Sleep Medicine 15 (2014) 1283–1284
Contents lists available at ScienceDirect
Sleep Medicine j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / s l e e p
Editorial
Sleeping with spinal cord injury
In the manuscript entitled “Sleep Apnea and Periodic Leg Movements in the First Year after Spinal Cord Injury,” Proserpio and coworkers evaluated a consecutive series of 35 patients with different kinds of spinal cord damage (paraplegic and tetraplegic with complete or incomplete lesions) by means of questionnaires and nocturnal polysomnography performed during the first year after injury (75% within the first 2 months) [1]. The topic is of high clinical interest because sleep complaints are common among patients with spinal cord injury (SCI) and encompass not only nocturnal symptoms such as difficulties in falling asleep, awakenings, poor sleep quality, use of sleeping medications, and snoring, but also increased frequency and duration of daytime napping [2]. However, only few studies have addressed sleep disorders in these patient populations and data on tailored therapeutic approaches are lacking [3]. Despite the negative results of the Berlin questionnaire (focused here on symptoms before SCI occurrence) and of subjective sleepiness in visual analog scale, Proserpio et al. [1] found that 9 (25.7%) patients had obstructive sleep disordered breathing (SDB) of different severities (two with an AHI > 30/h) and that 11 patients had respiratory events (AHI > 5/h) exclusively during rapid eye movement (REM) sleep. SDB had a negative impact on sleep (less slow wave sleep and more non-REM sleep stage 1) and was more common in tetraplegic versus paraplegic patients, while REM-related SDB was more common in older patients with complete spinal lesion. Conversely, drug treatment, body mass index (BMI), time from injury, and age did not show significant associations with SDB [1]. Considering the young age of SCI patients (mean of 38 years old), SDB seems more prevalent in these patients than in the general population and most probably is a consequence of SCI itself. In line with these findings, a previous longitudinal study on tetraplegic patients showed increasing SDB (i.e., AHI > 10/h) occurrence after SCI from 0% at 48 h, to 83% at 2 months, and 60% at 52 weeks [4]. While Berlowitz and coworkers [4] studied exclusively tetraplegic patients, the current study was able to document a strong impact of lesion site (i.e., cervical lesion causing tetraplegia) and is in line with previous observations [5,6] supporting the pathophysiological relevance of intercostal/abdominal muscles and diaphragm motility together with upper airway resistance and disrupted feedbacks from rib cage receptors in determining obstructive SDB in SCI. Intriguingly, SDB was not associated with subjective daytime sleepiness in SCI, thus differing from the classical picture in the general population. Absence of sleepiness in SDB patients after SCI was previously noted by Tran et al. [7]. This finding is reminiscent of that observed in heart failure patients with SDB. SDB in SCI may thus have peculiar clinical features that warrant further longitudinal studies aimed at establishing which symptoms and anthropomethttp://dx.doi.org/10.1016/j.sleep.2014.08.003 1389-9457/© 2014 Elsevier B.V. All rights reserved.
ric characteristics should guide the clinician to search for nocturnal breathing abnormalities. Alternatively, SDB may also evolve along with the SCI course and become symptomatic with sleepiness and fatigue during the chronic phase [8]. Also the compliance to CPAP treatment seems poor in SCI patients, especially in those with tetraplegia, possibly due to mask intolerance [6,9], or inability to reposition the mask [9]. Further research is thus needed to tailor adequate therapeutic strategies toward positively influencing the overall cardiovascular outcome [10]. Proserpio and coworkers [1] also found that 10 patients (28.6%) showed a PLMI > 15/h. Among patients with PLMs, five had a PLMI > 50/h, eight disclosed persistence of PLMs during REM sleep and some presented PLMs lasting minutes with unilateral movements. However, PLMs did not influence significantly nocturnal sleep and were prominent in patients with incomplete lesions, without differing in patients with different lesion sites, times from injury or age [1]. Even in the absence of a control group, the reported prevalence of 28.6% is higher than what is expected in the general population, considering the young age of SCI patients. While the studies on SDB in SCI suffer from methodological limitations (e.g., polysomnographic criteria applied, inclusion exclusively of tetraplegic or paraplegic patients), reports on motor disturbances during sleep are scarce and mainly based on little case series [3]. SCI indeed provides an unprecedented opportunity to mechanistically unravel the pathophysiological features of both PLMs and of restless legs syndrome (RLS) (not assessed in this study) [1] keeping in mind that among the hypotheses underlying PLMs is the activation during sleep of a spinal cord generator [11] interplaying with autonomic and cerebral arousal [12]. Further research is warranted to evaluate the intrinsic characteristics of PLMs, most notably their periodicity by means of the periodicity index, comparing SCI patients with and without RLS versus patients with idiopathic RLS and other sleep disorders with frequent PLMs such as narcolepsy type 1 [13,14], and taking into account the genetic background [15]. Ferri et al. [16] already performed a preliminary neurophysiological study in a subgroup of SCI patients with complete motor lesion (i.e., the subgroup with less frequent PLMs), and disclosed different heart rates and spectral EEG changes accompanying arousal and leg movements. Therefore, despite comparable complete spinal cord lesions, only 45% of patients showed a cerebral and autonomic response to leg movements [16], supporting the potential presence of surviving spinal or extra-spinal connections [17], or that the observed PLMs were part of a more complex motor pattern [18]. And as previously reported [19], PLMs and SDB also seemed associated in SCI patients, as well as in narcolepsy type 1, though not significantly.
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Editorial/Sleep Medicine 15 (2014) 1283–1284
To conclude, SCI patients suffer from a significant sleep comorbidity and the study of sleep abnormalities in these patients is clearly indicated not only to better manage SCI over time treating specific disorders with potential negative impact on longterm outcome but also to increase our knowledge of sleep disorders. Sleep disorders in SCI may present with distinct clinical challenges and could require tailored therapeutic approaches to improve quality of life of these young SCI patients who are expected to enjoy long life. Conflict of interest The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: http://dx.doi.org/10.1016/j.sleep.2014.08.003. References [1] Proserpio P, Lanza A, Sambusida K, Fraticci L, Frigerio P, Sommariva M, et al. Sleep apnea and periodic leg movements in the first year after spinal cord injury. Sleep Med 2014. [2] Biering-Sørensen F, Biering-Sørensen M. Sleep disturbances in the spinal cord injured: an epidemiological questionnaire investigation, including a normal population. Spinal Cord 2001;39:505–13. [3] Giannoccaro MP, Moghadam KK, Pizza F, Boriani S, Maraldi NM, Avoni P, et al. Sleep disorders in patients with spinal cord injury. Sleep Med Rev 2013;17:399– 409. [4] Berlowitz DJ, Brown DJ, Campbell DA, Pierce RJ. A longitudinal evaluation of sleep and breathing in the first year after cervical spinal cord injury. Arch Phys Med Rehabil 2005;86:1193–9. [5] Klefbeck B, Sternhag M, Weinberg J, Levi R, Hultling C, Borg J. Obstructive sleep apneas in relation to severity of cervical spinal cord injury. Spinal Cord 1998;36:621–8. [6] Burns SP, Kapur V, Yin KS, Buhrer R. Factors associated with sleep apnea in men with spinal cord injury: a population-based case-control study. Spinal Cord 2001;39:15–22. [7] Tran K, Hukins C, Geraghty T, Eckert B, Fraser L. Sleep-disordered breathing in spinal cord-injured patients: a short-term longitudinal study. Respirology 2010;15:272–6. [8] Sankari A, Bascom A, Oomman S, Badr MS. Sleep disordered breathing in chronic spinal cord injury. J Clin Sleep Med 2014;10:65–72. [9] Stockhammer E, Tobon A, Michel F, Eser P, Scheuler W, Bauer W, et al. Characteristics of sleep apnea syndrome in tetraplegic patients. Spinal Cord 2002;40:286–94.
[10] DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil 1993;74:248–54. [11] Yokota T, Hirose K, Tanabe H, Tsukagoshi H. Sleep-related periodic leg movements (nocturnal myoclonus) due to spinal cord lesion. J Neurol Sci 1991;104:13–18. [12] Ferri R, Zucconi M, Rundo F, Spruyt K, Manconi M, Ferini-Strambi L. Heart rate and spectral EEG changes accompanying periodic and non-periodic leg movements during sleep. Clin Neurophysiol 2007;118:438–48. [13] Ferri R, Zucconi M, Manconi M, Bruni O, Ferini-Strambi L, Vandi S, et al. Different periodicity and time structure of leg movements during sleep in narcolepsy/ cataplexy and restless legs syndrome. Sleep 2006;29:1587–94. [14] Plazzi G, Ferri R, Franceschini C, Vandi S, Detto S, Pizza F, et al. Periodic leg movements during sleep in narcoleptic patients with or without restless legs syndrome. J Sleep Res 2012;21:155–62. [15] Stefansson H, Rye DB, Hicks A, Petursson H, Ingason A, Thorgeirsson TE, et al. A genetic risk factor for periodic limb movements in sleep. N Engl J Med 2007;357:639–47. [16] Ferri R, Proserpio P, Rundo F, Lanza A, Sambusida K, Redaelli T, et al. Neurophysiological correlates of sleep leg movements in acute spinal cord injury. Clin Neurophysiol 2014;doi:10.1016/j.clinph.2014.05.016, S13882457(14)00291-0 [pii]. [17] Telles SC, Alves RC, Chadi G. Periodic limb movements during sleep and restless legs syndrome in patients with ASIA A spinal cord injury. J Neurol Sci 2011;303:119–23. [18] Provini F, Vetrugno R, Meletti S, Plazzi G, Solieri L, Lugaresi E, et al. Motor pattern of periodic limb movements during sleep. Neurology 2001;57:300–4. [19] Pizza F, Tartarotti S, Poryazova R, Baumann CR, Bassetti CL. Sleep-disordered breathing and periodic limb movements in narcolepsy with cataplexy: a systematic analysis of 35 consecutive patients. Eur Neurol 2013;70:22–6.
Fabio Pizza Department of Biomedical and Neuromotor Sciences (DIBINEM), University of Bologna, Via Ugo Foscolo 7, 40123, Bologna, Italy IRCCS Istituto delle Scienze Neurologiche, ASL di Bologna, Bologna, Italy Tel.: +39 051 4966924; fax: +39 051 4966098. E-mail address: [email protected]; [email protected] Giuseppe Plazzi Department of Biomedical and Neuromotor Sciences (DIBINEM), University of Bologna, Via Ugo Foscolo 7, 40123, Bologna, Italy IRCCS Istituto delle Scienze Neurologiche, ASL di Bologna, Bologna, Italy Available online 12 August 2014
Contents lists available at ScienceDirect
Sleep Medicine j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / s l e e p
Editorial
Sleeping with spinal cord injury
In the manuscript entitled “Sleep Apnea and Periodic Leg Movements in the First Year after Spinal Cord Injury,” Proserpio and coworkers evaluated a consecutive series of 35 patients with different kinds of spinal cord damage (paraplegic and tetraplegic with complete or incomplete lesions) by means of questionnaires and nocturnal polysomnography performed during the first year after injury (75% within the first 2 months) [1]. The topic is of high clinical interest because sleep complaints are common among patients with spinal cord injury (SCI) and encompass not only nocturnal symptoms such as difficulties in falling asleep, awakenings, poor sleep quality, use of sleeping medications, and snoring, but also increased frequency and duration of daytime napping [2]. However, only few studies have addressed sleep disorders in these patient populations and data on tailored therapeutic approaches are lacking [3]. Despite the negative results of the Berlin questionnaire (focused here on symptoms before SCI occurrence) and of subjective sleepiness in visual analog scale, Proserpio et al. [1] found that 9 (25.7%) patients had obstructive sleep disordered breathing (SDB) of different severities (two with an AHI > 30/h) and that 11 patients had respiratory events (AHI > 5/h) exclusively during rapid eye movement (REM) sleep. SDB had a negative impact on sleep (less slow wave sleep and more non-REM sleep stage 1) and was more common in tetraplegic versus paraplegic patients, while REM-related SDB was more common in older patients with complete spinal lesion. Conversely, drug treatment, body mass index (BMI), time from injury, and age did not show significant associations with SDB [1]. Considering the young age of SCI patients (mean of 38 years old), SDB seems more prevalent in these patients than in the general population and most probably is a consequence of SCI itself. In line with these findings, a previous longitudinal study on tetraplegic patients showed increasing SDB (i.e., AHI > 10/h) occurrence after SCI from 0% at 48 h, to 83% at 2 months, and 60% at 52 weeks [4]. While Berlowitz and coworkers [4] studied exclusively tetraplegic patients, the current study was able to document a strong impact of lesion site (i.e., cervical lesion causing tetraplegia) and is in line with previous observations [5,6] supporting the pathophysiological relevance of intercostal/abdominal muscles and diaphragm motility together with upper airway resistance and disrupted feedbacks from rib cage receptors in determining obstructive SDB in SCI. Intriguingly, SDB was not associated with subjective daytime sleepiness in SCI, thus differing from the classical picture in the general population. Absence of sleepiness in SDB patients after SCI was previously noted by Tran et al. [7]. This finding is reminiscent of that observed in heart failure patients with SDB. SDB in SCI may thus have peculiar clinical features that warrant further longitudinal studies aimed at establishing which symptoms and anthropomethttp://dx.doi.org/10.1016/j.sleep.2014.08.003 1389-9457/© 2014 Elsevier B.V. All rights reserved.
ric characteristics should guide the clinician to search for nocturnal breathing abnormalities. Alternatively, SDB may also evolve along with the SCI course and become symptomatic with sleepiness and fatigue during the chronic phase [8]. Also the compliance to CPAP treatment seems poor in SCI patients, especially in those with tetraplegia, possibly due to mask intolerance [6,9], or inability to reposition the mask [9]. Further research is thus needed to tailor adequate therapeutic strategies toward positively influencing the overall cardiovascular outcome [10]. Proserpio and coworkers [1] also found that 10 patients (28.6%) showed a PLMI > 15/h. Among patients with PLMs, five had a PLMI > 50/h, eight disclosed persistence of PLMs during REM sleep and some presented PLMs lasting minutes with unilateral movements. However, PLMs did not influence significantly nocturnal sleep and were prominent in patients with incomplete lesions, without differing in patients with different lesion sites, times from injury or age [1]. Even in the absence of a control group, the reported prevalence of 28.6% is higher than what is expected in the general population, considering the young age of SCI patients. While the studies on SDB in SCI suffer from methodological limitations (e.g., polysomnographic criteria applied, inclusion exclusively of tetraplegic or paraplegic patients), reports on motor disturbances during sleep are scarce and mainly based on little case series [3]. SCI indeed provides an unprecedented opportunity to mechanistically unravel the pathophysiological features of both PLMs and of restless legs syndrome (RLS) (not assessed in this study) [1] keeping in mind that among the hypotheses underlying PLMs is the activation during sleep of a spinal cord generator [11] interplaying with autonomic and cerebral arousal [12]. Further research is warranted to evaluate the intrinsic characteristics of PLMs, most notably their periodicity by means of the periodicity index, comparing SCI patients with and without RLS versus patients with idiopathic RLS and other sleep disorders with frequent PLMs such as narcolepsy type 1 [13,14], and taking into account the genetic background [15]. Ferri et al. [16] already performed a preliminary neurophysiological study in a subgroup of SCI patients with complete motor lesion (i.e., the subgroup with less frequent PLMs), and disclosed different heart rates and spectral EEG changes accompanying arousal and leg movements. Therefore, despite comparable complete spinal cord lesions, only 45% of patients showed a cerebral and autonomic response to leg movements [16], supporting the potential presence of surviving spinal or extra-spinal connections [17], or that the observed PLMs were part of a more complex motor pattern [18]. And as previously reported [19], PLMs and SDB also seemed associated in SCI patients, as well as in narcolepsy type 1, though not significantly.
1284
Editorial/Sleep Medicine 15 (2014) 1283–1284
To conclude, SCI patients suffer from a significant sleep comorbidity and the study of sleep abnormalities in these patients is clearly indicated not only to better manage SCI over time treating specific disorders with potential negative impact on longterm outcome but also to increase our knowledge of sleep disorders. Sleep disorders in SCI may present with distinct clinical challenges and could require tailored therapeutic approaches to improve quality of life of these young SCI patients who are expected to enjoy long life. Conflict of interest The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: http://dx.doi.org/10.1016/j.sleep.2014.08.003. References [1] Proserpio P, Lanza A, Sambusida K, Fraticci L, Frigerio P, Sommariva M, et al. Sleep apnea and periodic leg movements in the first year after spinal cord injury. Sleep Med 2014. [2] Biering-Sørensen F, Biering-Sørensen M. Sleep disturbances in the spinal cord injured: an epidemiological questionnaire investigation, including a normal population. Spinal Cord 2001;39:505–13. [3] Giannoccaro MP, Moghadam KK, Pizza F, Boriani S, Maraldi NM, Avoni P, et al. Sleep disorders in patients with spinal cord injury. Sleep Med Rev 2013;17:399– 409. [4] Berlowitz DJ, Brown DJ, Campbell DA, Pierce RJ. A longitudinal evaluation of sleep and breathing in the first year after cervical spinal cord injury. Arch Phys Med Rehabil 2005;86:1193–9. [5] Klefbeck B, Sternhag M, Weinberg J, Levi R, Hultling C, Borg J. Obstructive sleep apneas in relation to severity of cervical spinal cord injury. Spinal Cord 1998;36:621–8. [6] Burns SP, Kapur V, Yin KS, Buhrer R. Factors associated with sleep apnea in men with spinal cord injury: a population-based case-control study. Spinal Cord 2001;39:15–22. [7] Tran K, Hukins C, Geraghty T, Eckert B, Fraser L. Sleep-disordered breathing in spinal cord-injured patients: a short-term longitudinal study. Respirology 2010;15:272–6. [8] Sankari A, Bascom A, Oomman S, Badr MS. Sleep disordered breathing in chronic spinal cord injury. J Clin Sleep Med 2014;10:65–72. [9] Stockhammer E, Tobon A, Michel F, Eser P, Scheuler W, Bauer W, et al. Characteristics of sleep apnea syndrome in tetraplegic patients. Spinal Cord 2002;40:286–94.
[10] DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil 1993;74:248–54. [11] Yokota T, Hirose K, Tanabe H, Tsukagoshi H. Sleep-related periodic leg movements (nocturnal myoclonus) due to spinal cord lesion. J Neurol Sci 1991;104:13–18. [12] Ferri R, Zucconi M, Rundo F, Spruyt K, Manconi M, Ferini-Strambi L. Heart rate and spectral EEG changes accompanying periodic and non-periodic leg movements during sleep. Clin Neurophysiol 2007;118:438–48. [13] Ferri R, Zucconi M, Manconi M, Bruni O, Ferini-Strambi L, Vandi S, et al. Different periodicity and time structure of leg movements during sleep in narcolepsy/ cataplexy and restless legs syndrome. Sleep 2006;29:1587–94. [14] Plazzi G, Ferri R, Franceschini C, Vandi S, Detto S, Pizza F, et al. Periodic leg movements during sleep in narcoleptic patients with or without restless legs syndrome. J Sleep Res 2012;21:155–62. [15] Stefansson H, Rye DB, Hicks A, Petursson H, Ingason A, Thorgeirsson TE, et al. A genetic risk factor for periodic limb movements in sleep. N Engl J Med 2007;357:639–47. [16] Ferri R, Proserpio P, Rundo F, Lanza A, Sambusida K, Redaelli T, et al. Neurophysiological correlates of sleep leg movements in acute spinal cord injury. Clin Neurophysiol 2014;doi:10.1016/j.clinph.2014.05.016, S13882457(14)00291-0 [pii]. [17] Telles SC, Alves RC, Chadi G. Periodic limb movements during sleep and restless legs syndrome in patients with ASIA A spinal cord injury. J Neurol Sci 2011;303:119–23. [18] Provini F, Vetrugno R, Meletti S, Plazzi G, Solieri L, Lugaresi E, et al. Motor pattern of periodic limb movements during sleep. Neurology 2001;57:300–4. [19] Pizza F, Tartarotti S, Poryazova R, Baumann CR, Bassetti CL. Sleep-disordered breathing and periodic limb movements in narcolepsy with cataplexy: a systematic analysis of 35 consecutive patients. Eur Neurol 2013;70:22–6.
Fabio Pizza Department of Biomedical and Neuromotor Sciences (DIBINEM), University of Bologna, Via Ugo Foscolo 7, 40123, Bologna, Italy IRCCS Istituto delle Scienze Neurologiche, ASL di Bologna, Bologna, Italy Tel.: +39 051 4966924; fax: +39 051 4966098. E-mail address: [email protected]; [email protected] Giuseppe Plazzi Department of Biomedical and Neuromotor Sciences (DIBINEM), University of Bologna, Via Ugo Foscolo 7, 40123, Bologna, Italy IRCCS Istituto delle Scienze Neurologiche, ASL di Bologna, Bologna, Italy Available online 12 August 2014
