Nerve and Tendon Transfer Surgery in Cervical Spinal Cord Injury: Individualized Choices to Optimize Function

Over the last 50 years, the surgical approach to the SCI upper limb has been refined. The first procedures focused on establishing pinch and grasp.4–6 Eventually, a worldwide conference group of interested providers was convened, and the International Classification for Surgery of the Hand in Tetraplegia (ICSHT) was devised; this categorized the different injury patterns and treatment approaches.7,8 At the time ICHST was developed, most patients had complete cervical spine injuries with predictable patterns of recovery in the upper limb, and the ICSHT provided a clear algorithm to the treatment for these patients. Since that time, the injury patterns have changed with more incomplete injuries,9 which require a less algorithmic more individualized approach. These reconstructive procedures have been successful in improving function and have provided durable long-term results to these patients.10 

Nerve transfers have recently been carving out a space in the SCI upper limb reconstruction algorithm. The use of nerve transfers to restore function after SCI is not a novel concept. In 1966, Benassy described nerve transfer of the distal musculocutaneous nerve to the entire median nerve at 11 months post SCI.11 That individual gained pronation, wrist flexion, and some thumb and finger flexion with some loss of elbow flexion strength. Subsequently, Kiwerski described a case series of similar surgery in 20 individuals. He described gain in finger flexion in 15 of the 20 patients.12 

Since that time, nerve transfers have been increasingly used in the treatment of peripheral nerve and brachial plexus injury. This has led to a more detailed understanding of the internal anatomy of individual nerve fibers within the major peripheral nerves, which is termed the nerve topography. Improved microsurgical instrumentation and operative microscopy along with knowledge of the topography allow the surgeon to safely separate the different branches supplying the, for example, finger flexors from wrist flexor components of the median nerve. This gives a unique opportunity to target specific muscles for a specific function or outcome a patient may desire.

In the last decade, interest in the use of nerve transfers in SCI has been rekindled. Work by Bertelli, van Zyl, Friden and Gohritz, Fox, and Mackinnon have described use of these transfers to restore elbow extension, wrist extension, and hand opening and closing function.13–28 

A basic understanding of the physiologic underpinnings of nerve and tendon transfer surgery is helpful to appreciating the differences in these treatment options. For instance, understanding the preoperative assessment to perioperative care can aid in planning for logistics including transportation and level of assistance post operatively as well as in mediating expected outcomes. Both tendon and nerve transfers require a relatively expendable donor (musculotendinous unit or motor neuron) with normal function that is innervated above the level of the SCI and remains under upper motor neuron (UMN), brain, or volitional control. This donor is then used to restore an absent and more useful function that is no longer under UMN control. Synergistic function of the donor and recipient are helpful to subsequent physical therapy (motor re-education) and incorporation into activities of daily living.

Tendon transfers are tools well described in the field of hand surgery. Several guiding principles for tendon transfers have been established. (1) First is correction of any joint contracture. Tendon transfers are often biomechanically disadvantaged and will not be able to overcome a contracted joint. (2) The donor muscle must have adequate strength. Transferred muscles lose a grade of strength after transfer and thus must be strong preoperatively to successfully perform functional tasks postoperatively. (3) The donor muscle must be expendable. (4) Create a straight line of pull. To obtain the most strength, the most effective routing of muscle insertion to origin is a straight line. (5) The soft tissue bed must be stable. These surgeries must be performed in a supple bed with adequate skin coverage. Scarred beds will prevent tendon gliding and impair the result. (6) The donor muscle should have adequate excursion to perform the desired function. Finally, for people with SCI, spasticity must be considered. The donor muscle must have volitional control without too much tone. Overall level of spasticity can be improved with physical therapy and medications. A small amount of spasticity and tone is acceptable and sometimes beneficial to these reconstructive procedures.

In nerve transfer surgery, a relatively expendable functioning donor lower motor neuron (LMN) is transected and coapted to a nonfunctioning recipient within or below the level of SCI. Recipient dysfunction may be due to loss of UMN input with or without concomitant LMN involvement.29 Those with these more extensive injury patterns of LMN injury require more timely nerve transfer surgery to gain function. Once the surgery is completed, nerve fibers still have to regenerate from the transfer coaptation site at 1 mm/day to reach the target muscle. Muscles that are not reinnervated within 12 to 18 months will terminally degenerate and fibrose (see Figure 1).

Previous work, primarily in peripheral nerve injury, has contributed to our understanding of some of the unique attributes of nerve transfer surgery. Donor and recipient nerves that innervate muscles with very different biomechanical characteristics can be paired and coapted. One donor nerve may, with extensive therapy, motor re-education, and subsequent cortical remodeling, provide individually controlled separable recipient nerve functions. This has been most commonly described in radial nerve injury, where a single donor nerve successfully restored independent individual thumb and separable index, long, ring, and small finger extension.30 

In contrast to tendon transfer surgery, spasticity of the recipient muscles is not a contraindication to nerve transfer surgery. Spasticity of the muscles in the forearm and hand, in fact, suggests preservation of the LMN and prevents muscle atrophy. In people presenting even years post SCI, this may serve to preserve muscle bulk and function for successful restoration of UMN control by the nerve transfer procedures.31 

The goals of the preoperative evaluation are to (1) ensure biologic, psychologic, and social stability for semi-elective restorative surgery, (2) determine candidacy for nerve and/or tendon transfer, and (3) have a comprehensive and individualized discussion of treatment options and finalize the plan.

The initial history should review the general history of the initial SCI including time of injury, mechanism, associated injuries, surgeries (such as spine decompression and fusion procedures, tracheostomy, and treatment for other injuries such as fractures), and the course after injury (length of inpatient and rehabilitation facility stay). Determination of the course and extent of spontaneous recovery of function is imperative as this will affect the timing and type of surgical treatment. A thorough review of systems and pre- and post-SCI health issues is completed. See the eFigure, SCI Health History Form, provided as supplementary digital material (© 2014 Washington University in St. Louis, nervesurgery.wustl.edu. Used with permission). This health history form covers comorbidities and important information that will determine safe perioperative management of the person living with SCI. Additional questionnaires or measures such as a pain assessment tool, the Spinal Cord Independence Measure, and the Canadian Occupational Performance Measure may be helpful tools in discussing goals and planning surgery.

Additional questions to define expectations, goals, psychologic readiness, and social support will inform the discussion of the surgical treatment recommendations and perioperative course. Ensuring proper support for activities of daily living (particularly posttendon transfer), transportation, and other logistical support for postsurgery therapy (this may vary significantly depending on the practice setting and services available) is important. Finally, understanding the expectations of surgery (both of the person undergoing the surgery and their caretaker, friends, and family) will inform the recommendations for surgical treatment. Unrealistic expectations (such as a return to pre-SCI function) must be discussed in an empathetic but rigorous fashion. If all aspects of postoperative care are not optimized, delaying surgery must be considered.

Finally, extreme changes of function over time should be viewed as a red flag mandating additional exam or testing and a measured approach to surgical intervention. Those with improvement in motor function, specifically gain in new functions and not just improvement of strength, should be monitored over time. Early surgical intervention in the improving patient may burn bridges for future restoration of function and should be avoided. Loss of function, particularly in an ascending fashion, may indicate development or progression of a spinal cord syrinx or other neurodegenerative disease (secondary nerve compression, diabetic or other neuropathy, etc) and should be thoroughly investigated (such as with MRI).

The physical examination provides information on deficits and possible expendable motors. The patient should be evaluated in his or her chair with the power off/wheels locked. An assistant should be available to stabilize the trunk while the examiner pushes/pulls on the upper limb. A global assessment of overall physical fitness (including attention to the presence of any pressure sores, other skin breakdown, respiratory, pain, or other issues that might preclude safe general anesthesia and semi-elective surgery) should also be completed.

The examiner should note spasticity, contractures, and areas of allodynia. Although overall patterns of use and direct observation of functional activities should be done, we will limit the discussion to the more specific measures that permit preoperative planning.

The motor examination should proceed from proximal to distal with the goal to assess what are potential donors and what are the deficiencies. As stated earlier, donors must be strong and expendable. Manual muscle testing is fast and commonly used. However the Medical Research Council (MRC) grading system has limited reliability, especially for MRC grade 4.32 The underlying tenet is that the donor muscle must be strong or it will not provide useful work after transfer. A catalog of upper extremity function including shoulder stability and other muscles relevant to tendon and nerve transfer procedures should be performed (see Table 1).

The left and right side are examined separately as important differences are often seen. Careful exam includes palpation, observation, and manual muscle testing to avoid being misled by use of gravity, spasticity, and other compensatory moves.

Sensation is also an important piece of upper limb function. Providers have debated on the weight sensory deficits should be given in surgical planning. The examiner should be aware that if the patient cannot feel the hand, he or she would need to watch the limb to position and grasp.

The role of electrodiagnostic (EDX) and other preoperative testing is under development and primarily applies to those considering nerve transfer procedures.33 Both nerve conduction studies (NCS) and electromyography (EMG) provide information about putative donor and recipient motor units.

NCS provide information about the degree of LMN involvement. In particular, the compound muscle action potential (CMAP) and sensory nerve action potential (SNAP) reflect the number of motor or sensory fibers, respectively, present in the tested nerve segment. Absent or nonrecordable CMAPs (with normal SNAPs) suggest direct and complete LMN injury or involvement at the level of the anterior horn of the spinal cord. This information is critical to determining eligibility for nerve transfer surgery, as evidence of LMN at the level of the recipient motor unit would preclude late (>12–18 months post SCI) nerve transfer; the person would still be eligible for tendon transfers.

EMG testing of specific muscles provides information about denervation, reinnervation, and volitional control. Muscles with signs of acute denervation, such as fibrillations and positive sharp waves on needle insertion, require timely restoration of LMN input. Muscles with signs of reinnervation, such as motor unit potentials (MUPs), are under UMN control and are recovering. Although the degree of recovery cannot be accurately predicted, the presence of MUPs suggests intact UMN volitional control in these muscles. Performing nerve transfers into reinnervating muscles is typically not done because it would use up one of the very limited expendable donors and the patient may recover useful function spontaneously without the need for surgical intervention.

Finally, EDX provides information about co-existing peripheral nerve processes such as a concomitant brachial plexus injury or compressive neuropathy that may affect treatment with either nerve or tendon transfer surgery.

Our current working protocol for EDX in the setting of those with SCI considering nerve transfer surgery is included in Table 2. We typically use EDX to determine if individuals presenting >12 months post SCI are candidates for late nerve transfer surgery. For example, if the radial CMAP recorded in the forearm to EIP (extensor indicis proprius) segment is zero or nonrecordable in someone presenting years post injury, then the supinator to PIN nerve transfer surgery is not an option. Finally, intraoperative direct neuromuscular stimulation of donor and recipient units is used to augment the EDX findings as EMG, in particular, provides qualitative not quantitative information about muscle denervation.34 

The functional goals for most mid-cervical SCI upper limbs can be divided into three main categories: elbow extension and hand opening and closing. The surgical strategy is individualized to each limb. This article will not cover the details of the procedures but will provide information on the most common approaches. Both tendon and nerve transfer procedures will be discussed.

The surgery differs for tendon and nerve transfers. For a tendon transfer surgery, the incisions are generally more extensive to permit mobilization of the appropriate donor and recipient tendons; additional surgical sites for tendon graft harvesting may be needed (eg, the deltoid to triceps tendon transfer surgery often requires harvest of tendon graft from the thigh). The donor tendon is freed off of the bone and surrounding tissue to permit mobilization and attachment to the recipient tendon. The tendons are woven or almost braided into each other. Advances in the tendon repair have allowed for earlier mobilization after surgery,35 but weightbearing and sports are usually restricted for several months after tendon surgery (see Figure 2). In nerve transfer surgery, the incisions may be more limited. The nerves are identified and dissection of the donor and recipient nerve ends is carried out for a few centimeters. The ends are sutured to each other using an operating room microscope and microsutures that are approximately the size of a hair. There is no tension across the repair; this permits early mobilization, as the muscles and tendons are left in their normal position. Of note, the nerve fibers grow distally from the coaptation site to the recipient muscle; this does take time given the long distance from coaptation to muscle recipient in most cases (see Figure 3).

Elbow extension is highly important for the patient with tetraplegia. For a person who uses a wheelchair, lack of functional elbow extension results in a much-reduced reachable environment. In addition, stability of the elbow is required to obtain strong pinch and grasp.

There are two primary tendon transfer techniques to restore elbow extension: (1) biceps to triceps and (2) posterior deltoid to triceps. Biceps to triceps is the procedure of choice if there is a concomitant elbow flexion contracture.36 Both procedures require several weeks in a cast to prevent stretching of the repair.

Restoration of elbow extension with nerve transfer can be performed by using some portion of the axillary nerve branches to the deltoid musculature.19,26,37 It is important to note that certain nerve transfers to restore triceps function may preclude later tendon transfer procedures. For example, use of donor nerve branches to the posterior head of the deltoid muscle in a nerve transfer will result in denervation and preclude secondary deltoid to triceps tendon transfer if the nerve transfer was unsuccessful. The biceps to triceps tendon transfer could still be performed, but only if the nerve to the brachialis had not been used because that would sacrifice all the primary elbow flexors.

The choice of pinch reconstruction varies depending upon the available resources. For weaker people without a functioning brachioradialis (BR), there are no good options for restoration of hand function using tendon transfers. For them, surgical reconstruction relies on augmenting the thumb tenodesis. This Moberg procedure anchors the flexor pollicis longus (FPL) to the distal radius, tightening the tenodesis.38 The tenodesis requires strong wrist extension. Thus the first reconstructive goal is to ensure wrist extension, which can be obained by BR to ECRB tendon transfer. For stronger patients, the BR can be transferred to the FPL to power the pinch. For successful pinch, the pulp of the thumb must meet the radial side of middle phalanx of the index finger. Other procedures such as stabilizing the thumb interphalageal (IP) joint39 and fusing the carpometacarpal (CMC) joint are often required to optimize thumb position.

People with two strong elbow flexors (biceps and brachialis only; no brachioradialis) can undergo nerve transfer procedures to restore pinch by transfer of the nerve to brachialis to the anterior interosseous branch of the median nerve.16,17,23 The biceps muscle remains to maintain strong elbow flexion. Use of the nerves to the extensor carpi radialis brevis or brachioradialis as donors to the anterior interosseous nerve (AIN) has also been described.15 

The more resources a patient has, the more potential functions can be reconstructed. Additional functional muscles such as pronator teres, extensor carpi radialis longus, or flexor carpi radialis can be used in tendon transfer surgery to power finger flexion. These tendon transfer procedures require weaving of the single donor tendon into the finger profunda flexor tendons. This provides composite or grouped finger flexion.

Nerve transfers to restore finger flexion or grasp are typically combined with the previously noted “pinch” transfer into AIN. The median nerve branch to the flexor digitorum superficialis muscle may be included as a recipient to restore additional finger flexor function.14,16 

Most patients do not have active extension of fingers and thumb. Tendon transfers (FCR to finger and thumb extensors) can be performed, but most patients require augmenting hand opening with tenodesis procedures due to the absence of expendable donors. Historically this was done as a separate procedure and then the closing phase was performed as a second stage. Friden has advocated a single stage pinch/grasp and opening reconstruction with his “alphabet procedure” to minimize the patient's down time.40 

The supinator muscle is innervated and functions in mid-cervical level SCI. Its biomechanical properties preclude its used in tendon transfers, but its nerve may be used as a donor. The two nerve branches to the supinator muscle can be transferred to the posterior interosseous nerve to restore thumb abduction and digit extension,19 and it can also serve to augment weak wrist extension.

Most patients with tetraplegia lack intrinsics and have resulting hyperextension of their metacarpophalangeal (MP) joints with a resulting claw hand. (The intrinsic muscles flex the MP joint and extend the IP joints.) Thus to obtain grasp, the hand posture needs to be improved or the finger IP joints will flex first while the MPs remain straight, pushing any object out of the palm. There are several procedures to adress this, including the Zancolli lasso and the House substitution.41,42 Nerve transfer procedures to restore intrinsic function of the hand are generally not possible due to the distance between the available donor nerves and the target musculature.

Therapy is an integral part of the treatment of people with SCI and may be helpful both pre- and postoperatively. Preoperatively, a careful exam, as noted above, done in conjunction with a therapist is incredibly helpful to multidisciplinary planning. Additional preoperative therapy for evaluation and treatment of joint stiffness, discussion of options, and further education is often helpful. Postoperative therapy, time course of recovery, and outcomes differ for tendon and nerve transfer surgery and will be described separately.

After tendon transfer surgery, there is a time that the repairs must be protected. Early motion can be initiated in a supervised therapy setting to reduce swelling and allow gliding, but the patient is otherwise in a splint to protect the repair for several weeks. However, for those who are discharged home and have more limited access to therapy, the postoperative splint may be left in place for 2 weeks and then a cast is applied for 2 additional weeks. For most tendon transfer surgeries, the use of a manual wheelchair, shifting of the body weight onto the hands, and sports activities are restricted for 2 to 3 months postoperatively. Therapy includes all modalities to retrain the patient, and modalities such as electrical stimulation and biofeedback therapy have been used with improved results.

These procedures are well tolerated. Common complications consist of imperfect tensioning of the repairs or inefficient pinch due to poor position of thumb (eg, thumb is positioned in a too adducted posture). A systematic review attempted to quantify average results and found a range of results depending on exact procedure type (1.17 to 2.32 kg of pinch).43 Typical results for a tendon transfer surgery include writing and holding a drink can.

Because the nerve transfer coaptations are completed without tension, immediate use of the upper extremities for light activities of daily living is permitted. Typically, no splint, sling, or other immobilization is required. A simple airstrip Band-Aid–type dressing is applied and removed 48 hours after surgery.

In the first 2 to 4 weeks after surgery, repetitive activities at the surgical site are avoided. For example, manual wheelchair users are asked to limit elbow flexion–powered propulsion or to switch to an electric wheelchair to avoid seroma formation. Weightbearing for transfers is permitted when pain and healing permit. (Immediately after surgery, the arm may be used for support but not for vigorous pulling or pushing that might cause skin incision opening.) Sports and weightlifting are initially avoided to permit skin healing and can be resumed at about 4 weeks post surgery. These are the only formal limitations on function. Remaining existing upper extremity functions may be used.

At 1 month post surgery, formal therapy is instituted for motor re-education. This means exercises geared toward over-firing the donor, starting donor and recipient co-contracture activities, and detecting early reinnervation. This is followed by intermittent visits (once every 1 to 3 months post surgery for 1 to 2 years or more) and a focused and advancing home exercise program.

Time is required to see results because the nerve must regenerate from the transfer coaptation site down the new pathway and reinnervate the musculature, and then the brain (though cortical remodeling) must adapt to the new, rewired patterns. During this long period, all presurgical activities may be resumed. Signs of new gain in function are followed closely, exercises are continued for strengthening and motor re-education, and integration of new functions into daily activities (such as self-catheterization) is completed over years post surgery. Similar to work in the peripheral nerve injury population, improvement in function including increased strength and donor independent activation of recipients (or separation of the donor from recipient function and ability to achieve independent cortical control of that new function) is seen even years post surgery.44 

For example, in people who underwent nerve transfer to restore hand opening and closing, changes occur at the earliest at about 3 (for opening) and 8 to 12 months post surgery (for closing). Augmented tenodesis-type function progresses to tenodesis independent digit motion and incremental gains in tone and actual pinch and grip strength.

The outcomes after nerve transfer surgery are highly variable15,16; one case report describes a gain of up to 2.5 kg of pinch and 7 kg of grip.20 However, most others report outcomes after nerve transfer of much less gain in power than this. Results for a nerve transfer surgery include the ability to open a childproof medicine bottle.

Both nerve and tendon transfer surgeries produce gains in function and are valuable techniques that may be used alone or in combination. Augmenting the armamentarium of available treatment options provides individuals with choices that can be tailored to their goals and preferences (see Figure 4). Further comparative work and information about the long-term outcome of the nascent use of nerve transfer are needed.

Both are established, well-tolerated, and covered-by-insurance treatments that can provide gains in function for those living with cervical level SCI. These options should be discussed and made widely available even as concomitant efforts proceed to develop reliable neuroprosthetics and develop the cure.