The effects of intensive bimanual training with and without tactile training on tactile function in children with unilateral spastic cerebral palsy: A pilot study
Introduction
Impaired function in children with unilateral spastic cerebral palsy (USCP) does not purely result from motor impairments, but is also affected by concomitant sensory impairments. Tactile registration, tactile perception, and sensorimotor integration are essential for grasping and releasing objects (Gordon and Duff, 1999a, Gordon and Duff, 1999b), dexterous manipulation (Bleyenheuft & Gordon, 2013), and activities of daily living (Auld, Boyd, Moseley, Ware, & Johnston, 2012). There have been studies investigating sensory contribution to motor control in children with USCP (Auld et al., 2012, Auld et al., 2014, Gordon and Duff, 1999a). However, whether intensive bimanual training or tactile training is effective in modifying tactile impairments in children with USCP has never been investigated.
Early animal studies directly tested how sensory deprivation affected the motor system. Mott and Sherrington (1895) showed that deafferentation, an abolition of sensory input, impaired the performance of skilled movements in monkeys. Although the underlying pathophysiology is different in deafferented monkeys and in USCP, these studies highlighted the contribution of sensory input to fine motor control. Recently, neuroplastic changes were demonstrated in rats’ sensory cortex (S1) after enhanced environmental or motor training. Joo et al. (2012) showed increased somatosensory evoked potentials that paralleled motor recovery. Alwis and Rajan (2013) showed that 8 weeks of environment enrichment increased electrophysiological responses to tactile stimuli. These studies highlight the interaction between sensory and motor systems.
Studies investigating effects of somatosensory training programs on modifying sensorimotor functions in adult stroke are emerging (Carey, Macdonell, & Matyas, 2011). While it has been acknowledged that the sensory impairment is a major contribution to motor impairments in children with USCP (Bleyenheuft & Gordon, 2013), effective therapy in improving tactile impairment is lacking (Auld et al., 2014). The study by Charles, Lavinder, and Gordon (2001) is the only study using intensive hand therapy which reported an improvement in tactile discrimination in 3 children after constraint-induced movement therapy (CIMT). They attributed the improvement in tactile discrimination to an increase in tactile input and its subsequent change in cortical receptor fields for the fingers. More recently, studies investigating neuroplastic changes associated with intensive hand therapy using functional Magnetic Resonance Imaging (fMRI) or magnetoencephalography (MEG) demonstrated increased activation associated with CIMT (Juenger et al., 2013) or HABIT (Bleyenheuft et al., 2015) in S1 or M1 in USCP and in adult stroke (Laible et al., 2012). In summary, tactile function could be improved after intensive hand therapy in children with USCP, and neurophysiological changes associated with intensive therapy may be found in S1 or M1. These studies prompted us to probe deeper into the relationship among intensive hand training, tactile training, and their impact on tactile function in children with USCP.
Both unimanual and bimanual intensive therapy have been shown to improve hand motor function in children with USCP (Gordon et al., 2011, Gordon et al., 2008, Sakzewski, 2012, Sakzewski et al., 2011). Bimanual intensive therapy improved self-determined goals more than unimanual therapy as bimanual training allows use of both hands (e.g., tying shoes) (Brandao et al., 2012, Gordon et al., 2011). In addition, bimanual training improved bimanual coordination more than unimanual training (Hung, Casertano, Hillman, & Gordon, 2011). Consequently, we adopted bimanual training as a common ingredient in our study. We further aimed to compare the efficacy of two interventions in this pilot study: intensive bimanual training (hand–arm bimanual intensive therapy, HABIT) vs. intensive bimanual training that includes tactile training (HABIT + T) on modifying tactile function in children with USCP. We hypothesized that tactile function could be enhanced after HABIT due to the enriched environment created by exposure to objects of varied textures, and tactile function could be further enhanced with additional tactile training.
Section snippets
Participants
Participants included a sample of convenience that was recruited from a subset of two ongoing trials (Bleyenheuft et al., 2015a, Brandao et al., 2013). The inclusion criteria were established based on prior HABIT trials (Brandao et al., 2013, Gordon et al., 2011, Gordon et al., 2007): (1) age 6 to 18, diagnosed with congenital USCP, (2) the ability to lift the more-affected arm 15 cm above a table surface and grasp light objects, (3) cognition level defined as mainstreamed in school (Kaufman
Results
Patient flow is shown in the flow diagram (Fig. 2). Twenty children with USCP (ages 6–15.5 years; MACS level: I–III) met the inclusion criteria and were randomized to receive either HABIT or HABIT + T. One participant in the HABIT group in Brussels dropped out of the study. A total of 19 participants (ages 6–15.5 years; MACS level: I–III) completed 90 h of training. Clinical characteristics of participants are described in Table 1. There were no significant differences in the primary measures or
Discussion
This study aimed to investigate (1) changes in tactile function associated with intensive bimanual training in USCP, (2) the effects of additional tactile training to HABIT in enhancing tactile function. We hypothesized that tactile function would be improved after HABIT, and be further improved with added tactile training. Our results demonstrated that tactile function, specifically tactile spatial discrimination was modifiable immediately after intensive bimanual training. These improvements
Limitations
Our study has a small sample size, which may render insufficient power to determine differences between groups, and the results may not be generalizable. However, our study is the first study to examine the effect of HABIT with or without tactile training in modifying tactile function in children with USCP, and no comparable studies using same measures were conducted in the literature. Therefore it is difficult to estimate an appropriate sample size a priori. We acknowledge that replication
Conclusions
Our study is the first to report that tactile function can be enhanced in both hands after intensive bimanual training. Importantly, the improvements in outcome did not differ between the HABIT + T and the HABIT groups, suggesting the environment is driving the changes rather than specific tactile training. Our study suggests a window of opportunity for modifying tactile function by providing an enriched environment. The take-home message of our study is that tactile impairments can be improved
Conflict of interest statement
The authors declare that there are no conflicts of interest.
Acknowledgement
Grant support: HK & KF (NIH grant: NS K01062116). AH received a student scholarship from the Université catholique de Louvain. We thank children, families, and volunteers participating in our study.
References (39)
- et al.
Impact of tactile dysfunction on upper-limb motor performance in children with unilateral cerebral palsy
Archives of Physical Medicine and Rehabilitation
(2012) - et al.
Capturing neuroplastic changes after bimanual intensive rehabilitation in children with unilateral spastic cerebral palsy: A combined DTI, TMS and fMRI pilot study
Research in Developmental Disabilities
(2015) - et al.
Precision grip control, sensory impairments and their interactions in children with hemiplegic cerebral palsy: A systematic review
Research in Developmental Disabilities
(2013) - et al.
The effect of intensive bimanual training on coordination of the hands in children with congenital hemiplegia
Research in Developmental Disabilities
(2011) - et al.
Upper limb impairments and their impact on activity measures in children with unilateral cerebral palsy
European Journal of Paediatric Neurology
(2012) - et al.
Two-point discrimination tester
Journal of Hand Surgery (American Volume)
(1985) Bimanual therapy and constraint-induced movement therapy are equally effective in improving hand function in children with congenital hemiplegia
Journal of Physiotherapy
(2012)- et al.
Sensibility deficiencies in the hands of children with spastic hemiplegia
Journal of Hand Surgery (American Volume)
(1993) Fifty years of somatosensory research: From the Semmes-Weinstein monofilaments to the Weinstein Enhanced Sensory Test
Journal of Hand Therapy
(1993)- et al.
Environmental enrichment causes a global potentiation of neuronal responses across stimulus complexity and lamina of sensory cortex
Frontiers in Cellular Neuroscience
(2013)