Here, we present a protocol for the motor rehabilitation of patients with severe nerve injuries and selective nerve transfer surgery. It aims at restoring the motor function proposing several stages in patient education, early-stage therapy after surgery and interventions for rehabilitation after successful re-innervation of the nerve’s target.
After severe nerve injuries, selective nerve transfers provide an opportunity to restore motor and sensory function. Functional recovery depends both on the successful re-innervation of the targets in the periphery and on the motor re-learning process entailing cortical plasticity. While there is an increasing number of methods to improve rehabilitation, their routine implementation in a clinical setting remains a challenge due to their complexity and long duration. Therefore, recommendations for rehabilitation strategies are presented with the aim of guiding medical doctors and therapists through the long-lasting rehabilitation process and providing step-by-step instructions for supporting motor re-learning.
Directly after nerve transfer surgery, no motor function is present, and therapy should focus on promoting activity in the sensory-motor cortex areas of the paralyzed body part. After about two to six months (depending on the severity and modality of injury, the distance of nerve regeneration and many other factors), the first motor activity can be detected via electromyography (EMG). Within this phase of rehabilitation, multimodal feedback is used to re-learn the motor function. This is especially critical after nerve transfers, as muscle activation patterns change due to the altered neural connection. Finally, muscle strength should be sufficient to overcome gravity/resistance of antagonistic muscles and joint stiffness, and more functional tasks can be implemented in rehabilitation.
Selective nerve transfers provide an opportunity for restoring the motor function after nerve injuries when recovery by the use of neurolysis, nerve repair, or nerve grafting cannot be expected1,2. Possible indications for nerve transfers are severe distal nerve injuries, avulsion-type injuries, the lack of available nerve roots for grafting, the extensive scarring at the injury site and delayed reconstruction3,4. Following motor nerve injury, reconstruction is time-critical as degeneration of muscle tissue and motor end plates only allow for the successful muscle re-innervation within 1-2 years after injury5,6. Here, nerve transfers provide the advantage of a relatively short re-innervation time after surgery, as they allow nerve coaptation close to the target. This procedure, also known as neurotization, involves the surgical redirection of an intact nerve (donor nerve) to the distal part of the recipient nerve. As this connection is distal to the damaged site of the recipient nerve, it allows bypassing the injured nerve segment7.
As neural pathways are altered after nerve transfer surgery, patients cannot be treated with standard post-operative therapy protocols otherwise used after direct nerve repair8,9. While donor axons grow into the new target, they take over a function they did not have before while cortically still being connected to their original function. As an example, the Oberlin ulnar nerve transfer is used to restore elbow flexion after irreparable damage to the upper trunk or nerve roots C5 and C61. As shown in Figure 1, it involves transferring one or more ulnar nerve fascicles to the musculocutaneous motor branch of the biceps muscle10. However, after the successful re-innervation, these fascicles of the ulnar nerve are cortically still connected to their previous function of finger flexion and/or ulnar abduction and flexion of the wrist. On a functional level this implies that at the beginning of the rehabilitation, the patient needs to focus on the previous nerve function (hand closing) in order to activate and strengthen the recipient muscle (biceps contraction). This approach is also known as “donor activation focused rehabilitation approach”9.
Figure 1: Schematic illustration of the functional principle of an ulnar to musculocutaneous nerve transfer. (A) In a healthy person, there is a clear separation between activity in the motor cortex for functions of different nerves/joints as here the musculocutaneous nerve (red) and the ulnar nerve (blue). (B) After an injury of the musculocutaneous nerve, the biceps muscle cannot be activated, while the uninjured ulnar nerve (in blue) still functions. (C). After the Oberlin’s nerve transfer and re-innervation, fascicles of the ulnar nerve control the biceps muscles as well as all other muscles anatomically innervated by the ulnar nerve. Before cortical reorganization occurs, both muscles are activated together as there is no cortical separation between these nerve fibers (in blue). (D) With successful rehabilitation, the patient has learned to use certain cortical axons for “normal” ulnar nerve functions (in blue), while others (in purple) are now controlling the biceps muscle. This allows independent movement of both muscle groups. Please click here to view a larger version of this figure.
While comprehension of this concept is the foundation of successful rehabilitation, re-learning of new motor patterns can be challenging for patients and clinicians. This is due to the long duration of rehabilitation, the complexity of nerve regeneration and re-innervation and the limited amount of directly observable muscular activity during early re-innervation8. Apart from the changes in the peripheral nervous system, there is an increasing awareness among surgeons and therapists for the relevance of changes in the central nervous system (CNS), i.e., re-organization of the hand motor and sensory cortical areas occurring as a consequence to denervation11. When neural input to the CNS is deprived, the associated cortical area diminishes to a certain extent at the expense of adjacent areas12. Restoration of function, therefore, depends on the central recovery of its representation in the brain. Within the last years, the use of biofeedback methods8 and approaches to support cortical re-organization13,14,15 has led to extended possibilities in rehabilitation after nerve transfers. However, due to the complexity of post-surgical therapy, it is important to provide the right interventions at the right time13.
Therefore, the aim of this structured protocol for rehabilitation after selective nerve transfers is to provide a feasible and holistic approach to support motor recovery. It is based on current recommendations and the authors’ experience with incorporating it in a clinical setting. The protocol is meant to guide medical doctors, occupational and physical therapists as well as other health professionals through the long-lasting rehabilitation process.
This structured protocol for motor rehabilitation was evaluated in a feasibility study8 in five patients with brachial plexus injuries as shown in Table 1. All of them received several nerve transfers (some in combination with nerve grafts) to restore upper extremity function. Therefore, for the sake of clarity, when describing specific interventions in this protocol, they refer to the upper limb. In detail, we take the Oberlin ulnar nerve transfer10 as an example, which was performed in patients 1-3. For this, we refer to parts of the ulnar nerve as being the donor nerve and the musculocutaneous nerve being the recipient nerve. Thus, the biceps and brachialis muscles are the recipient muscles being re-innervated by parts of the ulnar nerve. Functionally, this means that following a donor activation focused approach9, movements associated with ulnar nerve activity (such as hand closing or ulnar abduction of the wrist) are used for the activation of the biceps muscle directly after re-innervation. However, exercises based on this approach can be performed in other body parts as well. If special considerations are necessary to implement this in other body parts (e.g., the lower extremity), this is pointed out within the protocol.
Independent from the body part affected, therapy sessions should not exceed 30 min as muscles become easily fatigued shortly after re-innervation8 and successful training requires a patient’s full commitment and focus.
Recently, nerve transfers have been increasingly used to restore function after severe proximal nerve injuries with promising outcomes1,4,31,32. However, while there is a consensus that structured training programs are necessary to promote beneficial neuroplastic changes33,34,35, there is no structured protocol available to describe motor rehabilitation approaches after nerve transfers step-by-step. Therefore, the aim of the presented protocol was to provide detailed instructions for post-surgical rehabilitation to embrace cortical changes and enhance surgical outcomes. In contrast to other protocols9,36, visualization of muscular activity via surface EMG biofeedback is a key element in the presented protocol.
Within therapy, patient education is a critical step as the patient needs to understand the rather complex surgical procedure and be educated on activities improving the health status in order to be actively involved in the long rehabilitation process8,13,37. There is broad agreement that repetition is fundamental and daily home exercises are needed to reinforce a well-established cortical representation of the hand8,34,38,39. Apart from pure patient information, the authors strongly recommend a patient-centered approach for rehabilitation. This additionally involves treating the patient as a unique person, the involvement of the patient in care, good clinician-patient communication and empowering the patient. In medical rehabilitation, this approach positively influences patient satisfaction and outcomes40. Regarding the motor rehabilitation itself, it is recommended to start interventions before re-innervation of the muscles and to follow a donor activation focused approach9. To ensure that muscular activity is detected as early as possible, EMG biofeedback devices can be used. While the authors are aware that EMG biofeedback devices are not yet clinical standard, their use is highly recommended as they allow to start early active motor rehabilitation and provide valuable feedback on newly re-innervated muscles8.
The principles described within this protocol can be applied for different types of nerve transfers, although modifications within the protocol might be necessary. While motor re-learning is relatively easy if synergistic muscles/nerves were used, the use of antagonistic muscles/nerves requires a longer rehabilitation time and the use of biofeedback might be of even greater importance3,8. Especially in those cases where a higher amount of repetitions is needed, future protocols might also include serious games to maintain patient motivation41.
As the timing of nerve regeneration and the amount of recovery hugely depends on the injury and surgical interventions, there is no strict timeline for rehabilitation. Instead, the therapist is asked to proceed depending on the signs of motor recovery as stated in the protocol. In the same way, it is important to note that the success of nerve transfer surgery is based on many factors including type and severity of the injury, the surgeon’s skills, and expertise as well as the patient’s age, health status, cognition and motivation8,13,42,43. While rehabilitation is a main pillar for regaining function after severe nerve injuries, even the best program for motor re-education cannot improve function, if there are inadequate peripheral nerve regeneration and muscle re-innervation. Thus, the authors strongly recommend seeing the patients regularly together within a multidisciplinary team to be able to discuss if recovery goes as expected or if any additional medical interventions are necessary. However, especially after severe injuries such as C8 and Th1 nerve root avulsions, realistic outcomes might not include full recovery of extremity function3,30. In these cases, the clinical team needs to communicate this to the patient as soon as a realistic prognosis can be stated (approximately one year after the nerve transfers). At this point, further possibilities in rehabilitation, assistive devices or surgical interventions (as tendon transfers) need to be discussed. In cases, where absolutely no hand function returns, replacing the functionless limb with a prosthetic device can be considered as an option as well44,45. This is, however, only recommended as a last resort and after in-depth physical and psychological assessment46.
While the focus of peripheral nerve surgery usually lies on the reconstruction of motor function, sensory nerve transfers are sometimes used to restore the sensation in the hand after severe median or ulnar nerve injury4,47. Similar to motor nerve transfers, this creates altered sensory neural pathways and results in sensations that are felt as if they were originating from the previous innervation area of the donor nerve. Even if no sensory nerve transfers were performed, there can still be changed/reduced sensation either due to the injury itself27 or due to donor-side morbidity48. In these cases, timely re-education can help to improve the sensory function49, and reduce unwanted hyper-sensitivity and pain that often occurs after such injuries. To ensure good motor and sensory function, the authors strongly recommend complementing motor re-education with tailored therapy approaches to promote re-organization in the corresponding sensory cortex as well39,50,51. Regarding sensory re-education, it is recommended to start interventions before re-innervation of the skin49,52,53. This can include substitution of sensation by other senses as vision53 or auditory feedback54, as well as making use of the overlap of sensory innervation areas27,52. As soon as the patient has regained a certain amount of sensitivity, tactile gnosis and object recognition can be trained, while maintaining a high amount of sensory input34. Typical materials that can be used for this, include self-made plates with different surfaces to be recognized with closed eyes (see Figure 2) or a box filled with beans/lentils/rice (see Figure 3).
Figure 2: Different surfaces can be used to support regaining of sensibility. Usually, the patient is asked to touch these with both hands first, while he/she might try afterwards to recognize the different surfaces without vision using only the hand with limited sensibility. Please click here to view a larger version of this figure.
Figure 3: A box filled with rice for sensory re-education of the hand. In therapy, the patient might put his/her hand with reduced sensitivity carefully in this box and slowly move the hand. To focus the patient’s attention, the therapist can put some small objects (e.g., wooden blocks or paper clips) in this box and ask to find them without visual control. Please click here to view a larger version of this figure.
However, in both sensory and motor re-education, there is only limited evidence regarding the choice of interventions needed to promote good recovery34. This limits the validity of the proposed rehabilitation protocol, as for other protocols. While the described protocol was assessed within a feasibility study and motor outcomes were similar or slightly better than those reported in the literature8, this study was performed on a small sample size and without a control group. This makes it impossible to compare the outcomes, advantages, and disadvantages of this protocol with respect to previous ones. Further research needs to include controlled studies in order to compare the possible advantages of using surface EMG biofeedback to conventional approaches.
The authors have nothing to disclose.
This study was funded by the Christian Doppler Research Foundation of the Austrian Council for Research and Technology Development and the Austrian Federal Ministry of Science, Research and Economy. We thank Petra Gettinger for her assistance in the preparation of filming and Aron Cserveny for the preparation of the illustrations included in the manuscript and the rehabilitation leaflet. Frontiers in Neuroscience granted permission for reproducing the data presented in the original paper.
EMG electrodes | Otto bock Healthcare, Duderstadt, Germany | electrodes 13E202 = 50 | The EMG electrodes used in this study were bipolar and included a ground and a 50 Hz filter. They were used with the Moby. |
Folding Mirror Therapy Box (Arm/Foot/Ankle) | Reflex Pain Management Therapy Store | This box was used for mirror therapy. | |
Myoboy | Otto bock Healthcare, Duderstadt, Germany | Myoboy | This EMG Biofeedback device that can be used as stand alone device or with a computer. While this device was used in the presented pilot study, other (cheaper) devices for sEMG biofeedback training are available as well. |
Recognise[TM] Flash Cards | noigroup | If no self-made cards for left-right discrimination are used, these can be purchased from noigroup.com. There, a mobile app for training is available as well. |