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The Egyptian Journal of Otolaryngology
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Oral motor weakness: a possible clinical marker for sleep-related difficulties in Down syndrome children — a preliminary study

The Egyptian Journal of Otolaryngology volume 39, Article number: 110 (2023) Cite this article

Abstract

Background

There is an increasing incidence of sleep difficulties in Down syndrome children. Identifying the clinical symptoms that are correlated with sleep difficulties for early diagnosis and treatment is critical.

Aim

To investigate whether oral motor weakness could be considered as an underlying factor for sleep-related difficulties in Down syndrome patients not previously treated with oral motor therapy to prioritize them for definitive objective testing.

Material and methods

The study included 45 Down syndrome children with and without congenital heart disease or hypothyroidism aged 2.5 years to 7 years without a history of prior oral motor therapy, adenotonsillar hypertrophy, and with an average body mass index. The parents were asked to fill in a questionnaire on sleep difficulties involving seven sections. The children were also subjected to 4 oral motor tasks.

Results

Symptoms of sleep-related difficulties were reported in 66.70 to 100% of the DS children. The highest percentage had severe oral motor weaknesses. There is no significant correlation between scores of sleep difficulties and scores of oral motor skills except for a significant negative correlation between scores of restless sleep and frequent awakening with score of Chewy Tubes.

Conclusion

The current study did not prove a significant correlation between oral motor skills and the symptoms of sleep difficulties.

Background

Down syndrome (DS) is the most common chromosomal aneuploidy in live born infants. The overall incidence of DS is approximately 1 in 800 births in the general population [1]. Incidences in Egypt varied between 1 in 555 in one study [2] to 1 in 770 in another [3]. There are mainly three cytogenetic types of trisomy 21 causing Down syndrome: free trisomy 21 (nondisjunction) in most of the cases (around 95% of the cases), mosaic trisomy 21 in approximately 1–2% of the cases, and Robertsonian translocation trisomy 21 which occurs only in 2–4% of the cases [4].

Down syndrome is associated with multiple medical and genetic comorbidities affecting cardiovascular, neurological, hormonal, and cognitive systems. Although prenatal diagnosis of DS has improved, the prevalence of DS is still high. The life expectancy of people with DS has been prolonged because of medical development and is currently 58.6 years. A total of 25% of people with DS live up to 62.9 years [5].

Children with DS are at risk of cardiac defects [6], celiac disease [7], congenital hypothyroidism [8], and otolaryngologic diseases [9, 10]. Correlations between DS and sleep problems have received increasing attention [11, 12].

Researches of sleep disturbance in children with Down syndrome have reported a high incidence of sleep difficulties in children with Down syndrome. There are two main underlying causes of sleep problems, namely behavioral sleep problems, which can be successfully managed using behavior modification techniques and physical/breathing-related sleep problems [13].

Physical causes of sleep problems include sleep apnea. Obstructive sleep apnea (OSA) is frequently diagnosed in children with DS [14]. Its incidence is estimated to range between 30 and 60% in the DS population. Obstructive sleep apnea is a common type of sleep abnormality in which complete or partial airway obstruction, caused by pharyngeal collapse during sleep, leading to loud snoring or choking, frequent awakenings, disrupted sleep, excessive daytime sleepiness, and desaturation [15].

Sleep-disordered breathing (SDB) could impair the development of children with DS causing more severe intellectual disability. There are variable guidelines for screening for OSA in DS across the world. The American Academy of Pediatrics recommends referring all children with DS for a sleep study or polysomnography by the age of 4 years [16]. The UK Royal College of Paediatrics and Child Health (RCPCH) recommend annual screening of children with DS from infancy until 3–5 years old, with a minimum of pulse oximetry [17]. The impracticality of such technology in some parts of the world suggests a need to investigate the validity and utility of simpler screening methods.

The identification of clinical symptoms and features that can help predict sleep-related difficulties is critical in facilitating early diagnosis and treatment [18]. Down syndrome children have numerous predisposing factors for breathing-related sleep difficulties. They are prone to OSA because of a combination of multiple anatomical and physiological factors, including midfacial hypoplasia (insufficient development of the upper jaw, cheekbones, and eye sockets compared with the rest of the face), micrognathia (small lower jaw), macroglossia (large tongue) and hypertrophy of the tonsils and adenoids [19,20,21], overweight [22], and poor muscle tone [23].

All these facts raised our interest to investigate if oral motor weakness could be considered a clinical marker to predict sleep-related difficulties in DS cases not previously treated with oral motor therapy, in order to facilitate early diagnosis of DS children at greater risk to be prioritized for definitive objective testing.

Methods

Study group

Following the Declaration of Helsinki, this study was approved by Medical Research Ethical Committee of the National Research Center under number 1425062022 on 12th May 2022. A number of 70 Down syndrome children were recruited from patients seeking medical advice and follow-up at the Developmental Assessment and Genetic Disorders Clinic, Clinical Genetics Department, National Research Centre. However, only forty-five patients fitted the following inclusion criteria and consequently have been included the following: cytogenetically proven trisomy 21; age between 2.5 years to 7 years old, with or without congenital heart disease or hypothyroidism being highly prevalent congenital anomalies in Down syndrome children; no history of prior oral motor therapy; and no current history of adenotonsillar hypertrophy. DS children with obesity or overweight were excluded. They were all of normal body mass index (BMI) ranging from 16 to 18.10 kg. A written consent was filled in by the caregivers of the children under the current study after explaining the study’s purpose and its procedures. The research was conducted from May 2022 until October 2022.

Methodology

The protocol of evaluation in this study was as follows:

  1. A)

    An interview and history taking by two well-trained clinical genetics researchers were carried out collecting data about the chromosomal analysis of patients; pedigree analysis; clinical examination, with special emphasis on the children’s current medical condition, and if they have or had a history of any associated cardiac anomalies or thyroid gland disorders.

  2. B)

    Then, the caregivers filled in the sleep-related difficulties/obstructive sleep apnea questionnaire [24], which did not take more than 10 min to be filled in. The questionnaire is composed of 7 sections: 33 questions. Three items corresponded to snoring, 8 items to breathing difficulties, 5 items to mouth breathing, 4 items to upper respiratory tract infections, 2 items to sleep position, 6 items to restless sleep and frequent awakening, and 5 items to daytime behavior (Additional file 1). The caregivers give a score of 0 for “never,” score 1 for “sometimes,” and score 2 for “always.”

Section 1: Snoring includes the frequency of snoring in the absence of cold, the loudness level of the child’s snoring, and frequency of hearing the child snoring from outside of the bedroom door. The total score of the highest difficulty is 6.

Section 2: Breathing difficulties include if the child stops or pauses breathing during sleep, if the child struggles to breathe while asleep, if the child struggles to breathe, if his/her chest suck sin, if the parent shakes his/her child to make him/her breathe again when asleep, if the parent has ever got concerned about his/her child’s breathing during sleep, the frequency the child has breath holding or pauses during sleep, the frequency the child made choking or gasping sounds while asleep, and the frequency of a period of silence in the child’s breathing followed by a gasp. The highest score of difficulty is 16.

Section 3: Mouth breathing includes if the child tends to breathe through the mouth during the day, if the child is a daytime mouth breather, the frequency the child has mouth breathing during sleep, if the child has a dry mouth on waking, and if the child is thirsty. The highest score of difficulty is 10.

Section 4: Upper respiratory tract infections include the frequency that the child has had colds or upper respiratory infections that affect breathing at night, the frequency that the child has had a runny nose, the frequency that the child had difficulty swallowing, and if the child has a persistent runny nose. The highest score of difficulty is 8.

Section 5: Sleep position includes the frequency the child sleeps in strange positions such as cocking the head backwards or sleeping while sitting upright on pillows or kneeling and if the child tends to sleep lying on his/her front. The highest score of difficulty is 4.

Section 6: Restless sleep and frequent awakening include the frequency if the child has restless sleep, the frequency the child has frequent awakening compared to children of a similar age, if the child rolls or moves around the bed while sleeping, if the child sweats a lot while asleep, if the child wakes up during night (more than a child of a similar age), and the frequency that the child has had difficulty waking up in the morning. The highest score of difficulty is 12.

Section 7: Daytime behavior includes if the child is unusually sleepy during the daytime, if the child appears sleepy more often in the daytime than children of the same age, and if the child appears to be “on the go” or often acts as if “driven by a motor, if the child appears to be more hyperactive than children of a similar age and if the child has stopped growing at a normal rate since birth. The highest score of difficulty is 10.”

The total score of the questionnaire is equal to 66. Then, the cohort was subjected to oral motor (OM) assessment checklist [25]. It is a checklist based on Oral Placement Therapy concepts and tools (Additional file 1).

Children were seated in a chair that establishes a stable seating posture. A chair with a tray was used for their hands to rest at midline to improve the mobility of their oral musculature. The assessor sat in front of the children, working face to face.

Task 1 (Chewy Tubes): Including a hierarchy of 4 Chewy Tubes: Chewy Tube red, yellow, purple, and green ark garber. The 4 Chewy Tubes are graded from 1 to 4 levels where the red is the lowest level and the green is the highest level. The tip of the Chewy Tube was placed on the surface of the lower back molars, extending from the right side of the mouth. The assessor used the palm of nondominant hand to support the jaw and keep the head at midline if necessary. The child was instructed to chew slowly with complete compression of the tube as the assessor counted out loud. The child gains a score of 1 for the level he/she is working at. Working at a certain level meant to achieve at least one successful bite at any side of the jaw without compensatory movements. The child gains a score of 0, if he/she does not achieve any successful trial at any side using the first Chewy Tube of the hierarchy. To move to the next level, the child has to achieve the success criteria of at least 2 successful trials on both sides of the jaw without compensatory behaviors such as the following: lateral jaw movement, excessive tension, or rapid chews. The assessor stops counting as the child shows any compensations or jaw jutting or jaw sliding. The score of Sect. 1 was calculated based on the number of levels the child is working at. The total score is 4.

Task 2 (jaw bite blocks): Including a hierarchy of 6 bite blocks graded from bite block numbers 2 to 7. The achievement with each bite block is further graded into 3 levels according to 3 relevant graded exercises: exercise A places the bite block on the surface of both back molars, extending from the front of the mouth. The assessor instructs the child to bite down on the bite block and maintain the bite without moving the jaw. The assessor monitors to ensure that the back molars are aligned. Once the bite is achieved, pull forward using resistance as the assessor counts up to 15 or until the child compensates or let go. If the child is able to hold the bite block for 15 s on both sides of the mouth, the assessor will progress to exercise B. Exercise B (using the back molar teeth of both sides of the jaw to hold two bite blocks at the same time) and exercise C (holding one bite block horizontally across the teeth of both sides of the jaw). Accordingly, the overall number of levels using the jaw bite blocks is 18 levels graded sequentially from level 1 (bite block number 2 exercise A) to level 18 (bite block number 7 exercise C). To be considered working at a certain level, the child has to hold the bite block for at least 1 s at any side of the jaw in exercise A or both sides of the jaw at exercises B and C without compensatory movements. To move to the next level of the jaw bite blocks, the child has to achieve the success criteria of 15 s on both sides of the jaw. The score of Task 2 was calculated based on the number of levels the child is working at. The total score is 18.

Task 3 (horns): Including a hierarchy of 12 horns gradually increase in difficulty with the easiest to blow horn number 1 to the most difficult to blow horn number 12. Accordingly, the overall number of levels is 12 levels. The assessor supported the child’s jaw. The assessor placed the mouthpiece of the horn on the surface of the child’s lower lip at midline telling the child to take a breath in and blow. The assessor began by requiring as many blows as possible of any duration while removing the horn after each successful blow. The child gains a score of 1 for the level he/she is working at. To be considered working at a certain level, he/she has to achieve at least one successful sustained uninterrupted blow/trial without compensatory movements. The child gains a score of 0, if he/she does not achieve any successful blow using the first horn of the hierarchy. To move to the next level of horns, he/she has to achieve the success criteria which are 25 successful trials. The score of Task 3 was calculated based on the number of levels the child was working at. The total score is 12.

Task 4 (straws): Including a hierarchy of 8 straws gradually increase in difficulty with straw number one is the easiest, and straw number 8 is the most difficult. Accordingly, the overall number of levels using the straws is 8 levels. The child gains a score of 1 for the level he/she is working at. To be considered working at a certain level, he/she has to use the straw to drink for at least 1 s without compensatory movements (dripping of water, using the teeth to bite on the straw, no lip rounding). To move to the next level of straws, he/she has to achieve the success criteria which are using the straw to drink 3 times for at least 10 s in each time without compensatory movements. The score of Task 4 was calculated based on the number of levels the child is working at. Total score is 8.

The total score of the OM checklist consists of the sum of the scores of all the sections; 4 tasks equal to 42.

  1. C

    Two sensitivity analyses were conducted to compare total and subtotal sleep-related difficulty scores between patients with and without congenital heart disease and patients with and without congenital hypothyroidism.

  2. D

    The sleep-related difficulties questionnaire was refilled in by the caregivers of Down syndrome children included in the study after 1 month for correlating the scores for the purpose of evaluating the test–retest reliability.

Data management and statistical analysis

Quantitative data were statistically represented in terms minimum, maximum, mean, standard division (SD), and median. Comparison between different groups in the present study was done using Mann–Whitney test for comparing two nonparametric groups. Qualitative data were statistically represented in terms of number and percent. Correlation between various variables was done using Spearman correlation coefficient (R). Reliability was calculated using Cronbach’s alpha and test–retest reliability correlation. A probability value (p-value) less than or equal to (0.05) was considered significant. All statistical calculations were done using computer program SPSS (Statistical Package for Social Science) statistical program version (21.0). Graphs were done using SPSS statistical program version (21.0) and Microsoft Excel program version 2016.

Results

Cohort characteristics

The cohort was 62.20% males and 37.80% females. The sex ratio was 1.68. About 53.3% have associated congenital heart anomalies, while 20% have associated congenital hypothyroidism. Cytogenetically, 43 (95.6%) patients had non-disjunction trisomy 21, and one case (2.2%) had Robertsonian translocation 14/2, while another case (2.2%) had mosaic trisomy 21. The 2 DS cases with mosaic and Robertsonian translocation trisomy 21 have comparable results to the majority of the patients with non-disjunction trisomy 21 regarding the sleep-related difficulties questionnaire and oral motor checklist.

Sleep-related difficulty questionnaire results

The results of the different responses in sleep-related difficulties questionnaire sections revealed the following: 31 (68.9%) have snoring, 30 (66.7%) have breathing difficulties, and 43 (95.6%) are mouth breathers and have a different sleep position. All the children under study have a restless sleep and frequent awakening, and 37 (82.20%) children have a daytime behavior as shown in Table 1.

Table 1 Frequencies and percentage of the different responses in sleep-related difficulties questionnaire
Full size table

Significant positive correlations were detected (r = 0.307 to 0.626; p < 0.05, 0.001) between scores of Sect. 1 (snoring) and scores of Sects. 2 (breathing difficulty), 4 (upper respiratory tract infections), and 5 (sleep position). There was a significant positive correlation between scores of Sect. 2 (breathing difficulty) and Sects. 3 (mouth breathing), 4 (upper respiratory tract infections), and 5 (sleep position). There was a significant positive correlation between score of Sect. 3 (mouth breathing) and scores of Sects. 4 (upper respiratory tract infection) and 6 (restless sleep & frequent awakening). There is a significant positive correlation between scores of Sect. 4 (upper resp. tract infections) with score of sleep-related difficulties questionnaire Sect. 5 (sleep position). There is a significant positive correlation between score of sleep-related difficulties questionnaire Sect. 5 (Sleep position) with score of Sect. 6 (restless sleep & frequent awakening).

Sleep-related difficulties across patients with and without congenital heart disease and congenital hypothyroidism.

There was a nonsignificant difference between DS children with and without associated congenital heart anomalies regarding the total and subtotal scores of sleep-related difficulties questionnaire (Table 2). However, there was a significant difference (p < 0.05) between DS children with and without associated congenital hypothyroidism regarding the total score of sleep-related difficulties and scores of both the sections of snoring and mouth breathing with higher scores in those with congenital hypothyroidism than those without (Table 3).

Table 2 Comparison between the total and subitems scores of breathing-related sleep difficulties questionnaire between Down syndrome children with associated and those without associated congenital heart anomalies
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Table 3 Comparison between the total and subitems scores of breathing-related sleep difficulties questionnaire between Down syndrome children with associated and those without associated congenital hypothyroidism using Mann–Whitney test
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Total score of sleep-related difficulties questionnaire showed good test–retest reliability (r = 0.915, p-value = 0.001) (Table 4). Also, this table shows good test–retest reliability in scores of almost all the items, with less test–retest reliability for the following items: Sect. 1 (snoring) (r = 0.709, p-value = 0.022), Sect. 3 (Mouth breathing) (r = 0.765, p-value = 0.010), and Sect. 6 (restless sleep and frequent awakening) (r = 0.694, p-value = 0.026).

Table 4 Test–retest reliability of scores of sleep-related difficulties questionnaire
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Table 5 revealed that the higher percentages of Down syndrome children were still working on level 1 of the four tasks of the OM test.

Table 5 Frequencies and percentage of the different responses in oral motor checklist sections
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There was a nonsignificant difference between Down syndrome children with and without associated congenital heart anomalies (Table 6) and congenital hypothyroidism regarding total and subtotal scores of OM checklist (Table 7).

Table 6 Comparison between the total and subitem scores of oral motor checklist between Down syndrome children with associated and those without associated congenital heart anomalies using Mann–Whitney test
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Table 7 Comparison between the total and subitem scores of oral motor checklist between Down syndrome children with associated and those without associated congenital hypothyroidism using Mann–Whitney test
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Table 8 revealed that there was a good internal consistency as shown by the significant positive correlation within the subitems of OM checklist (r = 0.374 to 0. 823, p-value ≤ 0.05, 0.001) except for the correlation between scores of Sect. 1 (Chewy Tubes) with scores of Sects. 3 and 4 (bite blocks and horns). Reliability of the OM checklist was measured in the current study and shows good reliability (r-value = 0.753).

Table 8 Correlation between total and subtotal scores of oral motor checklist
Full size table

Correlation between sleep-related difficulty scores and OM scores

There was a nonsignificant negative correlation between the total score of the sleep-related difficulties questionnaire and scores of total and subitems of OM checklist. However, there was only a significant negative correlation between score of Sect. 6 restless sleep and frequent awakening in sleep-related difficulties questionnaire with the score of Sect. 1 Chewy Tubes in OM checklist as shown in Table 9.

Table 9 Correlation between scores of sleep-related difficulties and scores of oral motor checklist
Full size table

Correlation of age and sleep-related and OM scores

There was no significant correlation between age of the children and scores of sleep-related difficulties questionnaire (r = 0.004, p-value = 0.981), while there was a significant positive correlation between the age of the children and the total score of OM checklist (r = 0.392, p-value n 0.008).

Discussion

The American Academy of Pediatrics in 2001 acknowledged that children with DS may have an increased risk of sleep abnormalities and recommends that primary care physicians ask parents about possible sleep disorders in their children [26]. However, no recommendations were made for specific testing [9].

Common and highly prevalent risk factors for sleep-related difficulties in DS children are related to oral motor deficits such as adenotonsillar hypertrophy, relative macroglossia [27] and craniofacial abnormalities [8] related to hypopharyngeal collapse during sleep, and reduced orofacial muscle tone [28].

Various treatment modalities for breathing-related sleep difficulties were described in the literature based on the underlying cause [29]. Several studies have shown that common pathophysiologic aspects related to breathing-related sleep difficulties in DS children do not change after surgical, medical, or orthodontic treatment, potentially explaining their lack of effectiveness. Other interventions were therefore necessary [30, 31].

The aim of this study was an attempt to investigate, if there is a correlation between sleep-related difficulties symptoms reported by parents of DS children and the children’s oral motor profile. We aimed at determining if oral motor difficulties can predict the presence of sleep-related difficulties and its degree of severity, which might help in picking up the cases for confirmation by the instrumental evaluation and then setting the appropriate rehabilitation program for management.

The sex ratio (SR) in patients with Down syndrome varies considerably from one study to another. In a study by Kovaleva et al. [32], there was a predominance of males with DS in almost all age groups and in all types of trisomy 21 including inherited ones. This fact was confirmed by the current study as males represented 62.20% of the sample under study while females represented 37.80%.

In literature, DS comorbidities were potentially associated with disrupted sleep such as obesity, the presence of adenotonsillar hypertrophy, and the associated congenital anomalies [33]. In this study, children were selected to be of average weight with no current or history for adenoidal hypertrophy. Therefore, it was also important to collect data about the associated anomalies of the sample under study to know the factors that might contribute and increase the risk of obstructive sleep apnea in them, such as associated congenital hypothyroidism and associated congenital cardiac anomalies being high prevalent congenital anomalies associated with Down syndrome. In this study, DS children with associated congenital heart anomalies represented 53.30% of cases while 20% of all Down syndrome children had hypothyroidism.

Regarding the percentages of responses to the used self-reported questionnaire in Table 1 which revealed the problems related to sleep, it showed that all the children under study had restless sleep and frequent awakening. About 95.60% of them were mouth breathers and had different sleep position. Nearly 82% of the DS children had a daytime behavior. About 68.9% of Down syndrome children had snoring, while 66.70% of them had breathing difficulties. These subjective impressions of the parents were reported extensively in the literature, such as bedtime resistance, sleep anxiety, night waking, parasomnias, and daytime sleepiness [11]. The percentages of the symptoms of the sleep-related difficulties in our study were higher than those reported in the study by Hizal et al. [34] whose parents of 81 DS children under their study reported snoring in 46.9% and frequent night awakening in 35.8%, and in their study, sleep-related symptoms (apnea and/or snoring and/or frequent night awakening) were documented in 51 (63%) DS children. About 89% of parents in Hizal et al.’s [34] study had very little knowledge of sleep disorders which could have contributed to the lower percentage in their study.

Regarding evaluating the contribution of the associated congenital anomalies in DS children under study to sleep-related difficulties, Table 2 clarified that the associated cardiac anomaly in children of the current study was not a contributing factor to their sleep-related difficulties as supported by the results of the comparison between the group with congenital cardiac anomaly and those without. This is in agreement with previous studies [35, 36]. On the other hand, congenital hypothyroidism in Down syndrome children under study was accompanied by increased symptoms of sleep-related difficulties with significant difference in the comparison than children without associated hypothyroidism in sections related to snoring and mouth breathing as shown in Table 3. This could be attributed to the fact that breathing-related sleep difficulties and hypothyroidism have many signs and symptoms in common [37]. Symptoms and signs common in both conditions include the following: obesity, fatigue, impaired concentration, snoring, and witnessed apneas [38]. This finding was not in agreement with previous studies which found no association between congenital hypothyroidism and breathing-related sleep difficulties [39, 40].

Good test–retest reliability was found in almost all the items with less test–retest reliability for the following items: Sect. 1 (snoring), Sect. 3 (mouth breathing), and Sect. 6 (restless sleep and frequent awakening) as shown in Table 4, although the number of DS children included in the study was small. Posada et al. [41] reported a reliability test for snoring that was able to predict sleep-related difficulties with a sensitivity of 61.7%, a specificity of 100%, and negative predictive value of 25%.

The current study revealed the oral motor profile of the included children as shown in Table 5. The DS children under study showed severe oral motor difficulties in the highest percentage of them. The oral motor profile did not exceed level 1 in the four sections of oral motor tasks. This is expected because of the oral structural abnormalities and hypotonia manifested in DS children; also, none of the studied cases has previously received oral motor therapy. Oral motor control has frequently been found to be impaired in Down syndrome, and this seems to stem not just from oral weaknesses but to involve some degree of dyspraxia [42, 43]. The oral motor skills’ development starts in the womb and develop through the first 2 to 3 years age in correspondence to the development of feeding and early linguistic skills. Although this system is ahead compared to other motor systems (it responds to touch stimulation from the seventh week of gestation), the complete refinement of its actions is not reached until the age of 6 or 7 years [44].

Regarding evaluating the contribution of congenital anomalies associated with DS children under study to oral motor difficulties, Tables 6 and 7 showed no contribution of both congenital heart disease and congenital hypothyroidism to the oral motor difficulties as there was no significant difference between the group who had congenital anomalies and those without the congenital anomalies in their performance in oral motor tasks. This result is not in agreement with the general clinical fact especially for congenital hypothyroidism that is known in causing myxedematous facies, macroglossia, and hypotonia [45]. However, this could be attributed to the small sample size (20%) of DS children having hypothyroidism in the current study.

The used oral motor checklist showed good internal consistency as shown in Table 8 and a good reliability with p-value of 0.753. This reliability is acceptable but is less than reliability found in the literature about few other oral motor tests in the review of standardized tests of nonverbal oral and speech motor performance in children by Maccauley and Strand [45]. It was found that only the Kaufman Speech Praxis Test for children (KSPT) and the Verbal Motor Production Assessment for Children (VMPAC) manuals provided information about reliability, which was reported for individual sections or subtests using the test–retest reliability. For KESPT, it was 0.90 for adequacy of reliability but was not described in terms of statistical significance, and the reliability study reported for the VMPAC was greater than 0.90 for focal oral motor control section of the test, but the manual did not indicate whether this coefficient was statistically significant. Although test–retest reliability for the oral motor checklist was not carried out in the current study, but the value of Cronbach’s alpha for this study points to the good reliability for the used oral motor checklist even with the relatively small sample size.

The current study did not prove the correlation between the self-reported symptoms of the sleep-related difficulties and the scores of oral motor checklist as shown in Table 9 except for the significant negative correlation between scores of symptoms of restless sleep and frequent awakening with score of oral motor checklist Task 1 (Chewy Tubes). To the best of our knowledge, there is no available data studied the correlation between the degree of severity of oral motor weakness and symptoms of breathing-related sleep difficulties in the literature. However, previous systemic review studies have confirmed the benefits of orofacial myofunctional therapy in terms of improvements in snoring, sleep quality, lowest oxygen saturation, daytime, and sleepiness [46, 47]. Orofacial myofunctional therapy helps to reposition the tongue, improve nasal breathing, and increase muscle tone. According to Koka et al. [48], the decrease in snoring and daytime sleepiness may result from improvements in muscle responsiveness, the coordinated recruitment of different compartments of tongue and other pharyngeal muscles, the coordinated action of pharyngeal and peripharyngeal muscles, and improvement of chewing, speech, breathing, and swallowing functions in OSA patients, thus improving quality of life. This implies that oral motor skills are necessary, but not sufficient, to be a clinical predictor for symptoms of breathing-related sleep difficulties.

The size of the sample under this study was limited because we were trying to decrease the bias of the presence of many factors that increase the symptoms of sleep-related difficulties such as obesity and the presence of adenotonsillar hypertrophy. Conveying the study on larger sample may prove the significance of the correlation. Applying the study on groups of Down syndrome children who receive oral motor therapy and those who do not receive oral motor therapy may help clarify this point.

The current study did not support the correlation between age and scores of sleep-related difficulties. This finding is in agreement with Durhan et al. [49]. There were two studies that reported a positive association between age and breathing-related sleep difficulties [50]. Shires et al. [51] found that patients with breathing-related sleep difficulties had a higher mean age, while Lee et al. [50] identified a higher median age in children with breathing-related sleep difficulties compared to those without sleep-related difficulties. Conversely, Skotko et al. [52] divided children according to age: < 8 years and ≥ 8 years and identified a significant association between younger age and the presence of OSA. On the other hand, age was significantly correlated with scores of oral motor checklist. This observation was not expected as one can predict that with age and without receiving any oral motor therapy, DS children might develop compensatory misbehaviors rather than acquiring proper oral motor skills. The compensatory misbehaviors were recorded in the literature [53] and was observed in the current study such as lateral jaw movement, excessive tension, rapid chews, and moving the jaw during biting. However, the compensatory behaviors might be partially explained by the improvement of the imitation ability of Down syndrome with age. This finding raised an interesting point to investigate in order to determine the extent to which age can play a role in the acquisition of oral motor skills in the genetic disorder of Down syndrome.

This study is limited by being single centered and cross-sectional. Additionally, the study was conducted in a tertiary center which limits its generalizability to primary care settings. The small sample size is another limitation. The current study was concerned about evaluating the oral motor weakness as an underlying cause of the sleep-related difficulties in Down syndrome children; this could not be proved in the sample under the current study. However, investigating other causes is warranted in future studies such as conveying the behavioral sleep assessment to exclude the behavioral cause. Performing a retest in future study will add to the reliability of the currently used oral motor checklist.

Conclusion

Symptoms of sleep-related difficulties were reported in 66.70 to 100% of the DS children under the study. The highest percentage of the children had severe oral motor weaknesses as they did not exceed score 1 in the four sections of the oral motor tasks. The current study did not prove a significant correlation between oral motor skills and the symptoms of sleep difficulties. The study raised interesting points to investigate such as the role played by age in acquiring oral motor skills, conveying the study on larger sample to help more clarification of the significance of the correlation in addition to applying on those who do not receive oral motor therapy and may help in investigating the effect of oral motor skills and their significance to symptoms of sleep-related difficulties.

Availability of data and materials

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. El-Gilany AH, Yahia S, Shoker M, El-Dahtory F (2011) Cytogenetic and comorbidity profile of Down syndrome in Mansoura University Children’s Hospital. Egypt Indian J Hum Genet 17(3):157–163. https://doi.org/10.4103/0971-6866.92092. PMID:22345986;PMCID:PMC3276983

    Article  PubMed  Google Scholar 

  2. Hafez M, El-Tahan M, Zedan MM, Eisa M (1984) Demographic trends of Down’s syndrome in Egypt. Hum Biol 56:703–712

    CAS  PubMed  Google Scholar 

  3. Temtamy SA, Abdel Meguid N, Mazen I, Ismael SR, Kassem NS et al (1998) A genetic epidemiological study of malformations at birth in Egypt. East Mediterr Health J 49:252–259

    Article  Google Scholar 

  4. Plaiasu V (2017) Down syndrome - genetics and cardiogenetics. Maedica (Bucur) 12(3):208–213

    PubMed  Google Scholar 

  5. Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery PD, Bittles AH (2002) The changing survival profile of people with Down’s syndrome: implications for genetic counseling. Clin Genet 62:390–393

    Article  CAS  PubMed  Google Scholar 

  6. Freeman SB, Taft LF, Dooley KJ et al (1998) Population-based study of congenital heart defects in Down syndrome. Am J Med Genet 80(3):213–217

    Article  CAS  PubMed  Google Scholar 

  7. George EK, Mearin ML, Bouquet J et al (1996) High frequency of celiac disease in Down syndrome. J Pediatr 128(4):555–557

    Article  CAS  PubMed  Google Scholar 

  8. Metwalley KA, Farghaly HS (2022) Endocrinal dysfunction in children with Down syndrome. Ann Pediatr Endocrinol Metab 27(1):15–21. https://doi.org/10.6065/apem.2142236.118. Epub 2022 Mar 31. PMID: 35368192; PMCID: PMC8984752

    Article  PubMed  PubMed Central  Google Scholar 

  9. Shott SR (2006) Down syndrome: common otolaryngologic manifestations. Am J Med Genet C Semin Med Genet 142C(3):131–140

    Article  PubMed  Google Scholar 

  10. Ramia M, Musharrafieh U, KhaddageW SA (2014) Revisiting Down syndrome from the ENT perspective: review of literature and recommendations. Eur Arch Otorhinolaryngol 271(5):863–869

    Article  PubMed  Google Scholar 

  11. Churchill SS, Kieckhefer GM, Landis CA, Ward TM (2012) Sleep measurement and monitoring in children with Down syndrome: a review of the literature, 1960–2010. Sleep Med Rev 16(5):477–488

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lal C, White DR, Joseph JE, Van Bakergem K, LaRosa A (2015) Sleep-disordered breathing in Down syndrome. Chest 147(2):570–579

    Article  PubMed  Google Scholar 

  13. Stores R, Stores G, Fellows B, Buckley S (1998) Daytime behavior problems and maternal stress in children with Down syndrome, their siblings and other intellectually disabled peers. J Intellect Disabil Res 42(3):228–237

    Article  PubMed  Google Scholar 

  14. Marcus CL, Keens TG, Bautista DB, Von Pechmann WS, Ward SL (1991) Obstructive sleep apnea in children with Down syndrome. Pediatrics 88(1):132–139

    Article  CAS  PubMed  Google Scholar 

  15. Mannarino MR, Di Filippo F, Pirro M (2012) Obstructive sleep apnea syndrome. Eur J Intern Med 23:586–593

    Article  PubMed  Google Scholar 

  16. Bull MJ (2011) Health supervision for children with Down syndrome. Pediatrics 128:393–406. https://doi.org/10.1542/peds.2011-160518

    Article  PubMed  Google Scholar 

  17. Royal College of Paediatrics and Child Health (2009) Working Party on Sleep Physiology and Respiratory Control Disorders in Childhood, Standards for Services for Children with Disorders of Sleep Physiology Report. pp 23–33

    Google Scholar 

  18. Hanna N, Hann Y, Blinder H, Bohaut J, Katz SL (2003) Predictors of sleep disordered breathing in children with Down syndrome: a systematic review and meta-analysis. Eur Respir Rev 31:220026. https://doi.org/10.1183/16000617.0026-2022

    Article  Google Scholar 

  19. Donnelly LF, Shott SR, LaRose CR, Chini BA, Amin RS (2004) Causes of persistent obstructive sleep apnea despite previous tonsillectomy and adenoidectomy in children with down syndrome as depicted on static and dynamic cine MRI. AJR Am J Roentgenol 183(1):175–181

    Article  PubMed  Google Scholar 

  20. Guimaraes CV, DonnellyLF SRS, Amin SR, Kalra M (2008) Relative rather than absolute macroglossia in patients with Down syndrome: implications for treatment of obstructive sleep apnea. Pediatr Radio 38(10):1062–1067

    Article  Google Scholar 

  21. Suri S, Tompson BD, Cornfoot L (2010) Cranial base, maxillary and mandibular morphology in Down syndrome. Angle Orthod 80(5):861–869

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cronk C, Crocker TM, Pueschel SM et al (1998) Growth charts for children with Down syndrome: 1 month to 18 years of age. Pediatrics 81(1):102–110

    Article  Google Scholar 

  23. Palisano RJ, Walter SD, Russell DJ et al (2001) Gross motor function of children with Down syndrome: creation of motor growth curves. Arch Phys Med Rehabil 82(4):494–500

    Article  CAS  PubMed  Google Scholar 

  24. Sanders E, Hill CM, Evans HJ, Tuffrey C (2015) The development of a screening questionnaire for obstructive sleep apnea in children with Down syndrome. Front Psychiatry 6:147. https://doi.org/10.3389/fpsyt.2015.00147

    Article  PubMed  PubMed Central  Google Scholar 

  25. Rosenfeld-Johnson S (2001) Oral –motor exercises for speech clarity. Innovative Therapists International, Tucson, AZ

    Google Scholar 

  26. American Academy of Pediatrics Committee on Genetics (2021) American Academy of Pediatrics: health supervision for children with Down syndrome. Pediatrics 107:442–449

    Article  Google Scholar 

  27. Rosen D (2011) Management of obstructive sleep apnea associated with Down syndrome and other craniofacial dysmorphologies. Curr Opin Pulm Med 17:1–6

    Google Scholar 

  28. Von Lukowicz M, Herzog N, Ruthardt S et al (2019) Effect of a 1-week intense myofunctional training on obstructive sleep apnea in children with Down syndrome. Arch Dis Child Epub 104(3):275–279. https://doi.org/10.1136/archdischild-2018-315064

    Article  Google Scholar 

  29. Villa MP, Brasili L, Ferretti A et al (2015) Oropharyngeal exercises to reduce symptoms of OSA after AT. Sleep Breath 19:281–289

    Article  PubMed  Google Scholar 

  30. Gipson K, Lu M, Kinane TB (2019) Sleep-disordered breathing in children. Pediatr Rev 40(1):3–13. https://doi.org/10.1542/pir.2018-0142. Erratum.In:PediatrRev.2019May;40(5):261.PMID:30600274;PMCID:PMC6557418

    Article  PubMed  Google Scholar 

  31. Kovaleva NV (2002) Sex ratio in Down syndrome. Tsitologiia i genetika. 36 (6): P. 90–105. ex ratio in Down syndrome. Studies in patients with confirmed trisomy 21 Kovaleva NV, Butomo IV, Körblein A. Tsitologiia i genetika 2001, N 6: 43–4 (translation: Körblein A.

  32. Kovaleva NV, Butomo IV, Korblein A (2001) Sex ratio in Down syndrome. Studies in patients with confirmed trisomy 21. Tsitologiia I genetika N 6:43–44

    Google Scholar 

  33. Howard JJM, Sarber KM, Yu W, Smith DF, Tikhtman RO, Simakajornboon N et al (2020) Outcomes in children with Down syndrome and mild obstructive sleep apnea treated non surgically. Laryngoscope 130(7):1828–1835. https://doi.org/10.1002/lary.28325. [PMCfreearticle][PubMed][CrossRef][GoogleScholar]

    Article  CAS  PubMed  Google Scholar 

  34. Hizal M, Satırer O, Polat SE, Tural DA, Ozsezen B, Sunman B, Karahan S, Emiralioglu N, Simsek-Kiper PO, Utine GE, Boduroglu K, Yalcin E, Dogru D, Kiper N, Ozcelik U (2022) Obstructive sleep apnea in children with Down syndrome: is it possible to predict severe apnea? Eur J Pediatr 181(2):735–743. https://doi.org/10.1007/s00431-021-04267-w. Epub 2021 Sep 25. PMID: 34562164; PMCID: PMC8475480

    Article  PubMed  Google Scholar 

  35. Austeng ME, Øverland B, Kværner KJ et al (2014) Obstructive sleep apnea in younger school children with Down syndrome. Int J Pediatr Otorhinolaryngol 78:1026–1029. https://doi.org/10.1016/j.ijporl.2014.03.030

    Article  PubMed  Google Scholar 

  36. Breslin J, Spanò G, Bootzin R et al (2014) Obstructive sleep apnea syndrome and cognition in Down syndrome. Dev Med Child Neurol 56:657–664. https://doi.org/10.1111/dmcn.12376

    Article  PubMed  Google Scholar 

  37. Skjodt NM, Atkar R, Easton PA (1999) Screening for hypothyroidism in sleep apnea. Am J Respir Crit Care Med 160(2):732–735. https://doi.org/10.1164/ajrccm.160.2.9802051. PMID: 10430754

    Article  CAS  PubMed  Google Scholar 

  38. Lin CC, Tsan KW, Chen PJ (1992) The relationship between sleep apnea syndrome and hypothyroidism. Chest 102:1663–1667

    Article  CAS  PubMed  Google Scholar 

  39. Nehme J, LaBerge R, Pothos M et al (2017) Predicting the presence of sleep-disordered breathing in children with Down syndrome. Sleep 36:104–108. https://doi.org/10.1016/j.sleep.2017.03.032

    Article  Google Scholar 

  40. Dyken ME, Lin-Dyken DC, Poulton S et al (2003) Prospective polysomnographic analysis of obstructive sleep apnea in Down syndrome. Arch Pediatr Adolesc Med 157:655–660. https://doi.org/10.1001/archpedi.157.7.655

    Article  PubMed  Google Scholar 

  41. Posada AM, Isaza N, Panqueva P et al (2019) High incidence of sleep-related breathing disorders in children with Down syndrome referred to a high-altitude sleep laboratory. High Alt Med Biol 20:231–235. https://doi.org/10.1089/ham.2017.0149

    Article  PubMed  Google Scholar 

  42. Kumin L, Adams J (2000) Developmental apraxia of speech and intelligibility in children with Down syndrome. Down Syndrome Quarterly 5(3):1–7

    Google Scholar 

  43. Kamrujjaman M (2018) Oral motor difficulties and speech intelligibility in Bangla speaking children with Down syndrome. Journal of Health and Medical Sciences 1(1):81–91

    Article  Google Scholar 

  44. Boshart C (1998) Oral-motor analysis and remediation techniques. Speech Dynamics Incorporated, Temecula, USA

    Google Scholar 

  45. Maccauley R, Strand E (2008) A review of standardized tests for non verbal oral and speech motor performance in children. Am J Speech Lang Pathol 17:81–91

    Article  Google Scholar 

  46. Rastogi MV, LaFranchi SH (2010) Congenital hypothyroidism. Orphanet J Rare Dis 10:5–17. https://doi.org/10.1186/1750-1172-5-17. PMID:20537182;PMCID:PMC2903524

    Article  Google Scholar 

  47. Ieto V, Kayamori F, Montes MI, Hirata RP, Gregório MG, Alencar AM, Drager LF, Genta PR, Lorenzi-Filho G (2015) Effects of oropharyngeal exercises on snoring: a randomized trial. Chest 148:683–691. https://doi.org/10.1378/chest.14-2953. [PubMed][CrossRef][GoogleScholar]

    Article  PubMed  Google Scholar 

  48. Koka V, De Vito A, Roisman G, Petitjean M, Filograna Pignatelli GR, Padovani D, Randerath W (2021) Orofacial myofunctional therapy in obstructive sleep apnea syndrome: a pathophysiological perspective. Medicina 57:323. https://doi.org/10.3390/medicina57040323

    Article  PubMed  PubMed Central  Google Scholar 

  49. Durhan MA, Agrali OB, Kiyan E et al (2019) Does obstructive sleep apnea affect oral and periodontal health in children with Down syndrome? A preliminary study, Niger. J Clin Pract 22:1175–1179. https://doi.org/10.4103/njcp.njcp_97_19

    Article  CAS  Google Scholar 

  50. Lee NC, Hsu WC, Chang LM et al (2020) REM sleep and sleep apnea are associated with language function in Down syndrome children: an analysis of a community sample. J Formos Med Assoc 119:516–523. https://doi.org/10.1016/j.jfma.2019.07.015

    Article  PubMed  Google Scholar 

  51. Shires CB, Anold SI, Schoumacher RA et al (2010) Body mass index as an indicator of obstructive sleep apnea in pediatric Down syndrome. Int J Pediatr Otorhinolaryngol 74:768–772. https://doi.org/10.1016/j.ijporl.2010.03.050

    Article  PubMed  Google Scholar 

  52. Skotko BG, Macklin EA, Muselli M et al (2017) A predictive model for obstructive sleep apnea and Down syndrome. Am J Med Genet 173:889–896. https://doi.org/10.1002/ajmg.a.38137

    Article  PubMed  Google Scholar 

  53. Cañizares-Prado S, Molina-López J, Moya MT, Planells E (2022) Oral function and eating habit problems in people with Down syndrome. Int. J. Environ. Res. Public Health. 19:2616. https://doi.org/10.3390/ijerph19052616

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Thanks to Professor Dr. Hanan Hosni Afifi, head of the developmental assessment and genetic disorders clinic, for her valuable guidance throughout the work and her cooperation to apply the study on cases presented to the genetic disorders clinic.

Funding

This research did not receive any specific grant for funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Phoniatric Unit, Otorhinolaryngology Department, Cairo University, Giza, Egypt

    Aisha Fawzy Abdel Hady

  2. Phoniatric Unit, Otolaryngology Department, Faculty of Medicine, Fayoum University, Faiyum, Egypt

    Rehab Abdel Hafeez Zaytoun

  3. Clinical Genetics Department, Human Genetics and Genome Research Institute, National Research Centre, Cairo, Egypt

    Mohamed Badie Taher & Mohammed Mamdouh Sayed-Ahmed

Authors
  1. Aisha Fawzy Abdel Hady
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  2. Rehab Abdel Hafeez Zaytoun
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  3. Mohamed Badie Taher
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  4. Mohammed Mamdouh Sayed-Ahmed
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Contributions

AF wrote the manuscript and interpreted the results. RA shared in writing and in the revision of the manuscript. MB shared in applying the protocol on cases and drafting the manuscript. MM applied the protocol on cases, collected data, and shared in writing the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Rehab Abdel Hafeez Zaytoun.

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Ethics approval and consent to participate

This study was approved by Medical Research Ethical Committee of the National Research Center under number (1425062022) on the 12th of May, 2022. A written consent was filled in and provided by the parents of the children under the study.

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Not applicable.

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The authors declare that they have no competing interests.

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Abdel Hady, A.F., Zaytoun, R.A.H., Taher, M.B. et al. Oral motor weakness: a possible clinical marker for sleep-related difficulties in Down syndrome children — a preliminary study. Egypt J Otolaryngol 39, 110 (2023). https://doi.org/10.1186/s43163-023-00463-7

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