Sleep and epilepsy

The intimate relationship between sleep and epilepsy has long been recognized, yet our understanding of the relationship is incomplete. In this article we address four key issues in this area. First, we consider the reciprocal interaction between sleep and epilepsy. Sleep state clearly influences seizure onset, particularly in certain epilepsy syndromes. The converse is also true; epilepsy may disrupt sleep, either directly through seizures and epileptiform activity, or indirectly through medication-related effects. Unraveling the influences of sleep stage, epilepsy syndrome, and drug effects is challenging, and the current state of knowledge is reviewed. Secondly, accurate diagnosis of sleep-related epilepsy can be difficult, particularly the distinction of nocturnal frontal lobe epilepsy (NFLE) from arousal parasomnias. The challenges in this area, along with work from the authors, are discussed. Thirdly, we will explore the putative relationship between obstructive sleep apnea (OSA) and epilepsy, including the effect of OSA on quality of life; this will lead us to a brief exploration of the effects of OSA on neuroendocrine function. Finally, we will review the evidence surrounding the role of sleep in sudden unexpected death in epilepsy (SUDEP).

[1]  P. Lavie,et al.  Disruption of the nocturnal testosterone rhythm by sleep fragmentation in normal men. , 2001, The Journal of clinical endocrinology and metabolism.

[2]  S Smirne,et al.  The macrostructure and microstructure of sleep in patients with autosomal dominant nocturnal frontal lobe epilepsy. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[3]  D. King,et al.  Pseudoseizures , 1982, Neurology.

[4]  L. Parrino,et al.  Sleep in Lennox–Gastaut syndrome: the role oft the cyclic alternating pattern (CAP) in the gate control of clinical seizures and generalized polyspikes , 2001, Epilepsy Research.

[5]  B. Malow,et al.  Obstructive sleep apnea is common in medically refractory epilepsy patients , 2000, Neurology.

[6]  C. Derry,et al.  The Sleep Manifestations of Frontal Lobe Epilepsy , 2011, Current neurology and neuroscience reports.

[7]  C. Guilleminault,et al.  Sleep apnea syndrome due to upper airway obstruction: a review of 25 cases. , 1977, Archives of internal medicine.

[8]  H. Shibasaki,et al.  Supplementary motor area seizure resembling sleep disorder. , 1996, Sleep.

[9]  J D Frost,et al.  Precise characterization and quantification of infantile spasms , 1979, Annals of neurology.

[10]  S. Grillner.  The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[11]  E. Neidhart,et al.  HLA and genetic susceptibility to sleepwalking , 2003, Molecular Psychiatry.

[12]  S. Duncan,et al.  Antiepileptic Drug Therapy and Sexual Function in Men with Epilepsy , 1999, Epilepsia.

[13]  J. Touchon,et al.  Sleep organization and epilepsy. , 1991, Epilepsy research. Supplement.

[14]  P. Coubes,et al.  The Relationship Between Sleep and Epilepsy in Frontal and Temporal Lobe Epilepsies: Practical and Physiopathologic Considerations , 1998, Epilepsia.

[15]  A. Sakamoto,et al.  Correlation of sleep macrostructure parameters and idiopathic epilepsies. , 2002, Arquivos de neuro-psiquiatria.

[16]  Simon Shorvon,et al.  Sudden unexpected death in epilepsy , 2011, The Lancet.

[17]  T. Corona,et al.  Sleep disturbances, socioeconomic status, and seizure control as main predictors of quality of life in epilepsy , 2005, Epilepsy & Behavior.

[18]  T. Walczak,et al.  Reduction of rapid eye movement sleep by diurnal and nocturnal seizures in temporal lobe epilepsy. , 2000, Archives of neurology.

[19]  J. Fine,et al.  Sleep Architecture in Children with Idiopathic Generalized Epilepsy , 2005, Epilepsia.

[20]  G. B. Young,et al.  Differential Aspects of Sleep Epilepsy , 1985, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[21]  M. Drake,et al.  Sleep and waking disturbances in epilepsy. , 1987, Clinical EEG.

[22]  A. Karlovasitou,et al.  Influence of sleep disturbance on quality of life of patients with epilepsy , 2008, Seizure.

[23]  J. Salas-Puig,et al.  Pure sleep seizures: risk of seizures while awake. , 2007, Epileptic disorders : international epilepsy journal with videotape.

[24]  M. Mahowald,et al.  Sleep-related eating disorders: polysomnographic correlates of a heterogeneous syndrome distinct from daytime eating disorders. , 1991, Sleep.

[25]  Michael C. Smith,et al.  Epileptic Encephalopathy of Late Childhood: Landau-Kleffner Syndrome and the Syndrome of Continuous Spikes and Waves During Slow-Wave Sleep , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[26]  D. Zutter,et al.  Sleep-wake habits and disorders in a series of 100 adult epilepsy patients—A prospective study , 2006, Seizure.

[27]  N. Fejerman,et al.  Acquired epileptic aphasia: neuropsychologic follow-up of 12 patients. , 1994, Pediatric neurology.

[28]  B. Yaqub,et al.  Nocturnal epilepsies in adults , 1997, Seizure.

[29]  Nicola Toschi,et al.  Physiologic autonomic arousal heralds motor manifestations of seizures in nocturnal frontal lobe epilepsy: implications for pathophysiology. , 2012, Sleep medicine.

[30]  C. Marsden,et al.  Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder. , 1995, Brain : a journal of neurology.

[31]  A. Buck,et al.  Stimulus-induced, sleep-bound, focal seizures: a case report. , 2011, Sleep.

[32]  Josemir W Sander,et al.  Sudden Death in Epilepsy: A Study of Incidence in a Young Cohort with Epilepsy and Learning Difficulty , 1995, Epilepsia.

[33]  P. Lavie,et al.  Decreased pituitary-gonadal secretion in men with obstructive sleep apnea. , 2002, The Journal of clinical endocrinology and metabolism.

[34]  R. Manni,et al.  The FLEP scale in diagnosing nocturnal frontal lobe epilepsy, NREM and REM parasomnias: Data from a tertiary sleep and epilepsy unit , 2008, Epilepsia.

[35]  Luigi Ferini-Strambi,et al.  Autosomal dominant nocturnal frontal lobe epilepsy , 2004, Journal of Neurology.

[36]  F. Cendes,et al.  Nocturnal temporal lobe epilepsy , 1998, Neurology.

[37]  E. Bixler,et al.  Hereditary Factors in Sleepwalking and Night Terrors , 1980, British Journal of Psychiatry.

[38]  G. Plazzi,et al.  Epileptic nocturnal wanderings. , 1995, Sleep.

[39]  M. Marciani,et al.  Nocturnal Sleep and Daytime Somnolence in Untreated Patients with Temporal Lobe Epilepsy: Changes After Treatment with Controlled‐Release Carbamazepine , 1997, Epilepsia.

[40]  R. Chervin,et al.  Identification and treatment of obstructive sleep apnea in adults and children with epilepsy: a prospective pilot study. , 2003, Sleep medicine.

[41]  L. Tassi,et al.  Intracerebral recordings of minor motor events, paroxysmal arousals and major seizures in nocturnal frontal lobe epilepsy , 2005, Neurological Sciences.

[42]  D. Janz,et al.  The Grand Mai épilepsies and the Sleeping‐Waking Cycle , 1962, Epilepsia.

[43]  R. Michelucci,et al.  Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia , 2000, Clinical Neurophysiology.

[44]  B. Vaughn,et al.  Sleep and epilepsy. , 2004, Seminars in neurology.

[45]  J. Goraya,et al.  Spectrum of polysomnographic abnormalities in children with epilepsy. , 2008, Pediatric neurology.

[46]  Andrea Grassi,et al.  Distinctive polysomnographic traits in nocturnal frontal lobe epilepsy , 2012, Epilepsia.

[47]  P. Lavie,et al.  Relationship between rapid eye movement sleep and testosterone secretion in normal men. , 1999, Journal of andrology.

[48]  R Yee,et al.  Clinical relevance of arrhythmias during sleep: guidance for clinicians , 2004, Heart.

[49]  J P Lieb,et al.  Sleep state and seizure foci related to depth spike activity in patients with temporal lobe epilepsy. , 1980, Electroencephalography and clinical neurophysiology.

[50]  Kannan Ramar,et al.  Updates on definition, consequences, and management of obstructive sleep apnea. , 2011, Mayo Clinic proceedings.

[51]  B. Malow,et al.  Relationship of epileptic seizures to sleep stage and sleep depth. , 2002, Sleep.

[52]  M. Brodie,et al.  Sexual Function in Women with Epilepsy , 1997, Epilepsia.

[53]  S. Noachtar,et al.  Response of polygraphic sleep to phenytoin treatment for epilepsy. A longitudinal study of immediate, short‐ and long‐term effects , 1987, Acta neurologica Scandinavica.

[54]  G Plazzi,et al.  Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases. , 1999, Brain : a journal of neurology.

[55]  Philippe Kahane,et al.  Nocturnal Hypermotor Seizures, Suggesting Frontal Lobe Epilepsy, Can Originate in the Insula , 2006, Epilepsia.

[56]  F. Drislane,et al.  Differential effects of antiepileptic drugs on sexual function and hormones in men with epilepsy , 2005, Neurology.

[57]  Gernot Riedel,et al.  The cholinergic system, EEG and sleep , 2011, Behavioural Brain Research.

[58]  N. Varma,et al.  Seizures and arousals from sleep--which comes first? , 1995, Sleep.

[59]  M. Aldrich,et al.  Interictal Spiking Increases with Sleep Depth in Temporal Lobe Epilepsy , 1998, Epilepsia.

[60]  P. Satishchandra,et al.  Sleep disturbances in juvenile myoclonic epilepsy: A sleep questionnaire-based study , 2012, Epilepsy & Behavior.

[61]  J. V. van Gerven,et al.  Subjective Sleep Disturbance in Patients with Partial Epilepsy: A Questionnaire‐based Study on Prevalence and Impact on Quality of Life , 2004, Epilepsia.

[62]  M. Portuguez,et al.  Evaluation of sleep quality in patients with refractory seizures who undergo epilepsy surgery , 2010, Epilepsy & Behavior.

[63]  P. Kwan,et al.  Association of subjective anxiety, depression, and sleep disturbance with quality‐of‐life ratings in adults with epilepsy , 2009, Epilepsia.

[64]  M. Terzano,et al.  The cyclic alternating pattern as a physiologic component of normal NREM sleep. , 1985, Sleep.

[65]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[66]  B. Malow,et al.  Predictors of sleepiness in epilepsy patients. , 1997, Sleep.

[67]  D. Bennett,et al.  Efficacy of sleep deprivation as an activation procedure in epilepsy patients. , 1984, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[68]  M. Sammaritano,et al.  Effect of anticonvulsants on sleep. , 2000, Neurology.

[69]  B. Ehrenberg,et al.  Epilepsy and sleep apnea syndrome , 1994, Neurology.

[70]  M. Marciani,et al.  Effects of lamotrigine on nocturnal sleep, daytime somnolence and cognitive functions in focal epilepsy , 2000, Acta neurologica Scandinavica.

[71]  G. Plazzi,et al.  Excessive Daytime Sleepiness and Subjective Sleep Quality in Patients with Nocturnal Frontal Lobe Epilepsy: A Case‐Control Study , 2006, Epilepsia.

[72]  R. Chervin,et al.  Treating obstructive sleep apnea in adults with epilepsy , 2008, Neurology.

[73]  C. Gurses,et al.  Sleep characteristics of patients with epilepsy with pure sleep-related seizures , 2011, Epilepsy & Behavior.

[74]  F. Provini,et al.  Nocturnal frontal lobe epilepsy: new pathophysiological interpretations. , 2011 .

[75]  I. Hindmarch,et al.  A double-blind study in healthy volunteers to assess the effects on sleep of pregabalin compared with alprazolam and placebo. , 2005, Sleep.

[76]  V. Somers,et al.  Day-night pattern of sudden death in obstructive sleep apnea. , 2005, The New England journal of medicine.

[77]  S. Duntley,et al.  Novel genetic findings in an extended family pedigree with sleepwalking , 2011, Neurology.

[78]  C. Bazil,et al.  Effects of levetiracetam on sleep in normal volunteers , 2005, Epilepsy & Behavior.

[79]  P. Höllinger,et al.  Epilepsy and Obstructive Sleep Apnea , 2006, European Neurology.

[80]  R. Guerrini,et al.  Benign childhood focal epilepsies , 2012, Epilepsia.

[81]  L. Tassi,et al.  Sleep-related hyperkinetic seizures of temporal lobe origin , 2004, Neurology.

[82]  M. Marciani,et al.  Effect of anticonvulsants on nocturnal sleep in epilepsy. , 2000, Neurology.

[83]  M. A. Bassetti,et al.  Gabapentin-induced modulation of interictal epileptiform activity related to different vigilance levels , 2000, Clinical Neurophysiology.

[84]  R. Loewenson,et al.  Ictal characteristics of pseudoseizures. , 1985, Archives of neurology.

[85]  E. Niedermeyer,et al.  Primary (Idiopathic) Generalized Epilepsy and Underlying Mechanisms , 1996, Clinical EEG.

[86]  C. Guilleminault,et al.  Atypical Sexual Behavior During Sleep , 2002, Psychosomatic medicine.

[87]  A. Declerck,et al.  Influence of antiepileptic drugs on sleep patterns. , 1991, Epilepsy research. Supplement.

[88]  P. Cowen,et al.  Effects of carbamazepine on sleep in healthy volunteers , 1989, Biological Psychiatry.

[89]  L. Ferini-Strambi,et al.  Nocturnal paroxysmal arousals with motor behaviors during sleep: frontal lobe epilepsy or parasomnia? , 1997, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[90]  G. Shukla,et al.  Markedly disturbed sleep in medically refractory compared to controlled epilepsy – A clinical and polysomnography study , 2012, Seizure.

[91]  M. Newton,et al.  Sleep deprivation increases cortical excitability in epilepsy , 2006, Neurology.

[92]  M. Walker,et al.  NREM arousal parasomnias and their distinction from nocturnal frontal lobe epilepsy: a video EEG analysis. , 2009, Sleep.

[93]  A. Wyler,et al.  Epilepsy complicated by sleep apnea , 1981, Annals of neurology.

[94]  D. Riemann,et al.  The influence of carbamazepine on sleep-EEG and the clonidine test in healthy subjects: Results of a preliminary study , 1994, Biological Psychiatry.

[95]  D. Cechetto,et al.  Insular cortex stimulation produces lethal cardiac arrhythmias: a mechanism of sudden death? , 1991, Brain Research.

[96]  E. Niedermeyer.  SLEEP ELECTROENCEPHALOGRAMS IN PETIT MAL. , 1965, Archives of neurology.

[97]  Philippe Coubes,et al.  Sleep influence on seizures and epilepsy effects on sleep in partial frontal and temporal lobe epilepsies , 2000, Clinical Neurophysiology.

[98]  Yang Si,et al.  Features of the K-complex waves in refractory nocturnal frontal lobe epilepsy , 2010, Epilepsy Research.

[99]  T S Walczak,et al.  Effects of Sleep and Sleep Stage on Epileptic and Nonepileptic Seizures , 1997, Epilepsia.

[100]  Mylan C. Cohen,et al.  Meta-analysis of the morning excess of acute myocardial infarction and sudden cardiac death. , 1997, The American journal of cardiology.

[101]  I. Scheffer,et al.  Distinguishing sleep disorders from seizures: diagnosing bumps in the night. , 2006, Archives of neurology.

[102]  M. Sammaritano,et al.  Distribution of partial seizures during the sleep–wake cycle , 2001, Neurology.

[103]  R. Manni,et al.  Obstructive Sleep Apnea in a Clinical Series of Adult Epilepsy Patients: Frequency and Features of the Comorbidity , 2003, Epilepsia.

[104]  B. Steinhoff.  Efficacy of perampanel: A review of pooled data , 2014, Epilepsia.

[105]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[106]  M. Aldrich,et al.  Usefulness of polysomnography in epilepsy patients , 1997, Neurology.

[107]  C. Marsden,et al.  Autosomal dominant frontal epilepsy misdiagnosed as sleep disorder , 1994, The Lancet.

[108]  B. Vaughn,et al.  Improvement of epileptic seizure control with treatment of obstructive sleep apnoea , 1996, Seizure.

[109]  O. Kiehn.  Locomotor circuits in the mammalian spinal cord. , 2006, Annual review of neuroscience.

[110]  Luigi Ferini-Strambi,et al.  NREM parasomnias: arousal disorders and differentiation from nocturnal frontal lobe epilepsy , 2000, Clinical Neurophysiology.

[111]  C. Bazil,et al.  Sleep Disturbances Reported by Refractory Partial‐onset Epilepsy Patients Receiving Polytherapy , 2006, Epilepsia.

[112]  Xihong Lin,et al.  Obstructive sleep apnea in epilepsy patients: the Sleep Apnea scale of the Sleep Disorders Questionnaire (SA-SDQ) is a useful screening instrument for obstructive sleep apnea in a disease-specific population. , 2003, Sleep medicine.

[113]  S. Tufik,et al.  The association of testosterone, sleep, and sexual function in men and women , 2011, Brain Research.

[114]  J. Gotman,et al.  Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy , 1991, Neurology.

[115]  P. Fenwick,et al.  SEX HORMONE CHANGES IN MALE EPILEPTICS , 1980, Clinical endocrinology.

[116]  S. Duncan,et al.  Erectile function, sexual desire, and psychological well-being in men with epilepsy , 2009, Epilepsy & Behavior.

[117]  P. Clarenbach,et al.  Gabapentin augments whole blood serotonin in healthy young men , 2005, Journal of Neural Transmission.

[118]  G. Plazzi,et al.  Increased frequency of arousal parasomnias in families with nocturnal frontal lobe epilepsy: A common mechanism? , 2010, Epilepsia.

[119]  P. Halász.  Generalized epilepsy with spike-wave paroxysms as an epileptic disorder of the function of sleep promotion. , 1981, Acta physiologica Academiae Scientiarum Hungaricae.

[120]  S. Duncan,et al.  Sexual function in men with epilepsy , 2008, Neurology.

[121]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.