pii: jc- 00486-15http://dx.doi.org/10.5664/jcsm.5606

S LE E P M ED IC IN E PEARLS

Perfect Periodicity: To Be Or Not To Be Periodic Leg Movements Elias G. Karroum, MD, PhD1; Han C. Phan, MD2,3; Daniel M. Torrez, MD2,3; Lynn M. Trotti, MD, MSc1,4 Emory Sleep Center, Emory University School of Medicine, Atlanta, GA; 2Department of Pediatrics, Emory University School of Medicine, Atlanta, GA; 3Children’s Healthcare of Atlanta-Egleston Campus, Atlanta, GA; 4Department of Neurology, Emory University School of Medicine, Atlanta, GA

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A 3-year-old girl with history of severe developmental delay, intractable seizures on multiple anti-epileptic medications (clobazam, rufinamide, benzodiazepines, and cannabidiol oil), and gastrostomy tube placement for feeding difficulties, was referred for a full-night video electroencephalogram (EEG) and polysomnogram (PSG) study. The full-night video EEG/ PSG study was considered because of nocturnal oxygen desaturations at home with concerns for possible nocturnal seizures and/or sleep-related respiratory events. Her physical examination was significant for hypertrophy of the inferior nasal turbinates and a modified Mallampati score of 3. Her neurological examination was significant for being nonverbal, opening her eyes intermittently without tracking, and having diffuse hypotonia without purposeful movements. Video EEG showed generalized slowing of background activity with burst suppression pattern but without seizures. Diagnostic PSG showed severe sleep apnea with an apnea-hypopnea index (AHI) of 23.3 events/h (including an obstructive

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AHI of 15.8 and a central AHI of 7.5). The oxygen desaturation index (ODI) was 19.7 events/h with a SpO2 nadir of 64%. There were no periods of prolonged hypoxemia (total sleep time with SpO2 < 90% was 6.6 min). There was no hypoventilation. Arousal index was one event/hour. Left and right surface electromyogram (EMG) derivations of the tibialis anterior muscles (TA) showed an abnormal electrical activity pattern. The pattern started at the beginning of the PSG while she was awake and continued through the whole PSG study while she was asleep. The electrical pattern was always bilateral, had duration of about 7 seconds, and was recorded every 60 seconds at exactly the same time in the left and right surface EMG of the TA (Figure 1). QUESTION: Is the intermittent leg EMG activity, shown in Figure 1, periodic leg movements?

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Figure 1

Upper panel: 5-min epoch of polysomnography showing an intermittent, regular (every 60 s), and bilateral electrical activity in the surface EMG derivations of the left and right tibialis anterior muscles (TA). Lower panel: 30-s epoch of polysomnography showing in more detail one single electrical pattern with a constant duration of 7 seconds (this is the second electrical signal extracted from the left side of the upper panel above it).

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EG Karroum, HC Phan, DM Torrez et al. Sleep Medicine Pearl

nerve stimulator (VNS) which is an adjunctive therapy used for treating medically intractable epilepsy.7 VNS rapid cycling mode (versus standard slow cycling mode) has “On” (usually 7 s) and “Off” (usually ≤ 30 s) durations that generate an electrical pattern recorded on EMG derivations as an artifact with similar duration and frequency of occurrence as PLM and can be noted in a PSG study on both chin and leg EMG derivations.7–12 However, our patient was not treated with a VNS. In conclusion, patient-related electrical artifacts from devices like feeding pumps or VNS should be thought of and corrected if possible in patients with refractory epilepsy and/or developmental disabilities as they can mimic PLM and cause clinical confusion for sleep specialists and technologists.

ANSWER: No. The intermittent leg EMG activity is interference due to a cycling feeding pump.

D I SCUS S I O N The electrical pattern shown in Figure 1 is not periodic leg movements (PLM) but an artifact related to “On” and “Off” durations of a cycling feeding pump (7 s and 53 s, respectively) that was placed in the patient’s bed close to her gastrostomy tube. These durations are automatically generated by the pump and vary with each desired preset rate of feeding. This interfering electrical activity can be differentiated from PLM by several features which point toward its nonphysiological nature. Although the duration and the frequency of occurrence of the artifact are in the accepted range of values for the duration (0.5 to 10 s) and frequency of occurrence or inter-leg movement interval (IMI, onset to onset: 5 to 90 s) of PLM,1 these values are too constant to be truly physiological. Indeed, PLM exhibit an intra-individual variability in their duration and their IMI, and these PLM variables are actually summarized in studies by calculating the mean PLM duration and the mean IMI of each subject in a sample group.2,3 Moreover, it has been shown that the IMI is even more variable and the PLM are less periodic in children than in adults.2,4 Even in patients with restless legs syndrome where the IMI has the least variability compared to healthy controls or patients with other sleep disorders (see Figure 1, Ferri et al.5), PLM are still not that perfectly periodic in adult and even less in pediatric RLS patients.6 In addition, the electrical interference was also apparent in some other PSG channels including chin EMG and chest belt signals (Figure 1), but also in some EEG derivations including T3-T5, T5-O1, and Cz-Pz derivations of the full EEG montage (Figure 2). Of note, these artifacts could have been misinterpreted as arousals, then leading to overscoring of respiratory events. However, our patient had only one scored arousal per hour of sleep. Further, the majority of her respiratory events were associated with oxygen desaturations, such that the ODI was very close to the AHI. After discussion with the sleep technologist who monitored the patient during the EEG/PSG study, it seems that this electrical pattern was not noticed as an artifact and therefore was not documented as such. In addition, there were no surface EMG leads placed on the legs of the patient during this study. Despite that, the EEG/PSG box which was placed at the head of the patient’s bed still picked up the electrical artifact mainly in the EMG (chin and TA) and some EEG derivations. We suspect that the electrical interference was detected by the EEG/PSG box because it fell within the EEG and EMG filtered range and because the feeding pump was placed in the bed of the patient in close proximity to the EEG/PSG box. The artifact signal could have been avoided by placing the pump away from the patient and the EEG/PSG box, or alternatively by changing the time of feeding of the patient and stopping the pump during the sleep study. Other sources of interference that could have mimicked PLM specifically in our patient would have been a vagus Journal of Clinical Sleep Medicine, Vol. 12, No. 3, 2016

S L E E P M E D I C I N E PE A R L S 1. Sleep clinicians and technologists should be aware of patient-related artifacts from devices like cycling feeding pumps. 2. These devices can generate electrical artifacts mimicking periodic leg movements. 3. These artifacts can be distinguished from periodic leg movements by their perfectly constant duration and periodicity and by their interference with multiple derivations including electromyogram and electroencephalogram derivations. C I TAT I O N Karroum EG, Phan HC, Torrez DM, Trotti LM. Perfect periodicity: to be or not to be periodic leg movements. J Clin Sleep Med 2016;12(3):452–455. R E FE R E N CES 1. Zucconi M, Ferri R, Allen R, et al. The official World Association of Sleep Medicine (WASM) standards for recording and scoring periodic leg movements in sleep (PLMS) and wakefulness (PLMW) developed in collaboration with a task force from the International Restless Legs Syndrome Study Group (IRLSSG). Sleep Med 2006;7:175–83. 2. Pennestri MH, Whittom S, Adam B, Petit D, Carrier J, Montplaisir J PLMS and PLMW in healthy subjects as a function of age: prevalence and interval distribution. Sleep 2006;29:1183–7. 3. Skeba P, Hiranniramol K, Earley CJ, Allen RP. Inter-movement interval as a primary stable measure of periodic limb movements of sleep. Sleep Med 2016;17:138–43 . 4. Scholle S, Scholle HC. Leg movements and periodic leg movements during sleep in the development across childhood and adolescence from 1 to 18 years. Sleep Med 2014;15:1068–74. 5. Ferri R. The time structure of leg movement activity during sleep: the theory behind the practice. Sleep Med 2012;13:433–41. 6. Ferri R, Manconi M, Lanuzza B, et al. Age-related changes in periodic leg movements during sleep in patients with restless legs syndrome. Sleep Med 2008;9:790–8. 7. Morris GL 3rd, Gloss D, Buchhalter J, Mack KJ, Nickels K, Harden C. Evidence-based guideline update: vagus nerve stimulation for the treatment of epilepsy: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 2013;81:1453–9.

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Figure 2

Upper panel: 5-min epoch of full EEG montage (same epoch as in the upper panel in Figure 1) showing the same intermittent, regular (every 60 s), electrical artifact in EEG derivations. Lower panel: 30-s epoch of full EEG montage (same epoch as in the lower panel in Figure 1) showing in more details that the artifact was only recorded by the EEG derivations T3-T5, T5-O1 and Cz-Pz (highlighted in red). 8. Bejanishvili S, Osborne LE, Messenger K, Olejniczak P, Gutierrez A. EMG vagus nerve stimulator artifact. Neurol Clin Neurophysiol 2005;2005:1. 9. Gschliesser V, Hogl B, Frauscher B, Brandauer E, Poewe W, Luef G. Mode of vagus nerve stimulation differentially affects sleep related breathing in patients with epilepsy. Seizure 2009;18:339–42. 10. Ebben MR, Sethi NK, Conte M, Pollak CP, Labar D. Vagus nerve stimulation, sleep apnea, and CPAP titration. J Clin Sleep Med 2008;4:471–3. 11. El-Kersh K, Senthilvel E. An 18-year-old woman with snoring and refractory epilepsy. Chest 2015;148:e48–51. 12. Hsieh T, Chen M, McAfee A, Kifle Y. Sleep-related breathing disorder in children with vagal nerve stimulators. Pediatr Neurol 2008;38:99–103.

SUBM I SSI O N & CO R R ESPO NDENCE I NFO R M ATI O N Submitted for publication November, 2015 Submitted in final revised form December, 2015 Accepted for publication January, 2016 Address correspondence to: Elias G. Karroum, MD, PhD, Emory Sleep Center, 12 Executive Park Drive NE 4th Floor, Atlanta, GA, 30329; Tel: +1 217891 1080; Email: [email protected] or [email protected]

D I SCLO S U R E S TAT E M E N T This was not an industry supported study. The authors have indicated no financial conflicts of interest.

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Perfect Periodicity: To Be Or Not To Be Periodic Leg Movements.

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