Advertisement

Sleep Abnormalities in Multiple Sclerosis

  • Giorgos K. SakkasEmail author
  • Christoforos D. Giannaki
  • Christina Karatzaferi
  • Mauro Manconi
Sleep Disorders (A Iranzo, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Sleep Disorders

Abstract

Purpose of review

This review summarizes the most well-documented sleep disorders seen in patients with multiple sclerosis (MS), with a special focus on the impact on quality of life.

Recent findings

Sleep abnormalities in patients with MS are a multifactorial and relatively complex issue affecting approximately 60% of the patients while the pathophysiology of these symptoms is not fully understood. Circadian rhythm disorders and increased levels of pro-inflammatory cytokines have been recognized as potential players in affecting sleep homeostasis in MS patients. Medication-related side effects such as in immunotherapy and other factors such as lesion load can contribute to the disruption of normal sleep patterns.

Summary

Most frequently encountered sleep disorders are insomnia, sleep-related movement disorders, sleep-related breathing disorders, and circadian rhythm disorders affecting both adults and paediatric MS populations. Aetiology still remains unknown with treatment options focusing on behavioural cognitive therapy and lifestyle modification including improvement in sleep hygiene as well as melatonin supplementation. Given MS prevalence is still rising affecting millions of people, more personalized medicine applications should possibly form the key approach for improving patients’ quality of life and quality years.

Keywords

Immune-mediated diseases Quality of life Melatonin Fatigue Survival Circadian 

Notes

Compliance with Ethical Standards

Conflict of Interest

Giorgos Sakkas, Christoforos D. Giannaki, Christina Karatzaferi, and Mauro Manconi each declare no potential conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Buysse DJ. Sleep health: can we define it? Does it matter? Sleep. 2014;37(1):9–17.  https://doi.org/10.5665/sleep.3298.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Cavalera C, Rovaris M, Mendozzi L, Pugnetti L, Garegnani M, Castelnuovo G, et al. Online meditation training for people with multiple sclerosis: a randomized controlled trial. Mult Scler. 2018;1352458518761187:135245851876118.  https://doi.org/10.1177/1352458518761187.CrossRefGoogle Scholar
  3. 3.
    Hughes AJ, Dunn KM, Chaffee T. Sleep disturbance and cognitive dysfunction in multiple sclerosis: a systematic review. Curr Neurol Neurosci Rep. 2018;18(1):2.  https://doi.org/10.1007/s11910-018-0809-7.CrossRefPubMedGoogle Scholar
  4. 4.
    Vitkova M, Gdovinova Z, Rosenberger J, Szilasiova J, Nagyova I, Mikula P, et al. Factors associated with poor sleep quality in patients with multiple sclerosis differ by disease duration. Disabil Health J. 2014;7(4):466–71.  https://doi.org/10.1016/j.dhjo.2014.05.004.CrossRefPubMedGoogle Scholar
  5. 5.
    Archer SN, Laing EE, Moller-Levet CS, van der Veen DR, Bucca G, Lazar AS, et al. Mistimed sleep disrupts circadian regulation of the human transcriptome. Proc Natl Acad Sci U S A. 2014;111(6):E682–91.  https://doi.org/10.1073/pnas.1316335111.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Calandra-Buonaura G, Provini F, Guaraldi P, Plazzi G, Cortelli P. Cardiovascular autonomic dysfunctions and sleep disorders. Sleep Med Rev. 2016;26:43–56.  https://doi.org/10.1016/j.smrv.2015.05.005.CrossRefPubMedGoogle Scholar
  7. 7.
    Harbo HF, Gold R, Tintore M. Sex and gender issues in multiple sclerosis. Ther Adv Neurol Disord. 2013;6(4):237–48.  https://doi.org/10.1177/1756285613488434.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Gilmour H, Ramage-Morin PL, Wong SL. Multiple sclerosis: prevalence and impact. Health Rep. 2018;29(1):3–8.PubMedGoogle Scholar
  9. 9.
    Browne P, Chandraratna D, Angood C, Tremlett H, Baker C, Taylor BV, et al. Atlas of multiple sclerosis 2013: a growing global problem with widespread inequity. Neurology. 2014;83(11):1022–4.  https://doi.org/10.1212/WNL.0000000000000768.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Matveeva O, Bogie JFJ, Hendriks JJA, Linker RA, Haghikia A, Kleinewietfeld M. Western lifestyle and immunopathology of multiple sclerosis. Ann N Y Acad Sci. 2018;1417(1):71–86.  https://doi.org/10.1111/nyas.13583.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Belbasis L, Bellou V, Evangelou E, Ioannidis JP, Tzoulaki I. Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses. Lancet Neurol. 2015;14(3):263–73.  https://doi.org/10.1016/S1474-4422(14)70267-4.CrossRefPubMedGoogle Scholar
  12. 12.
    Olsson T, Barcellos LF, Alfredsson L. Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis. Nat Rev Neurol. 2017;13(1):25–36.  https://doi.org/10.1038/nrneurol.2016.187.CrossRefPubMedGoogle Scholar
  13. 13.
    Kaynak H, Altintas A, Kaynak D, Uyanik O, Saip S, Agaoglu J, et al. Fatigue and sleep disturbance in multiple sclerosis. Eur J Neurol. 2006;13(12):1333–9.  https://doi.org/10.1111/j.1468-1331.2006.01499.x.CrossRefPubMedGoogle Scholar
  14. 14.
    • Amtmann D, Bamer AM, Kim J, Chung H, Salem R. People with multiple sclerosis report significantly worse symptoms and health related quality of life than the US general population as measured by PROMIS and NeuroQoL outcome measures. Disabil Health J. 2018;11(1):99–107.  https://doi.org/10.1016/j.dhjo.2017.04.008 Individuals with MS report clinically meaningful worse health compared to the general population across multiple health related domains. Symptom profiles utilizing PROMIS or NeuroQoL measures can be used to quickly assess symptom levels in an individual or group.CrossRefPubMedGoogle Scholar
  15. 15.
    Shahrbanian S, Duquette P, Kuspinar A, Mayo NE. Contribution of symptom clusters to multiple sclerosis consequences. Qual Life Res. 2015;24(3):617–29.  https://doi.org/10.1007/s11136-014-0804-7.CrossRefPubMedGoogle Scholar
  16. 16.
    Bamer AM, Johnson KL, Amtmann D, Kraft GH. Prevalence of sleep problems in individuals with multiple sclerosis. Mult Scler. 2008;14(8):1127–30.  https://doi.org/10.1177/1352458508092807.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    • Garland SN, Scurrey SRM, Ploughman M, Health L, Aging with MSCC. Factors associated with poor sleep in older adults with multiple sclerosis. Int J Behav Med. 2017;24(6):937–45.  https://doi.org/10.1007/s12529-017-9653-4 Individuals with MS who had clinically significant levels of anxiety were two times more likely to have trouble sleeping when compared to individuals without anxiety. Efforts should focus on early identification and effective interventions for poor sleep in individuals living with MS.CrossRefPubMedGoogle Scholar
  18. 18.
    Boe Lunde HM, Aae TF, Indrevag W, Aarseth J, Bjorvatn B, Myhr KM, et al. Poor sleep in patients with multiple sclerosis. PLoS One. 2012;7(11):e49996.  https://doi.org/10.1371/journal.pone.0049996.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    •• Morris G, Stubbs B, Kohler CA, Walder K, Slyepchenko A, Berk M, et al. The putative role of oxidative stress and inflammation in the pathophysiology of sleep dysfunction across neuropsychiatric disorders: Focus on chronic fatigue syndrome, bipolar disorder and multiple sclerosis. Sleep Med Rev. 2018.  https://doi.org/10.1016/j.smrv.2018.03.007 This review focus on chronic fatigue syndrome, bipolar disorder, and multiple sclerosis as exemplars of neuro-immune disorders. They concluded that novel therapeutic targets exploring immune and oxidative & nitrosative pathways (p.e. melatonin and molecular hydrogen) hold promise in alleviating sleep and circadian dysfunction in these disorders.
  20. 20.
    Schutte-Rodin S, Broch L, Buysse D, Dorsey C, Sateia M. Clinical guideline for the evaluation and management of chronic insomnia in adults. J Clin Sleep Med. 2008;4(5):487–504.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Chalah MA, Riachi N, Ahdab R, Creange A, Lefaucheur JP, Ayache SS. Fatigue in multiple sclerosis: neural correlates and the role of non-invasive brain stimulation. Front Cell Neurosci. 2015;9:460.  https://doi.org/10.3389/fncel.2015.00460.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Veauthier C, Radbruch H, Gaede G, Pfueller CF, Dorr J, Bellmann-Strobl J, et al. Fatigue in multiple sclerosis is closely related to sleep disorders: a polysomnographic cross-sectional study. Mult Scler. 2011;17(5):613–22.  https://doi.org/10.1177/1352458510393772.CrossRefPubMedGoogle Scholar
  23. 23.
    Bamer AM, Johnson KL, Amtmann DA, Kraft GH. Beyond fatigue: assessing variables associated with sleep problems and use of sleep medications in multiple sclerosis. Clin Epidemiol. 2010;2010(2):99–106.  https://doi.org/10.2147/CLEP.S10425.CrossRefPubMedGoogle Scholar
  24. 24.
    Merlino G, Fratticci L, Lenchig C, Valente M, Cargnelutti D, Picello M, et al. Prevalence of ‘poor sleep’ among patients with multiple sclerosis: an independent predictor of mental and physical status. Sleep Med. 2009;10(1):26–34.  https://doi.org/10.1016/j.sleep.2007.11.004.CrossRefPubMedGoogle Scholar
  25. 25.
    Neau JP, Paquereau J, Auche V, Mathis S, Godeneche G, Ciron J, et al. Sleep disorders and multiple sclerosis: a clinical and polysomnography study. Eur Neurol. 2012;68(1):8–15.  https://doi.org/10.1159/000335076.CrossRefPubMedGoogle Scholar
  26. 26.
    •• Group GBDNDC. Global, regional, and national burden of neurological disorders during 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Neurol. 2017;16(11):877–97.  https://doi.org/10.1016/S1474-4422(17)30299-5 This systematic analysis assess the global burden of neurological disorders. They concluded that the number has increased substantially over the past 25 years because of expanding population numbers and ageing, despite substantial decreases in mortality rates from stroke and communicable neurological disorders. The number of patients who will need care by clinicians with expertise in neurological conditions will continue to grow in coming decades. Policy makers and health-care providers should be aware of these trends to provide adequate services. CrossRefGoogle Scholar
  27. 27.
    Wade BJ. Spatial analysis of global prevalence of multiple sclerosis suggests need for an updated prevalence scale. Mult Scler Int. 2014;2014:124578–7.  https://doi.org/10.1155/2014/124578.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Melcon MO, Correale J, Melcon CM. Is it time for a new global classification of multiple sclerosis? J Neurol Sci. 2014;344(1–2):171–81.  https://doi.org/10.1016/j.jns.2014.06.051.CrossRefPubMedGoogle Scholar
  29. 29.
    Ebers GC. Environmental factors and multiple sclerosis. Lancet Neurol. 2008;7(3):268–77.  https://doi.org/10.1016/S1474-4422(08)70042-5.CrossRefPubMedGoogle Scholar
  30. 30.
    Wendel-Haga M, Celius EG. Is the hygiene hypothesis relevant for the risk of multiple sclerosis? Acta Neurol Scand. 2017;136(Suppl 201):26–30.  https://doi.org/10.1111/ane.12844.CrossRefPubMedGoogle Scholar
  31. 31.
    Brass SD, Li CS, Auerbach S. The underdiagnosis of sleep disorders in patients with multiple sclerosis. J Clin Sleep Med. 2014;10(9):1025–31.  https://doi.org/10.5664/jcsm.4044.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Manconi M, Fabbrini M, Bonanni E, Filippi M, Rocca M, Murri L, et al. High prevalence of restless legs syndrome in multiple sclerosis. Eur J Neurol. 2007;14(5):534–9.CrossRefGoogle Scholar
  33. 33.
    Manconi M, Ferini-Strambi L, Filippi M, Bonanni E, Iudice A, Murri L, et al. Multicenter case-control study on restless legs syndrome in multiple sclerosis: the REMS study. Sleep. 2008;31(7):944–52.CrossRefGoogle Scholar
  34. 34.
    Douay X, Waucquier N, Hautecoeur P, Vermersch P. G SEP. (high prevalence of restless legs syndrome in multiple sclerosis). Rev Neurol. 2009;165(2):194–6.  https://doi.org/10.1016/j.neurol.2008.06.001.CrossRefPubMedGoogle Scholar
  35. 35.
    Vavrova J, Kemlink D, Sonka K, Havrdova E, Horakova D, Pardini B, et al. Restless legs syndrome in Czech patients with multiple sclerosis: an epidemiological and genetic study. Sleep Med. 2012;13(7):848–51.  https://doi.org/10.1016/j.sleep.2012.03.012.CrossRefPubMedGoogle Scholar
  36. 36.
    •• Braley TJ, Chervin RD. A practical approach to the diagnosis and management of sleep disorders in patients with multiple sclerosis. Ther Adv Neurol Disord. 2015;8(6):294–310.  https://doi.org/10.1177/1756285615605698 This is a very important review. It summarizes the most common sleep disorders experienced by persons with MS, and offers a practical approach to diagnosis and management of these conditions.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    •• Veauthier C, Paul F. Sleep disorders in multiple sclerosis and their relationship to fatigue. Sleep Med. 2014;15(1):5–14.  https://doi.org/10.1016/j.sleep.2013.08.791 This review assess the impact of sleep disorders in relation to fatigue in patients with MS. The authors suggest that an effective treatment of sleep disorders can lead to an improvement of MS-related fatigue and they propose that in all MS studies, researchers should investigate sleep and considere it as a relevant confounder.CrossRefPubMedGoogle Scholar
  38. 38.
    Stanton BR, Barnes F, Silber E. Sleep and fatigue in multiple sclerosis. Mult Scler. 2006;12(4):481–6.  https://doi.org/10.1191/135248506ms1320oa.CrossRefPubMedGoogle Scholar
  39. 39.
    • Alhazzani AA, Alshahrani A, Alqahtani M, Alamri R, Alqahtani R, Alqahtani M, et al. Insomnia among non-depressed multiple sclerosis patients: a cross-sectional study. Egypt J Neurol Psychiatr Neurosurg. 2018;54(1):17.  https://doi.org/10.1186/s41983-018-0016-0 The study was conducted to assess insomnia among non-depressed MS patients in Saudi Arabia. Prevalence of insomnia among non-depressed MS patients is low while it is associated with educational and use of antidepressants.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Espie CA, Luik AI, Cape J, Drake CL, Siriwardena AN, Ong JC, et al. Digital Cognitive Behavioural Therapy for Insomnia versus sleep hygiene education: the impact of improved sleep on functional health, quality of life and psychological well-being. Study protocol for a randomised controlled trial. Trials. 2016;17(1):257.  https://doi.org/10.1186/s13063-016-1364-7.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    •• Morin CM, Beaulieu-Bonneau S, Belanger L, Ivers H, Sanchez Ortuno M, Vallieres A, et al. Cognitive-behavior therapy singly and combined with medication for persistent insomnia: Impact on psychological and daytime functioning. Behav Res Ther. 2016;87:109–16.  https://doi.org/10.1016/j.brat.2016.09.002 The study evaluated the impact of cognitive-behavior therapy alone and combined with medication, on various indices of daytime and psychological functioning. Following acute treatment, significant improvements of fatigue, quality of life (mental component), anxiety, and depression were obtained in the CBT alone condition but not in the combined CBT plus medication condition. Following extended treatment, further improvements were noted for the subgroup receiving extended CBT relative to that with no additional treatment, and for the subgroup receiving CBT and intermittent medication relative to that with CBT but no medication.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    • Sanchez-Barcelo EJ, Rueda N, Mediavilla MD, Martinez-Cue C, Reiter RJ. Clinical Uses of Melatonin in Neurological Diseases and Mental and Behavioural Disorders. Curr Med Chem. 2017;24(35):3851–78.  https://doi.org/10.2174/0929867324666170718105557 In this review article, the administration of melatonin to humans for various therapeutic purposes in the field of neuropathology was assessed. The authors concluded that melatonin has the potential to become a strong player in the improvement of sleep in patients with neurological disorders, however clinical trials with strong methodologies and appropriate doses of melatonin are necessary to further support the usefulness of melatonin.CrossRefPubMedGoogle Scholar
  43. 43.
    Becker PM, Sharon D. Mood disorders in restless legs syndrome (Willis-Ekbom disease). J Clin Psychiatry. 2014;75(7):e679–94.  https://doi.org/10.4088/JCP.13r08692.CrossRefPubMedGoogle Scholar
  44. 44.
    Allen RP, Picchietti DL, Garcia-Borreguero D, Ondo WG, Walters AS, Winkelman JW, et al. Restless legs syndrome/Willis-Ekbom disease diagnostic criteria: updated International Restless Legs Syndrome Study Group (IRLSSG) consensus criteria--history, rationale, description, and significance. Sleep Med. 2014;15(8):860–73.  https://doi.org/10.1016/j.sleep.2014.03.025.CrossRefPubMedGoogle Scholar
  45. 45.
    Hardy De Buisseret FX, Mairesse O, Newell J, Verbanck P, Neu D. While isolated periodic limb movement disorder significantly impacts sleep depth and efficiency, co-morbid restless leg syndrome mainly exacerbates perceived sleep quality. Eur Neurol. 2017;77(5–6):272–80.  https://doi.org/10.1159/000471920.CrossRefPubMedGoogle Scholar
  46. 46.
    Gomez-Choco MJ, Iranzo A, Blanco Y, Graus F, Santamaria J, Saiz A. Prevalence of restless legs syndrome and REM sleep behavior disorder in multiple sclerosis. Mult Scler. 2007;13(6):805–8.  https://doi.org/10.1177/1352458506074644.CrossRefPubMedGoogle Scholar
  47. 47.
    Giannaki CD, Hadjigeorgiou GM, Karatzaferi C, Pantzaris MC, Stefanidis I, Sakkas GK. Epidemiology, impact, and treatment options of restless legs syndrome in end-stage renal disease patients: an evidence-based review. Kidney Int. 2014;85(6):1275–82.  https://doi.org/10.1038/ki.2013.394.CrossRefPubMedGoogle Scholar
  48. 48.
    Manconi M, Ferri R, Feroah TR, Zucconi M, Ferini-Strambi L. Defining the boundaries of the response of sleep leg movements to a single dose of dopamine agonist. Sleep. 2008;31(9):1229–37.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Minar M, Petrlenicova D, Valkovic P. Higher prevalence of restless legs syndrome/Willis-Ekbom disease in multiple sclerosis patients is related to spinal cord lesions. Mult Scler Relat Disord. 2017;12:54–8.  https://doi.org/10.1016/j.msard.2016.12.013.CrossRefPubMedGoogle Scholar
  50. 50.
    Manconi M, Rocca MA, Ferini-Strambi L, Tortorella P, Agosta F, Comi G, et al. Restless legs syndrome is a common finding in multiple sclerosis and correlates with cervical cord damage. Mult Scler. 2008;14(1):86–93.  https://doi.org/10.1177/1352458507080734.CrossRefPubMedGoogle Scholar
  51. 51.
    •• Giannaki CD, Aristotelous P, Stefanakis M, Hadjigeorgiou GM, Manconi M, Leonidou E, et al. Restless legs syndrome in Multiple Sclerosis patients: a contributing factor for fatigue, impaired functional capacity, and diminished health-related quality of life. Neurol Res. 2018;40(7):586–92.  https://doi.org/10.1080/01616412.2018.1454719 The study was assessing whether RLS could affect the functional capacity and various contributing parameters related to quality of life and fatigue in MS patients. The aurthors concluded that RLS seems to contribute even further to impairments on sleep, fatigue, functional capacity, and therefore HRQoL levels in relapsing-remitting MS patients.CrossRefPubMedGoogle Scholar
  52. 52.
    •• Kotterba S, Neusser T, Norenberg C, Bussfeld P, Glaser T, Dorner M, et al. Sleep quality, daytime sleepiness, fatigue, and quality of life in patients with multiple sclerosis treated with interferon beta-1b: results from a prospective observational cohort study. BMC Neurol. 2018;18(1):123.  https://doi.org/10.1186/s12883-018-1113-5 This observational cohort study was aiming to investigate the relationship between sleep quality, fatigue, quality of life, and comorbidities in patients with MS. The authors confirm the high prevalence of poor sleep quality among patients with MS and its persistent correlation with fatigue and reduced quality of life over time. They highlight the importance of interventions to improve sleep quality.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Aurora RN, Kristo DA, Bista SR, Rowley JA, Zak RS, Casey KR, et al. The treatment of restless legs syndrome and periodic limb movement disorder in adults--an update for 2012: practice parameters with an evidence-based systematic review and meta-analyses: an American Academy of Sleep Medicine Clinical Practice Guideline. Sleep. 2012;35(8):1039–62.  https://doi.org/10.5665/sleep.1988.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    •• Hensen HA, Krishnan AV, Eckert DJ. Sleep-Disordered Breathing in People with Multiple Sclerosis: Prevalence, Pathophysiological Mechanisms, and Disease Consequences. Front Neurol. 2017;8:740.  https://doi.org/10.3389/fneur.2017.00740 This review was aiming to shed light in the pathophysiological mechanisms that contribute to sleep disordered breathing in people with MS or whether MS contributes to SDB disease progression. The authors concluded that recent evidence indicate that treatment of SDB in people with MS with conventional first-line therapy, continuous positive airway pressure therapy, can reduce fatigue and cognitive impairment. CrossRefPubMedGoogle Scholar
  55. 55.
    Sleep-related breathing disorders in adults: recommendations for syndrome definition and measurement techniques in clinical research. The Report of an American Academy of Sleep Medicine Task Force. Sleep. 1999;22(5):667–89.Google Scholar
  56. 56.
    Braley TJ, Segal BM, Chervin RD. Obstructive sleep apnea and fatigue in patients with multiple sclerosis. J Clin Sleep Med. 2014;10(2):155–62.  https://doi.org/10.5664/jcsm.3442.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kaminska M, Kimoff RJ, Benedetti A, Robinson A, Bar-Or A, Lapierre Y, et al. Obstructive sleep apnea is associated with fatigue in multiple sclerosis. Mult Scler. 2012;18(8):1159–69.  https://doi.org/10.1177/1352458511432328.CrossRefPubMedGoogle Scholar
  58. 58.
    Edwards BA, Eckert DJ, Jordan AS. Obstructive sleep apnoea pathogenesis from mild to severe: is it all the same? Respirology. 2017;22(1):33–42.  https://doi.org/10.1111/resp.12913.CrossRefPubMedGoogle Scholar
  59. 59.
    Dempsey JA, Veasey SC, Morgan BJ, O'Donnell CP. Pathophysiology of sleep apnea. Physiol Rev. 2010;90(1):47–112.  https://doi.org/10.1152/physrev.00043.2008.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Chotinaiwattarakul W, O'Brien LM, Fan L, Chervin RD. Fatigue, tiredness, and lack of energy improve with treatment for OSA. J Clin Sleep Med. 2009;5(3):222–7.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Rong ZH, Li WB, Liu W, Cai BH, Wang J, Yang M, et al. Nasal bi-level positive airway pressure (BiPAP) versus nasal continuous positive airway pressure (CPAP) in preterm infants </=32 weeks: a retrospective cohort study. J Paediatr Child Health. 2016;52(5):493–8.  https://doi.org/10.1111/jpc.13175.CrossRefPubMedGoogle Scholar
  62. 62.
    Najafi MR, Toghianifar N, Etemadifar M, Haghighi S, Maghzi AH, Akbari M. Circadian rhythm sleep disorders in patients with multiple sclerosis and its association with fatigue: a case-control study. Journal of research in medical sciences : the official journal of Isfahan University of Medical Sciences. 2013;18(Suppl 1):S71–3.Google Scholar
  63. 63.
    Lunde HM, Bjorvatn B, Myhr KM, Bo L. Clinical assessment and management of sleep disorders in multiple sclerosis: a literature review. Acta Neurol Scand Suppl. 2013;196:24–30.  https://doi.org/10.1111/ane.12046.CrossRefGoogle Scholar
  64. 64.
    Taphoorn MJ, van Someren E, Snoek FJ, Strijers RL, Swaab DF, Visscher F, et al. Fatigue, sleep disturbances and circadian rhythm in multiple sclerosis. J Neurol. 1993;240(7):446–8.CrossRefGoogle Scholar
  65. 65.
    Ferini-Strambi L, Filippi M, Martinelli V, Oldani A, Rovaris M, Zucconi M, et al. Nocturnal sleep study in multiple sclerosis: correlations with clinical and brain magnetic resonance imaging findings. J Neurol Sci. 1994;125(2):194–7.CrossRefGoogle Scholar
  66. 66.
    Wen J, Ariyannur PS, Ribeiro R, Tanaka M, Moffett JR, Kirmani BF, et al. Efficacy of N-acetylserotonin and melatonin in the EAE model of multiple sclerosis. J NeuroImmune Pharmacol. 2016;11(4):763–73.  https://doi.org/10.1007/s11481-016-9702-9.CrossRefPubMedGoogle Scholar
  67. 67.
    Tachibana N, Howard RS, Hirsch NP, Miller DH, Moseley IF, Fish D. Sleep problems in multiple sclerosis. Eur Neurol. 1994;34(6):320–3.  https://doi.org/10.1159/000117070.CrossRefPubMedGoogle Scholar
  68. 68.
    Sikes EM, Motl RW, Ness JM. Pediatric multiple sclerosis: current perspectives on health behaviors. Pediatric Health Med Ther. 2018;9:17–25.  https://doi.org/10.2147/PHMT.S140765.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Grover SA, Aubert-Broche B, Fetco D, Collins DL, Arnold DL, Finlayson M, et al. Lower physical activity is associated with higher disease burden in pediatric multiple sclerosis. Neurology. 2015;85(19):1663–9.  https://doi.org/10.1212/WNL.0000000000001939.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Grover SA, Sawicki CP, Kinnett-Hopkins D, Finlayson M, Schneiderman JE, Banwell B, et al. Physical activity and its correlates in youth with multiple sclerosis. J Pediatr. 2016;179:197–203 e2.  https://doi.org/10.1016/j.jpeds.2016.08.104.CrossRefPubMedGoogle Scholar
  71. 71.
    Zafar AB, Ness J, Dowdy S, Avis K, Bashir K. Examining sleep, fatigue, and daytime sleepiness in pediatric multiple sclerosis patients. Mult Scler. 2012;18(4):481–8.  https://doi.org/10.1177/1352458511424307.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Giorgos K. Sakkas
    • 1
    • 2
    Email author
  • Christoforos D. Giannaki
    • 3
  • Christina Karatzaferi
    • 1
    • 2
  • Mauro Manconi
    • 4
    • 5
  1. 1.School of Physical Education and Sport ScienceUniversity of ThessalyTrikalaGreece
  2. 2.Faculty of Sport, Health and WellbeingPlymouth Marjon UniversityPlymouthUK
  3. 3.Department of Life and Health SciencesUniversity of NicosiaNicosiaCyprus
  4. 4.Sleep and Epilepsy Center, Neurocenter of Southern SwitzerlandCivic Hospital (EOC) of LuganoLuganoSwitzerland
  5. 5.Neurology Department InselspitalBern University HospitalBernSwitzerland

Personalised recommendations