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1 A single session of mirror-based tactile and motor training improves tactile dysfunction in children with unilateral cerebral palsy: a replicated randomized controlled case series. This is the peer reviewed author accepted manuscript (post print) version of a published work that appeared in final form in: Auld, Megan L, Johnston, Leanne M, Russo, Remo N & Moseley, G Lorimer 2017 'A single session of mirror-based tactile and motor training improves tactile dysfunction in children with unilateral cerebral palsy: a replicated randomized controlled case series.' Physiotherapy research international, vol. 22, no. 4, article no. e1674, pp. 1-9 This un-copyedited output may not exactly replicate the final published authoritative version for which the publisher owns copyright. It is not the copy of record. This output may be used for noncommercial purposes. The final definitive published version (version of record) is available at: Persistent link to the Research Outputs Repository record: General Rights: Copyright and moral rights for the publications made accessible in the Research Outputs Repository are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognize and abide by the legal requirements associated with these rights. Users may download and print one copy for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the persistent link identifying the publication in the Research Outputs Repository If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.

2 The Library Educating Professionals, Creating and Applying Knowledge, Engaging our Communities This is the peer reviewed version of the following article: Auld, ML; Johnston, LM; Russo, RN; Moseley, GL., A single session of mirrorbased tactile and motor training improves tactile dysfunction in children with unilateral cerebral palsy: a replicated randomized controlled case series. In Physiotherapy Research International, online Doi: /pri This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for self-archiving.

3 RESEARCH ARTICLE A Single Session of Mirror-based Tactile and Motor Training Improves Tactile Dysfunction in Children with Unilateral Cerebral Palsy: A Replicated Randomized Controlled Case Series Megan L. Auld 1,2 *, Leanne M. Johnston 1,2, Remo N. Russo 3,4 & G. Lorimer Moseley 5 1 Cerebral Palsy League, Brisbane, Australia 2 School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Australia 3 Paediatric Rehabilitation Department, Women s and Children s Hospital Campus, Adelaide, Australia 4 The Flinders University School of Medicine, Bedford Park, Australia 5 Sansom Institute for Health Research, University of South Australia, Adelaide, Australia Abstract Introduction. This replicated randomized controlled crossover case series investigated the effect of mirror-based tactile and motor training on tactile registration and perception in children with unilateral cerebral palsy (UCP). Methods. Six children with UCP (6 18 years; median 10 years, five male, three-left hemiplegia, four-manual ability classification system (MACS) I, one MACS II and one MACS III) participated. They attended two 90-minute sessions one of mirror-based training and one of standard practice, bimanual therapy in alternated order. Tactile registration (Semmes Weinstein Monofilaments) and perception (double simultaneous or single-point localization) were assessed before and after each session. Change was estimated using reliable change index (RCI). Results. Tactile perception improved in four participants (RCI > 1.75), with mirror-based training, but was unchanged with bimanual therapy (RCI < 1.0 for all participants). Neither intervention affected tactile registration. Discussion. Mirror-based training demonstrates potential to improve tactile perception in children with UCP. Copyright 2016 John Wiley & Sons, Ltd. Received 20 January 2016; Revised 10 May 2016; Accepted 4 June 2016 Keywords cerebral palsy; mirror therapy; tactile; upper limb *Correspondence Megan Auld, PhD, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, QLD 4072, Australia. mauld@uq.edu.au Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: /pri.1674 Introduction Cerebral palsy is the most common physical disability in childhood, affecting one in 500 children (Surveillance of Cerebral Palsy in Europe (SCPE), 2002; Australian Cerebral Palsy Register (ACPR), 2009). Historically, upper-limb management in children with unilateral cerebral palsy (UCP) has focused on reducing motor impairments and improving movement quality. Recent studies demonstrate that tactile (touch) deficits are prevalent in over 70% of children with UCP, and that these deficits have implications for motor performance (Auld et al., 2012a). In other

4 Mirror-based Training in Cerebral Palsy M. Auld et al. paediatric populations, tactile deficits are associated with disabilities in reading, learning and behaviour (Stine et al., 1975; Summerfield and Michie, 1993; Nyden et al., 2004). Improving tactile function should promote motor performance and the ability to explore and interpret the environment. Therefore, tactile dysfunction is considered a viable therapeutic target for children with UCP. A recent systematic review established that there are currently no effective treatments for tactile dysfunction in children with UCP (Auld et al., 2014). Of treatments that are successful in adults, most would be unsuitable for use in children because they are invasive (electrical stimulation), potentially unsafe (ice therapy) or require bimanual function (topical anaesthesia, pneumatic cuff). The only successful therapies used in adults that would appear suitable for UCP are stimulus-specific training (Carey et al., 2011) and mirror-based tactile (Moseley and Wiech, 2009) and movement (Dohle et al., 2009) training. These approaches integrate multisensory methods (i.e. vision) to facilitate tactile function. However, stimulus-specific training is a multimodal intervention undertaken over multiple sessions, making it difficult to untangle which strategies contribute to the effect. Stimulus- specific training also requires extended periods of attention and draws on pre-injury sensory experience, both of which would be problematic for children with UCP. Incorporating vision into training appears important, but is not part of many treatments for tactile dysfunction, which occlude vision to interrogate touch. There is a growing body of evidence that noninformative visual input can actually enhance tactile function the so-called visual enhancement of touch effect (Kennett et al., 2001a, 2001b; Spence et al., 2004). Mirror-based tactile training is one easy and inexpensive method to exploit the visual enhancement of touch effect, and indeed, it is more effective for improving tactile function than identical stimulation without visual input, in people with pathological pain (Moseley and Wiech, 2009). We devised a mirror-based tactile and motor training protocol for use in children with UCP and established its feasibility in a clinical setting. Here we describe the initial trial in which we undertook a replicated randomised controlled crossover case series design. We hypothesized that mirror-based tactile and motor training would improve tactile perception more than standard practice in children with UCP. Method Participants Participants were children with UCP aged 6 18 years. Participants were excluded if they could not understand or follow test instructions due to intellectual or behavioural difficulties, had received an upper-limb intramuscular Botulinum toxin injection in the last 3 months and had previous upper-limb orthopaedic surgery, uncorrected visual impairment or known impairment in visual perception. A mail-out of project information went to parents of children who had UCP and were on the database of a statewide service for people with cerebral palsy. A follow-up telephone call was made to all families 2-weeks later. Thus, we used a convenience sample, self-selected by response to the mailout. Allocation to the order of condition was made by concealed randomisation, using sealed envelopes. Ethical approval was granted for both initial contact of parents and the trial itself, by the Institutional Ethics Committees. Assessment Handedness was established using the Edinburgh Handedness Inventory (Oldfield, 1971), and typical manual performance in daily activities for children with UCP was classified using the Manual Ability Classification System (Eliasson et al., 2006). During the physical assessment, the participant sat in a quiet, well-lit room with their arms resting on a table at elbow height. Over the upper forearms there was a frame supporting a curtain to occlude the child s view of their hands. The less impaired hand was always assessed first. Observations made during all assessments were recorded. Assessments were identical in structure and completed by the same therapist each time. Assessment took approximately 20 minutes. Tactile assessments Tactile assessments were selected according to a recent systematic review (Auld et al., 2011) and were undertaken according to methods of highest reliability (Auld et al., 2012b). Full methods and reliability are presented elsewhere (Auld et al., 2012b). At session one, children received a 20-minute tactile assessment. If it was established at this assessment that the child did not have a tactile impairment (Semmes Weinstein monofilament value < 2.83, single-point localization

5 M. Auld et al. Mirror-based Training in Cerebral Palsy score >10; double-simultaneous score >21), the child was excluded without receiving unnecessary treatment, and their data were not analysed. Tactile registration Tactile registration was measured using the full 20-item Semmes Weinstein monofilament kit (Bell-Krotoski, 1990). Spatial tactile perception Single-point localization was assessed using the largest of the monofilaments (from the Semmes Weinstein Monofilaments) according to Auld et al. (2012b). Double simultaneous was assessed using two identical tactile stimulators according to Auld et al. (2012b). The beneficial effect of multisensory training should be most obvious in measures of perception rather than registration (Gallace and Spence, 2008). As such, a hierarchy of tactile perception was used, such that the primary outcome for each participant was the measure for which a reliable score could be determined, in the following order: double simultaneous, single-point localization. That is, double simultaneous was used unless a reliable score could not be obtained, in which case single-point localization was used. To minimize the likelihood of false-positive findings within participants, only one outcome was analysed. Secondary outcome was tactile registration. Assessment was undertaken before and after each session. Intervention There were two interventions: mirror-based tactile and motor training, herein called mirror training, and standard practice bimanual motor-learning approach, herein called bimanual training. The active treatment: mirror training Children sat in a quiet, well-lit room. The impaired arm was placed inside a commercially available mirror box (noigroup.com, Adelaide, Australia), with the elbow and wrist extended and forearm supinated. The unimpaired limb also rested in the extended, supinated position, aligned so that the participant saw the mirror image of the unimpaired limb as though it was the impaired limb. There were two components to mirror training. Mirror-based tactile training: The protocol was similar to that reported by Moseley and Wiech (2009). Participants received tactile stimuli (SWM filament, one larger than threshold; 1.5-seconds duration; 20-seconds inter-stimulus interval) on their impaired hand inside the mirror box, randomly given to one of five locations. During stimulation, participants looked in the direction of their impaired hand but in doing so saw the image of their unimpaired hand in the mirror. After each stimulus, participants responded by pointing to the location on a picture of a hand or verbally indicating the finger that was touched. There were 24 stimuli in a block, which took 8 minutes. There were three blocks, separated by a 3-minute rest. To maintain the child s attention (i.e. younger children), and motivation, a game was played during the test session with the child progressing a game piece following each response. Some example games were the following: lego assembly (every correct answer achieves another piece with the Lego item being constructed at the end of the session) and making puzzles (every correct answer the child added a puzzle piece with the aim that they could complete the puzzle at the end of the session). So that the child did not need to move, the examiner moved the piece of the game within the child s visual display, before the child turned their attention back to the mirror image for the next stimulus. Mirror-based movement training: In the same position as for tactile training, participants copied upper-limb movement positions on verbal command as provided by the investigator. The methodology has been modified from Dohle et al., 2009 to be suitable for children. Hand positions copied were ageappropriate and are those specified in the upperlimb motor planning examination of the Neurosensory Motor Developmental Assessment (Burns, 2014). No tactile stimuli were provided during this condition. Children were asked to respond to the instructions of the next position as quickly as possible. This section lasted up to 30 minutes per session (in two 15-minute blocks), moving through the standardized movement positions within the physical and motor planning ability of the child. Tactile and motor components were alternated throughout the treatment session (Table 1). The control treatment: bimanual therapy A comparative standard therapy protocol targeting the development of specific hand skills and motor

6 Mirror-based Training in Cerebral Palsy M. Auld et al. planning abilities using repetitive practice of bimanual activities was carried out. To ensure that tasks were age-appropriate, directed play tasks similar to those included in the Assisting Hand Assessment (Krumlinde-Sundholm et al., 2007) were carried out for the treatment time (approximately 50 minutes), in a manner similar to that described in the comparative treatment in Hoare et al. (2013). Bimanual therapy is currently considered standard care for the upper limb in children with UCP (Sakzewski, 2012; Hoare et al., 2013). Procedure Participants attended two 1.5-hour treatment sessions at a clinic venue or at the child s home, carried out by an experienced physiotherapist. At both sessions, children were assessed, treated and then assessed again. In one treatment session, the child received mirrorbased training, and in the other, the child received control bimanual therapy, with the order of these therapy types randomized between children. Appointments were scheduled so that the duration between sessions varied across participants between 2 and 7 days, so as to comply with recommended best practice to control for time in replicated case series designs (Ferron and Onghena, 1996; Onghena and Edgington, 2005). Data analysis Reliable change index (RCI) (Jacobsen and Truax, 1991) was calculated for all participants for both interventions. RCI provides an indication of how sure we can be that a change in status was achieved, when the inherent reliability of the measurement tool and the minimum clinically detectable change are considered. RCI is recommended when individual responses are analysed, or for studies that involve small samples, such as in a replicated case series such as this. RCI is expressed as standard deviation unit, such that an RCI of greater than 1.7 means that we can be 90% confident, and an RCI of 1.96 means that we can be 95% confident, that there really was a clinically meaningful change in status for that individual. Results Ten children agreed to participate. Three children were excluded. One child dropped out prior to the second appointment. Thus, six children with UCP between the ages of 6 18 years (median 10 years, five male, three-left hemiplegia, four MACS I, one MACS II and one MACS III) (Table 2), participated. None of the participants received any other treatments that might have influenced tactile function during the course of the trial. Participant one (P1): A 7-year-old male with rightsided UCP; MACS I. Although P1 had a diagnosis of right UCP throughout the assessment and treatment sessions, he regularly used two hands together and would occasionally use his right hand to perform the dominant role in a task (e.g. hold a cup). At the time of assessment, P1 had also commenced a trial of Ritalin to aid concentration at school. On initial examination, P1 was unable to reliably report for double simultaneous and had a significant impairment in singlepoint localization and a mild impairment in tactile registration. P1 required several breaks during mirror therapy to maintain attention. P2: A 10-year-old female with right UCP, MACS III. P2 was born at weeks gestation (5 days overdue). P2 was diagnosed with right-sided UCP at 6 months of age. At 10 months of age, P2 began to experience seizures, which continued until 5 years of age when P2 had a hemispherectomy to alleviate these seizures. An MRI at 11 months and the surgical intervention at 5 years confirmed a diagnosis of left-hemispheric polymicrogyria. Although all assessment items were attempted, P2 s reporting was most consistent and reliable on single-point localization, in which understanding of the task could be easily confirmed with her achieving perfect perception on her unimpaired Table 1. Mirror-based training session schedule Activity Pre-assessment Sensory MT Motor MT Sensory MT Motor MT Sensory MT Post-assessment Time (minutes) Total time = 94 minutes MT, mirror-based training.

7 M. Auld et al. Mirror-based Training in Cerebral Palsy Table 2. Participant demographics Participant Age (years) Gender Side of CP MACS M Right F Right M Left M Left M Left M Right 1 M, male; F, female; MACS, manual ability classification system. hand and significant impairment on her impaired hand. P2 required several breaks during mirror training to maintain attention. P3: A 10-year-old male with left-sided UCP, MACS I. He was born prematurely at 32 weeks gestation and has a twin brother. P3 was diagnosed with CP at 2 years of age. Early in his life, he was receiving more regular therapy, which reduced to approximately three to four times per year in recent years for assistance with handwriting. P3 had almost typical results on initial tactile assessment, with only marginal deficits in tactile registration, with the attainment of monofilament 5 (log 3.22 one monofilament outside of typical registration). P3 required several breaks during mirror training to maintain attention. P4: An 11-year-old male with left-sided UCP, MACS II. He had not had upper-limb therapy since he was 8 years old, which also coincided with his most recent upper-limb Botulinum toxin injection. P4 was born at 38 weeks gestation, with no known cause for his cerebral palsy. On initial examination, P4 demonstrated a significant impairment in both single-point localization and double simultaneous. P4 was able to concentrate without any breaks during the mirror training intervention. P5: A 12-year-old male with left-sided UCP, MACS I. He was born at 27 weeks gestation following maternal diagnosis of pre-eclampsia. P5 had not received regular upper-limb therapy of recent years. On initial examination, P5 had a mild impairment in double-simultaneous perception. P5 was able to concentrate without any breaks during the mirror training intervention. P6: A 17-year-old male with right-sided UCP; MACS I. P6 was born at 41 weeks gestation and suffered a grade IV brain haemorrhage at 3 days of age. He had only minimal upper-limb therapy in the early years of his life, followed by exercises integrated into everyday life. On initial examination, his results in tactile registration and single-point localization were at the limits of performance. P6 was able to concentrate without any breaks during the mirror training intervention. Reliable change index For the session of bimanual training, no participant showed a reliable change in tactile perception (RCI < 1.0) (Table 3). Four participants had an RCI of greater than 1.7 for the mirror training, which means we can be at least 90% confident that an improvement in tactile perception occurred (Table 4). There were no changes in tactile registration for either condition. Discussion This pilot study examined the effect of mirror-based training on tactile registration and perception in children with UCP (Figure 1). Of the six participants, four showed an improvement in tactile perception that is likely to be clinically significant (Table 4) and takes into consideration the reliability of the assessment approach (Auld et al., 2012b), and in which we can be at least 90% confident. Two participants demonstrated no change with mirror-based training. One such participant was close to the ceiling of the tool, which Table 3. Tactile scores pre-bimanual and post-bimanual training (control) on the impaired hand Registration Single-point localization Double simultaneous Child Pre Post Pre Post Pre Post Reliable change index Scores within typical range are in italics.

8 Mirror-based Training in Cerebral Palsy M. Auld et al. probably means there was little room for improvement anyway. Bimanual therapy, the control condition, did not improve tactile perception in any participant. Given that it is known that over 77% of children with UCP have an impairment in tactile function (Auld et al., 2012a) and that there are currently no known treatments for managing this impairment (Auld et al., 2014), these results raise the possibility of better outcomes for children with UCP. Performance in single-point localization and double simultaneous has an established relationship with upper-limb motor function. Indeed, over 30% of the variance in unimanual capacity can be explained by outcomes in single-point localization, and over 30% of the variance in bimanual performance can be explained by outcomes in double simultaneous (Auld et al., 2012c). One might predict that improved tactile perception could facilitate improved motor function, although clearly this needs to be empirically evaluated. No significant changes in tactile perception were noted following the one-control session of bimanual therapy, concurring with the previous systematic review indicating that treatments aimed at motor impairments do not also improve tactile impairments (Auld et al., 2014). A recent study indicates that 90 hours of bimanual therapy delivered over 3 weeks leads to improvements in tactile perception, as measured by the grating orientation task (Kuo et al., Figure 1. Improvement in spatial tactile perception following mirror-based training and bimanual training

9 M. Auld et al. Mirror-based Training in Cerebral Palsy Table 4. Tactile scores pre-mirror and post-mirror training on the impaired hand Registration Single-point localization Double simultaneous Reliable change index Child Pre Post Pre Post Pre Post * * * * * 1.01 Scores within typical range are in bold. *Significant improvement pre-intervention and post-intervention (change greater than SDC and/or indicating typical performance postintervention). 2016). This same treatment only led to a trend in improvement in stereognosis and no improvements in either spatial tactile perception as measured by two-point discrimination or tactile registration as measured by the Semmes Weinstein Monofilaments (Kuo et al., 2016). Notably, however, the dose in the Kuo et al. paper was extremely high in comparison with the current study (90 hours compared with less than 1 hour). That clinically important change was observed after a single session of mirror training, strongly suggests that it may be a potent treatment approach. There are data from adults with pathological pain and tactile dysfunction that show similar improvements with one-training session (Moseley and Wiech, 2009), and in that group, repeated training has been shown to have a greater effect that is maintained for at least 3 months post-training (Moseley et al., 2008). For mirror-based training to be successful, it is essential that the child attends to the visual display of their unimpaired hand in the mirror for both the sensory and motor exercises (Kennett et al., 2001b; Dohle et al., 2009). In the current study, Participants 4, 5 and 6 showed the largest improvement in doublesimultaneous perception. They were also the eldest of the sample and able to complete the tasks without the interruption of games or breaks. Although attempts were made to maintain engagement in the younger children, it seems reasonable that the ability to attend was a limiting factor in improvement. One way to mitigate this may be to undertake repeated sessions that are shorter, or to incorporate mirror training into a regular aspect of life. Another factor that probably affects response to mirror training is the severity of initial tactile impairment those with the poorest performance initially showed the greatest improvement. Critically, however, those same participants did not respond to bimanual therapy, which rules out the possibility that the effect of mirror training was simply a reflection of tactile impairment severity. That non-informative vision augments tactile evoked cortical responses in healthy volunteers (Taylor-Clarke et al., 2002) responses that are consistent with primary sensory cortex activation raised the possibility that we would see improved performance on tests of registration. That we did not is consistent with a recent systematic review of behavioural evidence of tactile improvement with noninformative vision (Eades, 2015), which shows clear benefits on tests of tactile perception rather than registration. This finding might be predicted on the grounds that multisensory processing is important for awareness and occurs after the primary touch signal has been processed in the primary sensory cortex, yet before a percept is generated (Gallace and Spence, 2008). Further research incorporating evaluation of the effect of mirror-based training on cortically evoked responses to touch would cast light on this issue. Hand position during assessment and treatment may also be critical to the success of mirror-based training. This was particularly relevant for Participant 5, who achieved significant gains on double simultaneous (identifying the digits that were stimulated on both hands) but not on single-point localization (identifying the exact location of touch on the impaired hand). Participant 5 held an atypical posture with his impaired hand throughout treatment and assessment, so, although the therapy may have assisted his ability to distinguish between fingers, he remained

10 Mirror-based Training in Cerebral Palsy M. Auld et al. unable to distinguish specific locations on his impaired hand. It is not possible to determine from the current study whether the sensory or motor component of training had more effect on tactile perception, or if both were equally useful for improving function. In a previous pilot study in children with UCP, a version of motor mirror training was shown to improve upper-limb strength and function as measured by the Shriners Hospital Upper Extremity Evaluation (Gygax et al., 2011). However, our objective was to determine if a broad visual-enhanced tactile and motor programme was beneficial, rather than attempt to untangle the contributions of different components. If the current results are replicated in a randomized controlled trial, such a study would clearly be warranted. Interpretation of the current results should consider several limitations. A small sample increases the likelihood of erroneous results. However, we employed the gold standard design for replicated case series approach, which controls for time and order of conditions (Ferron and Onghena, 1996; Onghena and Edgington, 2005). We also implemented the RCI (Jacobsen and Truax, 1991), which provides a conservative estimate of how likely it is, in light of the variability of the score in the studied cohort, the reliability of the assessments used and the clinically important effect, that a true change in status occurred. That we can be over 90% confident that four out of six participants showed a clinically meaningful improvement in tactile function is very encouraging indeed. That our sample was heterogeneous adds to the weight of our finding but also reduces the likelihood of finding effects in either condition. We did not obtain neuroimaging data for the studied cohort. This is relevant because the location, timing and extent of lesion may be critical for patient selection (Staudt, 2010) and may also influence response to mirror-based training. Conclusion This study demonstrated for the first time the potential for a 1-hour mirror-based tactile and motor training session to improve tactile perception in children with UCP. That four out of six participants had a clinically important improvement in tactile impairment is promising but needs to be verified in a randomized controlled trial. Such a study might also permit investigation of dose response and evaluate the influence of age, attention and lesion characteristics to aid optimal patient selection. Subsequent studies should also investigate the specific treatment benefit of the separate tactile and motor components of the mirror-based training. Implications for physiotherapy practice A single session of mirror-based training shows potential to improve tactile perception in children with UCP. Acknowledgements The authors would like to thank the Cerebral Palsy League for assistance with recruitment and the children and families who participated in the study. G. L. M. was supported by a Research Fellowship from the National Health & Medical Research Council of Australia (ID ). REFERENCES Australian Cerebral Palsy Register (ACPR). Report of the Australian cerebral palsy register birth years 2009; Auld ML, Boyd RN, Moseley GL, Ware RS, Johnston LM. Tactile function in children with unilateral cerebral palsy compared to typically developing children. Disability and Rehabilitation 2012a; 34(17): Auld ML, Boyd RN, Moseley GL, Johnston LM. Tactile assessment in children with cerebral palsy: a clinimetric review. Physical and Occupational Therapy in Pediatrics 2011; 31(4): Auld ML, Ware RS, Boyd RN, Moseley GL, Johnston LM. Reproducibility of tactile assessments for children with unilateral cerebral palsy. Physical and Occupational Therapy in Pediatrics 2012b; 32(2): Auld ML, Boyd RN, Moseley GL, Ware RS, Johnston LM. Impact of tactile dysfunction on upper limb motor function in children with unilateral cerebral palsy. Archives of Physical Medicine and Rehabilitation 2012c; 93: Auld ML, Russo R, Moseley GL, Johnston LM. Determination of interventions for upper extremity tactile impairment in children with cerebral palsy: a systematic review. Developmental Medicine and Child Neurology 2014; 56(9): Bell-Krotoski J. In: Hunter J, Schneider L, Mackin E, Callahan A (eds), Light Touch Deep Pressure Testing

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