Introduction

Stuttering is a speech disorder which affects the normal flow of speech through the repetition or prolongation of sounds, syllables, or words. It can also be accompanied by secondary behaviours.

The autonomic nervous system controls involuntary movements and organ functions in the body and it plays a role in motor speech and development. Furthermore, emotions can cause physiological changes which activate the sympathetic part of the autonomic nervous system, which can disrupt speech patterns and affect the speed, rhythm, and fluency of speech (1,2).

Several theories have been proposed to explain the aetiology of stuttering. However, studies examining autonomic responses in individuals with stuttering problems are insufficient. Some studies have shown that a decrease in heart rate (HR) during speech tasks in adults with stuttering indicates that sympathetic arousal is accompanied by impairments in motor processes characteristic of stuttering (3,4). In their study, Doruk et al. (2) investigated the presence of autonomic nervous system dysregulation in young adult stutterers by analysing the results of 24-hour Holter electrocardiogram HR variability (HRV). Their study concluded that stuttering patients tended to have parasympathetic system dominance (2). In 2010, a study was conducted with young adult stuttering patients which obtained results supporting autonomic nervous system dysregulation through the application of the tilt test (5). In 2009, Tarkowski and Paprzcki (6) conducted a study which was not entirely compatible with previous research. They stated that autonomic responses were not significantly related to the fluency of speech (6).

Conture et al. (7) investigated childhood stuttering in order to determine whether emotional intelligence interacts with emotional stress. They found that increased sympathetic activity had a negative impact on speech (7). In 2016, Choi et al. (8) studied the relationship between mood, emotional stress, and stuttering in preschool children. They concluded that the autonomic nervous system plays a role in stuttering (8). Contrary to these findings, Walsh et al. (9) reported that speech-related sympathetic arousal was not a significant factor in early childhood stuttering. They suggested that developmental profiles in different age groups should be explored in future studies involving children who continue to stutter.

This study aimed to evaluate the severity of stuttering in school-age children and compare HRV between stuttering and healthy individuals. The hypothesis was that there are differences in HRV values between stuttering and non-stuttering children.

Materials and Methods

Study Design

This study was conducted jointly by the otorhinolaryngology and pediatric cardiology departments in accordance with the Declaration of Helsinki. The study was conducted with 41 patients who presented with stuttering complaints and met the inclusion criteria, as well as 41 healthy individuals without stuttering complaints. All of the individuals were between the ages of 6-17 years. The Clinical Research Ethics Committee of Ege University Faculty of Medicine approved this study (approval no.: 16-9/1, date: 14.10.2016).

This study excluded those individuals with hearing impairments, those outside the 6-18 year age range, those with a history of cardiac and circulatory disease, head trauma, metabolic disease, convulsions or central nervous system infection, and those using psychiatric drugs.

The volunteers were divided into two groups: the control group, consisting of patients with normal hearing and no stuttering complaints, and the subject group, consisting of patients diagnosed with stuttering. All patients received an Informed Consent Form, Case Report Form, and a hearing assessment with pure tone threshold audiometry. The severity of stuttering was evaluated using the Turkish version of the Stuttering Severity Instrument (SSI-4TR), and HRV analysis was conducted with a 24-hour Holter application. The Holter was applied in the cardiology department on the first day, and the findings were recorded and extracted the following day (10).

Stuttering Severity Instrument Fourth Edition

Stuttering Severity Instrument Fourth Edition (SSI-4) is a scale widely used to assess the severity of stuttering. SSI-4TR was adapted by Mutlu et al. (11) in 2014. This tool can be used for both clinical and screening purposes. The severity of stuttering in children and adults is measured by evaluating four areas of speech behaviours: frequency, duration, secondary behaviours, and the naturalness of speech. Frequency is expressed as a percentage and converted into scale scores ranging from 2 to 18, duration is scored on a scale of 2 to 18, and secondary behaviours are scored on a scale of 0 to 20. The total score determines the severity of stuttering, with higher scores indicating greater severity. Naturalness of speech is rated on a visual analogue scale from 1 (very natural speech) to 9 (very unnatural speech) (10,11).

HRV

HRV reflects physiological changes in HR resulting from the interaction between the sympathetic and parasympathetic nervous systems. HRV records are obtained through 24-hour Holter electrocardiography. The records are first transferred to a computer environment and evaluated using the Holter program. They are then visually examined by an experienced professional, who excludes any parasitic areas from the evaluation.

On the first day of testing, a Holter device is installed in the cardiology department. The findings are recorded and extracted the following day and evaluated by experienced paediatric cardiology physicians.

Statistical Analysis

This study analysed data using the SPSS 20.0 program (IBM SPSS Statistics for Windows, Version 27.0. Armonk, NY: IBM Corp, USA). Gender and age distributions are presented through cross-tabs. Normal distribution was assessed using the Shapiro-Wilk test. For data without normal distribution, the Mann-Whitney U test was used for comparison. Continuous variables are presented as mean ± standard deviation and categorical variables as numbers and percentages. Pearson’s correlation analysis was used to examine relationships between continuous variables, while chi-square analysis was used to analyse differences between categorical variables. A p value <0.05 was considered statistically significant.

Results

This study analysed data from 41 patients diagnosed with stuttering and 41 healthy controls, a total of 82 individuals. Table I shows the demographic characteristics of the patients included in this study. The mean duration of stuttering at the time of diagnosis was 16±4.7 months. There was no statistically significant difference between the two groups in terms of age or gender distribution. Analysis of family history in the stuttering group revealed that 16 individuals (39%) had a family history of stuttering, whereas 25 (61%) did not.

The severity of stuttering in the patient group ranged from mild in 1 patient (2.4%), moderate in 19 (46.3%), severe in 14 (34.1%), and to very severe in 7 (17.1%). The results of the assessment of stuttering frequency, duration, secondary behaviours and the naturalness of speech are given in Table II.

Upon examining the average distribution of the HRV parameters between the groups, the standard deviation of the mean NN intervals in 5-minute recordings (SDANN) values for the stuttering group were significantly higher than the control group (p<0.05). No significant differences were observed between the groups in terms of the other variables (p>0.05) (Table III).

When examining the correlation between reading, speaking, frequency, seconder behaviours, and duration values which make up the total SSI-4TR scores in the stuttering group, along with HRV parameters, a weak positive correlation was found between the secondary behaviour scores and the SDANN values, and a weak negative correlation was found between maxHR values and beats values (p<0.05) (Table IV).

When the correlation between the total score of SSI-4TR, severity and naturalness of speech values of the stuttering group were analysed with the HRV parameters, a weak negative correlation was found between the total score of SS1-4TR and beats values (Table V).

Discussion

Although many theories have been proposed to explain the aetiology of stuttering, our study focused on investigating the background of speech initiation. HRV parameters were examined in school-age children who stutter to examine possible differences in autonomic nervous system and these were compared with the values for children of similar age without any speech problems.

Our study found that the mean age in the stuttering group was 10.17±2.75 years, which was not significantly different from the control group’s mean age of 10.78±2.78 years. This provided an advantage when evaluating the parameters. Karabulut (12) reported significant positive correlations with age for SDNN, SDNN-index, SDANN-index, low-frequency band (LF), very-low-frequency band, and total power parameters in their study of 51 healthy children with a mean age of 10.78 years. The emergence of different correlations in adults and children was attributed to the incomplete development of the autonomic nervous system in children (12). Previous studies found a negative correlation between HRV parameters and age in adults, while a significant positive correlation was found in children (13). In our study, no significant difference was found between age and HRV parameters in the case group.

In a study of 106 healthy children aged 1-20 years, Silvetti et al. (14) found that SDNN and SDANN values were higher in boys, while SDNN-index, square root of the sum of the differences of consecutive NN intervals in the 24-hour recording (RMSSD), and pNN50 values did not differ between the genders. Similarly, Karabulut (12) reported no significant difference in HRV parameters between the genders in a study of 51 healthy children aged 4-17 years. Our study also found no significant difference in HRV parameters between genders.

Doruk et al. (2) investigated the presence of autonomic nervous system dysregulation in young adult stutterers by analysing their HRV using a 24-hour Holter monitor. Compared to the control group, the stuttering group exhibited high RMSSD and differences in LF, LF/high-frequency band (HF), normalised LF, pNN50, SDNN, HF, normalised HF, total power, and GSI values. Additionally, negative correlations were found between subjective and total anxiety scores and LF and total power. Their study concluded that stuttering patients tended to have parasympathetic system dominance (2). Based on an analysis of our study results, the SDANN values of those children who stutter were significantly higher than those of the control group (p=0.028). No statistically significant differences were observed between the groups in terms of the other variables (p>0.05). In our study, a weak positive correlation was identified between secondary behaviour values and SDANN values, a weak negative correlation with maxHR values, and a moderate negative correlation with Beats values (p<0.05).

SDANN is the standard deviation of the average NN intervals over short periods of 5 minutes. There are differing opinions regarding the SDANN parameter as a reflection of the autonomic nervous system. Fantoni et al. (15) interpreted an increase in SDANN as reflecting changes in autonomic tone, particularly changes in the interaction between the sympathetic and parasympathetic nervous systems in the heart. Adamson et al. (16) reported that a decrease in physical activity corresponds to a decrease in SDANN before clinical deterioration. Raj et al. (17) suggested that the change in SDANN value may not indicate a change in the autonomic nervous system, despite all these findings. The evidence supporting a positive correlation between the SDANN value and secondary behaviours in stuttering children suggests that physical activity may increase the SDANN value. Therefore, the significant SDANN value found in our study is interpreted as being related to the autonomic nervous system and secondary movements during speech in stuttering children. However, the lack of significant changes in the other HRV parameters does not support our hypothesis that the autonomic functions of stuttering children were different. In order to analyse the relationship between the autonomic nervous system and stuttering, it would be useful to use the autonomic nervous system in combination with other nervous dysfunction assessment tools.

To the best of our knowledge, there is no study in the literature investigating the relationship between stuttering and autonomic nervous system functions in school-age children using HRV measurements.

Study Limitations

There is the possibility of the population not being fully represented by both groups in our study. It would be beneficial to increase the number of participants in both groups and to work with more similar groups in terms of gender and age.

Conclusion

No significant correlation was found, except for the SDANN parameter, when examining the HRV parameters of school-age children with and without stuttering. The literature lacks sufficient and precise information regarding the ability of SDANN to show autonomic function alone, which does not support our hypothesis that the autonomic functions of stuttering children are different. When examining the demographic characteristics (gender, age, and family history) of the group with stuttering, a positive and significant correlation was found between the SDANN parameter and secondary behaviours (p>0.05). However, there were no significant correlations between the other parameters, including stuttering severity, speech spontaneity, and the HRV parameters. The literature suggests that physical activity increases the SDANN value and supports a positive correlation with the SDANN value of secondary behaviours in stuttering children. This is the first study to examine autonomic dysfunctions of stuttering children using the 24-hour Holter measurement HRV. Our study may contribute to future research into the aetiology of stuttering.

Ethics

Ethics Committee Approval: The Clinical Research Ethics Committee of Ege University Faculty of Medicine approved this study (approval no.: 16-9/1, date: 14.10.2016).

Informed Consent: All patients received an Informed Consent Form, Case Report Form, and a hearing assessment with pure tone threshold audiometry.

Authorship Contributions

Surgical and Medical Practices: E.D., M.Ş., Z.Ü.T., M.F.Ö., Concept: P.Ö.U., M.Ş., M.F.Ö., Design: P.Ö.U., M.Ş., M.F.Ö., Data Collection or Processing: P.Ö.U., E.D., Z.Ü.T., Analysis or Interpretation: P.Ö.U., E.D., M.Ş., Z.Ü.T., M.F.Ö., Literature Search: P.Ö.U., E.D., M.Ş., Writing: P.Ö.U., E.D., M.Ş., Z.Ü.T., M.F.Ö.

Conflict of Interest: No potential conflict of interest was reported by the authors.

Financial Disclosure: The author(s) received no financial support for the research, authorship, and/or publication of this article.