Introduction

Neurodevelopment disorders (NDDs) affect more than 2% of people worldwide [1]. Autism spectrum disorder is a developmental disorder that impacts behavior and communication [2]. It has been demonstrated to impact all demographic groups, irrespective of race, ethnicity, financial situation, or country of birth [3]. Although ASD can manifest in the first year of life, it can take till the child turns three years old to receive the diagnosis [4]. Children and adolescents with ASD often have a prevalence of sleep disturbance between 60% and 86%, which is two to three times higher than that of typically developing children [5, 6].

Children’s cognitive development and daily functioning, including attention, learning, memory, mood management, and behavior, can be negatively impacted by SDs [7, 8]. These domains are also affected by ASD, indicating that SDs may further obstruct learning and everyday functioning in children with ASD. It has also been demonstrated that parents’ sleep patterns and psychological well-being are significantly affected when their children with ASD have poor sleep [8,9,10].

Professional physicians use structured techniques such as the social responsiveness scale (SRS), Autism Diagnostic Observation Schedule Second Edition (ADOS-2), and Childhood Autism Rating Scale Second Edition (CARS-2) to observe the characteristics of ASD. The Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5) will be used to make a formal diagnosis after a multidisciplinary team evaluates cognitive function, thinking skills, language abilities, age-appropriate skills required to carry out daily tasks (such as eating, dressing, and using the restroom independently), genetic, metabolic, hearing, vision, and blood tests [3, 11,12,13]. Sleep problems can be assessed using both subjective (including sleep diaries and parental questionnaires) and objective techniques (including actigraphy, videosomnography, and polysomnography (PSG)) [11, 14, 15]. Many classification systems, such as the DSM-5 [12, 13], the International Classification of Sleep Problems, Third Edition (ICSD-3) [16], and the International Classification of Diseases, Tenth Edition (ICD-10) [16], have also been adopted to identify sleep problems formally.

As a result of recent advancements in the methods used for the diagnosis of psychological disorders and rising interest in the behaviors (like SDs) that are connected to these diseases, an increasing number of children are being diagnosed with ASD. The majority of prevalence studies of sleep problems in children diagnosed with ASD have been undertaken in developed countries and there are no particular data on the prevalence of sleep problems in children diagnosed with ASD in resource-constrained countries. Thus, the purpose of this study was to assess the pattern of common sleep disorders among Sudanese children who were diagnosed with ASD. It is difficult to diagnose and characterize every sleep disorder that often affects children diagnosed with ASD within the scope of this study. In light of the seven primary categories (insomnia, sleep-related breathing disorders, central disorders of hypersomnolence, circadian rhythm sleep-wake disorders, parasomnias, sleep-related movement disorders, and other sleep disorders) of the ICSD-3 [16], this study will mainly focus on sleep disorders, either as a single condition or as a common category for a variety of disorders. Interested readers are directed to the extensive book by Miano S., Giannotti F., and Cortesi F. on sleep problems and ASD for more information. [17].

Materials and methods

Study design, setting and duration

This descriptive, cross-sectional, facility-based study was carried out in Khartoum state between April and June of 2022 at four major specialized educational centres for ASD (the SAWA Center for Children with Autism and Developmental Disorders, the Ayadi la Teml Sudanese Organization for Autism and Developmental Disorders, the Early Interventional Center for Training of Autistic and Special Needs Children, and the Albraha International Centre for Training of Autistic Children).

Study population and eligibility criteria

Sudanese children, who were diagnosed with ASD, their ages between three and sixteen years and enrolled in ASD educational facilities were included in this study. Children with Rett’s syndrome, tuberous sclerosis complex syndrome, fragile X syndrome, or other underlying diagnoses linked to autism were excluded.

Sample size determination

Based on information gathered from the statistical departments of the autism centers included in the study, the estimated total number of cases in the chosen centers was approximately 120. With a response rate of 76.6%, 92 primary caregivers agreed to participate in the study.

Data collection and procedure

The data were collected using the Children’s Sleep Habit Questionnaire (CSHQ), a widely used sleep assessment tool for children. It is a parent questionnaire that has been used and validated retrospectively in several studies [17,18,19,20,21]. The original CSHQ has been modified with 25 items that cover common sleep disorders. The questionnaire was translated into the Arabic language, distributed to guardians and collected after 1 week.

Data analysis

The data were entered and organized, and the results of the statistical analysis were analysed using the Statistical Package for the Social Sciences (SPSS) version 26 and Microsoft Excel & Word (2016).

Results

The purpose of this study was to evaluate the patterns of sleep disorders among Sudanese children diagnosed with ASD who were receiving care at major autism institutions in Khartoum state. The study involved 92 participants. 13% were recruited from the Ayadi la Teml Center (Kafouri Branch), 30% from the Ayadi la Teml Center (Altaif Branch), 23% from the Early Interventional Center (Kafouri), 16% from the Al-Braha International Center, and 16% from the SAWA Center for Autistic Children.

Demographic data

The mean age was 6.9 ± 2.6 years. Of these children, 63 (68.5%) were boys, accounting for a boys to girls ratio of 2.17:1. Out of the 92 (100%) participants in this study, 88 (95.65%) had at least one or more SDs every day. Figure (1).

Fig. 1
figure 1

The prevalence of sleep disorders among children with ASD

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Frequency of common sleep disorders

The most prevalent sleep problems among these children were insomnia, with a range of symptoms, including 71 (77.2%) with sleep onset-associated symptoms, 52 (56.5%) with combined symptoms, 48 (52.2%) with resistant onset to sleep, and 30 (32.6%) with limited-setting symptoms. Figure (2). In the category of circadian rhythm sleep-wake disorders, the advanced sleep phase (ASP) was the second most prevalent sleep problem in these children (60.9%). In addition, narcolepsy type 2 (43,5%), nocturnal enuresis (32.6%), sleep-related movement disorder (31.5%), snoring (14.1%), narcolepsy type 1 (10.9%), and bruxism (7.6%) were among the other frequent sleep problems that were addressed. Table (1).

Fig. 2
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The prevalence of different types of insomnia

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Table 1 The prevalence of common sleep disorders other than insomnia
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Relationships of sleep disorders with gender and age

P values were greater than 0.05 for all sleep disorders (with the exception of limit-setting insomnia, circadian rhythm sleep-wake disorder (ASP type), and central disorder of hypersomnlence - (narcolepsy type 2)), according to the results of the t test used to investigate the relationship between sex and sleep disorders. Table (1). Furthermore, the association between age and sleep disorders was also examined, and P values greater than 0.05 were found for all sleep disorders (with the exception of sleep-related breathing disorder-snoring), for which the P value was 0.031. Table (2).

Table 2 Association between sleep disorders, sex and age
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Discussion

This research aimed to study the pattern of common sleep disorders among Sudanese children with ASD in Khartoum State. The results of our study indicate that children with ASD are predominantly boys, with a boy-to-girls ratio of 2.17:1. This ratio is less than the 3:1 ratio reported in Loomes’ R systematic review and meta-analysis [22].

According to our study findings, 95.65% of children diagnosed with ASD have aberrant sleep patterns daily. One of the most frequently reported medical conditions linked to ASD is sleep disorders, which affect 45–86% of children with ASD [22,23,24,25,26,27]. Studies have indicated that the chronicity of these illnesses is greater than that of children with typical development [26, 27], which has a substantial negative influence on the health and quality of life of both patients and their caregivers. It has been observed that in comparison to ASD children without sleep problems, children with ASD who suffer from sleep disorders exhibit higher levels of anxiety, depression, aggression, and attention deficit during the day, as well as more social impairment and lower performance on cognitive and sensory-motor tasks [28,29,30,31]. Although there is no consensus regarding the prevalence of sleep problems in children diagnosed with ASD, our documented prevalence is among the highest in the literature. This variation between reported prevalences is likely because different diagnostic tools were used (subjective and objective) to make ASD diagnosis, or because children of different ages were included. The most common sleep disorder reported among our study participants was insomnia, which occurred in various forms (sleep onset-associated type 71 (77.2%), limit setting 32 (32.6%), resistant onset to sleep 48 (52.2%), and combined 52 (56.5%)). Previous studies have shown that children with ASD are ten times more likely to experience insomnia than children without ASD [32]. Moreover, several behaviors have been linked to disordered sleep in individuals with ASD, including difficulty self-settling, frequent nighttime awakenings, greater sleep onset latency, early waking, and poor sleep efficiency (the ratio of total sleep time to total time spent in bed) [6]. Advanced sleep phase disorder was identified as the second most common sleep problem documented among our study participants. Despite its high incidence, ASP disorder mostly affects adolescents and adults and it is frequently confused with insomnia and early morning awakenings [32,33,34,35,36]. According to our study findings, nocturnal bedwetting 30 (32.6%) and night terrors 16 (17.4%) are the most prevalent parasomnias reported among our study participants. The data from previous research on the prevalence of parasomnias in children with ASD was inconclusive. Nonetheless, documented studies show that children with autism are frequently more susceptible to insomnia [37]. Additionally, Liu X et al. reported that the prevalence of bedwetting was 26.3% and that of parasomnias in general was 53% [23]. Our study used a single question about snoring 13 (14,1%) to screen for sleep-related breathing disorders; this question may or may not represent other sleep-related breathing disorders. Mutluer et al. reported a significant frequency of snoring and sleep problems in children diagnosed with ASD [38]. Sleep-related rhythmic movement disorder, restless leg syndrome (RLS), periodic limb movements (PLM) during sleep, and periodic limb movement disorder are among the movement disorders associated with ASD. Since the diagnosis of these disorders in the pediatric population is still difficult [16], we refer to them together as nonspecific movement disorders (NSMDs) 29 (31.5%). In addition to having trouble interacting during polysomnography, which is essential for diagnosing PLM, children with ASD may also struggle to communicate their symptoms, a skill that is necessary to permit the diagnosis of RLS. Since we are just looking at past data, we are not able to determine their actual prevalence. Furthermore, we particularly referred to the specific movement of the teeth when they clench while sleeping by sleep-related movement disorder-bruxism (7.6%). Since children with ASD frequently exhibit bruxism and rhythmic movement disorders both during the day and when they sleep, these conditions are equally concerning. The mentioned factors contribute to the challenge of accurately diagnosing sleep-related movement disorders, which in turn makes it challenging to carry out studies to determine the prevalence and management of these disorders in children diagnosed with ASD. An excessive amount of daytime sleepiness that cannot be linked to another sleep problem is referred to as a central disorder of hypersomnolence. Based on the presence or absence of cataplexy, 10 (10.9%) patients were classified as having narcolepsy type 1, and 40 (43.5%) patients were classified as having type 2 narcolepsy, respectively. There is a dearth of published research on the frequency of narcolepsy in children with ASD. This could be the result of a complex diagnosis, which was reached after a thorough physical examination, a thorough clinical history, and a neurological assessment along with a polysomnography. We cannot determine whether it is an actual prevalence or not; we are only screening for them based on history. Gender significantly influenced the likelihood of having insomnia, advanced sleep phase disorder, and type 2 narcolepsy (P values = 0.033, 0.009, and 0.037, respectively). Moreover, there was no associations between age and any type of sleep problems, with the exception of snoring (p value = 0.031). This is in contrast to the reported in Santapuram et al., who found no relationship between age and obstructive sleep apnea symptoms, such as snoring [39].

Conclusion

According to our study findings, there is a high frequency of sleep disorders among Sudanese children diagnosed with ASD. The most prevalent type of sleep disorder is insomnia, whereas the least common type is bruxism. Limit-setting insomnia, advanced sleep phase disorders, and narcolepsy type 2 are more prevalent in boys and have a strong gender relationship. Age-related increases have been observed in snoring.

Limitations, strengths and future prospects

There are a few limitations to our study. First, the demographic information for children with ASD is limited. Second, the sample size was relatively small, making it less representative. This may be related to the constraints imposed by the nation’s economic situation, particularly during the COVID-19 pandemic, which has limited and decreased parent-child communication with autism centres. Third, there was no control group. Fourth, because the study only included parent reports of their children’s sleep problems, recall bias may be a weakness. Finally, there is a lack of objective measures, such as structured in-depth interviews and objective evaluations, which may have provided greater information on sleep problems and permitted a more accurate diagnosis [40]. However, this research is the first in Sudan and most probably all of Africa that looks into the patterns of sleep disturbances in children diagnosed with ASD, which is a starting point toward a better understanding of these conditions. Future studies especially in resource-limited countries are required to develop national guidelines for the prevalence, presentation, screening, and treatment of SDs among children diagnosed with ASD.