Abstract
Objectives:
Literature presents conflicting results regarding malocclusions, Obstructive Sleep Apnea (OSA) and sleep bruxism in children with ADHD. Aim of this study was to evaluate the prevalence of these parameters.
Methods:
A prospective study was conducted on 40 consecutive ADHD children referred to the Paediatric Dentistry Unit of Fondazione Policlinico Universitario “A. Gemelli” IRCCS, Rome. All subjects underwent an orthodontic examination and were screened for OSA and sleep bruxism. Data were compared to a sex- and aged-matched control group.
Results:
Prevalence of high risk of OSA in children with ADHD was 62.5% compared to 10% in the control group (p < .00001). No differences were found in any of the occlusal variables examined between children with ADHD and controls (p > .05). An increased prevalence of sleep bruxism was observed in ADHD children (40%) compared to controls (7.5%) (p < .001).
Conclusions:
A higher prevalence of OSA risk and probable sleep bruxism were observed in ADHD patients compared with controls. No significant differences were observed in malocclusions d
Introduction
Obstructive sleep apnoea (OSA) is the most severe form of sleep-disordered breathing (SDB) in children (Villa et al., 2015), characterized by prolonged partial upper airway obstruction and/or intermittent complete obstruction, resulting in impaired gas exchange and/or sleep disruption. Signs and symptoms of OSA include disturbed sleep, daytime neurobehavioral problems, and/or snoring (nocturnal, often with intermittent pauses, snorts, or wheezes; Sateia, 2014). Presence of habitual snoring has been reported in 8% to 12% of children aged 2 to 8 years (Schlaud et al., 2004), while OSA in pediatric patients presents with a prevalence of 1.2% to 9.5% (Bixler et al., 2009).
Some risk factors for the etiopathogenesis of OSA in children include adenotonsillar hypertrophy, obesity, prematurity, asthma, craniofacial abnormalities, and a low socioeconomic status (Lumeng & Chervin, 2008). The pathophysiological causes of OSA likely vary considerably between individuals. Important components include upper airway anatomy, the ability of the upper airway dilator muscles to respond to respiratory challenge during sleep, the arousal threshold and the loop gain, among others (Eckert & Malhotra, 2008). Many studies have been conducted to evaluate possible association between malocclusions and OSA both in adults and pediatric patients, however conflicting results were reported (Aroucha Lyra et al., 2020; Galeotti et al., 2018; Ippolito et al., 2022; Luzzi et al., 2019; Pliska et al., 2017).
The impact of untreated OSA in children appears to be associated with severe sequelae including morbidity from the cardiovascular system (National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents, 2004), enuresis (Jeyakumar et al., 2012), somatic growth delay or growth failure (Bonuck et al., 2009), decreased quality of life (Baldassari et al., 2008) and morbidity from the central nervous system (Sadeh et al., 2006; Sedky et al., 2014). Despite the severe cognitive impairment associated with pediatric OSA, several studies have demonstrated resolution or improvement of signs and symptoms after OSA treatment (Garetz et al., 2015), thereby underlining the importance of an early diagnosis.
Attention deficit and hyperactivity disorder (ADHD) often overlaps with OSA symptoms (Kaditis et al., 2016), with attention deficits reported in up to 95% of pediatric OSA patients (Youssef et al., 2011). ADHD is characterized by a pattern of inattention, hyperactivity, and impulsivity that interferes with daily functioning in more than one setting (American Psychiatric Association, 2013). It has been suggested that obstructive sleep apnea is one of the five sleep phenotypes associated with ADHD, together with nocturnal awakenings, delayed onset sleep insomnia, restless legs syndrome/periodic limb movements during sleep, and epileptiform electroencephalographic (EEG) discharges in sleep (Miano et al., 2012).
A temporal relationship between sleep bruxism and OSA has been suggested (Manfredini et al., 2015); however recent literature does not indicate an association in the adult population (da Costa Lopes et al., 2020), while it is still under discussion in pediatric population (Pauletto et al., 2022); yet to the best of our knowledge, no studies so far have been conducted on ADHD subjects.
Therefore, the primary aim of the present study was to investigate the prevalence of OSA risk in children with ADHD. A secondary aim was to observe the prevalence of malocclusions and sleep bruxism in this sample, and to examine possible associations with OSA.
Participants and Methods
This prospective clinical study was conducted at the Paediatric Dentistry Unit of Fondazione Policlinico Universitario “A. Gemelli” IRCCS, Rome. Approval of the study was obtained by the Ethics Committee of Fondazione Policlinico Universitario “A. Gemelli” IRCCS, Rome with the protocol number 0045274/21 of 12/23/2021 prior to the beginning of the trial.
Participants
A sample size was calculated assuming a prevalence of OSA in ADHD subjects of 47% (Miano et al., 2019) and between 1.2% and 9.5% in the general pediatric population (Bixler et al., 2009). A 95% confidence interval and a power of 0.80 were used. The minimum sample size required was 18 subjects. Considering a drop-out rate of 20%, the sample size was calculated as 22 participants for the current study.
Forty consecutive ADHD pediatric patients referred to the Pediatric Neuropsychiatry Unit (PNU) were invited to participate in the study between January 2022 and May 2022.
Subjects were included if they were between 6 and 16 years old, had a body mass index (BMI) <25 kg/m2 (to limit confounding factors related to prevalence of OSA), have been diagnosed with ADHD with normal to borderline cognitive level (70–85 IQ), and had not undergone any previous orthodontic treatment. The diagnosis of ADHD was provided by an expert neuropsychologist and was based on the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-V) criteria (Iber et al., 2007). Children with a comorbid neurological disorder, with BMI > 25 kg/m2, with a history of orthodontic treatment, or those whose parents denied consent, were excluded.
Forty normal age- and sex-matched control children were recruited from the Pediatric dental clinic at the Paediatric Dentistry Unit of Fondazione Policlinico Universitario “A. Gemelli” IRCCS, Rome from patients presenting for regular oral hygiene check-ups.
Procedure
All subjects underwent a complete dental and orthodontic examination at the Dental Unit. During the appointment, parents and/or legal guardians of the participants were asked to complete a validated questionnaire for OSA screening.
Outcome Measures
Demographics: demographic data included biological sex (female, male), age, racial, and ethnic representation.
Dental measures: these were collected during the clinical examination, with the use of an intraoral scanner Carestream® 3600 (Atlanta, Georgia) to obtain objective measurements. Dental measures consisted of overjet, overbite, Angle’s molar and canine dental class relationship, palate width and shape, presence of occlusal wears, and crossbite.
OSA screening assessment: OSA risk assessment was evaluated through the Italian version of the Pediatric Sleep Questionnaire (PSQ) for OSA risk assessment (Chervin et al., 2000; Di Carlo et al., 2020). The PSQ was selected as a screening tool for pediatric OSA for its high sensitivity (Incerti-Parenti et al., 2021). It consisted of 22 questions, divided into three categories based on nocturnal, diurnal and cognitive symptoms. The questionnaire had a dichotomous answer: “yes” (1 point on the rating scale) or “no/do not know” (0 points on the rating scale). A score was calculated by dividing the number of “yes” by the number of “yes” plus “no,” while the “do not know” answers were excluded from the calculation (Freezer et al., 1995). The final value was comprised between 0 and 1, with scores greater than0.33 identifying an increased risk of OSA.
OSA severity: randomly selected subjects were provided with a home-use polysomnography (PSG) (PSG, Philips® Alice NightOne, Amsterdam, Netherlands) to confirm the presence of OSA as previously assessed with the PSQ, and assess its severity. Patients and their caregivers were given comprehensive instructions on the proper setup of the PSG equipment. They were specifically guided on recording the data for the subsequent night, and caregivers were responsible for returning the instrument the following morning for data scoring. To ensure sufficient data quality and duration, we implemented a criterion where recordings under 6 hr prompted subjects to undergo a second night recording. This step was essential to maintain the reliability and completeness of the recorded sleep data. Apneic events were classified according to the American Academy of Sleep Medicine criteria (Iber et al., 2007) by using the apnea/hypopnea index (AHI). AHI was defined as the average number of apneas and/or hypopneas per hour. The diagnosis of OSAS was established based on an AHI > 1 AND the presence of one of the following: snoring, aborted child’s sleep breathing and sleepiness. Hyperactivity or learning problems were not considered for diagnosis.
Self-reported parafunctional habits: presence of parafunctional habits such as tooth grinding/clenching was self-reported by the parents and/or legal guardians of the participant. Probable sleep bruxism was assessed based on a positive report by caregivers and at least one clinical sign, as recommended by the international consensus (Lobbezoo et al., 2013).
Statistical Analysis
Demographic data are presented as mean and standard deviation, and categorial variables are presented as percentage.
To test Aim 1 (e.g., assessing the prevalence of OSA risk in children with ADHD), the final score of the PSQ for OSA assessment was dichotomized into 1 in presence of scores > 0.33, and into 0 in presence of scores < 0.33. A value of 1 identified a positive risk of OSA. Next, the difference in the risk of OSA between ADHD subjects and controls was compared using Fisher’s exact test or chi-square test, as appropriate. The data on AHI derived from the PSG were also dichotomized into 1 = presence of OSA, and 0 = absence of OSA. Then, the difference in prevalence of OSA between ADHD subjects and controls was compared with Fisher’s exact test or chi-square test.
To test Aim 2 (e.g., assessing the prevalence of malocclusion and sleep bruxism, and investigating association with OSA), the outcomes of dental measures, probable sleep bruxism, and oral parafunctional habits were transformed into dichotomous variables, and were assigned a value of 1 in case of presence of the outcome, and a value of 0 in case of absence of the outcome. Then, the ADHD group was compared to the controls in terms of these outcome measures with Fisher’s exact test or chi-square. Pearson’s correlation was used to assess possible association between dental measures, malocclusions and probable sleep bruxism with risk of OSA.
All statistical analyses were performed using the Vassarstats® platform (©Richard Lowry 1998–2022). A significance level was set at p < .05 for all the analyses.
Results
All 80 participants (22.5% females) accepted to participate in the study and were included. No statistically significant difference was found in demographics between ADHD subjects (9 females, 31 males; mean age: 9.43 ± 2.15 years) and controls (9 females, 31 males, mean age: 9.60 ± 2.18 years, Table 1). All included patients were white Caucasian.
Demographics of children with Attention Deficit and Hyperactivity Disorder (ADHD) and controls.
Note. SD: standard deviation.
Difference in Risk of OSA Between ADHD Participants and Controls
Based on the values of the PSQ for OSA assessment, 25 ADHD participants (62.5%) presented with increased risk of OSA, compared to 4 (10.0%) in the control group, thus demonstrating a statistically significant difference between the two groups (p = .00001).
Twelve participants were randomly selected to undergo PSG recordings (six belonging to the ADHD group, and six healthy controls). In all participants undergoing PSG, the diagnosis of increased risk of OSA obtained by PSQ was confirmed, with no statically significant difference compared with the questionnaire (p > .05).
Comparison Between ADHD Participants and Controls in Outcome Measures
No statistically significant differences were found in any of the dental measures examined between participants with ADHD and controls. The difference in prevalence of Angle class 1 (60% and 63%, respectively); Angle class 2 (35% and 30%, respectively); Angle class 3 (5% and 7%, respectively); maxillary arch constriction (35% and 25%, respectively), and posterior crossbite (15% and 5%, respectively) was not significant (all p’s > .05, Table 2).
Comparison between children with Attention Deficit and Hyperactivity Disorder (ADHD) and controls in the outcome variables.
Denotes statistically significant difference.
When observing the prevalence of probable sleep bruxism, a statistically significant difference was found between ADHD participants and controls. Sixteen ADHD subjects presented with probable sleep bruxism compared to three controls (40.0%vs. 7.5%, p = .001). No significant association was found between risk of OSA and dental parameters, malocclusion, and probable sleep bruxism (all p’s > .05).
Discussion
The present study aimed at assessing the prevalence of OSA in ADHD pediatric patients as compared to healthy age- and sex-matched controls. A secondary aim was to examine whether a difference existed in any dental measures and oral parafunctional habits between ADHD subjects and healthy controls.
A significantly higher risk of OSA was observed in ADHD subjects as compared to healthy controls. This finding is in agreement with the available literature based on a reciprocal relationship between ADHD and OSA (Youssef et al., 2011). In fact, ADHD symptoms often overlap with the diagnosis of OSA, with attention deficits reported in up to 95% of pediatric OSA patients (Miano et al., 2019). Previous studies suggested that hypoxia in OSA may be responsible for ADHD symptomatology (Beebe & Gozal, 2002; Urbano et al., 2021), strengthening the importance of a sleep screening in all ADHD subjects. Similarly, a 10% prevalence of OSA risk in healthy controls as observed in the current study was consistent with data available in the literature (Di Carlo et al., 2020), corroborating the present results.
The sample analyzed consisted of a higher prevalence of male patients; this is in accordance with the scientific literature indicating a males-females ratio of 2 to 3:1 in ADHD population (Sayal et al., 2018).
Many studies have been conducted to evaluate a possible association between malocclusion and OSA in pediatric population, with so far inconsistent and contradictory results (Aroucha Lyra et al., 2020; Galeotti et al., 2018; Ippolito et al., 2022; Luzzi et al., 2019; Pliska et al., 2017). Specifically, a limited number of studies have investigated the presence of dental malocclusion in a cohort of ADHD children, failing to reveal any difference when compared to the general population (Friedlander et al., 2003; Sabuncuoglu, 2013). This lack of significant difference is in agreement with our results. These inconsistent data might be explained by a lack of standardization in both clinical measurements and sleep disordered-breathing diagnosis, and by a lack of adjustment for possible confounding factors like BMI. For these reasons, PSG recording were used to confirm questionnaire data and subjects with high BMI according to the standardized percentile curves of body-mass index for children and adolescents were excluded (Miano et al., 2012).
As supported by the literature, craniofacial signs associated with OSA include a constricted palatal vault, retrognathic mandible, increased overjet, labial incompetency, among others (Lee et al., 2020). Contrary to our expectation, the present study indicated that the majority of ADHD children with OSA did not exhibit any obvious signs of altered craniofacial morphology. As such, this suggests that clinicians should provide an adequate screening for snoring and other sleep-disorder breathing symptoms to all children, as recommended by the American Academy of Pediatrics (Erichsen et al., 2012), with specific attention to ADHD children, and not just to those who present with the classic features generally associated with OSA.
Finally, Roy et al. (2020) found that the main difference between healthy and ADHD children was the prevalence of bruxism. The results of the present study corroborated these findings. A possible correlation between bruxism and oppositional defiant disorder in children with ADHD has been suggested in the literature (Ghanizadeh, 2008). The difference appears to be even more significant in the present study, and it appears to be associated with the presence of OSA. The association between OSA and sleep bruxism in children has been suggested and seems to confirm these findings. However, future well controlled studies investigating an association between bruxism, OSA and other psychological and psychiatric conditions are needed.
Limitations
The present study presents some limitations. The first shortcoming was that not all the subjects were provided with a PSG to confirm their positive screening of elevated risk of OSA. However, the PSG recording performed on 12 randomly selected patients unanimously confirmed the data obtained from the PSQ, thus strengthening the present results. A second limitation was that the present study only focused on the presence of OSA, which is only one of the possible five phenotypes that correlate ADHD with sleep disturbance. Future studies screening and evaluating the presence of nocturnal awakenings, delayed onset sleep insomnia, restless legs syndrome, and epileptiform EEG discharges in sleep are advocated.
Conclusions
In the present study, a higher prevalence of OSA risk and probable sleep bruxism were observed in ADHD patients compared with controls. No significant differences were observed in malocclusions. The lack of these occlusal features suggest that anatomical components play a marginal role in OSA pathophysiology in ADHD children.
Footnotes
Author Contributions
Conceptualization, P.G., A.A.B.; methodology, P.G.; validation, C.B. and G.D.; formal analysis L.S. and F.G.; investigation, AAB., F.G. G.D.; data curation, P.G; A.A.B. and G.D.; writing, A.A.B., F.G. and G.D; original draft preparation, C.B.; writing—review and editing, P.G. and L.S.; supervision, P.G.; project administration, P.G. All authors have read and agreed to the published version of the manuscript.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval
This prospective study was conducted at the “General Dentistry and Orthodontics” Unit at the A. Gemelli Hospital (Rome, Italy). Approval of the study was obtained by the Ethics Committee of the A. Gemelli Foundation with the protocol number 45274/21, prior to the beginning of the trial. Normal age- and sex-matched control children were recruited from the Pediatric dental clinic at the A. Gemelli Hospital from patients presenting for regular oral hygiene check-ups.
Institutional Review Board Statement
All procedures were performed in accordance with the ethical standards of the Declaration of Helsinki (1964) and its later amendments. This protocol has been approved by the local ethical committee with the ID 45274/21.
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study: written informed consent has been obtained from the patient(s) to publish this paper.
