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DOI: 10.1016/J.JHSB.2005.10.017 © 2006 The British Society for Surgery of the Hand
Improved Sensory Relearning after nerve Repair Induced by Selective Temporary Anaesthesia – A New Concept in Hand RehabilitationFrom the Department of Hand Surgery, Lund University, University Hospital Malmö, Malmö, Sweden Correspondence: Mrs Birgitta Rosén, Department of Hand Surgery, Malmö University Hospital, SE-205 02 Malmö, Sweden. Tel.: +40 40 33 67 69; fax: +40 40 92 88 55. E-mail: birgitta.rosen{at}med.lu.se
The outcome after nerve repair in adults is generally poor. We hypothesized that forearm deafferentation would enhance the sensory outcome by increasing the cortical hand representation. A prospective, randomized, double-blind study was designed to investigate the effects of cutaneous forearm anaesthesia combined with sensory re-education on the outcome after ulnar or median nerve repair. During a 2 week period, a local anaesthetic cream (EMLA®) (n = 7) or placebo (n = 6) was applied repeatedly onto the flexor aspect of the forearm of the injured arm and combined with sensory re-education. Evaluation of sensory function was carried out at regular intervals and at 4 weeks after the last EMLA®/placebo session. The EMLA®group showed significant improvement compared to placebo in perception of touch/pressure, tactile gnosis and in the summarized outcome after 6 weeks. These results suggest that cutaneous forearm anaesthesia of the injured limb, in combination with sensory re-education, can enhance sensory recovery after nerve repair.
Key Words: nerve injury • anaesthesia • sensory relearning • hand function
The outcome after a peripheral nerve injury and repair depends on several factors, both in the peripheral and central nervous system (Lundborg, 2003, 2004). In spite of refined surgical technique, the clinical outcome in adults is generally poor with persisting sensory dysfunction and pain problems (Lundborg, 2003, 2004). A major reason for this is the profound cortical functional changes which are induced by a peripheral nerve injury, based on the misdirection of regenerating axons which follows surgical repair (Chen et al., 2002; Lundborg, 2004). Generally, children with nerve injury have a better functional outcome, presumably because of the superior ability of the young brain to adapt to the cortical reorganization. This adaptability is reduced, although not lost, in the older brain (Almquist et al., 1983; Birch and Raji, 1991; Lundborg, 2004; Lundborg and Rosén, 2001). The "new language" that the hand speaks to the brain after a nerve repair is difficult to interpret and the functional result – impairment in tactile gnosis (functional sensibility) – is a serious problem for the patient, taking into account the accompanying motor and pain problems (Jerosch-Herold, 2000; Lundborg et al., 2004; Rosén, 1996; Wynn-Parry, 1986). Therefore, we have to look for new ways to improve the outcome after nerve repair, focusing on the central nervous system. Strategies to improve the functional results should focus on a refinement of current sensory re-educational programmes in consideration of evolving neuroscientific concepts, utilizing the capacity for rapid and long-term cortical remodelling that is possible not only in the young brain but also in the adult brain (Chen et al., 2002; Lundborg, 2004; Rosén et al., 2003; Wall et al., 2002). Experimental deafferentation using tourniquet-induced anaesthesia, or an anaesthetic block, has been shown to induce cortical changes in both brain hemispheres (Calford and Tweedale, 1990; Chen et al., 2002; Werhahn et al., 2002a, b). In healthy persons and patients with peripheral nerve injuries, a temporary deafferentation of one hand with a nerve block, or a tourniquet, induced a rapid improvement in hand function on the contralateral side (Bjorkman et al., 2004b; Werhahn et al., 2002b). Selective deafferentation may also have effects on sensorimotor functions in the ipsilateral arm. Anaesthetic block of upper cervical roots in stroke patients results in increased grip strength in the hand being innervated by the lower cervical roots (Muellbacher et al., 2002). By analogy, a selective cutaneous anaesthesia of the forearm on healthy persons has been shown to induce improved hand sensation in the ipsilateral hand (Björkman et al., 2004a). This is probably due to expansion of cortical territories adjacent to the denervated forearm representation, including the hand representation (Björkman et al., 2004b; Muellbacher et al., 2002; Werhahn et al., 2002b). Our hypothesis was that deafferentation of the forearm would also allow an expansion of the cortical representation of the adjacent hand in nerve-injured patients and that this might enhance the effectiveness of sensory re-education. Accordingly, the aim of the present study was to investigate the effects on sensory hand function of repeated selective limited deafferentation of the forearm, in combination with sensory reeducation, in patients with median and/or ulnar nerve injuries at wrist level.
Thirteen patients with median (n = 7) or ulnar (n = 6) nerve injuries at wrist level (ten men and three women, of median age 38.2 (range 19–75) years) participated in the study. Some protective sensation at fingertip level, as assessed with Semmes–Weinstein monofilaments, was a prerequisite for participation. Mean time since surgery was 22 (range 11–52) months. The local ethics committee approved the study design and written informed consent was obtained from all participants. The study design was randomized, double blind, and the study subjects were randomized, using sealed envelopes, to receive either a local anaesthetic agent containing 2.5% lidocaine and 2.5% prilocaine (EM-LA®, AstraZeneca, Södertälje, Sweden) or a placebo of an oil and water emulsion. Prior to the randomization, a medical history was taken, with special emphasis on adverse effects from the use of local anaesthetic agents, including allergic reactions. The two agents were identical in colour, consistency and packaging. The EMLA®, or placebo, was applied under occlusive bandage for 1 hour to the flexor aspect of the forearm, in an area running proximally from the wrist for 15 cm, on the same side as the nerve injury. Seven patients received EMLA®(three women and four men, five median and two ulnar nerve injuries, median age 29 (range 19–75) years) and six patients received placebo (six men, two median and four ulnar nerve injuries, median age 39 (range 29–50) years). The participants received EMLA®, or placebo, twice a week for two consecutive weeks combined with an intense sensory reeducation programme with assisted supervised training during 1 hour while under the influence of EMLA®, or placebo, and strictly scheduled home training (Fig 1).
The training was standardized and performed according to principles described by Wynn-Parry and Salter (1976) and Dellon (1981), with, and without, the use of vision and under concentration. Exercises to identify textures, shapes and real objects were performed. The participants were instructed not to touch the forearm and the forearm was also covered with a dressing. After 1 hour, the EMLA®, or placebo, was carefully washed off. Over and above this, the participating patients had a training protocol during the period of the study. In order to stimulate compliance in home training and to standardize the training, we designed a new training device. A miniature Rubik’s cube was adapted in such a way as to remove one colour and 8 mm holes were drilled instead, giving one side with holes. The patient could practise with the cube and continuously change the surface pattern by twisting the cube (Fig 2). The cube being small can easily fit into a pocket and, hopefully, stimulate the patient to use it for practise, ensuring continuous training over a longer time. A written training protocol was given to each patient, including a minimum training frequency of 5 session/day with the cube. The patient was expected to record every performed session. All patients were also encouraged to use the affected hand very consciously for daily activities.
Assessment of Hand Function Assessment of hand function was performed in a standardized manner, according to the Model for Documentation of Outcome after Nerve Repair, including separate domains for sensory/motor/pain-discomfort and also a "total score" (Rosén and Lundborg, 2000). Since the study primarily addressed tactile gnosis, sensory testing was of primary interest. Semmes–Wein-stein monofilaments (SWM) were used for assessment of perception of touch. The summarized SWM measure points were the three "critical sites" described by Bell-Krotoski (ASHT, 1992; Bell-Krotoski, 2002; Rosén and Lundborg, 2000, 2003), i.e. pulps of the thumb and the index finger and proximal phalanx of the index finger in median nerve injuries, and pulp of the little finger, proximal phalanx of the little finger and proximal hypothenar eminence in ulnar nerve injuries. The STI-test (shape–texture identification test) (Rosén and Lundborg, 1998; Jerosch-Herold, 2005) and classic static 2PD (DiskCriminator®) (ASHT, 1992) were used for assessment of tactile gnosis. Assessments were performed according to standardized procedures and 2PD testing was carried out according to the "Moberg Method" (Moberg, 1991), described by the ASSH and ASHT (ASHT, 1992). The test is carried out in descending order, starting with 15 mm to assess the level at which responses were correct (7 out of 10 correct at just blanching of the skin), and quantification 0–3 (0 =  16 mm, 1 = 11–15 mm, 2 = 6–10 mm, 3 = <6 mm) (ASHT, 1992). Assessments were performed prior to the experiment and after 1 week training (prior to the third EMLA®/placebo application). A third test was done after the fourth application of EMLA®/placebo after 2 weeks training. A follow-up with tests, 4 weeks after the last EMLA®/placebo session, was also done (Fig 1).
Statistics
Level for significance was P
Perception of touch, measured with SWM, improved significantly in the EMLA®group between baseline assessment and 6 weeks later. In the placebo group, no significant changes were seen (Table 1).
Tactile gnosis was improved in both groups, with significantly better results already after 1 week training (Fig 3a,b). In STI-testing, P-values were 0.02 and 0.05, respectively, in the EMLA®and placebo group. Two-point discrimination improved significantly only in the EMLA, group at this point (P = 0.04) (Fig 3a,b). The group comparison showed that the tactile gnosis improvements were significantly better in the EMLA® group after 1 week (P = 0.03) (Table 1). The improvements remained for at least 4 weeks after the last EMLA®/placebo session and were also, at this point, significantly improved in both groups, but significantly better in the EMLA® group (Fig 3a and b and Table 1).
The "total score" of outcome, representing the summarized outcome from sensory, motor and pain/discomfort domains, showed a significant improvement between assessments before the study start and assessments after 4 weeks after the last session of EMLA®/placebo in the EMLA® group, as compared to the placebo group (Table 1). There were no side-effect in either the EMLA or the placebo group.
In this study, we showed a significant improvement in tactile gnosis (functional sensibility) in patients who had received a local anaesthetic cream (EMLA®) on the forearm in combination with intensive sensory reeducation, compared to those who received intensive sensory re-education but, only, a placebo cream applied to their forearms. All patients improved their tactile gnosis, presumably as a result of the intensive sensory re-education alone, but the EMLA®group was significant better than the placebo group (Fig 3a,b). The cortical representation of body parts is constantly changing in response to stimuli in the environment. An ulnar or median nerve injury leads to a bilateral cortical reorganization with expansion of adjacent, functionally intact, areas over the cortical area previously corresponding to the injured nerve (Chen et al., 2002; Lundborg, 2004). During the regeneration and re-innervation phase after a nerve repair, the injured nerve gradually tries to reclaim its original cortical area. However, because of axonal misdirection, a new and changed cortical representation of the target area belonging to the injured nerve is created. This changed cortical map and the corresponding difficulties for the brain in processing and interpreting the signals from the periphery have been postulated as major reasons for the usually poor outcome after nerve repair (Dellon, 1981; Lundborg, 2004; Wynn-Parry, 1986). Experimental hand deafferentation in the form of tourniquet-induced anaesthesia has been shown to improve contralateral hand function, both in healthy and nerve-injured persons (Björkman et al., 2004b, 2005). Tourniquet-induced anaesthesia, where the whole contralateral hand is anaesthetized and motor control is also lost, is a difficult method to use in a clinical setting, mostly because it causes pain. Selective deafferentation of the flexor aspect of the forearm in healthy persons has been shown to, significantly, improve hand function in the same side (Björkman et al., 2004a) and is, here, shown to have an effect, also, in nerve-injured patients. This method has clear advantages over tourniquet-induced anaesthesia. The tourniquet-induced anaesthesia is painful and can, therefore, not be combined with active training. In a clinical setting, selective anaesthesia of the flexor aspect of the forearm is easily accomplished. It can even be done by the patient himself. An advantage is that the selective anaesthesia does not affect the motor function of the hand. This is important in the context of the patient being able to use the hand while anaesthetized, thereby integrating sensory and motor re-learning. Repeated anaesthesia of the forearm should, hypothetically, keep a larger cortical area available for the injured hand and this, in turn, would increase the brain’s ability to interpret the signals from the territory of the injured nerve. This may open "a window of opportunity", during which it is possible for sensory reeducation to have a better, and more long lasting, effect. In this study, EMLA®was applied twice a week during a 2-week period. This is a small study, but we felt it interesting to apply this new concept in a homogeneous group of adult patients with major nerve injuries, since the clinical problem is most apparent in this group. The results were analysed accordingly and were very convincing. However, the optimal frequency for application is yet to be determined in future larger studies. This is a new and original concept, which may enhance the effect of sensory re-educational programmes. Interestingly, the effect may be long-lasting since the improvement in tactile gnosis persisted for at least 4 weeks after the last EMLA®treatment. Investigations have been initiated to clarify the long term effects. Tactile gnosis is a vital component in functional sensibility and one may ask if a change in tactile gnosis is a real improvement of functional sensibility. It has been demonstrated that the minimal detectable change (MDC) for the STI-test is an improved score of 1.2 (Rosén, 2003). Here, the median improvement between pre-test values and the 1, 2 and 4 week follow-up test values in the EMLA®group exceeded 2 points in the STI-test, thus representing true changes in tactile gnosis. This is in contrast to the improvement in the control group, who showed a median improvement of only 1 point (Fig 3a). The fact that we could see a significant improvement in "total score", i.e. the summarized outcome of sensory, motor and pain/discomfort, in the EMLA®group is interesting but, probably, mainly due to the "sensory domain" improvement. An earlier study has shown that "total score" correlates well with the patient’s subjective opinion on how much the nerve injury affects activities of daily living (Rosén and Lundborg, 2000). In a previous study, we have used fMRI technique to demonstrate that experimental deafferentation of an extremity results in rapid cortical reorganization, with a parallel increase in grip force in the contralateral hand (Bjorkman et al., 2004b). In this study, we concentrated on sensory functions. We hypothesize that the observed enhancement in sensory functions induced by cutaneous anaesthesia is also based on functional reorganizations in the central nervous system. We do not know, at present, whether these hypothesized changes occur solely in the cerebral cortex, in subcortical areas or if they represent a combination of both mechanisms, but the speed at which they occur indicates that already existing neural structures are involved (Chen et al., 2002; Lundborg, 2004; Wall et al., 2002). The rapid improvement in sensory functions which may occur within minutes after selective anaesthesia (Bjorkman et al., 2004a) is, presumably, due to unmasking of existing synapses which are normally inhibited, where more long-lasting effects may be due to a long-term potentiation of synapses or, even, formation of new synaptic sites (Chen et al., 2002; Wall et al., 2002). We believe the use of selective temporary anaesthesia in sensory training after nerve repair represents a new concept in hand rehabilitation, making use of the brains ability for rapid remodelling in response to defined extrinsic manipulation, in which active inducement of changes in the sensory inflow is used as a tool in the rehabilitation process. However, the optimal treatment protocol regarding the frequency and duration of EMLA treatment is yet to be defined.
This study was supported by grants from the Swedish Medical Research Council, project no 5188, The Swedish Brain Foundation, Torsten och Ragnar Söderbergs Stiftelse, the Faculty of Medicine Lund University and MalmöUniversity Hospital. Received for publication June 10, 2005. Accepted for publication October 28, 2005.
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