Introduction
Cerebral palsy (CP) is a group of conditions characterised by motor dysfunction due to non-progressive brain injury of the developing foetus or in infants [
1]. Cerebral palsy is the most common cause of childhood-onset lifelong physical disability in most countries [
2]. Presently, there are over 5 million patients with CP in China, with an annual increase of approximately 40,000–50,000 cases [
3]. Generally, hemiplegic CP (HCP) accounts for 38% of all cases of CP [
4]. These children’s motor and sensory disorders mainly occur on one side of the body [
5] and are characterised by the asymmetry of spatiotemporal kinematics parameters, such as the step length and support period [
6]. Consequently, the physical and mental health and the quality of life of children with CP are affected, imposing a heavy economic and mental burden on both society and families [
7,
8].
Over 80% of all children with CP present brain structural abnormalities on magnetic resonance imaging, with periventricular white matter softening, deep grey matter damage and brain dysplasia being the most common [
9]. The continuing presence of abnormalities observed on imaging seriously affects the neurological development and clinical symptom recovery of children. Abnormal posture and movement disorders are the core symptoms of CP. The symptoms of HCP in children are determined by the different areas of brain tissue damage, which manifest differently. Regular rehabilitation is sometimes combined with other therapies, including mental and speech training, physical therapy, acupuncture, massage, bracing and plaster orthopaedics [
10‐
13]. Orthopaedic surgery is only indicated for those with spasticity who are mentally competent and for whom non-surgical treatment is not effective [
14]. Currently, the clinical treatment methods for paediatric CP include medication, surgery, acupuncture, physical therapy and rehabilitation [
4]. Theoretically, compared with conventional regulation and remodelling of the central nervous system (CNS) by improving the function of the peripheral organs from the bottom to the top, a treatment that acts directly on the cerebral cortex or nerve cells can promote the development of the nervous system and compensate for the original dysfunction [
15].
Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive brain stimulation technology [
16] that has been applied to the monitoring, evaluation and treatment of nervous system disease and provides a new way to explore the structure and function of the brain [
17,
18]. According to domestic and international research, the application guidelines recommended by the International Federation of Clinical Neurophysiology and expert consensus on TMS therapy for CP in China, rTMS is both safe and feasible [
3,
19‐
21]. The technique has achieved significant results in the rehabilitation of adult patients with stroke [
22,
23] and can significantly improve gait, balance and lower limb function in such patients [
24]. In recent years, rTMS has gradually been applied to the rehabilitation treatment of children with CP. However, most studies have focused on the effect of rTMS on upper limb function [
25‐
28]. Accordingly, the present study mainly observed the rehabilitation effect of rTMS-assisted training on lower limb motor function in children with HCP to guide clinical treatment.
Discussion
In this study, we observed the effect of rTMS combined with conventional physical therapy on the lower limb motor function of children with HCP. The results showed that the application of rTMS had a significant therapeutic effect on the lower limb motor function of children with HCP and was well tolerated. This provides support for the application of rTMS in children with HCP.
The plasticity of the brain is the theoretical basis of physical therapy for children with HCP, who are mainly characterised by developmental disorders in posture and movement. Spasticity, posture and motor control disorders greatly affect the daily lives and learning of children with HCP. Therefore, early active and effective rehabilitation treatment is of great importance. At present, physical therapy for children with HCP mainly focuses on various manipulations and instruments, lacking direct stimulation to the functional areas of the cerebral cortex. Repetitive TMS compensates for the deficiency of conventional physical therapy, as it can inhibit the non-affected side or stimulate the affected side to promote the recovery of balance, rebuild hemispheric balance and improve lower limb motor function in children with HCP [
33]. Repetitive TMS can be used in the representative areas of the motor and non-motor cortexes. Through repeated, continuous and regular stimulation of the brain, it can exert a cumulative effect and produce local and remote effects on brain activity to achieve the regulation function of cortical excitability, help reconstruct the functional areas of the cortex and regulate neuroplasticity of the cerebral cortex [
33]. Due to its painless, non-invasive and safe characteristics, it has been widely studied in neurological rehabilitation, both domestically and internationally [
19,
20].
For children with HCP, rather than representing ‘reparative plasticity’, enhanced ipsilateral projections from the intact cortex could worsen disability since they competitively displace the surviving contralateral cortico-spinal projections from the affected hemisphere [
34]. Therefore, low-frequency rTMS was selected in this study to stimulate the contralateral cerebral hemisphere to inhibit the excitability of the contralateral cerebral cortex, weakening the inhibitory effect of the contralateral brain reduction on the affected side and enhancing the excitability of the affected cerebral cortex to promote the recovery of lower limb motor function on the affected side. Although the representative areas of the thumb and ankle in the brain motor cortex of children may overlap, and many studies have targeted the cortical area or bilateral cortical motor areas of the abductor pollicis brevis, researchers have observed an improvement in motor function after rTMS treatment [
34,
35]. As the present study mainly observed the motor function of the lower limbs of children with HCP, the target was selected as the cortical area in the primary motor cortex that can stimulate the tibialis anterior to produce MEP.
After 4 weeks of rTMS combined with conventional physical therapy, the 10MWT, 6MWD, GMFM and the symmetry ratio of the step length and stance time of the two groups were significantly improved, with the results in the experimental group being significantly better than those in the control group. After rTMS combined with conventional physical therapy, the walking speed, walking endurance and GMFM of the participants improved significantly, and the step length and stance time of both lower limbs tended to be further symmetrical. In addition, this study observed a significant change in the tone of the triceps surae on the affected side, but no improvement in the hamstrings was observed.
Parvin et al. used rTMS combined with occupational therapy (OT) to treat a 13 years and two months with HCP and found improvements in 10MWT, Timed Up and Go test and 6MWT results. Furthermore, after evaluating the excitability of the reflex through the H-reflex response, it was found that excitability also improved [
36]. This result is consistent with the research results of our study. We observed an improvement only in the muscle tone of the triceps surae and not the hamstrings. Although the lower limb muscles may overlap in the representative areas of the cortex, studies have shown that in most children under the age of 10, the phenomenon of proximal muscles being controlled by the uncrossed corticospinal tract is more common compared with distal muscles [
37]. In our study, rTMS stimulated more of the cross-cortico-spinal tract, so it may have had a greater impact on the triceps surae at the far end. In addition, the sample size of this study was relatively small, and no changes in the muscle tone of the hamstrings were observed. Therefore, the results should be interpreted with caution.
Dadashi et al.’s study indicated that compared with using OT alone, rTMS treatment can improve both the therapeutic effect of OT treatment and the dynamic balance of children with CP [
38]. Liang’s research also demonstrates that when low-frequency rTMS acts on the non-affected side of the cerebral cortex, it reduces its inhibitory effect on the affected side and promotes the function of the bilateral cerebral cortex to become balanced, thereby effectively improving the range of motion of the ankle joint and the motor function of the lower limb and shortening the recovery of motor balance function [
39]. Although the balance function of the participants was not measured in this study, the D-zone (standing) and E-zone (walking, running and jumping) GMFM scores in the experimental group were significantly improved, and the muscle tone of the triceps surae and the symmetry ratio of the stance time were significantly enhanced. These results indicated that the control ability of the affected ankle joint and the lower limb weight-bearing ability of the experimental group were improved, as were the coordination and stability of both lower limbs [
40]. This outcome can improve the walking efficiency and walking endurance of children with HCP, enable them to walk long distances and improve their independent living ability and quality of life.
Although our study confirmed significant immediate benefits of rTMS treatment in children with HCP, there were some limitations. First, the sample size was small, and, as such, the findings may have been subject to error. Second, there was no stratification of the differences in brain injury among individual participants, and the protocol is not yet perfect. Additionally, as the research indicators of GMFM and muscle tone are qualitative assessments of scales, there was subjective bias. More objective and direct assessment methods (such as surface electromyography, musculoskeletal ultrasound and functional magnetic resonance imaging) should be introduced in follow-up research. In future clinical studies, it will be necessary to continuously increase the sample size and complete follow-up to provide a basis for establishing the optimal mode of TMS treatment for children with HCP.
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