Sleep-wake Cycle Alterations in Children and Adolescents with Autism Spectrum Disorders (Narrative Review)

Autism spectrum disorders (ASDs) are heterogeneous group of neuropsychiatric developmental disorders characterized by abnormal social interactions, communication, and stereotypical behavior. Major part of children and adolescents with ASDs have comorbid sleep-wake cycle alterations such as insomnia, circadian dysregulation, breathing disorders during sleep, parasomnia, etc. The interaction between ASDs and sleep disorders is multifactorial and bidirectional. There is data on biological, psychological, socio-environmental factors that contribute to sleep problems development, including sensory hyperreactivity, alterations of melatonin circadian rhythm, genetic mutations, inter- and externalizing behavior, changes in the environment. Disease itself, comorbid conditions (attention deficient hyperactivity disorder, mood disorders, epilepsy), as well as drugs used to treat them often have negative effects on sleep macro- and microstructure. This review examines and discusses the problem of sleep-wake cycle alterations in children with ASDs, its prevalence, structure, etiopathogenesis, clinical manifestations, sleep architecture features, diagnostic principles, and management options. Timely detection and treatment of sleep-wake cycle alterations in patients with ASDs can lead to improvements not only in their sleep quality, but also in overall functioning and development, as well as in overall family well-being.

1. Т качук Е.А., Мартынович Н.Н., Рычкова Л.В., Поляков В.М. Проблемы диагностики расстройств аутистического спектра у детей // Тихоокеанский медицинский журнал. — 2020. — Т. 4. — № 82. — С. 35–43. — d oi: https://doi.org/10.34215/1609-1175-2020-4-35-43

2. Баландина О.В., Бондарь Е.А., Власов В.В. и др. Расстройства аутистического спектра: клинические рекомендации. — М.: Минздрав России; 2024. — 98 с.

3. Намазова-Баранова Л.С., Устинова Н.В., Кайтукова Е.В. и др. Пилотный проект «Раннее выявление расстройств аутистического спектра и других нарушений нейроразвития» // Педиатрическая фармакология. — 2024. — Т. 21. — № 5. — С. 470–472. — doi: https://doi.org/10.15690/pf.v21i5.2821

4. Hirota T, King BH. Autism spectrum disorder: a review. JAMA. 2023; 329(2):157–168. doi: https://doi.org/10.1001/jama.2022.23661

5. Ustinova NV, Namazova-Baranova LS, Basova AYa, et al. The prevalence of autism spectrum disorders in the Russian Federation: a retrospective study. Consort Psychiatr. 2022;3(4):28–37. doi: https://doi.org/10.17816/CP211

6. Tkachuk EA, Rychkova LV. Problems in diagnosing autism spectrum disorders in the Irkutsk region. Int J Biomed. 2021;11(3):337–341. doi: https://doi.org/10.21103/Article11(3)_OA9

7. Долгих В.В., Старовойтова Т.Е., Погодина А.В. и др. Соматическое здоровье детей с аутизмом // Педиатрия. Журнал им. Г.Н. Сперанского. — 2014. — Т. 93. — № 5. — С. 150–153.

8. Kas MJ, Glennon JC, Buitelaar J, et al. Assessing behavioral and cognitive domains of autism spectrum disorders in rodents: current status and future perspectives. Psychopharmacology (Berl). 2014;231(6):1125–1146. doi: https://doi.org/10.1007/s00213-013-3268-5

9. Sidhu N, Wong Z, Bennett AE, Souders MC. Sleep problems in autism spectrum disorder. Pediatr Clin North Am. 2024;71(2):253– 268. doi: https://doi.org/10.1016/j.pcl.2024.01.006

10. Кельмансон И.А. Нарушения сна у детей с расстройствами аутистического спектра // Журнал неврологии и психиатрии им. С.С. Корсакова. — 2015. — № 4. — С. 102–107. — doi: https://doi.org/10.17116/jnevro201511541102-107

11. Liu X, Hubbard JA, Fabes RA, Adam JB. Sleep disturbances and correlates of children with autism spectrum disorders. Child Psychiatry Hum Dev. 2006;37(2):179–191. doi: https://doi.org/10.1007/s10578-006-0028-3

12. Malow BA, Katz T, Reynolds AM, et al. Characterizing sleep in children with autism spectrum disorders: a multidimensional approach. Sleep. 2006;29(12):1563–1571. doi: https://doi.org/10.1093/sleep/29.12.1563

13. Buckley AW, Rodriguez AJ, Jennison K, et al. Sleep patterns in children with autism spectrum disorders: a comparison with typically developing children. J Autism Dev Disord. 2010;40(6):741–750. doi: https://doi.org/10.1016/j.ridd.2014.03.037

14. Elrod MG, Hood BS. Sleep differences among children with autism spectrum disorders and typically developing peers: a meta-analysis. J Develop Behav Pediatr. 2015;36(3):166–177. doi: https://doi.org/10.1097/dbp.0000000000000140

15. Mazurek MO, Sohl K. Sleep and behavioral problems in children with autism spectrum disorder. J Autism Dev Disord. 2016;46(6):1906– 1915. doi: https://doi.org/10.1007/s10803-016-2723-7

16. Goldman SE, Alder ML, Burgess HJ, et al. Characterizing sleep in adolescents and adults with autism spectrum disorders. J Autism Dev Disord. 2017;47(6):1682–1695. doi: https://doi.org/10.1007/s10803-017-3089-1

17. Diaz-Roman A, Zhang J, Delorme R, et al. Sleep in youth with autism spectrum disorders: systematic review and meta-analysis of subjective and objective studies. Meta-Analysis Evid Based Ment Health. 2018;21(4):146–154. doi: https://doi.org/10.1136/ebmental-2018-300037

18. Deliens G, Peigneux P. Sleep-behaviour relationship in children with autism spectrum disorder: methodological pitfalls and insights from cognition and sensory processing. Dev Med Child Neurol. 2019;61(12):1368–1376. doi: https://doi.org/10.1111/dmcn.14235

19. Tomkies A, Johnson RF, Shah G, et al. Obstructive sleep apnea in children with autism. J Clin Sleep Med. 2019;15(10):1469–1476. doi: https://doi.org/10.5664/jcsm.7978

20. Chen X, Liu H, Wu Y, et al. Characteristics of sleep architecture in autism spectrum disorders: A meta-analysis based on polysomnographic research. Psychiatry Res. 2021;296:113677. doi: https://doi.org/10.1016/j.psychres.2020.113677

21. Rana M, Kothare S, DeBassio W. The assessment and treatment of sleep abnormalities in children and adolescents with autism spectrum disorder: a review. J Can Acad Child Adolesc Psychiatry. 2021;30(1):25–35.

22. Ji Q, Li SJ, Zhao JB, et al. Genetic and neural mechanisms of sleep disorders in children with autism spectrum disorder: a review. Front Psychiatry. 2023;14:1079683. doi: https://doi.org/10.3389/fpsyt.2023.1079683

23. Zaffanello M, Piacentini G, Nosetti L, Zoccante L. Sleep disordered breathing in children with autism spectrum disorder: An in-depth review of correlations and complexities. Children (Basel). 2023;10(10):1609. doi: https://doi.org/10.3390/children10101609

24. Mohammed MA, Abdalkhalig EM, Ali IA, et al. Pattern of sleep disorders among children with autism spectrum disorder. BMC Psychiatry. 2024;24(1):539. doi: https://doi.org/10.1186/s12888-024-05981-z

25. Adams HL, Matson JL, Jang J. The relationship between sleep problems and challenging behavior among children and adolescents with autism spectrum disorder. Res Autism Spectr Disord. 2014;8(9):1024–1030. doi: https://doi.org/10.1016/j.rasd.2014.05.008

26. Бердина О.Н. Роль сна и его нарушений в формировании когнитивных функций в детском возрасте (обзор литературы) // Acta Biomedica Scientifica. — 2014. — Т. 6. — № 100. — С. 115–119.

27. Кожевникова О.В., Намазова-Баранова Л.С., Мытникова Ю.С. и др. Ожирение и нарушения сна у детей // Педиатрическая фармакология. — 2016. — Т. 13. — № 6. — С. 571–576. — doi: https://doi.org/10.15690/pf.v13i6.1671.

28. Berdina O, Madaeva I, Bolshakova S, et al. Alteration of sleep homeostasis and cognitive impairment in apneic obese adolescents. Sleep Biol Rhythms. 2021;19(3):285–295. doi: https://doi.org/10.1007/s41105-021-00317-w

29. Belli A, Breda M, Di Maggio C, et al. Children with neurodevelopmental disorders: how do they sleep? Curr Opin Psychiatry. 2022;35(5):345–351. doi: https://doi.org/10.1097/YCO.0000000000000790

30. Rychkova L, Madaeva I, Berdina O, et al. Inadequate sleep habits are associated with obesity in high school children. Russian Pediatric Journal. 2021;2(3):38.

31. Yang Z, Matsumoto A, Nakayama K, et al. Circadian-relevant genes are highly polymorphic in autism spectrum disorder patients. Brain Dev. 2016;38(1):91–99. doi: https://doi.org/10.1016/j.braindev.2015.04.006

32. Abel EA, Schwichtenberg AJ, Mannin OR, Marceau K. Brief report: a gene enrichment approach applied to sleep and autism. J Autism Dev Disord. 2020;50(5):1834–1840. doi: https://doi.org/10.1007/s10803-019-03921-5

33. Pagan C, Delorme R, Callebert J, et al. The serotonin-Nacetylserotonin-melatonin pathway as a biomarker for autism spectrum disorders. Transl Psychiatry. 2014;4(11):e479. doi: https://doi.org/10.1038/tp.2014.120

34. Howes OD, Rogdaki M, Findon JL, et al. Autism spectrum disorder: Consensus guidelines on assessment, treatment and research from the British Association for Psychopharmacology. J Psychopharmacol. 2018;32(1):3–29. doi: https://doi.org/10.1177/0269881117741766; 36: 2044–55

35. Liu Z, Li X, Zhang JT, et al. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature. 2016;530:98–102. doi: https://doi.org/10.1038/nature16533

36. Banaschewski T, Bruni O, Fuentes J, et al. Practice tools for screening and monitoring insomnia in children and adolescents with autism spectrum disorder. J Autism Dev Disord. 2022;52(8):3758– 3768. doi: https://doi.org/10.1007/s10803-021-05236-w

37. Кельмансон И.А. Сон ребенка в онтогенезе и использование стандартизованного опросника для оценки поведения детей во время сна // Российский вестник перинатологии и педиатрии. — 2017. — Т. 62. — № 3. — С. 37–52. — doi: https://doi.org/10.21508/1027-4065-2017-62-3-37-52.

38. Hatch B, Nordahl CW, Schwichtenberg AJ, et al. Factor structure of the Children’s Sleep Habits Questionnaire in young children with and without autism. J Autism Dev Disord. 2021;51(9):3126–3137. doi: https://doi.org/10.1007/s10803-020-04752-5

39. Berdina O, Madaeva I, Bolshakova S, et al. Applying a translated version of the adolescent sleep habits survey in Russian high school children with obesity. Int J Biomed. 2020;10(1):61–65. doi: https://doi.org/10.21103/Article10(1)_OA10

40. Гнездицкий В.В., Корепина О.С., Карлов В.А., Новоселова Г.Б. Патологические знаки эпилептической и неэпилептической природы, выявляемые при бодрствовании и во сне во время амбулаторного и палатного мониторинга ЭЭГ: проблемы интерпретации // Эпилепсия и пароксизмальные состояния. — 2017. — Т. 9. — № 2. — С. 30–40. — doi: https://doi.org/10.17749/2077-8333.2017.9.2.030-040.

41. Mansukhani MP, Dhankikar S, Kotagal S, Kolla BP. The influence of antidepressants and actigraphy-derived sleep characteristics on pediatric multiple sleep latency testing. J Clin Sleep Med. 2021;17(11):2179–2185. doi: https://doi.org/10.5664/jcsm.9338

42. Жукова М.А. Особенности ЭЭГ-ритмов у людей с РАС // Психологическая наука и образование. — 2016. — Т. 21. — № 3. — C. 47–55. — doi: https://doi.org/10.17759/pse.2016210306.

43. Старовойтова Т.Е., Долгих В.В., Михнович В.И. и др. Электрический эпилептический статус сна (клиническое наблюдение) // Журнал неврологии и психиатрии им. С.С. Корсакова. — 2014. — Т. 114. — № 4-2. — С. 8–10.

44. Lewine JD, Andrews R, Chez M, et al. Interictal epileptiform activity in autism spectrum disorders: Relationship to sleep and clinical features. Epilepsy Behav. 2019;92:45–52. doi: https://doi.org/10.1016/j.yebeh.2018.12.011

45. Farmer CA, Chilakamarri P, Thurm AE, et al. Spindle activity in young children with autism, developmental delay, or typical development. Neurology. 2018;91(2):e112–e122. doi: https://doi.org/10.1212/WNL.0000000000005759

46. Бердина О.Н., Мадаева И.М., Поляков В.М., Рычкова Л.В. Альтерация ЭЭГ-паттерна сна как специфический маркер нейропластичности у интеллектуально одаренных школьников // Медицинский академический журнал. — 2021. — Т. 21. — № 4. — С. 7–16. — doi: https://doi.org/10.17816/MAJ65945.

47. Tononi G, Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron. 2014;81(1):12–34. doi: https://doi.org/10.1016/j.neuron.2013.12.025

48. Berdina O, Madaeva I, Rychkova L. Sleep EEG pattern in childhood: from newborn through adolescent. Eur Phys J Spec Top. 2024;233(3):705–716. doi: https://doi.org/10.1140/epjs/s11734-023-01071-5

49. Kotagal S, Malow B, Spruyt K, et al. Melatonin use in managing insomnia in children with autism and other neurogenetic disorders — an assessment by the international pediatric sleep association (IPSA). Sleep Med. 2024;119:222–228. doi: https://doi.org/10.1016/j.sleep.2024.04.008

50. Wang JJ, Imamura T, Lee J, et al. Continuous positive airway pressure for obstructive sleep apnea in children. Can Fam Physician. 2021;67(1):21–23. doi: https://doi.org/10.46747/cfp.670121

51. Johnson CR, Turne KS, Foldes E, et al. Behavioral parent training to address sleep disturbances in young children with autism spectrum disorder: a pilot trial. Sleep Med. 2013;14(10):995–1004. doi: https://doi.org/10.1016/j.sleep.2013.05.013

52. Устинова Н.В., Намазова-Баранова Л.С. Роль педиатра в раннем определении риска развития, диагностике и медицинском сопровождении детей с расстройствами аутистического спектра // Вопросы современной педиатрии. — 2021. — Т. 20. — № 2. — С. 116–121. — doi: https://doi.org/10.15690/vsp.v20i2.2255.

53. Giannotta G, Ruggiero M, Trabacca A. Chronobiology in paediatric neurological and neuropsychiatric disorders: harmonizing care with biological clocks. J Clin Med. 2024;13(24):7737. doi: https://doi.org/10.3390/jcm13247737

54. Ruan H, Eungpinichpong W, Wu H, et al. Medicine insufficient evidence for the efficacy of massage as intervention for autism spectrum disorder: a systematic review. Evid Based Complement Alternat Med. 2022;2022:5328320. doi: https://doi.org/10.1155/2022/5328320

55. Yan J, Zhang Y, Wang J, et al. Effects of transcranial magnetic stimulation on sleep structure and quality in children with autism. Front Psychiatry. 2024;15:1413961. doi: https://doi.org/10.3389/fpsyt.2024.1413961

56. Горина А.С., Колесниченко Л.С., Михнович В.И. Аминокислоты сыворотки крови и спинно-мозговой жидкости у детей с синдромом Каннера // Вестник Российского университета дружбы народов. Серия: Медицина. — 2012. — № 3. — С. 76–82.

57. Almulla AF, Thipakorn Y, Tunvirachaisakul C, Maes M. The tryptophan catabolite or kynurenine pathway in autism spectrum disorder; a systematic review and meta-analysis. Autism Res. 2023;16(12):2302–2315. doi: https://doi.org/10.1002/aur.3044

58. Бородина Л.Г. Лекарственная терапия расстройств аутистического спектра у детей: опыт зарубежных психофармакологов // Аутизм и нарушения развития. — 2012. — Т. 4. — № 39. — С. 1–18.

59. Поляков В.М., Рычкова Л.В., Белогорова Т.А. и др. Влияние применения L-триптофана на динамику когнитивных функций в комплексной терапии задержек психоречевого развития у детей // Бюллетень сибирской медицины. — 2018. — Т. 17. — № 2. — С. 71–79. — doi: https://doi.org/10.20538/1682-0363-2018-2-71-79.

60. Al-Beltagi M. Autism medical comorbidities. World J Clin Pediatr. 2021;10(3):15–28. doi: https://doi.org/10.5409/wjcp.v10.i3.