Ethical Approval
This study was conducted with the approval of the Non-Interventional Clinical Research Ethics Committee under decision number 2017/22. Written informed consent forms were obtained from both participants and their parents.
Study design
63 children with CP who had applied to the tertiary healthcare institution were evaluated at the Swallowing Disorders Diagnosis and Treatment Center.Patients with a history of maxillary, head or neck surgery or botulinum toxin treatment, structural oropharyngeal abnormality, gastroesophageal reflux disease, medical and/or physical therapy for dysphagia, severe cognitive, visual, auditory, and sensory impairments, drug use due to seizure or spasticity, serious pulmonary or cardiac disease, or bleeding risk were not included. Relatives of the patients (at least one person) were informed about the study and their written consents were obtained at the beginning of the study.
n the Turkish version of the Pediatric Eating Assessment Tool (Pedi-Eat 10) used in our study, individuals who scored above 4 points (dysphagic) and were able to sit even with support were included. Some individuals were not included in the study: 12 participants did not fall within the age range (4–18 years), and 19 participants stated that they would not be able to attend the treatment sessions. The study started with 32 voluntary patients. However, the study was completed with a total of 26 participants (mean age 7.02 ± 2.40 years), with 16 volunteers from the treatment group and 10 from the control group (Fig. 1).
Study procedures
The study was performed by a group of independent experts blinded to treatment allocation. The study was conducted by a group of independent experts blinded to the treatment allocation. An ear, nose, and throat specialist (1.) performed the physical examination, videofluoroscopic (Philips, Amsterdam, Netherlands) swallowing evaluation and electrophysiological evaluation. Unaware of the evaluation, swallowing rehabilitation (2.) was administered by a swallowing therapist. Subsequently, the patients were reevaluated by another ear, nose, and throat specialist (3.) using endoscopic assessment, unaware of the initial findings and observations. The randomization of patients was arranged by a 4th expert in physical medicine and rehabilitation. Experimental and control groups were formed. The patients completed the study without knowing which group they were assigned to. However, the swallowing therapist who administered the treatment was aware of the group assignments. Evaluation parameters were repeated by the 3nd specialist 4 weeks after treatment.
Randomization
Randomization was performed in 32 patients according to the study criteria by independent (4nd) specialist. In accordance with the order of admission to the hospital, patients were randomly allocated by block randomization and a table of random numbers. The patients were numbered and grouped as 1.,4.,5.,8.,9.,… patients for Group 1, and 2.,3.,6.,7.,10.,... patients for Group 2. Allocation was performed before the initial evaluation. After randomization, 6 patients in Group 2 who were unable to adapt to rehabilitation programme were excluded and the study was completed with 26 patients.
Rehabilitation methods
All patients included in the study were included in the rehabilitation program for swallowing disorders, 3 sessions a week, 12 sessions in total for 4 weeks, by a specialist physiotherapist. All rehabilitation practices were carried out with the family member who took care of the child, and at the end of 12 sessions, the family was trained to continue the treatments as a home program. Applied as common Conventional Swallowing Rehabilitation approaches applied to both working groups; Oral motor exercises, tongue pulling by the physiotherapist using medical gloves with the help of fingers or abeslang, tongue pushing, right and left tongue passive and / or active movements, lip closing, blowing exercises in front of the mirror with the help of passive, active or abeslang each exercise 20 was done in the form of repetition (13).
Laryngeal mobilization application; It was mobilized for approximately 1 minute without causing pain or redness in the right-left and upward direction of the larynx, especially to facilitate laryngeal elevation during swallowing (14). Thermal-tactile stimulation application; Cold stimuli were applied to the anterior pharyngeal area with stimulation sticks in 5–6 contacts, considered as one application, and 200 applications were made to each side in each session (Fig. 2) (15). Gum massage; Circular massage was performed with the help of fingers from the front teeth towards the back on the upper and lower gums. The aim of gum massage is to enhance oral awareness and increase sensory input. Gum massage was applied for approximately 8–10 minutes in treatment sessions.
In addition to the conventional swallowing rehabilitation approaches mentioned, NMES was added to the study group, while Sham-NMES was applied to the control group. For NMES applied to the suprahyoid muscle group, a 80 Hertz frequency, with a transition time of 300–400 microseconds, 40 minutes of Vital Stim application was performed. In the Sham-NMES application, the same area, amplitude, and frequency of current were applied as in the NMES application, but the current was turned off after application for 40 minutes (Fig. 3). To eliminate ethical concerns in the Sham-NMES group, NMES application was performed for 12 sessions after obtaining study data, thus preventing possible bias.
Data Collection
Gender, birth dates, birth weeks, birth weights, presence of newborn intensive care history, sucking history, height, weight, clinical involvement and type of CP, motor effect levels (GMFCS), nutritional history, health-related self history was evaluated and recorded through face-to-face meetings. Clinical and electrophysiological evaluations were made for all participants.
Clinical evaluation
The severity of dysphagia was determined using the Penetration-Aspiration Scale (PAS) through Modified Barium Swallow Videofluoroscopic Swallowing Assessment performed by expert radiologists (13). In this test, the child is positioned in a seated posture and asked to swallow 3 ml of liquid three times. During videofluoroscopic observation in the sagittal plane, oral movements of the bolus are evaluated, and scoring is done on a scale of 1–8.To evaluate chewing, children were given a classic biscuit and observed for biting and chewing using the "Karaduman Chewing Performance Scale" (KCPS) (17,18). No physical or verbal intervention was made during the feeding behavior. Behavioral differences that could occur during feeding (shortness of breath, blueness, stress formation, hoarseness, coughing) were recorded. For the purpose of assessing oral motor function, particularly in children with CP and dysphagia, the "Swallowing Ability and Function Evaluation" (SAFE) battery was used (19). Evaluations were conducted with the child in a seated position (if necessary, supported) using inspection and palpation methods. In children with cognitive impairment, the SAFE application was modified by supporting verbal and visual commands. The fourth stage, which includes sensory and cognitive evaluation, was not included in the statistical analyses in our study as it was not deemed essential for determining the severity of swallowing disorders.
Electrophysiological evaluation
Before evaluating the activation of suprahyoid muscles in all patients, the skin was wiped with alcohol. The skin was allowed to dry, and self-adhesive electrodes measuring 1 x 2.5 cm were placed from the suprahyoid muscles to the body of the geniohyoid muscle. During the recording process, the surface area of each electrode, placed symmetrically and centrally at a distance of 1 cm from each other along the midline, was equal and suitable for the size of the muscle. To prevent slippage of the silver electrodes due to sweating and to avoid cable movements causing pulling artifacts, the electrodes and cables were secured with adhesive tape.In our study, swallowing was analyzed using the Digital Swallowing Workstation Model 7245C (Kay Pentax Corporation, Lincoln Park, NJ) integrated with Noraxon MyoResearch XP Master Edition 1.07 XP software. A dual-channel surface EMG device was used. During the test, muscle activations of the suprahyoid muscles were recorded in microvolts. For y-EMG recording, the high-pass filter was set to 20 Hz, the low-pass filter to 2 kHz, and the signal was amplified by 200 times. The signal pass range was set to 20 mV.For all patients, electromyographic evaluation of swallowing was performed in four different consistencies: spontaneous swallowing, liquid food (3 ml water administered with a syringe), viscous food (5 cc yogurt administered with a spoon), and solid food (biscuit administered by hand) (Fig. 4). In children with chewing difficulties, solid food (biscuit) was ground by an expert on the fingertip before administration. To standardize the head position, all children were fitted with a soft neck collar during the test. Any artifacts resulting from collar contact were disregarded due to the application of the test under the same conditions before and after treatment in the same childAll surface EMG recordings were repeated three times, with each recording followed by approximately 1 minute of rest for the child. The highest average and maximum values obtained from the measurements were accepted for statistical analysis in microvolts. EMG measurements for both groups were recorded before the treatment procedure and after completion of the 12-session exercise program.
The maximal activation amplitude of the suprahyoid muscle was measured to determine the muscle's maximum contraction force, while the minimal activation amplitude before swallowing (duration amplitude) and the resting muscle contraction force (tonus) were also measured. Additionally, the activation duration was used to determine the swallowing duration.
Sample size
The post hoc power analysis was performed to identify the power of the study using G*Power version 3.1.9.2. The hypothesis is that electrical stimulation will provide electrophysiological improvement in dysphagic patients. Null hypotheses of no difference were rejected if p values were less than 0.05. Our sample of 32 participants provided a power of 90% at a significance level of 5% and an effect size of 0.5. We used pre- and post-treatment Pedi-eat-10 level to calculate the effect size.
Statistical Analysis
Statistical evaluation of the data was made using the Statistical Package for the Social Sciences version 21.0 for Windows (IBM Corp., Armonk, NY, USA). Normality of the continuous variables was assessed by the Shapiro–Wilk test. Descriptive statistics were shown as mean ± standard deviation for continuous variables and frequencies and percentages (%) for nominal variables. Statistically significant differences in repeated measurements within the groups were evaluated with the Wilcoxon Signed Rank test. The Bonferroni correction was used to control possible Type I errors in intra-group comparisons (p < 0.025). As none of the continuous variables were normally distributed, the Mann–Whitney U test was used for the comparison of non-normally distributed continuous variables. On the other hand, the significance of difference for nominal variables was analyzed using Chi-square, Fisher’s exact test and when required the treatment effect and 95% confidence interval. The results were considered as significant for p < 0.05.