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A New Marker of Sleep Alteration In Cyclic Alternating Pattern: A New Marker of Sleep Alteration in Patients with Fibromyalgia? MAURIZIO RIZZI, PIERCARLO SARZI-PUTTINI, FABIOLA ATZENI, FRANCO CAPSONI, ARNALDO ANDREOLI, MARICA PECIS, STEFANO COLOMBO, MARIO CARRABBA, and MARGHERITA SERGI ABSTRACT. Objective. In the dynamic organization of sleep, cyclic alternating pattern (CAP) expresses a condi- tion of instability of the level of vigilance that manifests the brain’s fatigue in preserving and regu- lating the macrostructure of sleep. We evaluated the presence of CAP in patients with fibromyalgia (FM) compared to healthy controls. Methods. Forty-five patients with FM (42 women) were studied and compared with 38 healthy subjects (36 women) matched for age, sex, and body mass index. Entry criteria were diagnosis of FM according to 1990 American College of Rheumatology criteria; willingness to participate in the study; and having no other diagnosis of autoimmune, neoplastic, or other possible causes of secondary diffuse musculoskeletal pain. Patients in the study underwent polysomnography record- ings and a sleep questionnaire. Hypersomnolence was evaluated according to the Epworth Sleepiness Scale. Results. FM patients had less sleep efficiency (sleep time/time in bed) than controls (79 ± 10 vs 89 ± 6; p < 0.01), a higher proportion of stage 1 non-rapid eye movement (non-REM) sleep (20 ± 5 vs 12 ± 5; p < 0.001), and twice as many arousals per hour of sleep (9.7 ± 3.3 vs 4.1 ± 1.9; p < 0.01). The CAP rate (total CAP time/non-REM sleep time) was significantly increased in FM patients compared to controls (68 ± 6% vs 45 ± 11%; p < 0.001). CAP rate seemed to correlate with the severity of clinical symptoms in FM patients (tender points index; p < 0.01) and with less efficiency of sleep (p < 0.01). Conclusion. The increase of CAP rate indicates a worse quality of sleep in patients with FM. These data are strongly correlated to the severity of symptoms. (J Rheumatol 2004;31:1193–9) Key Indexing Terms: FIBROMYALGIA CYCLIC ALTERNATING PATTERN SLEEP POLYSOMNOGRAPHY Fibromyalgia syndrome (FM) is a common condition alpha wave intrusion on delta wave sleep, characterized by causing generalized musculoskeletal pain1. This syndrome alpha wave activity (frequency 7–11 cycles per second) that affects up to 3–4% of the general population and is one of is superimposed on the delta wave sleep (frequency 2 the most common diagnoses seen in ambulatory office cycles/s and amplitude > 75 µV), as a marker of the sleep settings; 80% to 90% of patients are women and the peak impairment typical of FM; however, this alteration in sleep age is 30–50 years2. The criteria used for diagnosis were macrostructure has not been confirmed by other studies9,10, formulated by the American College of Rheumatology whereas an association between alpha wave intrusion in (ACR) in 19903. The reported complaint of poor sleep4 is so non-REM sleep and other FM symptoms has been variously common in patients with FM that in some case series its confirmed11 and rejected5 by different trials. prevalence is nearly 100%5-7. The observation that a neuras- The hypothesis that other disorders causing sleep frag- thenic musculoskeletal pain syndrome can be elicited in mentation, such as sleep apnea syndrome12, might be healthy volunteers undergoing deep non-rapid eye move- blamed for the nonrefreshing sleep symptoms is reported in ment (non-REM) sleep deprivation7 seems to suggest that a another study13. In patients with FM, Sergi, et al6 recently cycle may be in operation, with pain-impaired sleep leading described a greater number of abrupt changes in electroen- to a worsening of the disease. Moldofsky, et al8 proposed an cephalographic (EEG) frequency, suggestive of an awake state, and/or brief increases in electromyographic (EMG) From the Center for Sleep and Respiratory Disorders, Rheumatology amplitude (arousal) accompanied by the presence of peri- Unit, University Hospital L. Sacco, IRCCS Policlinico University odic breathing. Hospital, Milan, Italy. Another condition that can cause sleep fragmentation is M. Rizzi, MD; P. Sarzi-Puttini, MD; F. Atzeni, Research Fellow; F. 14 Capsoni, Associate Professor of Rheumatology; A. Andreoli, MD; M. the cyclic alternating pattern (CAP) ; it corresponds to a Pecis, MD; S. Colombo, MD; M. Carrabba, MD, Chief, Rheumatology prolonged oscillation of the arousal level between two reci- Unit; M. Sergi, MD, Chief, Center for Sleep and Respiratory Disorders. procal functional states termed phase A (greater arousal) and Address reprint requests to Dr. M. Sergi, Fisiopatologia Respiratoria, phase B (lesser arousal), and in the dynamic organization of University Hospital L. Sacco, Via GB Grassi 74, 20157 Milan, Italy. E-mail:[email protected] sleep it expresses a condition of instability of the level of Submitted January 27, 2003; revision accepted December 30, 2003. vigilance that manifests the brain’s fatigue in preserving and Personal non-commercialPersonal, non-commercial use only. use The only. Journal The Journal of of Rheumatology.Rheumatology. Copyright Copyright© 2004. All rights © reserved. 2004. All rights reserved Rizzi, et al: CAP sleep alteration in FM patients 1193 Downloaded on September 28, 2021 from www.jrheum.org regulating the macrostructure of sleep. In phase A, 3 subtypes electrodes recorded airflow and ventilatory efforts, respectively. can be distinguished in the EEG pattern: A1, A2, A315. Oxyhemoglobin saturation was recorded by finger pulse oximetry (Pulsox- CAP is observed only in stage 1, 2, 3, 4 non-REM 7, Minolta, Osaka, Japan). The transducers and lead wires allowed normal positional changes during sleep. Bedtime and awakening time were at each 14,16 sleep , in accord with the Rechtschaffen and Kales clas- subject’s discretion: the polysomnography was terminated after final awak- sification17. CAP cycles are generally clustered in ening. To avoid first-night effect, each subject spent 2 nights in the sleep sequences; conversely, the portion of non-REM sleep asso- laboratory; only data recordered during the second night were evaluated. ciated with relative stability of arousal and autonomic activ- Sleep and breathing variables were stored on an optical disk and then ities, non-CAP, is expressed by stationary and homogeneous manually scored by 2 physicians, blinded, in 30 s epochs, according to stan- dard criteria17. Correlation between sleep, breathing, and body position was EEG patterns. analyzed automatically by the computer. We evaluated the presence of CAP in patients with FM The overnight EEG activity was recorded using 10 bipolar leads (Fp2- compared to healthy controls. F4, F4-C4, C4-P4, P4-O2, Fpl-F3, F3-C3, C3-P3, P3-O1, FZ-CZ, and CZ- PZ) and a classical unipolar C3-A2. MATERIALS AND METHODS Apneas were defined as 10-second pauses in respiration. Hypopnea was defined as a decrement in airflow ≥ 50%, associated with either an arousal Study population. Forty-five eligible consecutive Caucasian patients (42 at the end of the episode or a fall in arterial oxygen saturation ≥ 4%. The women) aged 52.2 ± 8.2 years, with FM diagnosed according to the 1990 respiratory disturbance index (RDI) was defined as the average number of ACR classification criteria, were invited to participate in this study and episodes of apnea and hypopnea per hour of sleep, and the desaturation were compared with 38 healthy controls (36 women) matched for age, sex, event frequency (DEF) was defined as the number of episodes of fall ≥ 4% and body mass index (Table 1). A 2-week washout period for any pharma- in oxyhemoglobin saturation per hour of sleep. Periodic breathing was cological treatment related to FM was requested of all patients. A sleep defined as a series of at least 3 successive cycles of waxing and waning in questionnaire and the Epworth Sleepiness Scale (ESS) were then adminis- ventilation, with apneas or hypopnea. Arousals were scored according to tered to all subjects. Informed consent was obtained in all cases, and the the American Sleep Disorders Association (ASDA) criteria19. Alpha-delta hospital Medical Ethics Committee approved the study. intrusion was defined as the spontaneous occurrence of alpha waves in Clinical evaluation. In all subjects the following clinical variables were delta wave sleep8. evaluated: examination of 18 tender points using the protocol of Wolfe, et CAP parameters were identified according to the scoring rules estab- 3 al ; intensity of somatic pain expressed on a 100 mm visual analog scale lished in a recent consensus report20. All CAP sequences include at least 2 (VAS); and anxiety, depression, and fatigue expressed on 100 mm VAS. consecutive CAP cycles and always begin with a phase A and a phase B. Study measures. A sleep questionnaire was administered to all subjects to Absence of a phase A for > 60 consecutive seconds creates a prolonged evaluate sleep complaints12. Hypersomnolence was evaluated according to stationary condition of arousal stability and is scored as non-CAP. the ESS18. The ESS is a questionnaire measuring the general level of CAP rate referred to non-REM sleep is a percentage ratio of total CAP daytime sleepiness and is the sum of 8 item scores. It can vary from 0 to time to total non-REM time. We also calculated the mean duration of B 24; the “clinically” normal range of the ESS score is 2 to 10 with a normal phases, and number and mean duration of A1, A2, and A3 subtypes. statistical distribution and a model score of 6. Through computer analysis, we were able to determine the sleep Polysomnography. Polysomnography was performed in the sleep labora- histogram of each patient to identify the sequences of the periods corre- tory, a sound-attenuated room with temperature control, using a computer- sponding to the CAP and to periodic breathing. assisted device (Alice 3, Healthdyne, Marietta, OH, USA). The Statistical analysis. Data were reported as mean ± standard deviation. electroencephalogram, electro-oculogram, and submental electromyogram Statistical analysis of the anthropometric data and polysomnographic were recorded with surface electrodes using standard techniques17.
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