Effects of antiepileptic treatment on sleep and seizures in nocturnal frontal lobe epilepsy.

OBJECTIVE To study the effects of antiepileptic treatment on sleep parameters and video-polysomnography (VPSG) seizures in nocturnal frontal lobe epilepsy (NFLE). METHODS Twenty patients with a clinical and VPSG diagnosis of NFLE (baseline polysomnography [PSG]) underwent a clinical follow-up and performed a second VPSG after effective antiepileptic treatment lasting for at least 6 months. Conventional sleep measures, cyclic alternating pattern (CAP) parameters, and objective VPSG seizures were assessed in NFLE patients before and after treatment and were compared with the results of 20 age- and gender-matched control subjects. RESULTS Antiepileptic treatment determined a partial reduction of objective VPSG seizures of approximately 25% compared to baseline condition. Alterations of most conventional sleep measures recovered normal values, but nonrapid eye movement (NREM) sleep instability remained pathologically enhanced (CAP rate, +26% compared to controls) and was associated with persistence of daytime sleepiness. CONCLUSIONS Residual epileptic events and high levels of unstable NREM sleep can define a sort of objective resistance of both seizures and disturbed arousal system to the therapeutic purpose of the antiepileptic drugs in NFLE. This finding could determine the need for new therapeutic options in this particular form of epilepsy.

[1]  C. Zucca,et al.  Sleep patterns in patients with late onset partial epilepsy receiving chronic carbamazepine (CBZ) therapy , 1990, Epilepsy Research.

[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]  L. Ferini-Strambi,et al.  Arousal Fluctuations in Non‐Rapid Eye Movement Parasomnias: The Role of Cyclic Alternating Pattern as a Measure of Sleep Instability , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

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

[6]  M. Terzano,et al.  Cyclic Alternating Pattern as a Provocative Factor in Nocturnal Paroxysmal Dystonia , 1997, Epilepsia.

[7]  G. Plazzi,et al.  Movement disorders in sleep: guidelines for differentiating epileptic from non-epileptic motor phenomena arising from sleep. , 2007, Sleep medicine reviews.

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

[9]  Liborio Parrino,et al.  Cyclic alternating pattern (CAP) and epilepsy during sleep: how a physiological rhythm modulates a pathological event , 2000, Clinical Neurophysiology.

[10]  G. Plazzi,et al.  From nocturnal paroxysmal dystonia to nocturnal frontal lobe epilepsy , 2000, Clinical Neurophysiology.

[11]  M Hirshkowitz,et al.  Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. , 2001, Sleep medicine.

[12]  P. Tinuper,et al.  Hyperkinetic manifestations in nocturnal frontal lobe epilepsy. Semeiological features and physiopathological hypothesis , 2005, Neurological Sciences.

[13]  M. Terzano,et al.  Combined influence of cyclic arousability and EEG synchrony on generalized interictal discharges within the sleep cycle , 2001, Epilepsy Research.

[14]  M. Terzano,et al.  Effects of Generalized Interictal EEG Discharges on Sleep Stability: Assessment by Means of Cyclic Alternating Pattern , 1992, Epilepsia.

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

[16]  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.

[17]  Maria Grazia Marciani,et al.  Effect of antiepileptic drugs on sleep , 2000, Clinical Neurophysiology.

[18]  Liborio Parrino,et al.  CAP, epilepsy and motor events during sleep: the unifying role of arousal. , 2006, Sleep medicine reviews.

[19]  P. Cortelli,et al.  Nocturnal Paroxysmal Dystonia with Short‐Lasting Attacks: Three Cases with Evidence for an Epileptic Frontal Lobe Origin of Seizures , 1990, Epilepsia.

[20]  L. Tassi,et al.  Sleep‐related Minor Motor Events in Nocturnal Frontal Lobe Epilepsy , 2007, Epilepsia.

[21]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

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

[23]  E. Sforza,et al.  Paroxysmal periodic motor attacks during sleep: clinical and polygraphic features. , 1993, Electroencephalography and clinical neurophysiology.

[24]  Christian Guilleminault,et al.  Erratum to “Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep” [Sleep Med. 2(6) (2001) 537–553] , 2002 .

[25]  Liborio Parrino,et al.  Modulation of Generalized Spike‐and‐Wave Discharges During Sleep by Cyclic Alternating Pattern , 1989, Epilepsia.

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

[27]  G. Plazzi,et al.  Diagnostic accuracy of a structured interview for nocturnal frontal lobe epilepsy (SINFLE): a proposal for developing diagnostic criteria. , 2012, Sleep medicine.

[28]  F. Provini,et al.  Parasomnias and nocturnal frontal lobe epilepsy (NFLE): lights and shadows--controversial points in the differential diagnosis. , 2011, Sleep medicine.

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

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

[31]  L. Ferini-Strambi,et al.  Autosomal Dominant Nocturnal Frontal Lobe Epilepsy: Electroclinical Picture , 1996, Epilepsia.

[32]  G. Cantalupo,et al.  Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias. A neuroethologic approach , 2005, Neurological Sciences.

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

[34]  L. Tassi,et al.  Coupling of minor motor events and epileptiform discharges with arousal fluctuations in NFLE , 2008, Epilepsia.

[35]  G. Plazzi,et al.  The wide clinical spectrum of nocturnal frontal lobe epilepsy. , 2000, Sleep medicine reviews.

[36]  Liborio Parrino,et al.  Cyclic alternating pattern (CAP): the marker of sleep instability. , 2012, Sleep medicine reviews.

[37]  M. Terzano,et al.  Activation of partial seizures with motor signs during cyclic alternating pattern in human sleep , 1991, Epilepsy Research.

[38]  H. Merica,et al.  A study of the interrupted REM episode , 1991, Physiology & Behavior.

[39]  C. Guilleminault,et al.  Sleepwalking, a disorder of NREM sleep instability. , 2006, Sleep medicine.

[40]  M. Terzano,et al.  Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. , 2002, Sleep medicine.

[41]  J. Duncan,et al.  Paroxysmal Motor Disorders of Sleep: The Clinical Spectrum and Differentiation from Epilepsy , 2006, Epilepsia.

[42]  L. Ferini-Strambi,et al.  Topiramate treatment for nocturnal frontal lobe epilepsy , 2006, Seizure.

[43]  M. Terzano,et al.  Cyclic alternating pattern sequences and non-cyclic alternating pattern periods in human sleep , 2007, Clinical Neurophysiology.

[44]  M. Terzano,et al.  Sleep Microstructure and EEG Epileptiform Activity in Patients with Juvenile Myoclonic Epilepsy , 1992, Epilepsia.

[45]  M. Baulac,et al.  K-complex-induced seizures in autosomal dominant nocturnal frontal lobe epilepsy , 2008, Clinical Neurophysiology.

[46]  M. Modugno,et al.  Autosomal dominant nocturnal frontal lobe epilepsy. A video-polysomnographic and genetic appraisal of 40 patients and delineation of the epileptic syndrome. , 1998, Brain : a journal of neurology.

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

[48]  Lino Nobili,et al.  Relationship of epileptic discharges to arousal instability and periodic leg movements in a case of nocturnal frontal lobe epilepsy: a stereo-EEG study. , 2006, Sleep.

[49]  L Parrino,et al.  Spike-wave discharge and the microstructure of sleep-wake continuum in idiopathic generalised epilepsy** * This work was performed with the support of the Hungarian Academy of Sciences Széchenyi professorship. , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.