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Clinical and Polysomnographic Characteristics of High Frequency Leg Movements

2010; American Academy of Sleep Medicine; Volume: 06; Issue: 05 Linguagem: Inglês

10.5664/jcsm.27931

1550-9397

Chang‐Kook Yang, John W. Winkelman,

Sleep and related disorders

Free AccessAntidepressantsClinical and Polysomnographic Characteristics of High Frequency Leg Movements Changkook Yang, MD, PhD, John W. Winkelman, MD, PhD Changkook Yang, MD, PhD Sleep Disorders Clinic, Busan Sleep Center, Busan, Korea , John W. Winkelman, MD, PhD Address correspondence to: John W. Winkelman, M.D., Ph.D., Division of Sleep Medicine, Department of Medicine, Brigham and Women's Hospital, 1505 Commonwealth Ave., Brighton, MA 02135(617) 783-1441(617) 527-2098 E-mail Address: [email protected] Sleep Medicine Division, Brigham and Women's Hospital, Harvard Medical School, Boston, MA Published Online:October 15, 2010https://doi.org/10.5664/jcsm.27931Cited by:20SectionsAbstractPDF ShareShare onFacebookTwitterLinkedInRedditEmail ToolsAdd to favoritesDownload CitationsTrack Citations AboutABSTRACTStudy Objectives:The aim of this study was to describe the clinical and polysomnographic characteristics of patients with high frequency leg movements (HFLM) on polysomnographic recording.Methods:Among 486 patients (male 232, female 254) referred for overnight diagnostic PSG over a 9-month period, 37 patients demonstrated HFLM: 19 males (8.2% of PSGs) and 18 females (7.1% of PSGs). An equal number of age- and sex-matched consecutive patients who did not show HFLM were selected. HFLM was defined as ≥ 4 discrete leg movements occurring at a frequency of 0.3–4.0 Hz.Results:Two-thirds (64.3%) of all HFLMs occurred during waking; 35.7% occurred during sleep. Of those HFLM episodes occurring during sleep, 44.8% occurred during stage 1, 45.1% during stage 2, 0.6% during stages 3 and 4, and 9.5% during REM. The movements usually appeared unilaterally, but sometimes they showed a bilateral pattern. The mean frequency was 1.6 ± 0.6 Hz (range 0.4-3.7), the mean number of episodes of HFLM per subject per night was 26.5 ± 30.5 (range 2-111), and the mean duration per episode was 17.6 ± 35.4 sec (range 1.5 sec-6.1 minutes). The mean HFLM index, (total number of HFLM divided by the time in bed, in hours), was 107.7 ± 254.5 (range 2.0–1078.3). Patients with HFLM complained of RLS symptoms significantly more often than the group without HFLM (p < 0.05).Conclusion:Further studies are needed to establish criteria for scoring HFLM. Examination of other patient cohorts with HFLM will be needed to determine whether HFLM are in fact associated with RLS.Citation:Yang C; Winkelman JW. Clinical and polysomnographic characteristics of high frequency leg movements. J Clin Sleep Med 2010;6(5):431-438.INTRODUCTIONAnterior tibialis EMG in standard polysomnography is used primarily to record periodic leg movements of sleep (PLMS), which is defined as a series of ≥ 4 consecutive movements lasting 0.5 to 5 seconds with an intermovement interval of 5 to 90 seconds. Although rhythmic leg movements with a much shorter intermovement interval and duration than observed with PLMS have been previously reported, few studies have described the clinical and polysomnographic characteristics of patients with these leg movements. For instance, parkinsonian tremor consists of alternating activity in opposing muscle groups which occur at a frequency of 3-6 Hz1; hypnagogic foot tremor (HFT) was observed in pre-sleep wakefulness and light sleep only2; alternating leg muscle activation (ALMA) was observed in patients with sleep apnea and consisted only of alternating movements between legs.3We now describe movements, which we call high frequency leg movements (HFLM), which overlap with, but are distinct from, those previously reported in the literature. We believe the previous terms are inappropriate to describe such phenomena in a number of ways: (1) these fast leg movements are not limited to hypnagogic (or light) sleep, and are even recorded during REM and slow wave sleep; (2) the movements are not "tremor," as this term is defined as a rhythmic alternating movement of agonist and antagonist muscles with > 3 Hz frequency, while it is unclear whether HFLM involve agonist and antagonist muscles, and often occur at frequencies below 3 Hz; and (3) the majority of the movements observed with HFLM occur unilaterally rather than alternately. The aim of this study was to describe the clinical and polysomnographic characteristics of patients with HFLM on overnight diagnostic polysomnographic recording.BRIEF SUMMARYCurrent Knowledge/Study Rationale: Rhythmic leg movements with a rate of 1-3 Hz are often observed during the standard PSG, but their characteristics have not been well described. This study was done to ascertain the clinical and polysomnographic characteristics of high frequency leg movements (HFLM) in detail.Study Impact: This study will contribute to establishing the polygraphic criteria for scoring HFLM and to an understanding of their pathophysiology and clinical implications.METHODSSubjectsAmong 486 patients (male 232, female 254) referred for overnight diagnostic polysomnography performed at the sleep center over 9 consecutive months, 37 cases with HFLM were retrospectively identified (7.6%), of whom 19 were male. Subjects' characteristics are shown in Table 1. Thirty-seven age- and sex-matched patients without HFLM also were selected. These 37 patients were the first 4 to be studied in each month of this period. The most common reason for performing polysomnography was to rule out sleep related breathing disorder, accounting for 30 (82.5%) of the experimental group and 34 (91.9%) of the group without HFLM. Clinical information was obtained from clinical evaluation and a standard questionnaire including the 4 essential diagnostic criteria for restless legs syndrome.4 Subjects with a history of head trauma or neurologic disorders including Parkinson disease, and those taking dopamine agonists were excluded. This study was approved by the Committee on Human Subjects at Brigham and Women's Hospital.Table 1 Demographic and clinical characteristicsPatients with HFLM (N = 37)Patients without HFLM (N = 37)p-valueAge (y)51.2 ± 2.6 (range 18-76)50.5 ± 2.2 (range 18-82)0.8445Gender (male)19 (51.4)19 (51.4)1.0000Ethnicity (Caucasian)28 (75.7)29 (78.4)0.9521BMI (kg/m2)27.1 ± 0.828.9 ± 1.20.2312ESS8.9 ± 0.37.8 ± 0.80.3280ESS 31015 (40.5)11 (29.7)0.4328RLS15 (40.5)6 (16.2)0.0495Alcohol (glass/week)0.8 ± 0.31.8 ± 0.50.0886Caffeine (cup/day)1.9 ± 0.31.7 ± 0.30.7554Tobacco (piece/day)2.8 ± 1.32.8 ± 1.60.9743Antidepressant12 (32.4)7 (18.9)0.2514Benzodiazepine4 (10.8)3 (8.1)0.6912Anticonvulsant4 (10.8)1 (2.7)0.1647Values represent M ± SE or n (%).HFLM, high frequency leg movements; BMI, body mass index; ESS, Epworth Sleepiness Scale; RLS, restless legs syndromeProceduresSleep studies were recorded using the Alice 3 (v. 1.19) (Healthdyne Inc., Marietta, GA) with standard method. Four EEG derivations (C4/A1, C3/A2, C4/O1, C3/O2), 2 EOG, submentalis EMG, EKG, separate right and left anterior tibialis EMG, and body position were recorded, as well as readings from one nasal-oral thermistor, one nasal pressure monitor, a snore microphone, chest and abdominal respiratory effort belts, and a finger pulse oximeter. The EMG amplifiers were set at a sensitivity of 1, with high filters set at 39.5 Hz and low filters set at 0.5 Hz. The sleep records were scored visually by trained technicians according to standard criteria.5HFLM were defined as follows: (1) ≥ 4 discrete leg movements (either unilateral, bilateral, or alternating) occur with < 2 seconds between individual leg movements; (2) leg movements occur at a frequency of 0.3-4.0 Hz; and (3) each leg movement lasts between 0.1-0.5 seconds. EEG arousal was defined based on the ASDA criteria.6 A leg movement (LM) was considered to be associated with arousal from sleep if the onset of EEG arousal occurred concurrent with or after the onset of, and was closely related to an LM. The arousal should follow the LM termination by ≤ 2 seconds.For statistics, Student t-test and χ2 test were used to compare variables, and the logistic regression was calculated.RESULTSClinical CharacteristicsSelected demographic and clinical characteristics are shown in Table 1. Final polysomnographic diagnoses for the HFLM group were: obstructive sleep apnea (OSA) 23 (62.2%), periodic limb movement disorder (PLMD) 5 (13.5%), both OSA and PLMD 7 (18.9%), and no significant finding 2 (5.4%); for the group without HFLM: OSA 26 (70.3%), PLMD 1 (2.7%), both OSA and PLMD 7 (18.9%), and no significant finding 3 (8.1%).There were no statistically significant differences between groups with and without HFLM in ethnicity, body mass index, Epworth Sleepiness Scale (ESS) scores, consumption of alcohol, caffeine, or tobacco, or antidepressant prescription. However, a larger number of those in the HFLM group reported RLS symptoms than in the group without HFLM (p < 0.05). The odds ratio of having RLS among patients with HFLM was 3.52 (95% CI: 1.18-10.51). However, the odds ratio of having an ESS ≥ 10, which represents the lower limit of clinical significance,7 and of taking an antidepressant at the time of polysomnography among patients group were not significant.Polysomnographic CharacteristicsSelected polysomnographic measures are shown in Table 2. Mean sleep latency in the HFLM group tended to be shorter compared to that of the group without HFLM (p < 0.06). There were no significant differences in sleep stages distribution, respiratory disturbance index (RDI), arousal index, and PLMI between groups with and without HFLM. The odds ratio of having a PLMI ≥ 15 was 1.740 (95% CI: 0.654-5.334), which was not significant.Table 2 Comparison of sleep measures between patients with or without HFLMPatients with HFLM (N = 37)Patients without HFLM (N = 37)p-valueSleep latency (min)16.3 ± 3.135.4 ± 9.10.0534REM latency (min)120.1 ± 14.3132.9 ± 13.00.5119Sleep efficiency (%)72.3 ± 2.769.3 ± 3.50.4963TST (min)309.5 ± 15.4278.6 ± 14.60.1503Stage 1 (%)19.4 ± 2.116.7 ± 1.60.3066Stage 2 (%)58.6 ± 1.760.6 ± 1.50.3647Stage 3 + 4 (%)8.4 ± 1.46.3 ± 1.20.2563Stage REM (%)13.6 ± 1.316.4 ± 1.40.1527AHI18.8 ± 2.923.5 ± 3.50.2991Lowest SaO2 (%)87.6 ± 0.988.1 ± 0.80.6247Arousal index31.1 ± 2.429.4 ± 1.60.5750PLMI13.3 ± 3.88.5 ± 3.00.3225Values represent M ± SE or n (%).TST, total sleeping time; AHI, apnea hypopnea index; PLMI, periodic leg movement indexCharacteristics of HFLMHFLM-related measures are listed in Table 3, and some examples of HFLM are shown in Figures 1–5. HFLM usually appeared unilaterally (Figure 1), but sometimes showed a bilateral alternating (Figure 2) or bilateral synchronous pattern (Figure 3). In some cases, each of these patterns (i.e., unilateral, bilateral, and alternating) appeared in a single subject at different times of night (Figure 4).Table 3 HFLM-related measures (N = 37)M ± SERangeNumber of HFLM sequences per subject per night26.5 ± 5.02–111Total number of individual HFLM per subject per night797.7 ± 330.915–9768Duration of HFLM sequence (sec)17.6 ± 1.11.5–367.8Rate of HFLM (Hz)1.6 ± 0.00.4–3.7% of total time with HFLM/duration of TIB1.8 ± 0.60.1–17.0HFLM index (/hr TIB)107.7 ± 42.42.0–1078.3TIB, time in bed; HFLM index was derived by dividing the total number of individual HFLM by the time in bed (in hours).Figure 1 Extended HFLM train from 60-sec segment of waking to sleep transitionDownload FigureFigure 2 Cardiac acceleration is observed during HFLM without arousalDownload FigureFigure 3 HFLM develops during stage REM sleepDownload FigureFigure 4 Unilateral, bilateral synchronous, and alternating patterns coexist in an individual epochDownload FigureFigure 5 Arousal associated with respiratory event can rarely induce HFLMDownload FigureAs shown in Table 3, HFLM-related measures showed wide variation both between and within individual subjects. The mean number of HFLM sequences was 26.5 (SD 30.5, range 2-111); the mean total number of HFLM during the night was 797.7 (SD 2012.8, range 15–9768); and the mean number of HFLM per sequence was 30.1 (SD 68.5, range 4-736). The mean duration of HFLM sequences was 17.6 sec (SD 35.4), ranging from 1.5 sec to 6.1 minutes. The most common HFLM frequency was between 1 and 2 Hz, ranging from 0.4 to 3.7 Hz (Figure 6). Single leg movement durations varied between 100 and 700 msec. The mean total HFLM duration as a percentage of time in bed (hours) was 1.8% (SD 3.7%), ranging from 0.1% to 17.0%. We also calculated an HFLM index, derived from dividing the total number of HFLM by the time in bed (in hours), to help understand how frequently HFLM appears. The mean HFLM index was 107.7 (SD 254.5), ranging from 2.0 to 1078.3.Figure 6 Distribution of HFLM frequencyDownload FigureHFLM developed mostly during wake (64.3%), but was also observed during sleep (35.7%), of which 16.0% emerged during stage 1, 16.1% during stage 2, 0.2% during stages 3 and 4, and 3.4% during stage REM (Figure 7). Among HFLMs which occurred during sleep, 28.0% occurred independent of ASDA defined EEG arousal, 24.4% during arousal, and 47.6% developed immediately prior to (< 2 sec) arousal (Figure 7).Figure 7 HFLM development by stageDownload FigureMost HFLMs observed during sleep closely preceded or followed an arousal or awakening and gradually diminished as the patient returned to sleep. Of note is that such arousals were rarely associated with a respiratory event (Figure 5), even though the mean RDI was 18.8/h. HFLM activity occurred throughout the night. However, 35.3% of all HFLMs appeared during the first third of the night, 27.9% during the second third, and 36.7% during the last third, being significantly less common during the second third compared to the remainder of the night (p < 0.05). HFLM associated cardiac accelerations were observed during sleep (Figure 2).There were no significant differences in HFLM duration (as a percentage of total TIB) or HFLM index between males and females, patients on and not on antidepressants, or those with and without RLS.DISCUSSIONThe authors describe clinical and polysomnographic characteristics of 37 patients with high frequency leg movements (HFLM). Although HFLM is not uncommon among those referred for polysomnography (7.6% of nearly 500 studies), investigation into this phenonemon has been limited, and its clinical and polysomnographic characteristics have not been well described.Various forms of wake and sleep related pathological movement have been reported in the literature. These include periodic leg movements in sleep (PLMS) and while awake (PLMWA), excessive fragmentary myoclonus,8 propriospinal myoclonus,9 sleep related rhythmic movement disorder,10 resting tremor in Parkinson disease,1 drug-induced akathisia,11 hypnagogic foot tremor (HFT),2 rhythmic feet movements while falling asleep (RFM),12 and alternating leg muscle activation (ALMA).3 Among these conditions, PLMS, resting tremor in Parkinson disease, drug-induced akathisia, HFT and RFM, and ALMA should be differentiated from HFLM because of their polygraphic similarities.HFLM, like PLMS, is stereotyped and periodic. HFLM, however, is distinct from PLMS in its frequency (1-2 Hz vs. an average of 20-40 sec), and movement duration (100 to 700 msec vs. 0.5 to 5.0 sec). PLMS is also most prominent in the first three hours of the night,13 whereas HFLM appear roughly equivalently in all parts of the night.The resting tremor of Parkinson disease (PD) can involve the legs, but it is faster (3-6 Hz) than HFLM and usually disappears as the patient falls asleep.1 Furthermore, we excluded patients with PD from our sample.Drug-induced akathisia (DIA), most commonly seen with dopaminergic antagonists, is characterized by a coarse tremor of the legs/feet and/or myoclonic jerks of the feet. The tremor in DIA can be polygraphically recorded at 0.5-3.0 Hz for seconds to minutes.11 However, DIA usually disappears with sleep. None of our subjects was taking a neuroleptic, although 12 of 37 were taking antidepressants, which can rarely cause DIA.14Broughton described and coined the term of HFT in two patients with severe head trauma, showing short series of rhythmic oscillating movements of the whole foot or toes with the rate of 0.5-1.5 Hz.2 These movements developed in pre-sleep wakefulness and light sleep but not in slow wave sleep and REM sleep. In distinction, 50% of HFLM had a frequency of greater than 1.5 Hz, and HFLM was observed in all sleep stages. Wichniak et al. investigated 375 subjects, mainly consisting of patients with sleep-breathing disorder, and found that 7.5% of them had rhythmic foot movements (RFM) while falling asleep, a term corresponding to HFT.12 RFM was described as a rhythmic, oscillating movement of the whole foot or toes, with a 1-2 Hz frequency, 300-700 msec of single EMG burst duration, and 10-15 sec of sequence duration. RFM generally occurred bilaterally but asynchronously in both legs. RFM was primarily recorded in presleep wakefulness and light NREM sleep, and sometimes during arousals from light NREM and REM sleep, but not in slow wave sleep. The prevalence of RFM (7.5%) in that study is the same as that of HFLM (7.6%), and RFM resembles HFLM polygraphically in its frequency, single burst duration, and sequence duration. However, compared to RFM, HFLM occurred in all sleep stages including slow wave sleep and it was mostly unilateral rather than bilateral. In addition, HFLM was either asynchronous or synchronous when it occurred bilaterally.Chervin et al. described alternating leg muscle activation (ALMA) in 16 patients, predominantly with mainly sleep-breathing disorders.3 ALMA was characterized by rapidly alternating movements of the right and left anterior tibialis muscles at a frequency of 1 to 2 Hz, each contraction lasting 0.1 to 0.5 sec, with trains lasting less than 20 sec. ALMA occurs in all sleep stages. Consentino et al. reported a case of ALMA in a 33-year-old male who complained of nonrestorative sleep and excessive daytime sleepiness, not taking an antidepressant and having no other abnormality on polysomnography.15 They suggested that ALMA in their case might be considered as a sleep instability phenomenon (i.e., arousal) and that it may have clinical consequences such as sleep disturbance and heart rate increase. Given the alternating pattern in the cases of Chervin et al., the authors were led to speculate that ALMA may represent transient facilitation of a spinal central pattern generator for locomotion. Furthermore, as 75% of these cases were taking antidepressants, from which they hypothesized that ALMA was perhaps due to dopaminergic insufficiency caused by the serotonergic effects of antidepressants. ALMA resembles HFLM in polygraphic appearance, rate (1 to 2 HZ), burst duration (0.1 to 0.5 sec), and occurrence in all sleep stages (including REM sleep). However, HFLM mostly had a unilateral pattern rather than alternating one. Many HFLM sequences lasted longer than those observed in the ALMA case series, and HFLM was more common than ALMA (7.6% vs. 1.1%). It is possible that ALMA represents a subtype of HFLM characterized by an alternating pattern of activation.The cause of HFLM is uncertain. Its increased prevalence in those with RLS suggests a common etiology between the two disorders. As dopaminergic and iron hypotheses have been suggested in RLS,16 it is feasible that these have some role in HFLM as well.Clinical implications of HFLM are unclear at this point. Given its association with RLS, it may either be a polysomnographic marker of that disorder (akin to periodic limb movements while awake), or in some cases, may represent a form fruste of RLS. Like PLMWA, which often continue as PLMS during sleep, HFLM are seen in waking and sleep. However, the former movements have greater variability over time in appearance and rhythmicity than HFLM, potentially suggesting that HFLM are less voluntary than PLMW. Alternately, HFLM may be an independent sleep related movement disorder with some association with RLS. Careful interview of patients with HFLM regarding leg sensations and movements prior to sleep and during arousals from sleep may be of value. On the other hand, HFLM may be predominantly an incidental polysomnographic finding without significant clinical importance and thus may represent a quasi-physiological phenomenon. The lack of clinical and polysomnographic findings distinguishing those with and without HFLM is evidence in favor of this perspective. However, there is some suggestion that HFLM, especially when severe, may have clinical significance. Roughly one-third of HFLM in our study occurred during sleep, and most (72%) were associated with EEG arousal. Futhermore, cardiac activation occurred in association with HFLM, even in the absence of AASM-defined arousal. Leg movements such as PLMS may cause poor sleep quality and non-restorative sleep by provoking EEG arousals or awakenings.17 It also has been suggested that sympathetic overactivity associated with PLMS, as manifested by increased heart rate and blood pressure, may lead to cardiovascular and cerebral diseases such as hypertension, heart disease, and stroke.18 In many of our subjects, there were repeated (up to 111 times per record) and/or long-lasting HFLM (up to 6 min in duration and up to 17% of time in bed) which resulted in EEG arousal and increased heart rate. Therefore, it is conceivable that repetitive and long-lasting HFLM may have clinical significance in terms of sleep continuity (insomnia), daytime functioning (sleepiness), and cardiovascular and cerebrovascular consequences.When interpreting these findings, the limitations of this study should be considered. This was a retrospective study and patients were thus enrolled in an uncontrolled fashion. RLS was diagnosed by self-reported RLS symptoms, not by face-to-face interview. HFLM was observed only in the legs, not in other limbs, because our sleep laboratory recorded only anterior tibialis EMG in the routine polysomnogram, so we cannot describe its distribution. The sample size of patients with HFLM was small, which may limit the power of this study. It is possible that the failure to detect differential effects of HFLM on clinical and polysomnograhpic findings is due to the small sample size of this sample. For instance, although subjects with HFLM had higher mean PLM index and took more antidepressants than the group without HFLM, these comparisons failed to reach statistical significance. A larger sample size may have yielded statistically significant results. Video recording of HFLM is warranted in future studies, by which we can analyze the inter-relationship between video-monitored movements and EMG recordings in the polysomnogram. Lastly, this study was performed only in patients with sleep disorders, mainly sleep-breathing disorder. Therefore, generalization of our results is limited. Further studies on a larger number of sleep clinic patients and on the general population are required to determine the characteristics of HFLM.In conclusion, HFLM is a common rhythmic electromyographic phenomenon that is recorded during the standard polysomnogram. It occurs mainly during waking, but can develop from all sleep stages. Further studies are needed to understand its similarities and differences from other reported wake and sleep related movements, and by this means to establish criteria for scoring HFLM. Furthermore, its clinical implications and pathophysiology are yet to be explored. HFLM and other similar movement disorders have been reported mostly among patients with primary sleep disorders. Examination of other patient cohorts and non-patient samples with HFLM will be needed to determine whether HFLM are in fact associated with RLS.DISCLOSURE STATEMENTThis was not an industry supported study. The authors have indicated no financial conflicts of interest.References1 Askenasy JJYahr MDParkinsonian. 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Yeh P, Siddiqui F and Walters A The Evolution of Diagnostic Rules and Standards for Sleep-Related Movement Disorders Encyclopedia of Sleep, 10.1016/B978-0-12-378610-4.00378-8, (1-9), . Volume 06 • Issue 05 • October 15, 2010ISSN (print): 1550-9389ISSN (online): 1550-9397Frequency: Monthly Metrics History Submitted for publicationJanuary 1, 2010Submitted in final revised formMay 1, 2010Accepted for publicationJune 1, 2010Published onlineOctober 15, 2010 Information© 2010 American Academy of Sleep MedicineKeywordsLeg movementsanterior tibialisperiodic leg movements of sleeprestless legs syndromePDF download