| | Sleep-Disordered Breathing in Fatigued Postpoliomyelitis Clinic PatientsPresented in part to the American Academy of Physical Medicine and Rehabilitation, October 28, 2005, Philadelphia, PA. Abstract Dahan V, Kimoff RJ, Petrof BJ, Benedetti A, Diorio D, Trojan DA. Sleep-disordered breathing in fatigued postpoliomyelitis clinic patients. ObjectiveTo determine the frequency, predictive factors, and symptoms predictive of sleep-disordered breathing (SDB) in fatigued postpoliomyelitis clinic patients. DesignCross-sectional, retrospective chart review. SettingUniversity-affiliated hospital postpolio clinic. ParticipantsPostpolio clinic charts (N=590) were reviewed. Ninety-eight patients were included, and 492 patients were not included, primarily because of the lack of a polysomnogram. InterventionsNot applicable. Main Outcome MeasureThe Apnea-Hypopnea Index (AHI) calculated as the total number of sleep-related breathing events/total sleep time. ResultsThe frequency of SDB defined by an AHI score of 5 or more was 65% and by an AHI score of 10 or more was 50%. Obstructive hypopnea was the predominant form, occurring in 86%. Age, sex, age at acute polio, time since polio, weakness and respiratory difficulties at acute polio, bulbar involvement at acute polio and at evaluation, body mass index, pulmonary function measures, alcohol use, sedative drug use, smoking, fibromyalgia, kyphoscoliosis, and scoliosis and ear-nose-throat surgery were not predictive of SDB (AHI scores ≥5 and ≥10). Snoring was more common in subjects with SDB (AHI score ≥5 and ≥10). Some pulmonary function measures correlated with oxygen saturation during sleep in SDB (AHI scores ≥5). ConclusionsSDB was very common in fatigued postpoliomyelitis clinic patients referred for sleep evaluation. Obstructive hypopnea was the most frequent type. In this preliminary study, snoring tended to predict SDB. POSTPOLIOMYELITIS SYNDROME (PPS) is characterized by new weakness or muscle fatigability usually several decades after recovery from paralytic polio.1, 2 Fatigue occurs in most patients, is usually the most disabling symptom,3, 4, 5 and can be either generalized or muscular.1 However, generalized fatigue in patients with previous polio can also be due to other disorders that are common in the general adult population.2 It is essential to identify and treat these other causes before attributing fatigue to PPS. Sleep-disordered breathing (SDB) is the general term used to describe different types of disorders of respiration during sleep, including obstructive, central, and mixed events.6 The most prevalent form of SDB is obstructive sleep apnea (OSA) and hypopnea syndrome, which are characterized by repeated episodes of upper-airway collapse during sleep, resulting in repeated hypoxemia and sleep fragmentation. This in turn leads to neurocognitive sequelae, the most prominent of which is excessive daytime sleepiness or chronic fatigue, which are shown to show dramatic improvement with treatment such as nasal continuous positive-airway pressure (CPAP).7 OSA is estimated to affect 2% of women and 4% of men in the general population.8 Central apnea-hypopnea syndrome is characterized by recurrent apneic events that occur without upper-airway obstruction and inspiratory effort. Mixed events have both central and then obstructive features.6 SDB is a potential important treatable cause of general fatigue in a person with previous polio. SDB may be responsible for some of the neurocognitive difficulties reported by people with previous polio such as problems with attention, concentration, and maintaining wakefulness.9 Research suggests that patients with previous polio appear to have a significantly higher frequency of SDB than the general population, but the literature is very sparse.10, 11, 12, 13 The few studies completed are limited by small sample size and other factors such as suboptimal ascertainment of SDB. The criterion standard for the diagnosis of SDB is in-laboratory, technician-attended, complete overnight polysomongraphy,14 which was not performed in all studies. Clearly, there is a need to study SDB in the fatigued postpolio patient population using the criterion standard for diagnosis. By identifying the predictive factors and symptoms for SDB specific to this population, the physician caring for postpolio patients will be better able to refer patients for sleep evaluation and with treatment possibly alleviate a proportion of fatigue. The objectives of this study were (1) to estimate the frequency (as well as the severity and type) of SDB, (2) to determine the predictive factors for SDB, (3) to determine which presenting symptoms characteristic of sleep apnea are predictive of the presence of SDB, and (4) to evaluate the relation of pulmonary function measures with oxygen saturation during sleep in SDB in a population of fatigued postpolio clinic patients. Methods  Study Design and Population This was a cross-sectional study, involving a retrospective chart review. The study was approved by the institutional research ethics board. All available university-affiliated postpolio clinic charts belonging to 1 physician were reviewed. Two physicians work in the clinic, and new referrals are generally directed to the first available physician. At the initial clinic visit, all patients were evaluated with a standardized form that included an examination for fibromyalgia as per the 1990 American College of Rheumatology criteria.15 Data for the study were obtained from the initial visit and subsequent follow-up visits. Approximately 17% of patients evaluated were referred for sleep studies if they were reporting moderate or severe fatigue or somnolence, atypical for that usually attributed to PPS. General fatigue in PPS is usually described as a flu-like exhaustion that is aggravated by physical activity, is absent in the morning, and progresses during the day.16 In general, patients referred for sleep evaluation had a complaint of prominent generalized fatigue or somnolence in the morning or throughout the day with or without other symptoms typical for SDB. Essentially all patients were evaluated at the sleep clinic of an adjacent medical hospital (96/98 [98%]). Sleep clinic charts were reviewed, as necessary. Study data were gathered for patients evaluated from 1994 to 2004. Inclusion criteria were (1) a history and physical examination consistent with previous paralytic poliomyelitis and a new symptom of fatigue or somnolence and (2) a valid sleep study evaluation. A sleep study was considered to be valid if there was greater than 3 hours of recording and all signals were recorded to permit calculation of (1) total sleep time (in minutes); (2) number of spontaneous arousals; (3) number of respiratory arousals; (4) number of movement arousals; (5) total arousal index (number of arousals/total sleep time in hours); (6) sleep efficiency (total sleep time/total recording time multiplied by 100%); (7) number of stage changes; (8) number of awakenings; (9) duration (in minutes) and proportion (percentage of total sleep time) of stage 1, 2, 3, and 4, and rapid eye movement (REM) sleep; (10) mean oxygen saturation during non-REM and REM sleep; (11) nadir oxygen saturation; (12) number of obstructive, central apneas and mixed apneas and hypopneas; (13) number of myoclonus events (while asleep); and (14) snoring time (in minutes). Reasons for noninclusion were (1) history and physical examination not consistent with previous paralytic poliomyelitis, (2) presence of other significant neurologic difficulties (other than paralytic poliomyelitis and PPS), and (3) presence of other significant pulmonary or otorhinolaryngologic disorders. Data Collection and Outcome Measures Data on the dependent variables were obtained from polysomnogram results. The presence or absence of SDB was determined by the Apnea-Hypopnea Index ([AHI] AHI score ≥5 and AHI score ≥10). The AHI was calculated as the total number of sleep-related events ([obstructive hypopnea and apnea, central apnea, mixed apnea]/[total sleep time]) and was assessed as events per hour of sleep. An AHI score of 5 or more is usually used for the definition of OSA along with the presence of symptoms of excessive daytime sleepiness, unrefreshing sleep, or chronic fatigue.7 However, some investigators have suggested the use of a higher AHI score such as 10.17 The type of SDB was determined by the interpretation of the polysomnogram results by a pulmonary sleep specialist and the American Academy of Sleep Medicine Task Force (AASMTF) criteria.6 Three types of SDB were identified: obstructive apnea and hypopnea, central apnea and hypopnea, and mixed apnea. The severity of SDB was rated based on the classification suggested for obstructive apnea and hypopnea by the AASMTF. Mild was defined as 5 to 15 events per hour, moderate 15 to 30 events per hour, and severe greater than 30 events per hour. Data on the following independent variables were obtained: age, sex, body mass index ([BMI] in kg/m2), age at acute polio, weakness at acute polio, severity of respiratory difficulties at acute polio, presence of bulbar involvement at acute polio and at evaluation (determined by symptoms of dysphagia, dysphonia, or dysarthria), time since acute polio, pulmonary function test results, sedative drug use (at time of referral for sleep evaluation), history of ear-nose-throat surgery, history of scoliosis surgery, presence of thoracic kyphosis and/or scoliosis, alcohol use (none, occasionally, every day), currently smoking (at time of referral for sleep evaluation), presence of fibromyalgia as per the 1990 American College of Rheumatology criteria,15 and presence of symptoms characteristic of sleep apnea (snoring, daytime sleepiness [as determined by the need to take naps during the day], fatigue, witnessed apnea, nocturnal awakenings, morning headaches, nightmares, nocturnal choking, and dyspnea). Weakness at acute polio was assessed on a 0 to 6 scale, with 6 being most severe. The measure was based on subjective patient estimates of percent weakness in each of 4 limbs (0, no weakness; 0.5, partial weakness; 1, complete paralysis for each of 4 limbs), respiratory muscle weakness (0, no respiratory involvement; 0.5, partial involvement but no use of iron lung or respirator; 1, use of iron lung or respirator), and speech and swallowing difficulties (0, no difficulties; 0.5, mild difficulties with speech or swallowing; 1, significant difficulties with speech or swallowing or any degree of difficulty with both speech and swallowing). The reliability and validity of a similar measure has been described elsewhere18 and was adequate. To more specifically examine respiratory involvement, the severity of respiratory difficulties at acute polio was estimated as follows: 0 referred to no difficulties, 1 referred to partial difficulty but no use of iron lung or respirator, and 2 referred to use of iron lung or respirator. Pulmonary function test results were available for 77 included patients and 41 nonincluded patients. Measurements of the following variables were obtained: (1) forced vital capacity ([FVC] in liters and percentage predicted), (2) forced expiratory volume in 1 second ([FEV1] in liters and percentage predicted), (3) total lung capacity ([TLC] in liters and percentage predicted), (4) maximum inspiratory pressure (MIP) of the mouth (in cmH2O and percentage predicted), (5) maximum expiratory pressure (MEP) of the mouth (in cmH2O and percentage predicted), and (6) diffusion capacity (in mL·min–1·mmHg–1 and percentage predicted). Statistical Analysis Standard statistical tests were used to compare potential predictive factors and potential predictive symptoms for SDB in patient groups. We used t tests for continuous data and chi-square or Fisher exact tests for categorical data. Pearson correlation coefficients were calculated to evaluate the association of pulmonary function test results (percentage predicted FVC, TLC, FEV1, MIP, MEP, and diffusion capacity) with nadir oxygen saturation during sleep and mean oxygen saturation during non-REM and REM sleep. For the analyses of predictive factors and symptoms in included patients, we present P values that were and were not adjusted for multiple comparisons. The adjusted P values were obtained by using the method developed by Benjamini and Hochberg,19 which controls strongly for the false discovery rate, and is usually more powerful than other adjustments such as Bonferroni.20 The statistical software used for data analysis was SAS.a Results Five hundred ninety postpolio clinic charts were reviewed. Ninety-eight patients were included (1 patient had an incomplete sleep study but sufficient detail to determine AHI index and severity and type of SDB). Four hundred ninety-two patients were not included because of the absence of a polysomnogram in 383 (most had other reasons for noninclusion), presence of significant other neurologic or pulmonary disorders in 69, and absence of paralytic poliomyelitis in 40. To evaluate the comparability of patients included in the study to the more general postpolio clinic population, patients included (n=98) were compared with those not included (solely because of the absence of a polysomnogram, n=156). There were no significant differences between the 2 patient groups with regard to age, sex, FVC, MIP, scoliosis, BMI, and history of current smoking. However, patients included in the study were significantly weaker at acute polio (mean ± standard deviation [SD], 2.7±1.7 vs 2.3±1.5; P=.05), had a reduced MEP (percentage predicted value ± SD, 78.1%±42.8% vs 93.6%±27.3%, P=.003), a greater use of sedatives (45.9% vs 32.7%, P=.03), a more frequent diagnosis of PPS using the March of Dimes criteria1 (91.8% vs 47.4%, P<.001), and a more frequent diagnosis of fibromyalgia (32.6% vs 18.5%, P=.05). The frequency of SDB in postpolio clinic patients referred for sleep evaluation was 64 out of 98 (65.3%) for an AHI score of 5 or more and 49 out of 98 (50%) for an AHI score of 10 or more. Table 1 presents the types of SDB found. Obstructive hypopnea, present in 86%, was the predominant type. Most patients had mild (27/63 [42.8%]) or moderate (26/63 [41.8%]) SDB, whereas a minority (10/63 [15.9%]) had severe SDB. | | |  | Predominant Type of SDB | Patients (n=63) | AHI Score | Nadir Oxygen Saturation (%) | |
|---|
| Obstructive apnea | 4(6.3) | 10.1±2.0 | 87.8±3.7 | | | Obstructivehypopnea | 54(85.7) | 22.0±20.2 | 85.7±6.9 | | | Centralapnea | 3(4.7) | 25.8±21.5 | 75.2±19.3 | | | Mixedapnea | 2(3.2) | 16.1±14.1 | 87.5±0.8 | | | | |
A comparison of potential predictive factors in patients with and without SDB (AHI score ≥5) is presented in Table 2, Table 3. Because OSA is usually defined as AHI score of 5 or more7 and for ease of presentation, only the results for SDB (AHI score ≥5) are presented. However, analyses were performed by using both definitions for SDB (AHI score ≥5 and AHI score ≥10). When the results were corrected for multiple comparisons, patients with SDB did not differ significantly from those without SDB with regard to any of the predictive factors considered. However, based on results uncorrected for multiple testing, there was a suggestion that patients with SDB (AHI scores ≥5 and ≥10) differed from those without SDB with regard to sex (49.0% men in those with SDB [AHI score ≥10], 26.5% men in those without SDB; 95% confidence interval [CI] of difference, 3.8–41.1). In addition, patients with SDB (AHI score ≥10) tended to have a higher BMI (28.2±5.7kg/m2 in patients with SDB, 25.9±5.0kg/m2 in those without SDB; 95% CI of difference, 0.2–4.5). Patients with SDB (AHI score ≥5) also tended to be more likely to have a diagnosis of fibromyalgia. | | | | Variable | SDB | No SDB | P | Adjusted P | |
|---|
| Current acute (y) | 57.6±8.9(n=64) | 56.3±11.5(n=34) | .54 | .80 | | | Age at acute polio (y) | 5.1±5.2(n=64) | 6.7±8.4(n=34) | .26 | .58 | | | Time since acute polio (y) | 52.4±8.6(n=64) | 49.6±11.6(n=34) | .22 | .58 | | | Weakness at acute polio (0–6) | 2.7±1.6(n=63) | 2.8±1.8(n=33) | .64 | .85 | | | BMI (kg/m2) | 27.7±5.4(n=62) | 25.7±5.4(n=34) | .08 | .43 | | | FVC (% predicted) | 90.9±24.2(n=47) | 91.2±29.1(n=30) | .97 | 1.00 | | | MIP (% predicted) | 85.1±5.8(n=45) | 77.2±30.6(n=28) | .24 | .58 | | | MEP (% predicted) | 78.0±23.5(n=45) | 78.1±27.3(n=28) | .98 | 1.00 | | | | |
| | | | Variable | SDB (%) (n=64) | No SDB (%) (n=34) | P | Adjusted P | |
|---|
| Men | 45.3 | 23.5 | .03 | .28 | | | Bulbar involvement at acute polio | 9.7 | 20.0 | .19 | .56 | | | Respiratory difficulties at acute polio | | | | | | | 0 | 71 | 62.5 | .26 | .58 | | | 1 | 14.5 | 9.4 | | | | | 2 | 14.5 | 28.1 | | | | | Bulbar involvement at evaluation | 11.3 | 19.3 | .34 | .61 | | | Alcohol use | | | | | | | None | 38.1 | 52.09 | .19 | .56 | | | Occasionally | 57.1 | 38.2 | | | | | Daily | 4.8 | 8.8 | | | | | Sedative drug use | 45.3 | 47.1 | .87 | 1.00 | | | Smoking history | 27.0 | 14.7 | .17 | .56 | | | Fibromyalgia | 25.0 | 47.1 | .03 | .28 | | | Kyphoscoliosis | 32.8 | 44.1 | .27 | .58 | | | Scoliosis surgery | 14.1 | 17.6 | .64 | .85 | | | Ear-nose-throat surgery | 20.3 | 5.9 | .06 | .43 | | | | |
A comparison of potential predictive symptoms in patients with and without SDB (AHI ≥5) is presented in table 4. There was a tendency for patients with SDB to snore more frequently than those without SDB. Similar results were obtained for patients with and without SDB by using the threshold of AHI score of 10 or more. Snoring was the only predictive symptom (65.3% vs 34.7%; 95% CI of difference, 11.8–49.5; adjusted P=.08). | | | | Symptom | SDB (%) (n=64) | No SDB (%) (n=34) | P | Adjusted P | |
|---|
| Snoring | 60.9 | 29.4 | 0.003 | .08 | | | Daytime sleepiness | 21.9 | 20.6 | 0.88 | 1.00 | | | Fatigue | 84.4 | 79.4 | 0.54 | .80 | | | Witnessed apneas | 10.9 | 2.9 | 0.25 | .58 | | | Nocturnal awakening | 28.1 | 14.7 | 0.13 | .49 | | | Morning headaches | 28.1 | 44.1 | 0.11 | .44 | | | Nightmares | 10.9 | 23.5 | 0.09 | .43 | | | Nocturnal choking | 7.8 | 5.8 | 1.00 | 1.00 | | | Dyspnea | 34.4 | 32.3 | 0.84 | 1.00 | | | | |
The association of pulmonary function test parameters and oxygen saturation during sleep was evaluated in patients with SDB (AHI score ≥5). The results are presented in table 5. A correlation (r≥0.4) was observed between several pulmonary function parameters (FVC, FEV1, TLC, diffusion capacity) and oxygen saturation parameters during sleep (nadir saturation, mean oxygen saturation during non-REM sleep, mean oxygen saturation during REM sleep). | | | | Pulmonary Function Measures (% predicted) | Nadir Oxygen Saturation | Mean Oxygen Saturation (non-REM Sleep) | Mean Oxygen Saturation (REM Sleep) | |
|---|
| FVC | .54(.30to.72)n=46 | .39(.11to.61)n=46 | .53(.28to.71)n=45 | | | FEV1 | .55(.31to.72)n=46 | .41(.14to.63)n=46 | .55(.31to.73)n=45 | | | TLC | .50(.24to.69)n=44 | .38(.09to.61)n=44 | .52(.26to.71)n=43 | | | MIP | .21(−.09to.48)n=44 | .21(−.09to.48)n=44 | .31(.01to.56)n=43 | | | MEP | .05(−.25to.34)n=44 | .22(−.08to.49)n=44 | .17(−.14to.45)n=43 | | | Diffusioncapacity | .43(.16to.64)n=45 | .38(.10to.61)n=45 | .43(.15to.64)n=44 | | | | |
Discussion We found that SDB (AHI score ≥5) was common, being present in 65% of 98 postpolio clinic patients with generalized fatigue atypical for PPS who were referred for sleep evaluation. Most patients (86%) had obstructive hypopnea; a few had obstructive apnea, central apnea, and mixed apnea. A majority of patients with SDB (84%) had mild or moderate SDB. In our exploratory study, none of the potential predictive factors evaluated were associated with SDB. The only symptom that tended to predict SDB was snoring. Reductions in FVC, FEV1, TLC, and diffusion capacity were associated with the severity of oxygen desaturation during sleep. Our study, performed by using complete overnight polysomnography, demonstrated that obstructive SDB is prevalent in a large group of fatigued postpolio patients and provides important new data. These results support observations made in previous smaller studies, some of which used more limited recording techniques.10, 11, 12, 13 OSA and obstructive-hypopnea was reported to be predominant in most previous work.10, 11, 13 Other factors in addition to SDB may contribute to poor sleep quality and daytime somnolence or fatigue in patients with previous polio. In our experience, these may include sleep disruption related to pain, anxiety, depression, limited physical activity or medications, poor sleep hygiene or sleep-phase delay, and restless legs syndrome-periodic limb movement disorder.21, 22, 23, 24 Clinical evaluation and polysomnographic recording are required to assess the contribution of such factors, some of which are amenable to behavioral and/or pharmacologic intervention. However, the findings of the present study strongly suggest that SDB is a prominent contributing factor to the complaint of fatigue in this population. In this exploratory study, in unadjusted analyses, there was a suggestion that male sex and increased BMI predicted SDB in a fatigued postpolio clinic population. Because our patients had primarily obstructive hypopnea, these findings are consistent with previous reports of risk factors for obstructive apnea and hypopnea in the general population7, 17 and 1 report in a PPS patient population.13 We found that snoring was the only presenting symptom that tended to predict SDB. This finding is consistent with that found in a previous report in a population of PPS patients.13 Snoring is very common in OSA patients in the general population and is one of the main presenting symptoms.7 An unexpected finding in our study was that many polio-related clinical parameters studied were not predictive of SDB. Previous investigators have suggested that parameters such as respiratory and bulbar involvement at acute polio and at the time of evaluation, as well as scoliosis and kyphosis, would be important for the development of SDB in this population12, 25 and in other neuromuscular disorders.21 However, we did observe that pulmonary function abnormalities were related to the severity of nocturnal oxygen desaturation associated with SDB. Our study had several potential limitations. Patients included in the study came from a university-affiliated postpolio clinic and were probably more likely to be symptomatic than the general postpolio population. Therefore, our estimates on the frequency of SDB may be overestimations. In addition, there were several differences between patients included and not included in our study that could have affected our results. For example, patients referred for sleep evaluation and therefore included in the study were those thought to have symptoms consistent with SDB. Therefore, the control population (patients who underwent polysomnography but did not have SDB) was likely more symptomatic than the general postpolio population. This could have produced an underestimation of some of the differences between patients with and without SDB and thus made it more difficult to establish the presence of significant differences. In addition, because of the large number of statistical tests conducted, we have presented P values that are adjusted for multiple testing. However, this may have resulted in a decreased power to detect any associations.20 This study focused on postpolio patients with moderate to severe fatigue that was believed to be atypical for PPS. It is possible that other postpolio patients such as those with fatigue typical for PPS or those with “nonparalytic polio”26 may also have SDB. Although it is theoretically possible that this study may also have underestimated the frequency of SDB in the general postpolio population, it is unlikely because patients were selected by the presence of symptoms suggestive of SDB. Our study had potential for bias because some potential predictors were ascertained by self-report and retrospectively. However, there was consistency in data acquisition and ascertainment of SDB because all data were gathered by 1 physician by using a standardized form, and essentially all patients were evaluated at the same sleep clinic with complete polysomnography. Conclusions In our retrospective, cross-sectional study, we found that SDB, especially obstructive hypopnea, was very prevalent among postpolio clinic patients referred for sleep evaluation. Many postpolio patients had SDB even though they did not have many of the factors previously identified or proposed to be predictive for SDB in this population (eg, history of bulbar or respiratory involvement at acute polio). However, alterations in some measures of pulmonary function were related to oxygen desaturation during sleep. Based on these results, we recommend that all postpolio patients with daytime fatigue or somnolence atypical for PPS undergo evaluation for SDB. Our anecdotal clinical experience suggests that treatment of SDB in this population with nasal CPAP can lead to a substantial improvement of the symptom of fatigue. Because of the exploratory nature of this study, we recommend further prospective studies of SDB in a more general population of postpolio patients as well as randomized controlled trials to evaluate the effects of treatment of SDB. Supplier References 1. 1Trojan DA, Cashman NR. Post-poliomyelitis syndrome. Muscle Nerve. 2005;31:6–19.
CrossRef
2. 2Jubelt B, Cashman NR. Neurological manifestations of the post-polio syndrome. Crit Rev Neurobiol. 1987;3:199–220. MEDLINE 3. 3Codd MB, Mulder DW, Kurland LT, Beard CM, O’Fallon WM. Poliomyelitis in Rochester, Minnesota, 1935–1955: epidemiology and long-term sequelae (A preliminary report). In: Halstead LS, Wiechers DO editor. Late effects of poliomyelitis. Miami: Symposia Foundation; 1985;p. 121–134. 4. 4Halstead LS, Rossi CD. Post-polio syndrome: clinical experience with 132 consecutive outpatients. In: Halstead LS, Wiechers DO editor. Research and clinical aspects of the late effects of poliomyelitis. White Plains: March of Dimes Birth Defects Foundation; 1987;p. 13–26. 5. 5Schanke AK, Stanghelle JK. Fatigue in polio survivors. Spinal Cord. 2001;39:243–251. MEDLINE |
CrossRef
6. 6Sleep-related breathing disorders in adults: recommendations for syndrome definition and measurement techniques in clinical research (The report of an American Academy of Sleep Medicine Task Force). Sleep. 1999;22:667–689. MEDLINE 7. 7Collop NA. Obstructive sleep apnea syndromes. Semin Respir Crit Care Med. 2005;26:13–24. MEDLINE |
CrossRef
8. 8Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230–1235. MEDLINE |
CrossRef
9. 9Bruno RL, Sapolsky R, Zimmerman JR, Frick NM. Pathophysiology of a central cause of post-polio fatigue. Ann N Y Acad Sci. 1995;753:257–275. MEDLINE |
CrossRef
10. 10Ulfberg J, Jonsson R, Ekeroth G. Sleep apnea syndrome among poliomyelitis survivors [letter]. Neurology. 1997;49:1189–1190. MEDLINE 11. 11Steljes DG, Kryger MH, Kirk BW, Millar TW. Sleep in postpolio syndrome. Chest. 1990;98:133–140. MEDLINE |
CrossRef
12. 12Dean A, Graham BA, Dalakas M, Sato S. Sleep apnea in patients with postpolio syndrome. Ann Neurol. 1998;43:661–664. MEDLINE |
CrossRef
13. 13Hsu AA, Staats BA. “Postpolio” sequelae and sleep-related disordered breathing. Mayo Clin Proc. 1998;73:216–224. MEDLINE 14. 14Chesson AL, Berry RB, Pack A. Practice parameters for the use of portable monitoring devices in the investigation of suspected obstructive sleep apnea in adults. Sleep. 2003;26:907–913. MEDLINE 15. 15Wolfe F, Smythe HA, Yunus MB, et al. The American College of Rheumatology 1990 criteria for the classification of fibromyalgia (Report of the Multicenter Criteria Committee). Arthritis Rheum. 1990;33:160–172. MEDLINE |
CrossRef
16. 16Berlly MH, Strauser WW, Hall KM. Fatigue in postpolio syndrome. Arch Phys Med Rehabil. 1991;72:115–118. MEDLINE 17. 17Flemons WW. Obstructive sleep apnea. N Engl J Med. 2002;347:498–504.
CrossRef
18. 18Trojan DA, Cashman NR, Shapiro S, Tansey CM, Esdaile JM. Predictive factors for post-poliomyelitis syndrome. Arch Phys Med Rehabil. 1994;75:770–777. MEDLINE 19. 19Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289–300. 20. 20Bender R, Lange S. Adjusting for multiple testing—when and how? (J Clin Epidemiol). 2001;54:343–349. 21. 21Perrin C, D’Ambrosio C, White A, Hill NS. Sleep in restrictive and neuromuscular respiratory disorders. Semin Resp Crit Care Med. 2005;26:117–130. 22. 22Ting L, Malhotra A. Disorders of sleep: an overview. Prim Care. 2005;32:305–318. Full Text |
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|
CrossRef
23. 23Bruno RL, Frick NM, Creange S. Nocturnal generalized random myoclonus as a postpolio sequelae. Arch Phys Med Rehabil. 1995;76:594;. 24. 24Mahowald MW, Schenck CH. Insights from studying human sleep disorders. Nature. 2005;437:1279–1285.
CrossRef
25. 25Bach JR, Tilton M. Pulmonary dysfunction and its management in post-polio patients. NeuroRehabilitation. 1997;8:139–153.
CrossRef
26. 26Halstead LS, Silver JK. Nonparalytic polio and postpolio syndrome. Am J Phys Med Rehabil. 2000;79:13–18. MEDLINE |
CrossRef
a Department of Neurology and Neurosurgery, Montreal Neurological Institute and Hospital, McGill, University Health Centre, McGill University, Montreal, QC, Canada b Respiratory Division and Sleep Laboratory, McGill University Health Centre, McGill University, Montreal, Canada c Departments of Medicine and Epidemiology, Biostatistics, and Occupational Health, McGill University, Montreal, QC, Canada d Department of Medicine, University of Montreal, Montreal, QC, Canada.  Correspondence to Daria A. Trojan, MD, Montreal Neurological Hospital, McGill University Health Centre, 3801 University St, Montreal, QC H3A 2B4, Canada
Supported by the Polio Quebec Association and the Montreal Neurological Institute (salary support). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(06)00842-2 doi:10.1016/j.apmr.2006.07.256 © 2006 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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