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Loss of upper-limb function in patients with tetraplegia, following a spinal cord injury, is a major barrier to regain autonomy. The functional abilities of a tetraplegic patient increase substantially for instance if the patient can extend the elbow. This can increase the workspace and give a better use of a manual wheelchair. To be able to hold objects a patient needs to have a functional pinch grip, this can be useful for performing daily living activities. A large survey in patients with tetraplegia demonstrated that these patients give preference to improving upper extremity function above other lost functions like being able to walk or sexual function.

Surgical procedures do exist to improve the function of the tetraplegic patient's arms, but these procedures are performed in fewer than 10% of the tetraplegic patients. Each tetraplegic patient is unique, and therefore surgical indication should be based on the remaining physical abilities, wishes and expectations of the patient.

In 2007 a resolution was presented and accepted at the world congress in reconstructive hand surgery and rehabilitation in tetraplegia, that stated that every patient with tetraplegia should be examined and informed about the options for reconstructive surgery of the tetraplegic arms and hands. This resolution demonstrates mostly the necessity to increase the awareness on this subject amongst physicians.

History
Reconstructive surgery of the upper limb in tetraplegic patients began during the mid-20th century. The ﬁrst attempts at regaining gripping function of the hand probably took place in Europe at the end of the 1920s with the construction of ﬂexor-hinge splints.

In the early 1940s, a surgeon called Sterling Bunnell (1882–1957) was probably one of the ﬁrst to refer to the reconstruction of gripping function for the tetraplegic hand. He described surgeries of combining tenodeses and tendon transfers to restore hand function. He also advocated transferring the m. brachioradialis to the wrist extensors when these muscles are paralyzed.

In the 1950s, understanding of the tenodesis effect inﬂuenced the development of surgical techniques such as the static ﬂexor tenodesis. These procedures provided the basic functions of grasp and pinch. Tendon transfers were developed to accomplish both digital release and gripping functions in two surgical stages. The originators of these procedures were Lipscomb et al. [20], Zancolli, House et al. House et al. contributed important clinical investigations while showing the value of different surgical procedures.

According to Zancolli, transfer of the m. brachioradialis to the m. extensor carpi radialis tendons was proposed by Vulpius and Stoffel in 1920. In tetraplegia, this was ﬁrst proposed by Wilson. and ﬁrst described fully by Freehafer.

In 1967, Alvin Freehafer of Cleveland, Ohio, contributed valuable ideas towards achieving independence in the arms of tetraplegic patients. He and his team published the results of six patients who underwent transfer of the m. brachioradialis to restore active wrist extension. In 1974, Freehafer et al. recommended opposition transfers and ﬁnger-ﬂexion transfers.

In 1971, surgery of the tetraplegic upper limb experienced a revival after Moberg’s clinical investigations. His main contributions were (1) to restore elbow extension through transfer of the posterior deltoid to triceps (the initial procedure); and (2) to reconstruct a key pinch. Moberg’s idea of posterior deltoid transfer to restore elbow extension has been used extensively by many surgeons, such as Bryan and DeBenedetti.

In 1983, Douglas Lamb of Edinburgh, Scotland, gave great headway to surgery of the tetraplegic upper extremity when Lamb and Chan recommended reconstruction of elbow extension by transferring the posterior deltoid to the triceps according to Moberg’s technique, which was published in 1975.

A publication by Friedenberg was the starting point for future indications of biceps-to-triceps transfers, including those of Zancolli, Hentz et al., Kuts et al., Allieu et al. and Revol et al.

Another major change was the change to one-step procedures, reconstructiong opening and closing phases at the same time. Especially Jan Friden, from Gothenburg, with major experience in this area championed this thought, partially driven by the transport problems in Sweden during winter, it saved the patients an operation and minimized hospital stay.

The development of hand surgery for tetraplegia has received important contributions through published reports and by the international conferences initiated with the inﬂuence of Erik Moberg from Goteborg, Sweden. Conferences have been of great interest because of the convergences of hand surgeons interested in the ﬁeld, promoting discussion and comparison of different surgical methods and experiences.

Goals for surgery
A common goal of surgical reconstruction of the arms in patients with tetraplegia is to restore key pinch, palmar grip and elbow extension. Restoration of these functions, results in increasing a patient's independence. The key pinch is a simple grasp in which the thumb applies force to an object to hold it against the lateral side of the index finger. Restoring this function allows a patient to hold objects such as a fork or pen that are necessary for activities of daily living such as eating, self-grooming and self-catheterization.

Elbow extension is an important part of upper limb surgical reconstruction in patients with tetraplegia. Active elbow extension results in functional gains including increasing available workspace, performing pressure relief maneuvers, propelling a manual wheelchair, enhancing self-care and leisure activities, and promoting independent transfer. Elbow extension against gravity further enhances these activities above the shoulder level and reachable workspace.

Palmar grip allows the patient to grasp objects in the palm of the hand and secure the object by flexing the fingers at the metacarpal joint. This gives the patient the possibility to hold objects such as a cup and also permits use of the hand for wheelchair propulsion. A social aspect of regaining the palmar grip is that the patient is able to give a handshake.

Classification of the injury
Spinal cord injuries are classified as complete and incomplete by the American Spinal Injury Association (ASIA) classification. The ASIA scale grades patients based on their functional impairment as a result of the injury, grading a patient from A to D. (see table 1 for criteria) This has considerable consequences for surgical planning and therapy.

Table 1: ASIA impairment scale

Complete spinal-cord lesions
Pathophysiologically, the spinal cord of the tetraplegic patient can be divided into three segments which can be useful for classifying the injury.

First there is an injured functional medullary segment. This segment has unparalysed, functional muscles; the action of these muscles is voluntary, not permanent and strength can be evaluated by the British Medical Research Council (BMRC) scale. This scale is used when upper limb surgery is planned, as referred to in the 'International Classification for hand surgery in tetraplegic patients' (see table 2).

A lesional segment (or an injured metamere) consists of denervated corresponding muscles. The lower motor neuron (LMN) of these muscles is damaged. These muscles are hypotonic, atrophic and have no spontaneous contraction. The existence of joint contractures should be monitored.

Below the level of the injured metamere there is an injured sublesional segment with intact lower motor neuron. Which means that medullary reflexes are present, but the upper cortical control is lost. These muscles show some increase in tone when elongated and sometimes spasticity, the trophicity is good.

Incomplete spinal-cord lesions
Incomplete spinal cord injuries result in varied post injury presentations. There are three main syndromes described, depending on the exact site and extent of the lesion.

The central cord syndrome: most of the cord lesion is in the gray matter of the spinal cord, sometimes the lesion continues in the white matter.

The Brown-Sequard syndrome: hemi section of the spinal cord.

The anterior cord syndrome: a lesion of the anterior horns and the anterolateral tracts, with a possible division of the anterior spinal artery.

For most patients with ASIA A (complete) tetraplegia, ASIA B (incomplete) tetraplegia and ASIA C (incomplete) tetraplegia, the International Classification level of the patient can be established without great difficulty. The surgical procedures according to the International Classification level can be performed. In contrast, for patients with ASIA D (incomplete) tetraplegia it is difficult to assign an International Classification other than International Classification level X (others). Therefore it is more difficult to decide which surgical procedures should be performed. A far more personalized approach is needed for these patients. Decisions must be based more on experience than on texts or journals.

The results of tendon transfers for patients with complete injuries are predictable. On the other hand, it is well known that muscles lacking normal excitation perform unreliably after surgical tendon transfers. Despite the unpredictable aspect in incomplete lesions tendon transfers may be useful. The surgeon should be confident that the muscle to be transferred has enough power and is under good voluntary control. Pre-operative assessment is more difficult to assess in incomplete lesions. Patients with an incomplete lesion also often need therapy or surgery before the procedure to restore function to correct the consequences of the injury. These consequences are hypertonicity/spasticity, contractures, painful hyperesthesias and paralyzed proximal upper limb muscles with distal muscle sparing. Spasticity is a frequent consequence of incomplete injuries. Spasticity often decreases function, but sometimes a patient can control the spasticity in a way that it is useful to their function. The location and the effect of the spasticity should be analyzed carefully before treatment is planned. An injection of Botulinum toxin (Botox) into spastic muscles is a treatment to reduce spasticity. This can be used to prevent muscle shorting and early contractures.

Over the last ten years an increase in traumatic incomplete lesions is seen, due to the better protection in traffic.

Pre-operative assessment
A group of hand surgeons realized in the 1970s that the level of injury did not predict the number of available muscles in the upper limb very well. Therefore the international classification was established in 1979, at the Edinburgh meeting. It was called “The international classification (IC) of hand surgery in tetraplegic patients” (table 2) and it describes the number of possible transferable muscles. To measure and evaluate hand strength each muscle is tested and all muscles with a BMRC grade of M4 or more are recorded.

Table 2: International Classification of Hand surgery in Tetraplegic Patients A muscle not included in the International Classification, but of great importance, is the triceps muscle. When assessing a patient pre-operatively the triceps strength must also be recorded. An active triceps means a patient can reach in space, and the elbow can be stabilized against gravity and against other muscles to be transferred. (see further)

Furthermore, to classify patients it is essential to record sensation in at least the thumb and index pulpa. Patients with a two point discrimination of less than 10mm are classified as cutaneous sensation (OCu) and patients with a two point discrimination of more than 10mm are classified as ocular sensation (O) (meaning that control of the to be operated limb cannot be performed by normal sensation, but is controlled visually).

Therefore patients are classified as: O or OCu, IC gr(0-X), Triceps + or –

For example: a patient has sensation of 8 mm in thumb and index pulpa, and has a good brachioradialis, extensor carpi radialis longus and brevis and a pronator teres (all of M4) but no Triceps. This patient is classified as OCu 4, Tr -.

Patient oriented goals
The pre-operative assessment of patients has turned more patient-goal oriented. This means that the patients are asked to define their goals before surgery. In order to evaluate this the Canadian Occupational Performance Measure (COPM) was developed. This test is based on the World Health Organisation's framework of measuring health and disability: The International Classification of Function(ICF): This framework measures health and disability by means of two lists: a list of body functions and structure, and a list of domains of activity and participation. Functional deﬁcits can be measured according to the level of loss of structure and function, the level of activity limitations, and the level of restriction in social participation. Reaching or gripping represents the integration of strength, sensation and range of motion, and therefore occur at the individual level rather than at the organ system level. For this reason, reaching and gripping are on the ICF level of activities. However, this level includes a broad range of activities, from basic activities (for example grasping and moving objects) to complex activities (such as dressing, grooming). It is useful to make a distinction between basic activities and complex activities.

COPM
As mentioned above, The Canadian Occupational Performance Measure (COPM) is used to measure a tetraplegic patient's performance and satisfaction before and after upper limb surgery. This is done by identifying important goals of hand surgery and evaluating patient-perceived performance and satisfaction of hand surgery for these goals. Goals are identiﬁed through an interview between the therapist and the patient based on past experience. Published reports are provided about the expected outcomes of elbow extension transfers on strength and function of patients with a spinal cord injury. For each goal, the subject rated performance and satisfaction using a 10-point Likert scale, in which 1 was negative (“cannot perform,” “not satisfied”) and 10 was positive (“performs very well,” “very satisfied”). After surgery, performance and satisfaction are rated again for each goal.

A positive change is seen in patient-perceived performance and satisfaction with self-identiﬁed goals after tendon transfers. A good example of the use of the COPM can be found in a report published by Scott Kozin, thirty-three goals for surgery were established. Following the biceps-to-triceps transfer, improvement in at least one goal was seen in all patients. Performance and satisfaction were greatly improved (an improvement of at least 4 points) in certain activities of daily living, including reaching for objects, recreational activities, wheelchair propulsion, and transfers. Although improvement was seen in most goals, a reduction was reported in 2 goals (one pertaining to dressing and the other to transfer). After tendon transfers, the total mean score statistically increased from 2.6 to 5.6 for performance (p .001) and from 1.8 to 5.7 for satisfaction (p .001).

Criteria for surgery
General indications for functional surgery of the hand and arm in tetraplegic patients:

There are different views on optimal timing of surgery after a spinal cord injury. The general consensus is to operate the patient when he or she is neurologically stable. Some surgeons try to operate a patient as early as possible. The advantages of this are that the patient can take advantage of the new functional possibilities before new adjustments and apaptations develop. Other surgeons operate when it becomes feasible. This is usually 12–18 months after injury (can be shortened to 6–7 months) and only after stabilization of motor function. Important spasticity (see further) and neurovegetative complications (i.e. bladder function, bowel function, pulmonary function and pressure sores) must have been treated already. The patient must be able to sit in a wheelchair so that he/she can move the arm against gravity. Usually a compromise is found between the patient’s wishes and the surgeon when timing the surgery.

It is important that the psychological condition of the patient is evaluated before surgery. The dramatic change in the patient’s life requires a psychological adjustment. This should be evaluated and addressed before surgery. Follow-up by a psychologist is necessary. Patient must be psychologically ready to understand the surgical planning, aims and possible outcomes. The patient must be motivated, well-informed, in sound psychological condition and must have a precise and realistic need for rehabilitation. Individual factors must be taken into account. (age, profession, hobbies, education, family support and social background). This is especially important in associated brain injury.

Contraindications
Contraindications for surgery are severe pressure sores, severe spasticity, inability to stabilize the trunk.

Spasticity, if present, can be very important. It is not a contraindication per se, but severe spasticity must be treated first depending in which muscle groups it is present. Spascticity can be treat with botox or myotomies. In some cases spastic tone can be useful to facilitate hand grasp and grip. Harmful spasticity that does not respond to medication or surgical treatment is a contraindication. The shoulder muscles, pectoralis major and latissimus dorsi, must be evaluated. The shoulder must not only have good motor condition but also good proprioceptive control. The trophicity and articular condition of the upper limb must also be considered. A poor condition requires a preoperative rehabilitation program.

Before any hand surgery is performed, the patient should be able to actively extend the elbow. Therefore, if there is now active elbow extension, elbow extension reconstruction surgery should precede any hand surgery.

A contraindication specifically for posterior deltoid to triceps transfer is a flexion contracture of the elbow, biceps to triceps transfer might then be a possible transfer for elbow extension reconstruction.

The contraindications for biceps-to-triceps transfer relate to the muscle balance surrounding the elbow. The m. supinator and m. brachialis function is a prerequisite for this surgery. If one of these muscles is nonfunctional the patient will lose forearm supination and elbow flexion if the tendon is transferred.

Surgical procedures – active and passive tendon transfers
In general, reconstruction of the upper limb can only be performed if active elbow extension is present. This stabilizes the elbow and gives the patient a reach. It will also allow the transfer of the other muscles crossing the elbow joint (like the m. brachioradialis and m. extensor carpi radialis longus). It is also an operation whose results allow the patient to gain confidence in the rest of the treatment.

Wrist-related tenodesis effect means that wrist flexion passively opens the hand and wrist extension passively closes the hand. (see pictures below) Wrist-related tenodesis effect is the key point of any functional surgery in a paralyzed hand, therefore active wrist extension is required and reconstruction of this active wrist extension is of utmost importance for the tetraplegic hand. If no active wrist extension is available (IC group 0 and 1), the brachioradialis (only IC group 1) can be transferred to achieve wrist extension.

Active tendon transfers are possible if m. extensor carpi radialis longus and m. extensor carpi radialis brevis are present. The use of the m. extensor carpi radialis longus and the m. brachioradialis are possible to restore hand function.

Elbow
There are two major techniques used to gain elbow extension.

Deltoid-to-triceps transfer: For this transfer, the posterior part of the deltoid muscle is released from its origin and attached to the triceps muscle (usually by means of a tendon graft or a synthetic graft) leaving the rest of the deltoid muscle intact. This transfer is usually very successful because the line of pull of the posterior deltoid muscle is in the same direction as the triceps muscle. Also, there is hardly any loss of function.

There are two important aspects of the procedure that must be considered. First, the deltoid tendon itself does not have the sufficient length to be directly inserted into the triceps tendon. Therefore, the tensor fascia lata, extrinsic toe extensors, tibialis anterior and the triceps tendon have all been used to bridge the gap. Second, this tendon transfer has a high risk of being stretched, during the postsurgical period. It is extremely important that a challenging and precise post-surgical rehabilitation program is implemented, in order to maximize the results and prevent the tendon from becoming stretched.

Biceps-to-triceps transfer: The biceps muscle can only be used for this transfer if the other elbow flexors are intact (m. brachialis and m. brachioradialis). The biceps is rerouted and passed through a tunnel at the medial aspect of the arm and inserted to the triceps tendon or olecranon.

Hand
Restoration of Key Pinch: In general for Key Pinch the thumb has to be activated. In the lower groups according to the International Classification (IC groups 0–1) this can only be done by means of tenodesis. In IC groups 2 and higher the m. brachioradialis is used to strengthen the thumb flexor. Usually the thumb extensor is fixed to the extensor retinaculum and the CMC1 joint is arthrodesed/fused in the right position.

Restoration of palmar grip: When active wrist extension is present, it must not be weakened. Therefore the extensor carpi radialis longus can only be used on patients in IC 3 and higher where active extension is supplied by both the extensor carpi radialis longus and the extensor carpi radialis brevis. In IC 2 patients active extension of the wrist depends only on the m. extensor carpi radialis longus, therefore this muscle must not be used for a transfer in this group of patients.

The brachioradialis muscle is a versatile motor muscle and is used for different transfers in tetraplegic patients. In IC 1 it is used to restore wrist extension, while in IC 2–8 it is used to restore finger extension (m.extensor digitorum communis) and finger (m.flexor digitorum profundus) or thumb flexion (m.flexor pollicis longus). Surgical techniques are mainly the same for the different transfers.

Technique for transferring the m. extensor carpi radialis longus: the m. extensor carpi radialis longus tendon is divided at its insertion on the second metacarpal. The muscle is separated, and freed entirely from the surrounding tissues. The m. extensor carpi radialis longus tendon is strongly attached to the planned tendon under maximum tension. The m. extensor carpi radialis longus can be transferred to the flexor digitorum profundus or flexor pollicis longus.

Technique for transferring the m. brachioradialis: The brachioradialis is freed entirely from the surrounding tissues up to the elbow to get extra excursion. The brachioradialis tendon is strongly attached to the planned tendon.

Rehabilitation
The post-operative regimens depend on the surgical procedures used. However, they tend to constrain the tetraplegic patient considerably. During most regimens it is not allowed to drive hand-driven wheelchairs, or to make transfers alone, because of the risk of rupturing a tendon suture.

In general the elbow extension reconstructions are immobilised for 2 weeks in 30 degrees elbow flexion and then slowly allowed to flex the elbow in the following weeks, at a rate of 10 degrees per week. After 10 weeks the patient is allowed to move freely again.

With the emergence of the one step procedures for the hand, the post-operative rehabiltation programmes became even more important, since early movement is essential. Patients are mobilised 24 hrs post-operatively, with protective splints. The regimen takes approximately 12 weeks, before the hand is allowed to be fully loaded. Patients are not required to stay as an in-patient for the entire regimen, but can be treated as an outpatient after 1–4 weeks, depending on the centre where the procedures are performed.