Social anxiety disorder in adolescents who stutter: A risk for school refusal

Background: Stuttering is a childhood‐onset fluency disorder. Part of the counseling for middle and high school students with persistent stuttering is related to school refusal. Anxiety disorders are known to contribute to school refusal. However, it is not known whether social anxiety disorder (SAD) is a factor in school refusal among adolescents who stutter.

individuals who stutter, [15][16][17][18] and dopamine is believed to play a central role in the etiology of stuttering. 19,20lthough drugs have been shown to be effective in randomized controlled trials of pharmacotherapy for adults who stutter, 21,22 none has yet been approved by the US Food and Drug Administration. 23Evidence-based stuttering treatments include the Lidcombe Program 24,25 and the RESTART Demands and Capacities Model (RESTART-DCM) 26,27 for early childhood.However, high-level, evidence-based treatment for elementary school children and adolescents is still lacking, 28 and a support system for adolescents who stutter is yet to be established.

The relationship between stuttering and social anxiety disorder
Social anxiety disorder (SAD) involves an excessive fear of embarrassment in social situations and can result in educational, occupational, and interpersonal underachievement throughout adulthood. 29,30SAD is one of the most common mental disorders with a lifetime prevalence of 8% to 13%. 31,32The median age at onset of SAD in the United States is 13 years, with 75% of affected individuals aged between 8 and 15 years. 29The co-occurrence of SAD with major depressive disorders is about 20%. 335][36] A study found that approximately 24% of 7 to 12-year-olds who stutter have SAD, with the stuttering group being six times more likely to have SAD compared to the nonstuttering control group. 37Although there have been reports of effective Internet-based cognitive behavioral therapy for adolescents who stutter and have SAD, 38 there is insufficient research on SAD among adolescents who stutter.

School refusal and social anxiety disorder
School refusal refers to a child or adolescent's reluctance or refusal to attend school, usually combined with emotional distress. 39School refusal has both short-and longterm negative effects on adolescents, families, schools, and the community.Absence from school is associated with lower academic achievement 40 and a higher rate of dropping out from school, 41 which is associated with unemployment 42 and lower life expectancy. 43Numerous studies have shown that anxiety and anxiety disorders are associated with school refusal.A study analyzing 143 children aged 5-17 years who refused to attend school revealed diagnoses of separation anxiety disorder, generalized anxiety disorder, SAD, oppositional defiant disorder, and depression. 44In addition, approximately two out of three school children between the ages of 9 and 16 years who refused to attend school met the criteria for a psychiatric disorder with anxiety disorders, depression, and oppositional defiant disorder being the most common. 45A retrospective study examining the relationship between trait anxiety and school attendance among 162 adolescents aged 12-13 years revealed that elevated trait anxiety was associated with higher rates of absenteeism. 46In addition, in a study of 201 adults with anxiety disorders, 49% were found to have dropped out of school due to anxiety problems. 47Individuals who drop out of school tend to have more lifetime diagnoses of SAD and substance use than those who do not drop out.[50]

School refusal and stuttering support in Japan
The Ministry of Education, Culture, Sports, Science and Technology (MEXT) compiles data on school refusal in Japan.MEXT defines school refusal as students who do not attend or are unable to attend school for 30 or more days in a given school year due to psychological, emotional, or physical reasons, or due to sociological factors or background issues.Approximately 0.13% of elementary school students refused to attend school in 2021, and this figure is expected to increase sharply to 0.5% for middle school students.Among high school students, the rate of school refusal was 0.26%, but since high school education is not compulsory, students could have dropped out due to school refusal.In fact, the high school dropout rate was 1.1%, higher than the school refusal rate among middle school students. 51ver since the introduction of special education classes for the hearing and speech impaired throughout Japan in 1958, elementary school students who stutter have received treatment, primarily within the school system.They are typically taken out of their regular classes once or twice a week for therapy sessions. 52Although there are many special education classes in elementary schools, the number of these classes drastically decreases in middle and high school, highlighting the lack of ongoing support for students who stutter.

Motivation for this study
In our hospital, we deal with stuttering from childhood to adolescence and adulthood.The problems of middle and high school students who stutter are particularly serious and often lead to school refusal.Therefore, this study aimed to conduct two investigations: the first (Experiment 1) examined whether middle school and high school students who stutter and refuse to attend school have more comorbid SAD; the second (Experiment 2) examined the relationship between SAD and factors related to speech.

M ET HOD S
We included only middle and high school students in the study, out of a total of 622 patients with stuttering as the main complaint who presented to the Kyushu University Hospital from 2011 to 2022.
Experiment 1 included 84 middle and high school students who stuttered.For this experiment, the inclusion criteria for the school refusal group included students who had been absent from school for more than 30 days as well as those who had missed less than 30 days but had clearly been absent owing to a fear of attending school caused by their stuttering.Their mean age was 14.7 years; 65 were males and 19 were females; 22 were in the school refusal group (18 had been out of school for 30 days or more), and 62 were in the school attendance group.To assess SAD, we used the reliable and valid Liebowitz Social Anxiety Scale for Children and Adolescents (LSAS-CA). 53,54It consists of 24 social situations, with a total of 48 items related to fear/anxiety and avoidance for each situation.The maximum score is 144.As all the participants in this study were Japanese, we used the Japanese version of the LSAS-CA. 55orty of the 84 participants from Experiment 1, who were middle and high school students who stutter, participated in Experiment 2. In Experiment 2, the Japanese version of the LSAS-CA was used and the cut-off value for SAD was set at 46. SAD has been found to have a sensitivity of 97.5% and a specificity of 93.8%. 56Therefore, a score of 46 or higher was considered to indicate SAD, while a score of 45 or lower was considered not to reflect.The mean age of students was 14.6 years; 30 were males and 10 were females.Stuttering frequency was assessed by the Japanese Standardized Test for Stuttering and was calculated by dividing the number of core stuttering symptoms by the total number of utterances and multiplying the result by 100. 57 past study hypothesized a vicious cycle wherein people who stutter are prone to comorbid SAD, based on their conditions before, during, and after speaking.58 Based on this hypothesis, we created 10 original questions regarding speech (see Table 1).
The response options were "completely correct," "probably correct," "probably not," and "not at all."The first two responses were considered to be "Yes," while the last two were summarized as "No."The number of yes and no answers for each participant's 10 questions is shown in Table 1.

Statistical analysis
In Experiment 1, we used a t-test to compare the groups.A significant difference was set at p < 0.05.In Experiment 2, we used the χ-2 test for the 10 questions and betweengroup comparison, and the t-test for stuttering frequency and between-group comparisons.Bonferroni correction for multiple comparisons was performed and significance was set at p < 0.004.All statistical analyses were performed using JMP statistical software, version pro 17 (SAS Institute Inc.).
This study was approved by the institutional review board of Kyushu University (2021-2025) and was performed in accordance with the Declaration of Helsinki.

R E SU LT S Experiment 1
The mean ± SD (standard deviation) scores of the LSAS-CA Japanese version for the school refusal and school attendance groups were 71.4±6.4 and 48.9±4.0,respectively (Figure 1).The school refusal group had a significantly higher score on the LSAS-CA Japanese version than the school attendance group (p = 0.004).

Experiment 2
There were 20 students each in the SAD and non-SAD groups in Experiment 2. Stuttering frequency averaged 9.5% and the LSAS-CA Japanese version score averaged 46 (0-132).Twenty (50%) of the 40 middle and high school students whose score on the LSAS-CA Japanese version exceeded 45 comprised the SAD group.The remaining 20 comprised the non-SAD group.Scores on Q7: "When speaking in public, do you experience tremors in your limbs?" and Q8: "After you stutter, do you have negative thoughts about yourself?"were significantly higher in the SAD group.Q1-Q6, Q9, and Q10 showed no T A B L E 1 "Yes" and "No" answers for each of the 10 items for all participants.significant difference between the SAD and non-SAD groups.The mean stuttering frequency was 10%±2.0% in the SAD group and 9%±2.0% in the non-SAD group, which was not significantly different (Table 2).

DI SC US SION
This study was the first to examine school refusal among adolescents who stutter in Japan.It revealed that a significantly higher percentage of adolescents who stutter and were in the school refusal group had concomitant SAD.The results were consistent with previous findings. 47,48SAD is associated with anxiety regarding talking to strangers in a new environment and fear of presenting in class with many classmates present.
The study also examined the rate of SAD and found that 50% of adolescents who stutter had co-occurring SAD.Following the DSM-IV diagnostic criteria, it was found that 38% of 37 adolescents who stutter were diagnosed with at least one psychiatric disorder, which was, in most cases, anxiety-related. 595][36] In our study, adolescents who stutter had a comparable rate of comorbid SAD.
Furthermore, among the 10 items related to speech, adolescents who stutter and had SAD had significantly higher scores on Q7: "When speaking in public, do you experience tremors in your limbs?" and Q8: "After you stutter, do you have negative thoughts about yourself?"Q8 involves a form of repetitive negative thinking (RNT).By assessing the RNT of people who stutter clinicians can better understand individual differences in their patients. 60Targeting the development of unhelpful, intrusive, and repetitive thoughts about stuttering can reduce its harmful effects.Many treatments for stuttering acknowledge the effectiveness of directly addressing where exactly the stutterer directs their thoughts.][63][64] Q7 describes one of the physical symptoms of individuals with anxiety disorders. 65Adolescents who stutter and have SAD may have even more difficulty speaking calmly because they experience physical symptoms other than with their speech when communicating.
No significant relationship was found between stuttering frequency and SAD.Stuttering frequency in those who stutter does not necessarily correspond to affect and cognition. 66Therefore, for better treatment and  counseling of adolescents stutter, it is necessary to assess SAD as well as stuttering frequency.Despite these insightful findings, there are several limitations to this study.First, the school refusal group was deficient in many of the stuttering frequencies, a characteristic measure of stuttering.Adolescents who refuse to attend school may be brought to the hospital forcefully and may be defiant or lack the motivation to speak.Therefore, the relationship between stuttering frequency and school refusal was not clarified.Second, we did not collect data on violence, injury, substance use, psychiatric disorders, and economic deprivation related to school refusal. 67Therefore, we were not able to analyze factors other than SAD.Third, as the participants in this study included only those who stuttered, it was not possible to compare the rate of SAD with a control group.Fourth, the 10 questions used to assess speech were original to this study and were not verified for reliability or validity.

CONC LUSIONS
This study revealed that 26% of adolescents who stutter refused to attend school.This school refusal group had significantly higher rates of SAD than the school attendance group.Moreover, 50% of adolescents who stutter met the criteria for SAD.Thus, when examining adolescents who stutter, checking for comorbid SAD may result in the provision of better support.In addition, in adolescents who stutter, assessing repetitive negative thinking and observing nervousness and trembling during speech may help to resolve SAD.

AU T HOR CON T R I BU T ION S
Yoshikazu Kikuchi, Masamutsu Kenjo, Eriko Yoshida, and Saburo Takahashi.designed the study.Yumi Yamaguchi, Daisuke Murakami, and Yumi Yamaguchi performed the experiments and collected and analyzed data.Yoshikazu Kikuchi wrote the manuscript.Kazuo Adachi, Motohiro Sawatsubashi, Masahiko Taura, Takashi Nakagawa, and Toshiro Umezaki provided conceptual advice.All authors read and approved the final manuscript.

AC K NOW L E DGM E N T S
This work was supported by JSPS KAKENHI Grant Numbers JP21KK0238, JP21K02688, JP20K02299.We thank Editage (www.editage.com) for the English language editing.

CON F L IC T OF I N T E R E ST STAT E M E N T
The authors have no conflicts of interest to disclose.

F I G U R E 1
Comparison of the mean LSAS-CA score between the school refusal group (n=22) and school attendance group (n=62).Error bars indicate standard deviation.T A B L E 2 Differences in the percentage of "Yes" responses to each question and stuttering frequency between the SAD (n=20) and non-SAD groups (n=20 ).
Note: Application of the Bonferroni correction for multiple comparisons indicates statistical significance at p < 0.004.*p < 0.004.