Abstract
Study Objectives:
Reduced mobility during sleep characterizes a variety of movement disorders and neuromuscular diseases. Facioscapulohumeral muscular dystrophy (FSHD) is the third most common form of muscular dystrophy in the general population, and people with FSHD have poor sleep quality. The aims of the present study were to evaluate nocturnal motor activity in patients with FSHD by means of videopolysomnography and to verify whether activity was associated with modifications in sleep structure.
Methods:
We enrolled 32 adult patients affected by genetically confirmed FSHD (18 women and 14 men, mean age 45.1 ± 13.4 years) and 32 matched control subjects, (18 women and 14 men, mean age 45.5 ± 11.4 years). Major body movements (MBM) were scored in videopolygraphic recordings in accordance with established criteria. An MBM index was calculated (number of MBM per hour of sleep).
Results:
The FSHD group showed a decrease in the MBM index (FSHD: 1.2 ± 1.1; control subjects: 2.3 ± 1.2, analysis of variance F = 13.672; p = 0.008). The sleep pattern of patients with FSHD, as compared with that of controls, was characterized by longer sleep latencies, shorter sleep durations, an increased percentage of wake during sleep, and a decreased percentage of rapid eye movement sleep. In the patient group, the MBM index was inversely correlated with severity of disease (Spearman test: r30 = −0.387; p < 0.05).
Conclusions:
The present findings suggest that patients with FSHD have a reduced number of nocturnal movements, which is related to disease severity. Reduced movement in bed may contribute to the sleep modifications observed in these patients.
Citation:
Marca GD; Frusciante R; Dittoni S; Vollono C; Losurdo A; Testani E; Scarano E; Colicchio S; Iannaccone E; Tonali PA; Ricci E. Decreased nocturnal movements in patients with facioscapulohumeral muscular dystrophy. J Clin Sleep Med 2010;6(3):276-280.
Keywords: Facioscapulohumeral muscular dystrophy, sleep, body movements, sleep quality, polysomnography
Facioscapulohumeral muscular dystrophy (FSHD) is the third most common form of muscular dystrophy in the general population (after dystrophinopathies and myotonic dystrophy) and the second most common form of muscular dystrophy in adults (after myotonic dystrophy).1 FSHD results from a heterozygous partial deletion of a critical number of repetitive elements (D4Z4) on chromosome 4q35. The number of KpnI repeats left on the shortened chromosome 4 inversely correlates with the severity of disease, but this relationship appears very strong only in the presence of EcoRI fragment sizes ranging from 10 to 13 kb.2,3 (For a detailed review of the genetics of FSHD see Tupler et al.4)
BRIEF SUMMARY
Current Knowledge/Study Rationale: Patients with neuromuscular disease have poor sleep quality, and on possible mechanism of sleep disruption is reduced mobility during sleep. The aim of the present study was to quantify body movements during sleep in a group of patients with Facioscapulohumeral Muscular Dystrophy.
Study Impact: The results of this study indicate that nocturnal motility is decreased in FSHD patients, and the reduction of body movements is related to the severity of the disease. Nocturnal motility is a possible mechanism of sleep disruption, and should be evaluated in patients with neuromuscular diseases.
The phenotypic spectrum of FSHD is wide and heterogeneous. Disease severity ranges from mild, in which the patient may be unaware of the disease, to severe muscle impairment in wheelchair-bound patients. High clinical variability is observed among members of different families, as well as among members of the same family.1 Age at onset is variable: most patients become symptomatic in the second decade, but also forms of FSHD have been reported that have an onset in childhood.5 The disease initially involves facial and scapular muscles, followed by spread to humeral and abdominal muscles and, finally, to muscles of the lower limbs. At disease onset, difficulty in reaching above shoulder level is the most common symptom, whereas initial presentation in the lower extremities is less common and is generally characterized by footdrop.5 Another typical characteristic of FSHD is asymmetric muscle weakness.
Patients with neuromuscular disorders such as FSHD are prone to having poor-quality sleep,6 but sleep in FSHD, per se, has not been objectively evaluated. In our earlier study,7 50% of our patients subjectively reported having poor sleep quality, and sleep quality was inversely related to the severity of muscle impairment. These subjective findings suggest that muscle weakness may represent a pathogenic mechanism of sleep disruption, but objective data have not yet been collected. Therefore, the aims of the present study were to objectively evaluate nocturnal motor activity in a group of patients with FSHD by means of videopolysomnography8 and to verify whether reduced motor activity is associated with modifications in sleep structure.
METHODS
The study design was approved by the local ethics committee; all patients and control subjects were fully informed, and all gave written consent to participate in the study.
Subjects
Patients
The study participants were selected from 52 consecutive patients with FSHD who underwent full-night, laboratory-based, attended polysomnography with recording of respiratory parameters. Inclusion criteria were age greater than 18 years and a diagnosis of FSHD genetically confirmed by a deleted fragment of less than 40 kb. Exclusion criteria were age younger than 18 years, genetic mosaicism, a genetically confirmed diagnosis of FSHD but a deleted fragment size of 40 kb or greater, and the presence of polysomnographic findings consistent with sleep disordered breathing (SDB; apnea-hypopnea index, including obstructive and mixed events of 5 or more events per hour of sleep or an oxygen desaturation index of 10 or more events per hour of sleep).9,10 Only patients with FSHD without SDB were enrolled in the present study because the presence of SDB can affect nocturnal arousals and body movements.11
The diagnosis of FSHD was made on a clinical basis and confirmed by genetic testing. In particular, restriction of genomic DNA, 32P labeling, and hybridization with L1LA5 (D4S163), pH30 (D4S139), and p13E-11 (D4F104S1) were performed, as has been described elsewhere.12,13 Pulsed-field gel electrophoresis analysis of p13E-11 alleles12 was performed.
All patients underwent a full medical and neurologic evaluation and a detailed sleep history, which included a subjective evaluation of sleep. The protocol for subjective sleep evaluation, which has been described previously in detail,7,10 included the Pittsburgh Sleep Quality Index,14 the Italian version of the Epworth Sleepiness Scale,15 and the ascertainment of clinical signs and symptoms predictive of SDB. Muscle strength was evaluated by using the Manual Muscle Test, and a score was assigned according to the Medical Research Council Scale16—ranging from 0 (no movement, no visible or palpable contraction) to 5 (segment movement through full range of motion against gravity and ability to hold against resistance). To measure the clinical severity of muscle impairment, a 10-grade Clinical Severity Scale (CSS)3 was adopted, with scores ranging from 0.5 (facial weakness) to 5 (wheelchair bound). According to this scale, a CSS score of 2 or less is assigned to patients with facial- and shoulder-muscle weakness, whereas higher scores (> 2) are assigned to patients showing weakness of muscles of both the pelvic and lower limbs. The CSS scores in our patients were assessed by clinical neurologists with special expertise in the clinical management of patients with FSHD (RF, EI, ER).
Control Subjects
Data from healthy subjects, matched for age and sex, were randomly extracted from the database of our sleep laboratory and comprised the group of control subjects.
Polysomnography
Full-night, laboratory-based polysomnograms were recorded in acclimatized, sound-proof rooms following adaptation. The recording montage included electroencephalography (C3, C4, F3, F4, O1, O2) with reference electrodes applied to the left (A1) and right (A2) mastoids, 2 electrooculographic electrodes applied to the outer ocular canthus and referred to the contralateral mastoid, surface electromyography of submental and intercostal muscles, airflow measured by nasal-cannula pressure transducers, thoracic and abdominal effort, electrocardiogram, and peripheral hemoglobin saturation measured by a clip sensor placed on a finger or an earlobe. Continuous audio and video recording was performed by means of infrared cameras.
Sleep recordings were analyzed on a computer monitor, and sleep stages were visually classified according to the criteria of the American Academy of Sleep Medicine.17 The main methodologic difference between our scoring system and that described by De Koninck et al.8,18 was in the acquisition of the video recordings. De Koninck et al. used a super-8 camera with an 8-second exposure, set to capture a frame every 8 seconds, whereas we performed a continuous digital infrared videorecording, with 2 cameras synchronized with the polysomnography tracing.
Major body movements (MBM) were defined on the basis of videopolygraphic findings in accordance with the criteria established by the American Academy of Sleep Medicine.17 MBM were defined, on the polysomnography tracings, as movements obscuring the electroencephalogram for more than half an epoch. The occurrence of an MBM was verified on the video recordings. An MBM index was calculated—defined as the number of MBM per hour of sleep. To verify the reliability of our normative data, the number of MBM in the control group was compared with that reported in literature.18 We scored the body movements associated with major change in body position. The time spent during sleep in each main body position—supine, prone, left side, right side, undefined—was calculated.
Statistical Analysis
Statistical comparisons were performed on data from patients with FSHD and control subjects. Continuous variables (demographic variables and sleep parameters) were compared by means of 1-way analysis of variance followed by the Tukey posthoc test, since the 2 groups—patients with FSHD and control subjects—showed equal variances. The level of significance was set at p < 0.05.
Within the FSHD group, correlations among polysomnography findings were tested by means of the Pearson correlation index. In particular, the values of the Pearson index were calculated between parameters of sleep macrostructure and the MBM. The critical value of the Pearson product-moment correlation coefficient was set to r30 = 0.349, corresponding to a significance level p < 0.05. Since the CSS scores are noncontinuous, rank-ordered data—correlations between polysomnography findings and CSS—were tested by means of the Spearman correlation matrix. The critical value of the Spearman correlation coefficient was set to r30 = 0.350, corresponding to a significance level p < 0.05.
Statistical analysis was performed using the SYSTAT version 12.02.00 for Windows (SYSTAT Software Inc., Chicago, IL).
RESULTS
Subjects
Patients
Of the 52 patients with FSHD who met the age- and genetic-based inclusion criteria, 20 had polysomnographic evidence of SDB and were therefore excluded from the study. The remaining 18 women and 14 men, who comprised the patients in this study, had a mean age of 45.1 ± 13.4 years (range: 26-72 years).
Control Subjects
The 18 women and 14 men who comprised the control group had a mean age of 45.5 ± 11.4 years (range: 25-62 years).
Clinical and Genetic Evaluations
The CSS scores in the patients ranged from 1 to 5 (mean: 3.1 ± 1.1); 1 patient was wheelchair bound (CSS score = 5). No patients had other medical, neurologic, or psychiatric illnesses, and none consumed central nervous system-active drugs in the 4 weeks prior to the study. The results of the sleep questionnaires are listed in Table 1. Fifteen patients had Pittsburgh Sleep Quality Index scores of 5, which is considered to be the cutoff score for poor sleep quality; 4 patients had Epworth Sleepiness Scale scores of 10 or greater, which is considered to be pathologically sleepy. The mean length of the deleted fragment in our FSHD sample was 22.7 ± 5.3 kb (range: 10-33 kb).
Table 1.
| Parameter | Patients with FSHD (n = 32) |
|---|---|
| Age, y | 45.1 ± 13.4 |
| Men | 14 |
| EcoRI, kb | 22.7 ± 5.3 |
| CSS score | 3.0 ± 1.1 |
| BMI, kg/m2 | 22.8 ± 2.8 |
| Neck circumference, cm | 36.8 ± 4.0 |
| PSQI score | 6.1 ± 3.7 |
| ESS score | 4.7 ± 3.6 |
| Reported | |
| Snoring | 13 |
| Apneas | 5 |
| Nocturia | 11 |
| Morning headache | 5 |
| Arterial hypertension | 6 |
Data are presented as mean ± SD or number.
FSHD refers to facioscapulohumeral muscular dystrophy; CSS, Clinical Severity Scale; BMI, body mass index; PSQI, Pittsburgh Sleep Quality Index; ESS, Epworth Sleepiness Scale.
Polysomnography
The results of sleep analysis in patients and control subjects (expressed as mean ± SD), as well as the results of the statistical comparison of the 2 groups, are summarized in Table 2. When compared with control subjects, patients with FSHD had longer sleep latencies, shorter sleep durations (characterized by similar time in bed but significantly shorter total sleep time and sleep period time) and an increased percentage of wake during sleep (although the number of awakenings and the wake time after sleep onset did not significantly differ ).
Table 2.
Comparison of polysomnographic parameters between patients with FSHD and control subjects
| Sleep parameters | Patients with FSHD | Control subjects | p value |
|---|---|---|---|
| SOL, min | 55.7 ± 43.4 | 33.5 ± 23.9 | 0.014 |
| TIB, min | 482.7 ± 45.1 | 495.8 ± 36.6 | 0.208 |
| TST, min | 352.0 ± 66.9 | 403.0 ± 57.9 | 0.002 |
| SPT, min | 420.6 ± 57.3 | 454.1 ± 39.1 | 0.008 |
| Total awake time, min | 23.5 ± 12.0 | 19.1 ± 10.5 | 0.125 |
| Awakenings > 1 min, no. | 9.8 ± 5.1 | 8.0 ± 6.0 | 0.199 |
| WASO, min | 75.5 ± 40.4 | 59.7 ± 52.3 | 0.182 |
| Time spent in various sleep stages, % | |||
| Wake | 16.8 ± 10.1 | 11.3 ± 10.4 | 0.036 |
| REM | 13.6 ± 4.4 | 16.7 ± 7.1 | 0.042 |
| 1 | 10.1 ± 7.5 | 11.7 ± 9.1 | 0.431 |
| 2 | 41.0 ± 12.5 | 39.4 ± 10.4 | 0.589 |
| 3 | 18.6 ± 9.1 | 20.7 ± 10.7 | 0.381 |
| Time spent in various body positions, % | |||
| Abdomen | 5 .6 ± 14.0 | 3.1 ± 8.0 | 0.352 |
| Back | 37.7 ± 30.3 | 37.1 ± 19.8 | 0.963 |
| Left side | 33.0 ± 28.5 | 24.3 ± 20.1 | 0.195 |
| Right side | 21.8 ± 20.7 | 33.4 ± 20.7 | 0.014 |
| Undefined | 1.9 ± 3.5 | 2.2 ± 6.3 | 0.820 |
Data are expressed as mean ± SD. The p values are derived from analysis of variance.
FSHD refers to facioscapulohumeral muscular dystrophy; SOL, sleep-onset latency; TST, total sleep time; TIB, time in bed; SPT, sleep period time; WASO, wake time after sleep onset; REM, rapid eye movement sleep.
When comparing the percentages of the various sleep stages, we found the only significant difference to be the duration of rapid eye movement sleep, which was slightly reduced in the FSHD group. The primary objective of our study—the MBM index—was significantly reduced in the FSHD group, as compared with in the control subjects. The mean MBM index in patients with FSHD was 1.2 ± 1.1, versus 2.3 ± 1.2 in the control group (analysis of variance F = 13.672; p = 0.008; see Figure 1). The mean number of MBM throughout the entire night was 9.8 ± 8.7 in the FSHD group and 19.1 ± 10.7 in the control group. This control-group value is similar to that reported in literature: 16.4 ± 7.1 to 27.1 ± 8.9 body-position changes per night in the 18- to 80-year-old age group.8,18
Figure 1.
Statistical comparison between the index of major body movements in patients with facioscapulohumeral muscular dystrophy (FSHD, white column) and control subjects (black column).
For the scoring of MBM, we applied the criteria established by the American Academy of Sleep Medicine.17 In the FSHD group, the MBM index showed an inverse correlation with the severity of muscle impairment, as evidenced by the CSS scores (Spearman r30 = −0.387; p < 0.05) (see Figure 2). Moreover, Pearson correlations for MBM index were significant for sleep latency (r30 = −0.43; p < 0.02), sleep period time (r30 = 0.42; p < 0.02), and duration of sleep stage 3 (r30 = −0.37; p < 0.05).
Figure 2.
Inverse correlation between the index of major body movements and severity of muscle impairment in the group with facioscapulohumeral muscular dystrophy.
DISCUSSION
The main finding of the present study was a striking reduction in the number of nocturnal body movements in patients with FSHD, as compared with control subjects: patients with FSHD had an MBM index that was one-half that of the control population. Moreover, within the FSHD group, an inverse correlation (Figure 1) was observed between the MBM index and the severity of muscle impairment, as measured by the CSS.3 This suggests that the reduced nocturnal motility appears to be a direct consequence of the muscle deficit.
The present polygraphic study confirms our previous observation7 (based on subjective evaluations) that patients with FSHD have poor sleep quality. Polysomnographic recordings in our population of patients with FSHD revealed that these patients have difficulty initiating sleep, shorter sleep durations, an increased amount of wake time during sleep, and a reduced percentage of rapid eye movement sleep, as compared with control subjects. Interestingly, no differences between FSHD and control subjects were detected in the number of short (< 1-min) and long (> 1-min) awakenings. This pattern of sleep disruption, characterized by a longer sleep latency and increased duration of nocturnal awakenings, suggests that the main disturbance in patients with FSHD is the ability to fall asleep, both at the beginning of the night and after nocturnal awakenings.
Poor sleep quality is generally associated with an increased number of position shifts during the night.8,18 However, in our patients with FSHD, we observed the opposite finding—a decrease in the number of MBM, as compared with control subjects, despite a worse quality of sleep. All of these findings are consistent with the hypothesis that reduced motility, due to muscle impairment, may contribute to sleep disruption in FSHD. The finding of significant correlations between the MBM index and sleep latency, sleep duration, and the amount of slow wave sleep further suggests that reduced motility contributes to sleep disruption.
It has already been reported in patients with movement disorders that the ability to change body position is a critical issue in the initiation of sleep.19 Decreased motility in bed has been considered to be a cause of sleep disruption in patients who have one of several neurologic diseases and, in particular, in patients with movement disorders20,21 and neuromuscular diseases.13 Nevertheless, most polysomnographic studies of patients with neuromuscular disorders, and particularly muscular dystrophies, have focused primarily on the sleep-related respiratory patterns,22–26 and the issue of nocturnal motility appears to have been neglected.
In the present series, the presence of SDB was an exclusion criterion, and the evaluation of nocturnal motility and sleeping postures was the primary endpoint. Evaluation of nocturnal MBM can be easily performed in routine videopolysomnography recordings; the MBM index is a useful index of nocturnal motility and can provide a clinically relevant index of motor function that is not influenced by patient compliance. The assessment of nocturnal motility, together with respiratory studies, appears to be essential for the objective evaluation of sleep disorders in patient with muscular dystrophies.
In conclusion, the present findings support the hypothesis that patients with FSHD have reduced nocturnal motility related to the severity of the muscle impairment and that the decreased motility in bed may contribute to the alterations in sleep that have been observed in these patients.
DISCLOSURE STATEMENT
This was not an industry supported stuyd. The authors have indicated no financial conflicts of interest.
ACKNOWLEDGMENTS
The work was performed at the Catholic University, Rome, Italy.
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