Abstract
Sleep is a major concern in Down syndrome children. Obstructive sleep apnea, delayed sleep onset, night-time and early awakenings have been reported contributing to the cognitive and behavioral outcomes. The aim is to evaluate sleep related difficulties in Down syndrome young children. A questionnaire of sleep related difficulties was translated and validated into Arabic language then was filled in by caregivers of 45 Down syndrome and 48 normal children. The questionnaire consisted of sections related to snoring, breathing difficulties, mouth breathing, upper respiratory tract infections, sleep position, restless sleep and frequent awakening, and daytime behavior. The results show highly significant differences between the total and subtotal questionnaire scores with higher scores in the control group. The questionnaire has a good reliability. Test–retest reliability of the questionnaire revealed a significant positive correlation in the total questionnaire and all the subitems except for the 7th subitem of the daytime behavior which showed no significant correlation. The questionnaire showed 100% sensitivity and 70.8% Specificity with at cut-off value of 8.5. The sleep related difficulties questionnaire has good psychometric properties and could detect significant sleep problems in Down syndrome children.
Supplementary Information
The online version contains supplementary material available at 10.1007/s12070-023-04090-9.
Keywords: Sleep related difficulties questionnaire, Down syndrome children, Snoring, breathing difficulties
Introduction
Sleep is an opportunity for the body to conserve energy, restore its normal processes, promote physical growth, and support mental development [1]. Children who do not get enough sleep are at increased risk for negative consequences such as irritability, behavioral, learning difficulties and poor academic performance [2].
Sleep is important for children’s learning. In typical infants, sleep facilitates the abstraction of grammar rules and is required soon after learning for long-term retention to occur [3]. Nighttime sleep has been shown to improve the acquisition of novel vocabulary in school-age children [4]. Relations between poor sleep and language impairment, including difficulties processing increasing levels of linguistic complexity, have been found in studies of children diagnosed with sleep disordered breathing (SDB) [5].
Obstructive sleep apnea (OSA) is characterized by upper airway obstruction, despite respiratory effort, that disrupts normal sleep patterns and ventilation [3]. OSA can be associated with obesity, excessive soft tissue in the upper airway, decreased upper airway lumen size, or failure of pharyngeal dilator muscles [4].
In children, the obstruction is primarily due to enlarged tonsils and adenoids [6, 7]. Onset usually occurs between two and 8 years of age, coinciding with peak tonsil growth [8]. Subjective grading of tonsil size in children does not always correlate with objective findings [9].
Snoring and apneas are the classic symptoms of OSA [7, 10]. Other common symptoms include unusual sleeping positions, sleep-related paradoxical breathing, morning headaches, and excessive daytime sleepiness. Sleepiness in children is more likely to manifest as depressed mood, poor concentration, or behavioral issues [11–13].
Sleep is a major concern, especially in people with Down syndrome (DS). Obstructive sleep apnea, delayed sleep onset, night-time awakenings, and early morning awakenings have been reported in children with DS contributing to cognitive and behavioral outcomes of DS [14]. In a study by Bassell et al. [15], 76% of the children with DS were identified as having sleep problems. This prevalence is similar to the rates observed in children with autism spectrum disorders (78%) but higher than reported for other developmental disabilities [16] and typically developing children [17].
Children with DS are susceptible to the negative effects of sleep problems as they have co-occurring conditions, such as congenital heart disease [18, 19]. The presence of sleep problems in children with DS has been associated with a wide variety of negative consequences that may contribute to lower quality of life [20, 21]. If sleep problems are left untreated in children with DS, serious adverse consequences can result [22, 23].
The increased prevalence of sleep problems in children with DS is most likely related to the presence of risk factors, including craniofacial abnormalities and co-occurring conditions (e.g. congenital heart disease, obesity, hypotonia, hypothyroidism, gastroesophageal reflux and frequent ear infections) [19, 24].
The American Academy of Pediatrics recommends referring all children with DS for a sleep study or polysomnography by the age of 4 years [25]. 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 [26]. The impracticality of such technology in some parts of the world suggests a need to investigate the validity and utility of simpler screening methods.
Questionnaires of the history and physical examination show a sensitivity of 78% for findings of OSA [7]. Therefore, children with suspected OSA should be referred for objective measures as polysomnography [27, 28]. However questionnaires help to indicate the high priority groups to send to thorough objective measures.
There are few studies in Egypt addressing the sleep difficulties even fewer addressing this issue in young children and those with DS [29–32]. The questionnaires used concerned with the sleep habits and the related behavioral and psychological aspects.
This raised our concern to evaluate sleep related difficulties in DS young children. This will help send DS children with higher risk into detailed objective evaluation as an attempt to prevent adverse effects on behavioral, cognitive aspects and consequently on linguistic acquisition.
Materials and Methods
Population of the Study
This case–control study was approved by Faculty of medicine, Fayoum University ethical committee with a reference number R 385. The study was conducted on a number of 48 normal children and a number of 45 Down syndrome children who were recruited from patients seeking medical advice and follow up at Fayoum Phoniatric unit and the Developmental Assessment and Genetic disorders Clinic, Clinical Genetics Department, National Research Centre. Control group was relatives of the DS cases. DS children were cytogenetically trisomy 21 and 2 were of mosaic trisomy 21 and Robertsonian translocation 14/2; aged 2.5–7 years old. They were all of average Body Mass Index. There is no history of adenotonsillar hypertrophy. The research was conducted in December 2022.
Methodology
-
(A)
An interview and history taking by two well-trained clinical genetics researchers and a phoniatrician were carried out collecting data about the chromosomal analysis of patients, clinical examination, children’s current medical condition and if they currently have or had a history of any associated cardiac or thyroid disorders.
-
(B)
A questionnaire of Sleep related difficulties [33] was translated into Arabic language. For the purpose of validation, the questions were translated into Arabic then the Arabic version in turn was translated into English and the two versions were compared to ensure that it gives the same meaning. A pilot questionnaire in both languages was distributed first to 15 friends to apply on their children to assess the integrity of questions and evaluate any difficulties.
-
(C)
The caregivers of the normal and DS children filled in the translated questionnaire taking no more than 10 min. The questionnaire is composed of 7 sections; 33 questions corresponded to snoring, breathing difficulties, mouth breathing, upper respiratory tract infections, sleep position, restless sleep and frequent awakening, and daytime behavior. The caregivers give a score of 0 for Never, score 1 for “sometimes” and score 2 for “always”. The total score of the questionnaire is equal to 66 (see Online Appendix). Test retest was conducted on the DS children after two weeks for a reliability study.
Statistical Analysis
Quantitative data were statistically represented in terms minimum, maximum, mean, standard division (SD) and median. Comparison between different groups in the presents study was done using Mann–Whitney Test for comparing two nonparametric groups. 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).
Results
Characteristics of Subjects Under Study
The two age groups were age and gender matched (p = 0.074 for age, p = 0.813 for gender). Down syndrome children were 62% males and 38% females. Control group children were 64.60% males and 35.40% females. About 50% had associated congenital heart anomalies. About 25% of Down syndrome children had associated congenital hypothyroidism. Cytogenetically, 95.6% patients had non-disjunction trisomy 21, and two patients (4.4%) had mosaic trisomy 21 and Robertsonian translocation 14/2. The previous two DS children with mosaic trisomy 21 had comparable results to the majority of the patients with non-disjunction trisomy 21 regarding the sleep-related difficulties questionnaire.
Comparison and Correlation Studies
Comparison between the control group and Down syndrome group regarding the total and subtotal scores of sleep related difficulties questionnaire. There are highly significant differences between the total and subtotal questionnaire scores with higher scores in the control group (Table 1).
Table 1.
Comparison between control group and Down syndrome children regarding the total and subtotal scores of sleep related difficulties questionnaire
| Parameters | Groups | N | Min. | Max. | Mean ± S.D. | Median | p value |
|---|---|---|---|---|---|---|---|
| Total questionnaire score (out of 66) test | Control | 48 | 0.00 | 28.00 | 6.71 ± 7.28 | 3.50 | 0.001 |
| Cases | 45 | 9.00 | 57.00 | 26.04 ± 11.00 | 26.00 | ||
| Questionnaire section 1 score (snoring) (out of 6) test | Control | 48 | 0.00 | 6.00 | 0.96 ± 1.38 | 0.00 | 0.003 |
| Cases | 45 | 0.00 | 6.00 | 1.98 ± 1.84 | 2.00 | ||
| Questionnaire section 2 score (breathing difficulties) (out of 16) | Control | 48 | 0.00 | 5.00 | 0.33 ± 1.14 | 0.00 | 0.001 |
| Cases | 45 | 0.00 | 14.00 | 2.91 ± 3.76 | 1.00 | ||
| Questionnaire section 3 score (mouth breathing) (out of 10) T | Control | 48 | 0.00 | 5.00 | 0.65 ± 1.18 | 0.00 | 0.001 |
| Cases | 45 | 0.00 | 10.00 | 5.93 ± 2.90 | 6.00 | ||
| Questionnaire section 4 score (upper respiratory tract infections) (out of 8) | Control | 48 | 0.00 | 6.00 | 1.94 ± 1.62 | 2.00 | 0.001 |
| Cases | 45 | 0.00 | 8.00 | 3.33 ± 1.93 | 3.00 | ||
| Questionnaire section 5 score (sleep position) (out of 4) Test | Control | 48 | 0.00 | 3.00 | 0.40 ± 0.76 | 0.00 | 0.001 |
| Cases | 45 | 0.00 | 4.00 | 3.00 ± 1.31 | 4.00 | ||
| Questionnaire section 6 score (restless sleep and frequent awakening (out of 12) | Control | 48 | 0.00 | 9.00 | 1.73 ± 2.35 | 0.00 | 0.001 |
| Cases | 45 | 1.00 | 12.00 | 6.51 ± 3.09 | 7.00 | ||
| Questionnaire section 7 score (daytime behavior) (out of 10) | Control | 48 | 0.00 | 5.00 | 0.75 ± 1.39 | 0.00 | 0.001 |
| Cases | 45 | 0.00 | 7.00 | 2.38 ± 1.87 | 2.00 |
Sleep related difficulties questionnaire has a good reliability (r = 0.725) (Table 2). Test–retest reliability of the questionnaire revealed a significant positive correlation in the total questionnaire and all the subitems except for the 7th subitem of the daytime behavior which showed no significant correlation (Table 3).
Table 2.
Reliability of sleep related difficulties questionnaire
| Cronbach’s Alpha for breathing related sleep difficulties questionnaire | 0.752 |
Table 3.
Test retest reliability of scores of sleep related difficulties questionnaire
| Parameters | R (Correlation coefficient) | p value | |
|---|---|---|---|
| Total questionnaire score with re-total questionnaire score | 0.915** | 0.001 | Pa |
| Questionnaire section 1 score (snoring) with re-questionnaire section 1 score (snoring) | 0.709* | 0.022 | Pa |
| Questionnaire section 2 score (breathing difficulties) with re questionnaire section 2 score (breathing difficulties) | 0.927** | 0.001 | Pa |
| Questionnaire section 3 score (mouth breathing) with re- questionnaire section 3 score (mouth breathing) | 0.765** | 0.010 | Pa |
| Questionnaire section 4 score (upper resp. tract infections) with re-questionnaire section 4 score (upper resp. tract infections) | 0.868** | 0.001 | Pa |
| Questionnaire section 5 score (sleep position) with re-questionnaire section 5 score (sleep position) | 0.807** | 0.005 | Pa |
| Questionnaire section 6 score (restless sleep and frequent awakening) with re- questionnaire sect. 6 score (restless sleep and frequent awakening) | 0.694* | 0.026 | Pa |
| Questionnaire section 7 score (daytime behavior) with re-questionnaire sect. 7 score (daytime behavior) | 0.100 | 0.784 | Pa |
*Correlation is significant at the 0.05 level
**Correlation is significant at the 0.01 level
aPositive correlation. correlation between parameters using Spearman correlation
Total sleep related difficulties questionnaire score is the perfect marker for sleep related difficulties with area under the curve; AUC = 0.931, the marker has Sensitivity = 100% and Specificity = 70.8% at cut-off value = 8.5 (Table 4).
Table 4.
ROC-Curve Results of sleep related difficulties Questionnaire for Down syndrome group according to control group as a reference group
| Parameters | AUC | Cut-off value | Sensitivity % | Specificity % | p value | 95% CI |
|---|---|---|---|---|---|---|
| Total OSA questionnaire score (out of 66) test | 0.931 | 8.500 | 100.0% | 70.8% | 0.000 | 0.884–0.979 |
| OSA questionnaire section 1 score (Snoring) (out of 6) test | 0.668 | 0.500 | 68.9% | 58.3% | 0.005 | 0.558–0.778 |
| OSA questionnaire section 2 score (breathing difficulties) (out of 16) | 0.786 | 0.500 | 66.7% | 91.7% | 0.000 | 0.688–0.883 |
| OSA questionnaire section 3 score (mouth breathing) (out of 10) T | 0.945 | 2.500 | 88.9% | 91.7% | 0.000 | 0.897–0.993 |
| OSA questionnaire section 4 score (upper resp# tract infections) out of 8) | 0.714 | 2.500 | 66.7% | 70.8% | 0.000 | 0.609–0.820 |
| OSA questionnaire section 5 score (sleep position) (out of 4) test | 0.922 | 1.500 | 86.7% | 87.5% | 0.000 | 0.862–0.981 |
| OSA questionnaire section 6 score (restless sleep and frequent awakening out 12) | 0.891 | 1.500 | 93.3% | 64.6% | 0.000 | 0.828–0.953 |
| OSA questionnaire section 7 score (daytime behavior) (out of 10) | 0.776 | 0.500 | 82.2% | 70.8% | 0.000 | 0.680–0.873 |
Discussion
Very few validated subjective pediatric assessments for sleep difficulties have been investigated in DS. This is important because polysomnography (PSG) is often burdensome to families and standardized alternatives are recommended in this population [34]. Among the alternatives, sleep questionnaires have been proposed when evaluating patients [35, 36]. However, the psychometric properties and validity of measures of sleep disturbances have not received much attention among DS children [22].
Comparing the responses of the questionnaire for DS children with a typically developing group is important to understand the severity sleep difficulties. In the current study, the total and subtotal scores of the used translated questionnaire showed a significant difference between normal and DS groups (Table 1). This indicates the more prevalence of sleep difficulties among the DS children. This goes with the evidence indicating that children with intellectual disabilities experience problems with sleep more regularly than do normal children [37, 38]. Among the important causes of intellectual disability in DS is the presence of associated factors including structural and co-occurring medical conditions [19, 24]. This finding goes with a study done by Schwla et al. [39]
The proportion of children who had a significant sleep problem was much higher in their DS children. This is consistent with Halstead et al’s findings that found a much higher prevalence in neurodevelopmental disorders children [40].
It is important to examine the individual subscales. This helps both alerting the clinician of a potential sleep disorder providing information that serves as the starting point in evaluation [41]. Among the lower mean scores in the questionnaire was breathing difficulties. This finding was not in agreement with a study previously done by Fuca et al. [14] on preschool DS children by the use of Sleep Disturbance Scale in nearly the same age group as children in our study. DS commonly have global developmental delays resulting in behavioral problems impacting responses to the domains addressing breathing difficulty in unexpected ways [42].
The higher means were related to the subsections of restless sleep and frequent awakening and mouth breathing. This is in agreement with a previous study by Chawla et al. [39] that showed a total of 86% of his participants had a Child Sleep Habits Questionnaire-Abbreviated (CSHQ) score that was indicative of a sleep problem. Restlessness and moving a lot during sleep was a particularly common feature (76%). Night awakenings once or more than once a night was reported “always” or “usually” by 43% of their respondents, indicating that a significant proportion of children with DS have regular disturbed night-time sleep.
Key finding of this study includes the high prevalence of behavioural sleep problems highlighting the need for sleep evaluation not focused on only breathing difficulties [39].
This translated questionnaire has a good internal consistency (Table 2) showing good test retest reliability except for the subsection of daytime behavior (Table 3). Applying the questionnaire on larger scale is recommended to investigate the low reliability of this subsection. Other widely used questionnaires as the Children’s Sleep Habits Questionnaire (CSHQ), and the Sleep Disturbances Scale for Children (SDSC) showed good reliability while the alpha values for the total scores were questionable for the Behavioral Evaluation of Disorders of Sleep (BEDS) [41].
Although the number of DS children included in the study was relatively small. However, the questionnaire showed good psychometric properties. This questionnaire was 100% sensitive and could detect cases with sleep related difficulties and was 70.8% specific meaning that around 71% of Down syndrome children who don’t have sleep difficulties tested negative. The questionnaire could also detect those who do not have breathing related difficulties with a cut off level of 8.5 points (Table 4). Thus the cut off level score of the sleep related difficulties questionnaire was set at a level that maximized sensitivity to minimize false negatives that may be suggestive but not conclusive of clinical significance.
Conclusion
The results of sleep related difficulties questionnaire translated in this study could detect significant sleep problems in DS. It has good psychometric with good internal consistency, test–retest reliability, 100% sensitive and nearly 71% specific.
Limitation of the Study
Limitations included the role of both parental and retrospective bias in completing the scale, understanding the factors affecting the sleep difficulties presented by the children. Prospective studies are needed to follow up the cases in addition to correlating the findings of high risk children based on the questionnaire with polysomnography.
Supplementary Information
Below is the link to the electronic supplementary material.
Author Contribution
MM applied the protocol on cases and collected data. MB shared in applying the protocol on normal and cases and drafting the manuscript. RA edited the manuscript and contacted the journal. AF constructed the idea, wrote the manuscript, and interpreted the results. All authors read and approved the final manuscript.
Funding
No funding was obtained.
Data Availability
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
Declarations
Conflict of interest
The authors declare no conflict of interest.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.