, FCR flexor carpi radialis.

Table 2
Muscle Grading System of the British Medical Research Council, muscle function ranged from 0 (no contraction) to 5 (normal power).
GROUPS Description
0 No contraction
1 Flicker or trace of contraction
2 Active movement with gravity eliminated
3 Active movement against gravity
4 Active movement against gravity and resistance
5 Normal power

It’s important to select the most appropriate donor muscle in order to preserve function of anatomical region without creating another functional deficit after tendon transfer which can be used alone or in combination with tenodesis and arthrodesis showing interesting and reproducible results ( ).

According to function importance, a priority order to choose the correct sequence of donor muscles ( ; ) is well established:

  • (1)

    wrist extension recovery,

  • (2)

    pinch recovery,

  • (3)

    grasp recovery,

  • (4)

    finger and thumb extension recovery,

  • (5)

    intrinsic muscles function recovery.

When transfer options are ended, the remaining functions are reached using tenodesis and arthrodesis ( ).

In the setting of arm dysfunction, nerve transfer is also a successful surgical procedure approaching proximal brachial plexus injury with avulsion of nerve roots or more peripheral nerve injuries. Nerve transfers are commonly used where anatomic repair of original motor nerve is not possible as well as where it’s possible to rapidly restore function by rerouting expendable donor nerves ( ). Recently, some Authors introduced nerve transfers in tetraplegia, reporting interesting outcomes ( ; ). According to our previous work ( ), the current authors propose a new surgical strategy based on classical tendon transfer surgery combined with nerve transfer techniques ( Table 3 ). The use of both surgical approaches allows avoiding a frequent concern about the use of nerve transfer in reconstructive surgery: the risk of using sources of “predictable” results for “unpredictable” results.

Table 3
Combining Nerve and Tendon Strategy in tetraplegia.
Group 0
Primary procedure Positive outcome? Secondary procedure
  • Teres minor to triceps nerve transfer

  • Brachialis to ECRL nerve transfer

NO Posterior deltoid to triceps tendon transfer
YES Flexor pollicis longus tenodesis + Moberg key pinch procedure
Group 1 (BR ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Teres minor to triceps nerve transfer

NO Posterior deltoid to triceps tendon transfer
  • Brachialis to AIN/FDS nerve transfer

YES Extensor digitorum communis tenodesis + Extensor pollicis longus tenodesis
NO Flexor pollicis longus tenodesis + Moberg key pinch procedure
  • BR to ECRB tendon transfer

Group 2 (ERCL ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Teres minor to triceps nerve transfer

NO Posterior deltoid to triceps tendon transfer
  • Supinator to PIN nerve transfer

NO Extensor digitorum communis tenodesis + Extensor pollicis longus tenodesis
  • Brachialis to AIN/FDS nerve transfer

YES BR to opposition
NO BR to FPL tendon transfer
Group 3 (ECRB ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Teres minor to triceps nerve transfer

NO Posterior deltoid to triceps tendon transfer
  • Supinator to PIN nerve transfer

NO Extensor digitorum communis tenodesis + Extensor pollicis longus tenodesis
  • Brachialis to AIN/FDS nerve transfer

YES BR to opposition
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5°
  • ECRL to FDP (3°-4°-5° finger) tendon transfer

Group 4 (PT ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Supinator to PIN nerve transfer

NO Extensor digitorum communis tenodesis + Extensor pollicis longus tenodesis
  • Brachialis to AIN/FDS nerve transfer

YES BR to opposition
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5°
  • ECRL to FDP (3°-4°-5° finger) tendon transfer

Group 5 (FRC ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Supinator to PIN nerve transfer

NO Extensor digitorum communis tenodesis + Extensor pollicis longus tenodesis
  • Brachialis to AIN/FDS nerve transfer

YES BR to opposition
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5°
  • ECRL to FDP (3°-4°-5° finger) tendon transfer

Group 6 (EDC ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Brachialis to AIN/FDS nerve transfer

YES BR to opposition
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5°
  • ECRL to FDP (3°-4°-5° finger) tendon transfer

  • EPL tenodesis

Group 7 (EPL ➔ M 4)
Primary procedure Positive outcome? Secondary procedure
  • Brachialis to AIN/FDS nerve transfer

YES EDM to APB or EIP to APB
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5° + EDM to APB or EIP to APB
  • ECRL to FDP (3°-4°-5° finger) tendon transfer

Group 8 (partial finger flexion)
Primary procedure Positive outcome? Secondary procedure
  • ECRB to AIN nerve transfer

YES EPI/EDM to opposition
NO BR to FPL tendon transfer + Tenodesis FDP 2° to FDP 3°-4°-5° + EPI/EDM to opposition
Group 9 (intrinsic deficit)
Primary procedure Positive outcomes Secondary procedure
  • Intrinsic reconstruction (Zancolli lasso/house intrinsic procedure)

  • Opponensplasty

YES None
NO
A new proposal of surgical treatment based on ICSHT group. In case of failure of the proposed treatment, a salvage procedure (actual treatment) is always possible.

In this proposed technique, the choice of the most appropriate nerve donor site is crucial in order to avoid the subtraction of useful muscles; in this way, it is always possible to perform a second stage surgery according to classical tenodesis or tendon transfer surgeries.

Indications and timing

The standard patient candidate to combined nerves and tendons transfer is a patient with cervical spine injury, with incomplete or partial paralysis of the upper limb and a stabilized upper extremity motor function.

Their general condition should be considered stable, with good pain control, no spasticity and infection free. The passive range of motion could be almost complete and they should be very motivated for the long postoperative rehabilitation ( ).

Patients should be correctly informed before surgery, especially about the difference in terms of recovery time: nerve transfer needs a long time before they can show their results, and often they need a second stage procedure to achieve the set objectives. Great motivation and realistic objectives are strongly requested to obtain good improvement in hand function ( ).

Conversely, contraindications for nerve and tendon transfer surgery which could lead to poor results, are ( ) spasticity contractures, chronic pain problems, psychological instability with unrealistic expectations and insufficient motivation.

However, there is no consensus about timing of nerve transfers in tetraplegia. Unfortunately, within the year from injury, all possible spontaneous recovery has already occurred; for this reason, it is recommended to perform tendon transfer after 1 year from SCI. Nevertheless, the neurological recovery usually occurs in the first 6 months from trauma ( ).

It is usually accepted that terminal muscular atrophy is established after 1 year of denervation, with no possibility of function restoration ( ). According to these premises, Lamb and Chan observed that if a muscle is completely paralyzed during the initial assessment and it will remain paralyzed 1 month later, it will be rare to observe any significant improvement, even 1 year later ( ). On the contrary, Bertelli et al. reported functional muscle reinnervation after distal nerve transfers performed 18 months after SCI ( ).

Furthermore, Fox et al. described two type of lesions with different indications about the appropriate surgical time for intervention ( ) ( Fig. 1 ).

Fig. 1, Time-dependent and time-independent injury based on the level of spinal cord lesion.

First, time-independent lesions: clear-cut SCI with a little zone of cell damage located at the anterior horn of the spinal cord. Peripheral nerve transfer can restore segment movement by reconnecting functional motor unit to brain. This transfer switches the motor control from an expendable donor to a muscle group distal to lesion level, bypassing the site of lesion. It can be done at any time after trauma.

Second, time-dependent lesions: injury site is more extensive; roots can be involved as a peripheral nerve lesion. To restore the voluntary control or to reinnervate muscles that would become atrophic nerve transfer should be used. Denervated muscles might benefit from early surgery before the onset of muscular atrophy, while paralyzed muscles leave more time for surgery ( ; ).

Taking into account all these factors, an ideal time for surgery should be performed between 6 and 12 months from trauma, before the onset of irreversible muscle atrophy. Procedures could be anticipated only if muscles denervation is recorded by electromyography (EMG) ( ).

In the following paragraphs, we will describe primary and secondary procedures for each group of ICSHT classification ( Table 3 ).

Group 0

Neurological level of injury: C5.

Residual motor function: no muscle of grade 4 below the elbow.

Current reconstructive strategy: In this group, tendon transfer procedures can be performed to restore elbow extension:

  • Moberg’s procedure based on posterior deltoid to triceps transfer.

  • Zancolli’s procedure based on biceps to triceps transfer ( ; ; ). Conventional surgery considers useless any tendons transfers to restore wrist and hand function in this group. The restoration of wrist extension is really important, since tenodesis can allow thumb-to-index key pinch, due to wrist motion. It is also important because it increases patient autonomy, and it improves some daily life activities such as eating, personal care and wheelchair propulsion.

In one larger series, groups 0 and 1 are often together and represent almost 30% of the lesions ( ).

Our proposal: It is possible to treat this condition with nerve transfer:

  • teres minor to triceps nerve transfer.

  • brachialis to extensor carpi radialis longus nerve transfer.

The transfer of teres minor motor branch to triceps long head motor branch allows patients to restore elbow extension without any deficit to the donor site area ( ). Infraspinatus muscle is able to compensate external rotation deficit due to the teres minor nerve transposition. Moreover, teres minor transfer is not typically used in tetraplegia since this transfer doesn’t preclude Moberg’s procedure as a second surgery in case of failure or to improve a partial recovery.

Bertelli also proposed the use of the posterior division of the axillary nerve to the triceps long and medial head nerve ( ); however, if this procedure fails, it is not possible to use posterior deltoid tendon transfer to triceps (Moberg procedure) as salvage procedure.

It is extremely important to fully evaluate shoulder function and to explore any partial deficit of deltoid or teres minor muscle function, since if a deficit is present, it is not possible to use deltoid to restore elbow extension.

Fridén suggested the selective nerve transfer of brachialis to extensor carpi radialis longus (ECRL) to restore wrist extension ( ). Brachialis muscle is primarily innervated by a single branch of the musculocutaneous nerve deriving from the spinal roots C5/6; if biceps is working, this branch can be used as a donor. However, this will not allow a secondary Zancolli’s procedure to restore elbow extension.

If brachialis transfer will have positive outcome, the lesion will upgrade from type 0 to type 1 and it is possible to perform flexor pollicis longus tenodesis and Moberg procedure for passive key pinch reconstruction ( ).

Group 1

Neurological level of injury: C5.

Residual motor function: only brachioradialis (BR) is graded as 4 or more. Elbow flection is still possible since brachioradialis and biceps are functioning.

Current reconstructive strategy: As for group 0, Moberg or Zancolli’s procedure can be used to restore elbow extension. The transfer of BR tendon to radial wrist extensors is able to provide enough strength to extend wrist against resistance.

Our proposal : It is possible to transfer:

  • Teres minor to triceps nerve.

  • Brachialis to anterior interosseous nerve (AIN) and flexor digitorum superficialis (FDS) nerve transfer.

  • BR to extensor carpi radialis brevis (ECRB) tendon transfer.

  • BR to ECRB tendon transfer is able to restore active wrist extension and passive key pinch reconstruction thanks to flexor pollicis longus (FLP) tenodesis with some tricks ( ; ; ).

About 10 years ago, Mackinnon described the brachialis to AIN transfer in patients with spinal cord injury ( ). In this way, it is possible to improve intrinsic hand muscles function, which are very important to increase grip strength and ability, allowing patients to self-feeding ( ).

If it is possible to partially restore flexor pollicis longus function, this will improve tenodesis effects grasp and provide extra strength and holding power as described by Fox et al. They used brachialis to AIN and FDS nerve transfer for this purpose ( ).

If these procedures have good results, with restoration of pinch function, a second stage procedure can be planned to increase grip strength. ECD and EPL can improve hand opening and grasp function. In case of failure, FLP tenodesis can be performed anyway at any time.

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