http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2015; 29(2): 221–227 ! 2015 Informa UK Ltd. DOI: 10.3109/02699052.2014.983978
REVIEW
Sleep disturbances in athletic concussion Michael S. Jaffee1, W. Christopher Winter2, Christine C. Jones2, & Geoffrey Ling3 Department of Neurology, University of Virginia, Charlottesville, VA, USA, 2Charlottesville Neurology and Sleep Medicine, Charlottesville, VA, USA, and 3Defense Advanced Research Projects Agency (DARPA), Washington, DC, USA
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
1
Abstract
Keywords
Background: Sleep disturbances are a common symptom following concussions to include athletic concussion. Review: This review applies literature on sleep following traumatic brain injury and concussion to sport concussions and places these considerations in the context of sleep and athletic performance. It also includes a description of sleep abnormalities in sleep duration, quality and timing as well as recommended treatment approaches. Finally, it includes a brief discussion of emerging paradigms of sleep and concussion recovery.
Concussion, sleep disturbance, sport
Introduction Research demonstrates the importance of sleep as a contributing factor to optimal athletic performance and sleep disturbances are common following concussion [1, 2]. Understanding and addressing sleep complaints following concussion may help not only with recovery from concussion, but may also have the potential to support a more rapid return to athletic activities. Despite the frequency of post-concussive symptoms, the literature on sleep following concussion is limited. Within this literature, there is very little research evaluating sleep disturbances specifically in the context of sports concussion. The purpose of this paper is to review the literature on sleep disturbances in athletic performance and sleep disturbances following concussion extrapolating data from literature on mild TBI (mTBI). PubMed is the primary source used for information regarding sleep disturbances in concussion, particularly for clinical human/adult studies published in English from 2000–2011. Brain injury, concussion, head injury, head trauma, TBI and traumatic brain injury together with secondary terms to include circadian, sleep hypersomnia, insomnia, narcolepsy, nightmare, parasomnia and sleep apnea are the search terms and combinations included in the search.
Limitations of medical literature evaluating concussion and sleep disturbances There are a number of limitations in current research on sleep and TBI. Most studies have relatively small sample sizes,
Correspondence: Michael S. Jaffee, Department of Neurology, University of Virginia, PO Box 800394, Charlottesville, VA 22908, USA. E-mail: [email protected]
History Received 21 April 2014 Revised 20 October 2014 Accepted 31 October 2014 Published online 13 January 2015
variability in age ranges, differing severities of injury and do not clearly stratify by time following injury (acute effects vs. chronic effects). The biological aspects of co-morbid psychiatric syndromes are not yet fully explored and research designs do not always control for factors such as pain and medications. Studies do not consistently clarify the relationship between impaired sleep and other co-morbid symptoms following TBI and data is often lacking to understand the contribution of pre-morbid issues. Finally, the majority of studies do not correlate findings with neuroimaging or EEG evaluations. Furthermore, some inconsistencies remain within the literature of the definition and use of the term concussion. Current understanding reflects the consensus definitions of the International Conference on Concussion and Sport that defines concussion as a complex pathophysiological process affecting the brain, induced by biomechanical forces. It typically results in the rapid onset of transient impairment of neurological function. There is an association with a graded set of clinical responses that may or may not involve loss of consciousness. Many professionals often refer to concussions as mild traumatic brain injury (TBI) [3].
Importance of sleep and athletic performance The role of sleep in athletic performance is relatively new in comparison to the role of strength and conditioning, proper nutrition and hydration therapy. Until recently, the primary focus for preparing the elite athlete centred on his or her waking hours, with the period of sleep largely ignored. As the attention on performance enhancement and competitive advantage increases, more interest and effort is being generated toward the manipulation of sleep and sleep-related variables for athletic gain. These variables can be separated into categories not unlike the categories used to classify sleep
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
222
M. S. Jaffee et al.
disorders: sleep quantity, sleep quality and sleep timing (commonly referred to circadian factors). Perhaps the most obvious sleep-related variable is the amount of sleep an athlete is able to achieve. There is no shortage of research looking at the ill-effects on general performance when paired with varying levels of sleep deprivation [4–6]. For athletic performance to be at its best, all aspects of mental concentration, motor memory, strength and speed must be primed. While research on the negative effects of inadequate sleep provide the foundation for this field of study, a more novel concept has been advanced in recent years examining the benefits of sleeping beyond what is considered adequate sleep for the athlete. Much in the way a free diver might overfill his lungs with air before his descent; can an athlete ‘oversleep’ for a period of time and derive benefit from the practice? Several studies support this concept, which conclude that the amount of time spent in bed is tied to improved athletic performance [7–9]. Equally important to the amount of sleep an athlete achieves is the quality of that sleep. There are a host of sleep disorders that can disrupt normal architecture and create issues with sleep and performance. Given the extent to which growth hormone (GH) is secreted during slow wave sleep, one key factor in performance is protecting this sleep stage from disruption [10, 11]. While adequately powered studies looking at disrupted sleep and athletics are few, they do exist. Perhaps the most ambitious study of this kind evaluated the presence of sleep apnea within Canadian professional football players [12]. While there were no direct measures of performance made, the high prevalence within this group of athletes opened the door for future investigations and study. Considerations of sleep quality can be made by analysis of sleep architecture. There are reports of altered sleep architecture following mild TBI (concussion). This includes decreased Rapid Eye Movement (REM) and higher amounts of Non-REM Stage 1 (N1) and Non-REM Stage 2 (N2) sleep [13]. This change in architecture is different than that reported in moderate–severe injuries which have been associated with increased slow wave sleep after controlling for depression and anxiety. One study evaluated the sleep characteristics of teenagers who had complaints about sleep quality 3 years after sustaining a mild TBI. Measurements with polysomnography and actigraphy revealed poorer sleep efficiency than controls in those who had mild TBI [14]. Studies using advanced technologies not routinely employed in diagnostic sleep disorder centres are also being conducted. These studies involve the use of quantitative EEG and spectral EEG. One study evaluating spectral EEG in athletes with concussion identified a pattern of more delta activity and less alpha activity during wakefulness [1]. The authors suggested that spectral EEG may have a potential application for prognosis and ‘return to play’ determinations following athletic concussion. Beyond the quality and quantity of sleep, it is the research into the timing of sleep that has thus far been the area of research yielding the most information about links between sleep and performance [15]. In 1994, Atkinson et al. [16] published evidence that young cyclists performed better in afternoon and evening hours when compared to morning
Brain Inj, 2015; 29(2): 221–227
races. Smith and Dement’s [17] study of elite Olympic athletes yielded a similar tendency for peak performance in later afternoon events. An article in the journal Sleep evaluating the role of travel for Monday Night Football games opened the door for scientific study of athletic performance during travel across time zones [18]. Recht et al. [19] conducted studies looking at the teams’ transcontinental travel’, while Winter et al. [20] examined the more subtle roles of travel and team performance as it pertained to ‘circadian advantage’. Sleep-deprivation as a pre-concussion condition is described as a risk factor for the development of postconcussive symptoms [21]. Adolescents have a high incidence of athletic concussions [22]. The adolescent population at baseline has a high prevalence of disruptions in sleep quantity, quality and circadian factors affecting sleep timing [23]. Disruptions in sleep quality or timing may also be a premorbid contributing factor to post-concussive symptoms. Therefore, sleep disturbances may increase the risk of sustaining an athletic concussion, particularly if performance is compromised in a contact sport. Furthermore, if an athlete is returned to play and athletic performance is not back to baseline due to disturbances in sleep, there may be an increased risk of sustaining a recurrent concussion.
Prevalence of sleep disturbances following concussion The pathophysiology of concussion involves the triggering of diffuse axonal injury, which preferentially affects midline structures to include deep grey matter, the dorsolateral pons and mid-brain. These are all structures that are known to be related to sleep–wake mechanisms. In addition, the secondary effects of concussion lead to a neurometabolic cascade and release of neurotransmitters that are involved in the regulation of sleep–wake circuits as well as being implicated in co-morbidities to include psychiatric symptoms. Of symptoms and complaints that are most evident following concussion of all aetiologies, sleep disturbances are described subjectively as one of the most common factors. A challenge in interpreting prevalence data is that many of the studies included the entire spectrum of traumatic brain injury from mild (concussions) to moderate–severe. Furthermore, studies have evaluated subjective complaints of sleep following TBI, as well as objective tests to include polysomnogram (PSG), multiple sleep latency testing (MSLT), advanced electroencephalogram (EEG) techniques and circadian rhythm markers. Common complaints include excessive daytime somnolence, insomnia and unusual behaviours during sleep or transition stages (parasomnias). Prevalence studies based on subjective report estimate the presence of any sleep disturbance following TBI of any severity as ranging from 42–70% [24, 25]. Several studies also exist which evaluate sleep disturbance following TBI with objective measures through the use of PSG and MSLT. Objective evaluation of sleep complaints following TBI has several limitations and challenges, including the inherent limitations to polysomnographic studies, such as the first night effect observed in sleep laboratories which may not accurately reflect the quality of
DOI: 10.3109/02699052.2014.983978
sleep in a patient’s home environment. Another limitation is the effects of medications that may be used for concurrent conditions such as headaches and depression. An additional limitation is that, if a disorder is seen on a diagnostic test, it is difficult to determine if the disorder is pre-morbid or a result of the traumatic injury. Finally, there is inconsistency in the medical literature in which sleep disorder diagnoses are made solely on the basis of results of diagnostic tests as opposed to those diagnosed with clinical correlation of sleep lab findings. Diagnostic evaluations conducted 3 months after TBI show abnormalities in polysomnography (PSG) in 47% of patients and abnormal multiple sleep latency test (MSLT) in 25% of patients [26].
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
Insomnia Within the TBI population the most common subjective sleep complaints include excessive daytime somnolence (EDS) and insomnia [27]. These symptoms are not always distinguished from one another [27]. Insomnia following traumatic brain injury is self-reported in 33% of patients [27]. Of the patients who reported insomnia, approximately half have sleep onset insomnia associated with increased latency and approximately half report sleep maintenance insomnia associated with increased awakenings during the night. Patients with sleep onset insomnia had higher anxiety scores, while patients with sleep maintenance insomnia had higher depression scores [27]. On subjective reports, mild TBI is more associated with insomnia than more severe forms of TBI. Insomnia can be reported acutely or chronically (greater than 3 months after injury). A higher acute post-concussive symptom load tends to predict a higher risk for persistent insomnia complaints [28]. When post-concussive insomnia is evaluated with objective parameters, the severity of subjectively reported insomnia appears to be over-estimated [29]. Insomnia can be associated with states of increased arousal, which may adversely affect one’s self-perception of insomnia symptoms and severity. There are some theories regarding the pathophysiology and explanation for insomnia being reported more often in mild TBI than with more severe injuries. One theory involves the role of awareness. Patients with more severe injuries may not have as much awareness of their sleep difficulty. Conversely, those with concussions may have hyper-awareness as a function of hyper-arousal or other contributing post-concussive symptoms such as anxiety. Some hypothesize that more diffuse injuries (i.e. diffuse axonal injury) that occur in mild TBI lead to higher impairment in global functioning such as arousal than more severe or focal traumatic injuries [30]. Another theory is that there is dysregulation of shifting between sleep states or sleep state maintenance [31].
Excessive daytime sleepiness and hypersomnia Excessive daytime somnolence is reported in 50% of patients [27]. A clinical challenge is determining whether the excessive daytime sleepiness may have contributions from other sleep disorders such as insomnia or a disturbance in circadian rhythms or whether the excessive daytime sleepiness is due to an underlying hypersomnolence syndrome.
Sleep disturbances in athletic concussion
223
The entity of post-traumatic hypersomnia receives attention and consideration in patients following TBI who report excessive daytime sleepiness. In one study, 25% of chronic TBI patients demonstrated a mean sleep latency of 10 minutes or less via Multiple Sleep Latency Test (MSLT), the standard evaluation for hypersomnolence syndromes [27]. However, this study also illustrates no correlation between subjective sleepiness reporting on the Epworth Sleepiness Scale and objective MSLT results. This implies there may be a lack of awareness of sleepiness. There are some analytical challenges with studies such as these. Analyses of trauma patients 1 month after injury illustrate that problems of hypersomnia are more prominent with injuries involving the head than in injuries not involving the head. Hypersomnolence improves in many trauma patients, but 25% may have persistent symptoms at 1 year post-injury [27]. In patients with TBI, studies demonstrate a correlation between injury severity and both the degree of hypersomnia and its persistence. Following a severe TBI, 98% of patients report excessive daytime somnolence 15 months after TBI [32]. A diagnosis of narcolepsy is made in 6% of patients. The problem of hypersomnolence following severe TBI has been hypothesized to be due to injury to the posterolateral hypothalamus whose cells synthesize hypocretin-1, which is important in maintaining the wakefulness state. Low CSF levels of hypocretin-1 have been reported in 95% of patients following moderate–severe injury [33]. Many patients with TBI are thought to normalize their hypocretin levels within 6 months post-injury. Although mild TBI has higher subjective reports of sleep disturbance, when post-traumatic sleep data is analysed by severity of injury, objective evidence of hypersomnia is equivocal. It is important to not confuse the complaint of excessive daytime sleepiness with a manifestation of a circadian disruption.
TBI and circadian disruption Sleep disturbance following TBI may be associated with alterations in timing and rhythm of sleep. This can result in a mismatch between the biological sleep–wake schedule and the desired 24-hour environmental and social schedule. Such mismatches are associated with altered rhythm and timing of melatonin secretion and body temperature. Studies show a reduction in the evening production of melatonin following traumatic brain injury [34]. The most commonly described circadian rhythm disturbance following traumatic brain injury is delayed sleep phase syndrome. This is a condition in which an individual’s normal sleep cycle is shifted such that their biological rhythm is disrupted and they cannot fall asleep until late at night and, thus, have a later morning wake time. Often the requirements of work or school schedule result in insufficient sleep for these individuals. Delayed sleep phase syndrome can be often misinterpreted as insomnia. One study evaluating patients with mild TBI and insomnia revealed that 15 of 42 patients (36%) were more properly diagnosed with delayed sleep phase syndrome [35]. This correlates with the study describing decreased melatonin
224
M. S. Jaffee et al.
release in patients following mild TBI [34]. For comparison, a circadian rhythm disorder was found in the context of subjective insomnia in 7–10% of the general population. An additional challenge of interpretation in sports concussion is one of epidemiology. There are studies illustrating that teenagers and young adults have a baseline biological predilection for a delayed circadian phase [36]. As many athletic concussions occur in this age demographic, it is a challenge to determine if this finding is pre-morbid or found as a result of injury. It is possible that injury may exacerbate such a premorbid tendency. Head trauma with concomitant eye injuries can be associated with a free-running circadian rhythm in which the sleep and wake times gradually shift forward around the clock each day due to the loss of the ability for light to entrain the circadian rhythm [37].
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
Other disorders of sleep It is unclear if the diagnoses of obstructive sleep apnea and restless legs syndrome/periodic limb movements of sleep and parasomnias represent a result of injury or represent a previously unrecognized primary sleep disorder or possibly exacerbation of a pre-existing condition. If these conditions are pre-existing, it raises the question as to whether they may have either contributed to sub-optimal athletic performance or were a risk factor in sustaining the concussion. Parasomnias Parasomnias are noted in 25% of patients [27]. The most commonly reported parasomnia is REM Behaviour Disorder in which individuals lose their normal physiological paralysis of skeletal muscles during REM sleep and, therefore, have dream enactment behaviours. The theory is that this indicates damage or dysfunction of the brainstem mechanisms responsible for inhibiting spinal motor neurons during REM sleep [27]. Another challenge of evaluation in the concussion population is that this symptom can sometimes be provoked by medications such as antidepressants that may be used in the treatment of other post-concussive symptoms. Sleep-disordered breathing Observational studies from PSG and MSLT following TBI led to abnormal findings and diagnoses based on sleep study criteria in 46% of patients [26]. Obstructive sleep apnea was observed in 23% of patients following TBI in the general population. This is compared to a clinical report of 4–9% in the general population without TBI and is noted to occur in more obese patients. Abnormal leg movements Periodic limb movements of sleep have been reported in 17% of patients following TBI [38]. This is compared to a reported prevalence of 5% in the general population. Periodic limb movements of sleep can correlate with Restless Legs Syndrome, which has a strong familial and genetic predisposition. Some cases of periodic limb movements following injury are transient. Some medications that may be used in the management of other post-concussive symptoms such as
Brain Inj, 2015; 29(2): 221–227
antidepressants are correlated as being an iatrogenic aetiology of Restless Legs Syndrome and Periodic Limb Movements of sleep. In some cases, the periodic limb movements may adversely affect sleep quality.
Considerations of co-morbidities and other post-concussive symptoms Cognitive neuropsychological deficits following concussion with associated sleep dysfunction can be a challenge to analyse. Some objective studies in non-TBI patients with sleep deprivation or a primary sleep disorder such as obstructive sleep apnea, where cognitive deficits in attention, memory and processing speed are noted [39]. In addition, there are well-described cognitive deficits in attention, memory and processing speed that can be seen as part of a post-concussive syndrome. With such overlapping profiles, it may be difficult to attribute residual cognitive deficits following concussion to the injury itself or sleep deprivation. Sideline assessments with computer based tests in sports concussion have demonstrated deficits in reaction time. Bloomfield et al. [40] demonstrated that sleep disruption also contributes to poor testing on reaction time and divided attention in patients with moderate–severe TBI. These computer-based tests are sometimes used to inform returnto-play decisions and the effects of sleep disruption on reaction time and divided attention in sports concussion may be contributing to the results and return-to-play decisions as well as effects on performance. There are other co-morbid conditions such as psychiatric syndromes following concussion that can further complicate sleep. During the first 3 months following injury, an acute post-TBI anxiety disorder was considered the most significant risk factor associated with worsening sleep [40]. In addition, it has been shown that patients with mild TBI and psychiatric syndromes have a higher prevalence for reporting post-concussive symptoms such as sleep disturbance than do patients with mild TBI or a psychiatric syndrome independently [41, 42]. Furthermore, there may be an independent relationship between TBI and/or psychiatric syndromes to obstructive sleep apnea. Despite the challenge of co-morbidities, the symptom of sleep disturbance remains a target symptom in the overall management plan. In addition to direct treatment, there may be a role for incorporating considerations of adverse effects of sleep disturbance on school and academic performance, regardless of aetiology [43].
Treatment issues Treatment of sleep complaints follows a target symptom approach using similar approaches as those used in the nonTBI population. There is limited literature on the efficacy of insomnia treatment in the TBI or concussion population. For insomnia, recommended treatment modalities include pharmacological therapy and non-pharmacological behavioural interventions. Non-pharmacological behavioural interventions include Cognitive Behavioural Therapy for Insomnia (CBT-i). CBTi interventions include stimulus control, sleep restriction to improve consolidation, cognitive restructuring, fatigue management and sleep hygiene education. Sleep
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
DOI: 10.3109/02699052.2014.983978
hygiene alone has not been shown to be effective in insomnia populations. Successful use of CBTi treatment was reported in a TBI case report [44]. Management of insomnia with medications (prescription and over-the-counter) remain the most common and accessible. A pharmacological trial showed efficacy of both melatonin and low dose amitriptyline with improvements in alertness, sleep duration, sleep latency, and sleep quality in patients with post-TBI and insomnia [45]. Another review recommended the use of Zopiclone and Lorazepam, while Melatonin, Amitriptyline and Sertraline were not recommended [46]. There are Clinical Practice Guidelines specifically for mild TBI that include management recommendations for sleep disturbances. These include the VA/DoD Clinical Practice Guidelines, the American Association of Neuroscience Nurses/Association of Rehabilitation Nurses Clinical Practice Guidelines, and the Ontario Neurotrauma Foundation Guidelines. Each of the guidelines emphasizes cognitive and behavioural management [47]. The VA/DoD Clinical Practice Guidelines and the Ontario Neurotrauma Foundation Guidelines recommend pharmacotherapy acutely with limitations [48, 49]. Agents recommended are selective alpha-1 Benzodiazepine receptor agonist or selective serotonin reuptake inhibitors. The Ontario Neurotrauma Foundation Guideline recommends limiting pharmacotherapy to 7 days, while the VA/DoD Clinical Practice Guideline for TBI recommend limiting the duration of Ambien usage to a maximum of 10 days. When using pharmacotherapy, it is important to consider the potential effects on cognitive recovery following concussion, especially for agents that may have anti-cholinergic sideeffects. Furthermore, certain antidepressant medications may lower seizure threshold. The use of Benzodiazepines is discouraged. This class of medications is thought to have an adverse effect on both cognition and neuroplasticity. Agents that bind more specifically to the alpha-1 complex of the GABA receptor are thought to not have as persistent adverse effects. Examples of these medications include Zolpidem and Zaleplon. There is general consensus that pharmacological therapy is suggested for acute but not chronic insomnia. Combination therapies for insomnia with pharmacotherapy acutely combined with CBTi interventions over a longer term have not been adequately studied and would be of interest in the sports concussion population. There have been associated reports of sleep improvement in mild TBI when other associated symptoms have been targeted. When symptoms of post-traumatic stress have been managed with Prazosin in a TBI population, there has been improvement in sleep [50]. There is also a case report of hyperbaric oxygen (HBO) therapy improving sleep in two patients being treated for posttraumatic headaches [51]. Circadian rhythm disorders are treated with exogenous melatonin and phototherapy. Hypersomnia can be managed with Modafinil or Armodafanil as a first-line therapy with consideration of usage of stimulant medications with more severe cases. Conditions of sleep-disordered breathing can be managed with the appropriate positive
Sleep disturbances in athletic concussion
225
airway pressure therapy such as CPAP (continuous positive airway pressure). Treatment of sleep disorders following TBI may result in polysomnographic resolution without change in subjective sleepiness or neuropsychological function [52]. This phenomenon requires further investigation. A possible theory for this phenomenon may be derived from a recent study which demonstrated that, in subjects with mild TBI who were 2 weeks or less post-injury, there were abnormalities on sleep electroencephalogram power spectra as compared to controls, while both populations had normal polysomnograms [30]. This suggests a possibility that there may be more subtle brain electrical changes on power spectral analyses that are first to present and last to resolve.
Research and clinical directions Sleep disturbances following concussion have traditionally been viewed as a post-concussive symptom that needs to be targeted and managed for relief similar to the way posttraumatic headaches are regarded. There are evolving paradigms that focus on the pathophysiology of concussion and the underlying pathophysiology of sleep. Current understanding of pathophysiology of concussion describes an initial metabolic storm and subsequent neurometabolic energy mismatch between brain glucose supply and demand. Sleep pathophysiology is thought to be restorative to brain energy patterns. Synaptic activity returns to baseline during sleep as compared to wake when synaptic activity consumes 80% of the brain’s energy [53]. This implies that adequate sleep duration, quality, and timing may be important for neuroplastic recovery following concussion. This paradigm shifts sleep as a target symptom to be managed to a neurorestorative process to be utilized. Newer treatments are being developed to address sleep complaints such as insomnia. These include a variety of devices and novel pharmacological approaches to include Hypocretin antagonists. It is not clear what effect these agents may have on neuroplastic recovery and if there may be a potential application in the management of sports concussion. More information is emerging regarding the role of recurrent concussions in athletes and the increased risk of chronic traumatic encephalopathy (CTE). A key feature of this entity is cognitive disturbances. The interface of sleep disruption and the physiological cascades that trigger these changes has yet to be fully elucidated. Key points regarding sleep dysfunction and traumatic brain injury include: Sleep issues and TBI are very intertwined and complicated by co-morbidities that have their own sleep dysfunction. Disturbances in sleep either prior to concussion or following concussion can affect athletic performance. Mild TBI patients tend to have more subjective sleep complaints, with the most common complaints being excessive daytime somnolence and insomnia. Delayed Circadian Phase can present as insomnia. Prevalence of post-injury hypersomnia, which is likely related to decreased hypocretin, is more of an issue in moderate–severe TBI.
226
M. S. Jaffee et al.
Consider sleep screening in TBI patients with sleep complaints. More research is needed to further guide evaluation and management and to harness potential plastic recovery processes of sleep.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
References 1. Gosselin N, Lassonde M, Petit D, et al. Sleep following sports related concussion. Sleep Medicine 2009;10:35–46. 2. Gosselin N, Tellier M. Patients with traumatic brain injury are at high risk of developing chronic sleep-wake disturbances. Journal of Neurology, Neurosurgery & Psychiatry 2010;81:1297. 3. McCrory P, Meuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: The 4th international conference on concussion in sport held in Zurich, 2012. British Journal of Sports Medicine 2013;47:250–258. 4. Oliver SJ, Costa RJ, Laing SJ, Bilzon JL, Walsh NP. One night of sleep deprivation decreases treadmill endurance performance. European Journal of Applied Physiology 2009;107: 155–156. 5. Dinges DF, Pack F, Williams K, et al. Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 1997; 20:267–277. 6. Belenky G, Wesensten N, Thorne D, et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: A sleep dose-response study. Journal of Sleep Research 2003;12:1–12. 7. Mah CD, Mah KE, Kezirian EJ, Dement WC. The effects of sleep extension on the athletic performance of collegiate basketball players. Sleep 2011;34:943–950. 8. Mah CD, Mah KE, Dement WC. Extended sleep and the effects on mood and athletic performance in college swimmers. Sleep 2008; 31:128. 9. Taub JM, Globus GG, Phoebus E, Drury R. Extended sleep and performance. Nature 1971;233:142–143. 10. Sassin JF, Parker DC, Mace JW, Gotlin RW, Johnson LC, Rossman LG. Human growth hormone release: Relation to slow-wave sleep and sleep-walking cycles. Science 1969;165:513–515. 11. Van Cauter E. Slow wave sleep and release of growth hormone. Journal of the American Medical Association 2000; 284:2717. 12. George CF, Kab V, Kab P, Villa JJ, Levy AM. Sleep and breathing in professional football players. Journal of Clinical Sleep Medicine 2003;4:317–325. 13. Schreiber S, Barkai G, Gur-Hartman T, et al. Long-lasting sleep patterns of adult patients with mild traumatic brain injury (mTBI) and non-mTBI subjects. Sleep Medicine 2008;9: 481–487. 14. Kaufman Y, Tzischinsky O, Epstein R, et al. Long-term sleep disturbaces in adolescents after minor head injury. Pediatric Neurology 2001;24:129–134. 15. Winget CM, DeRoshia CW, Holley DC. Circadian rhythms and athletic performance. Medicine & Science in Sports & Exercise 1985;17:498–516. 16. Atkinson G, Coldwells A, Reilly T, et al. The influence of age on diurnal variations in competitive cycling performances. Journal of Sport Science 1994;12:127–128. 17. Smith RS, Jamieson M, Dement WC. A comparison of peak performance, competition, and training times in elite athletes. Sleep Research 1996;25:574. 18. Rice TB, Dunn RE, Lincoln AE, et al. Sleep-disordered breathing in the National Football League. Sleep 2010;33:819–812. 19. Recht LD, Lew RA, Schwartz WJ. Baseball teams beaten by jet lag. Nature 1995;377:583.
Brain Inj, 2015; 29(2): 221–227
20. Winter WC, Hammond WR, Green NH, Zhang Z, Bliwise DL. Measuring circadian advantage in Major League Baseball: A 10-year retrospective study. International Journal of Sports Physiology & Performance 2009;4:394–401. 21. Mihalik JP, Lengas E, Register-Mihalik JK, Oyama S, Begalle RL, Guskiewicz KM. The effects of sleep quality and sleep quantity on concussion baseline assessment. Clinical Journal of Sport Medicine 2013;23:343–348. 22. Halstead ME, Walter KD; Council on Sports Medicine and Fitness. American Academy of Pediatrics. Clinical report – sports-related concussion in children and adolescents. Pediatrics 2010;126: 871–881. 23. Carskadon MA, Wolfson AR, Acebo C, Tzischinsky O, Seifer R. Adolesent sleep patterns, circadian timing, and sleepiness at a transition to early school days. Sleep 1998;21:871–881. 24. Fichtenberg NL, Zafonte RD, Putnam S, et al. Insomnia in a psotacute brain injury sample. Brain Injury 2002;16:197–206. 25. Makley MJ, English JB, Drubach DA, et al. Prevalence of sleep disturbance in closed head injury patients in a rehabilitation unit. Neurorehabilitation & Neural Repair 2008;22:341–347. 26. Castriotta RJ, Wilde MC, Lai JM, et al. Prevalence and consequences of sleep disorder s in traumatic brain injury. Journal of Clinical Sleep Medicine 2007;3:349–356. 27. Verma A, Anand V, Verma NP. Sleep disorders in chronic traumatic brain injury. Journal of Clinical Sleep Medicine 2007;3: 357–362. 28. Lundin A, de Boussard C, Edman G, Borg J. Symptoms and disability until 3 months after mild TBI. Brain Injury 2006;20: 799–806. 29. Ouellet MC, Morin CM. Subjective and objective measures of insomnia in the context of traumatic brain injury: A preliminary study. Sleep Medicine 2006;7:486–497. 30. Rao V, Bergey A, Hill H, et al. Sleep disturbance after mild traumatic brain injury: Indicator of injury? Journal of Neuropsychiatry & Clinical Neurosciences 2011;23:201–205. 31. Murillo-Rodrı´guez E, Arias-Carrio´n O, Sanguino-Rodrı´guez K, et al. Mechanisms of sleep-wake cycle modulation. CNS & Neurological Disorders - Drug Targets 2009;8:245–253. 32. Guilleminault C, Yuen KM, Gulevich MG, et al. Hypersomnia after head-neck trauma: A medicolegal dilemma. Neurology 2000;54: 653–659. 33. Baumann CR, Stocker R, Imhof HG, et al. Hypocretin-1 (Orexin A) deficiency in acute traumatic brain injury. Neurology 2005;65: 147–149. 34. Shekelton JA, Parcell DL, Redman JR, et al. Sleep disturbance and melatonin levels following traumatic brain injury. Neurology 2000; 74:1732–1738. 35. Ayalon L, Borodkin K, Dishon L, et al. Circadian rhythm sleep disorders following mild traumatic brain injury. Neurology 2007; 68:1136–1140. 36. Gruber R, Sheshko D. Circadian sleep disorders in children and adolescents. In: Ivanenko A, editors. Sleep and psychiatric disorders in children and adolescents. USA: Informa Healthcare; 2008. pp 61–78. 37. Carter KA, Lettieri CJ, Pena JM. An unusual case of insomnia following IED-induced traumatic brain injury. Journal of Clinical Sleep Medicine 2010;6:205–206. 38. Masel BE, Scheibel RS, Kimbark T, et al. Excessive daytime sleepiness in adults with brain injuries. Archives of Physical Medicine & Rehabilitation 2001;82:1526–1532. 39. Yaffe K, Laftan AM, Harrison SL, et al. Sleep-disordered breathing, hypoxia, and risk of mild cognitive impairment and dementia in older women. Journal of the American Medical Association 2011;306:613–619. 40. Rao V, Spiro J, Vashnavi S, et al. Prevalence and types of sleep disturbances acutely after traumatic brain injury. Brain Injury 2008; 22:381–386. 41. Brenner LA, Ivins BJ, Schwab K, et al. Traumatic brain injury, posttraumatic stress disorder, and postconcussive symptom reporting among troops returning from Iraq. Journal of Head Trauma Rehabilitation 2010;25:307–312. 42. Defense Centers of Excellence for Psychological Health and Traumatic Brain Injuries Webinar. Treating sleep problems in Post-traumatic Stress Disorder (PTSD) and Traumatic Brain Injury (TBI). 2012.
DOI: 10.3109/02699052.2014.983978
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
43. Dewald JF, Meijer AM, Oort FJ, et al. The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: A meta-analytic review. Sleep Medicine Reviews 2010;14:179–189. 44. Oulette MC, Morin CM. Efficacy of cognitive-behavioral therapy for insomnia associated with traumatic brain injury: A single-case experimental design. Archives of Physical Medicine & Rehabilitation 2007;88:1581–1592. 45. Kemp S, Biswas R, et al. The value of melatonin for sleep disorders occurring in post-head injury. A pilot RCT. Brain Injury 2014;18: 911–919. 46. Zeltzer JM, Friedman L, Ohara R. Insomnia in the context of traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:827–836. 47. West TA, Bergman K, Biggins MS, et al. Care of the patient with mild traumatic brain injury. AANN and ARN clinical practice guideline series. Silver Spring, MD: Defense and Veterans Brain Injury Center; 2011. pp 1–35. 48. Management of Concussion/mTBI Working Group. VA/DoD clinical practice guideline for management of concussion/mild traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:CP1–68.
Sleep disturbances in athletic concussion
227
49. Ontario Neurotrauma Foundation. Guidelines for mild traumatic brain injury and persistent symptoms. Ontario, Canada: Guideline Development Team; 2011. 50. Ruff RL, Ruff SS, Wang XF. Improving sleep: Initial headache treatment in OIF/OEF veterans with blast-induced mild traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:1071–1084. 51. Wright JK, Zant E, Groom K, et al. Case report: Treatment of mild traumatic brain injury with hyperbaric oxygen. Undersea & Hyperbaric Medical Society 2009;36: 391–399. 52. Castriotta RJ, Atanasov S, Wilde MC, et al. Treatment of sleep disorders after traumatic brain injury. Journal of Clinical Sleep Medicine 2009;5:137–144. 53. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscience 2008;11:200–208. 54. Bloomfield IL, Espie CA, Evans JJ. Do sleep difficulties exacerbate deficits in sustained attention following traumatic brain injury? Journal of the International Neuropsychological Society 2010;16: 17–25.
REVIEW
Sleep disturbances in athletic concussion Michael S. Jaffee1, W. Christopher Winter2, Christine C. Jones2, & Geoffrey Ling3 Department of Neurology, University of Virginia, Charlottesville, VA, USA, 2Charlottesville Neurology and Sleep Medicine, Charlottesville, VA, USA, and 3Defense Advanced Research Projects Agency (DARPA), Washington, DC, USA
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
1
Abstract
Keywords
Background: Sleep disturbances are a common symptom following concussions to include athletic concussion. Review: This review applies literature on sleep following traumatic brain injury and concussion to sport concussions and places these considerations in the context of sleep and athletic performance. It also includes a description of sleep abnormalities in sleep duration, quality and timing as well as recommended treatment approaches. Finally, it includes a brief discussion of emerging paradigms of sleep and concussion recovery.
Concussion, sleep disturbance, sport
Introduction Research demonstrates the importance of sleep as a contributing factor to optimal athletic performance and sleep disturbances are common following concussion [1, 2]. Understanding and addressing sleep complaints following concussion may help not only with recovery from concussion, but may also have the potential to support a more rapid return to athletic activities. Despite the frequency of post-concussive symptoms, the literature on sleep following concussion is limited. Within this literature, there is very little research evaluating sleep disturbances specifically in the context of sports concussion. The purpose of this paper is to review the literature on sleep disturbances in athletic performance and sleep disturbances following concussion extrapolating data from literature on mild TBI (mTBI). PubMed is the primary source used for information regarding sleep disturbances in concussion, particularly for clinical human/adult studies published in English from 2000–2011. Brain injury, concussion, head injury, head trauma, TBI and traumatic brain injury together with secondary terms to include circadian, sleep hypersomnia, insomnia, narcolepsy, nightmare, parasomnia and sleep apnea are the search terms and combinations included in the search.
Limitations of medical literature evaluating concussion and sleep disturbances There are a number of limitations in current research on sleep and TBI. Most studies have relatively small sample sizes,
Correspondence: Michael S. Jaffee, Department of Neurology, University of Virginia, PO Box 800394, Charlottesville, VA 22908, USA. E-mail: [email protected]
History Received 21 April 2014 Revised 20 October 2014 Accepted 31 October 2014 Published online 13 January 2015
variability in age ranges, differing severities of injury and do not clearly stratify by time following injury (acute effects vs. chronic effects). The biological aspects of co-morbid psychiatric syndromes are not yet fully explored and research designs do not always control for factors such as pain and medications. Studies do not consistently clarify the relationship between impaired sleep and other co-morbid symptoms following TBI and data is often lacking to understand the contribution of pre-morbid issues. Finally, the majority of studies do not correlate findings with neuroimaging or EEG evaluations. Furthermore, some inconsistencies remain within the literature of the definition and use of the term concussion. Current understanding reflects the consensus definitions of the International Conference on Concussion and Sport that defines concussion as a complex pathophysiological process affecting the brain, induced by biomechanical forces. It typically results in the rapid onset of transient impairment of neurological function. There is an association with a graded set of clinical responses that may or may not involve loss of consciousness. Many professionals often refer to concussions as mild traumatic brain injury (TBI) [3].
Importance of sleep and athletic performance The role of sleep in athletic performance is relatively new in comparison to the role of strength and conditioning, proper nutrition and hydration therapy. Until recently, the primary focus for preparing the elite athlete centred on his or her waking hours, with the period of sleep largely ignored. As the attention on performance enhancement and competitive advantage increases, more interest and effort is being generated toward the manipulation of sleep and sleep-related variables for athletic gain. These variables can be separated into categories not unlike the categories used to classify sleep
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
222
M. S. Jaffee et al.
disorders: sleep quantity, sleep quality and sleep timing (commonly referred to circadian factors). Perhaps the most obvious sleep-related variable is the amount of sleep an athlete is able to achieve. There is no shortage of research looking at the ill-effects on general performance when paired with varying levels of sleep deprivation [4–6]. For athletic performance to be at its best, all aspects of mental concentration, motor memory, strength and speed must be primed. While research on the negative effects of inadequate sleep provide the foundation for this field of study, a more novel concept has been advanced in recent years examining the benefits of sleeping beyond what is considered adequate sleep for the athlete. Much in the way a free diver might overfill his lungs with air before his descent; can an athlete ‘oversleep’ for a period of time and derive benefit from the practice? Several studies support this concept, which conclude that the amount of time spent in bed is tied to improved athletic performance [7–9]. Equally important to the amount of sleep an athlete achieves is the quality of that sleep. There are a host of sleep disorders that can disrupt normal architecture and create issues with sleep and performance. Given the extent to which growth hormone (GH) is secreted during slow wave sleep, one key factor in performance is protecting this sleep stage from disruption [10, 11]. While adequately powered studies looking at disrupted sleep and athletics are few, they do exist. Perhaps the most ambitious study of this kind evaluated the presence of sleep apnea within Canadian professional football players [12]. While there were no direct measures of performance made, the high prevalence within this group of athletes opened the door for future investigations and study. Considerations of sleep quality can be made by analysis of sleep architecture. There are reports of altered sleep architecture following mild TBI (concussion). This includes decreased Rapid Eye Movement (REM) and higher amounts of Non-REM Stage 1 (N1) and Non-REM Stage 2 (N2) sleep [13]. This change in architecture is different than that reported in moderate–severe injuries which have been associated with increased slow wave sleep after controlling for depression and anxiety. One study evaluated the sleep characteristics of teenagers who had complaints about sleep quality 3 years after sustaining a mild TBI. Measurements with polysomnography and actigraphy revealed poorer sleep efficiency than controls in those who had mild TBI [14]. Studies using advanced technologies not routinely employed in diagnostic sleep disorder centres are also being conducted. These studies involve the use of quantitative EEG and spectral EEG. One study evaluating spectral EEG in athletes with concussion identified a pattern of more delta activity and less alpha activity during wakefulness [1]. The authors suggested that spectral EEG may have a potential application for prognosis and ‘return to play’ determinations following athletic concussion. Beyond the quality and quantity of sleep, it is the research into the timing of sleep that has thus far been the area of research yielding the most information about links between sleep and performance [15]. In 1994, Atkinson et al. [16] published evidence that young cyclists performed better in afternoon and evening hours when compared to morning
Brain Inj, 2015; 29(2): 221–227
races. Smith and Dement’s [17] study of elite Olympic athletes yielded a similar tendency for peak performance in later afternoon events. An article in the journal Sleep evaluating the role of travel for Monday Night Football games opened the door for scientific study of athletic performance during travel across time zones [18]. Recht et al. [19] conducted studies looking at the teams’ transcontinental travel’, while Winter et al. [20] examined the more subtle roles of travel and team performance as it pertained to ‘circadian advantage’. Sleep-deprivation as a pre-concussion condition is described as a risk factor for the development of postconcussive symptoms [21]. Adolescents have a high incidence of athletic concussions [22]. The adolescent population at baseline has a high prevalence of disruptions in sleep quantity, quality and circadian factors affecting sleep timing [23]. Disruptions in sleep quality or timing may also be a premorbid contributing factor to post-concussive symptoms. Therefore, sleep disturbances may increase the risk of sustaining an athletic concussion, particularly if performance is compromised in a contact sport. Furthermore, if an athlete is returned to play and athletic performance is not back to baseline due to disturbances in sleep, there may be an increased risk of sustaining a recurrent concussion.
Prevalence of sleep disturbances following concussion The pathophysiology of concussion involves the triggering of diffuse axonal injury, which preferentially affects midline structures to include deep grey matter, the dorsolateral pons and mid-brain. These are all structures that are known to be related to sleep–wake mechanisms. In addition, the secondary effects of concussion lead to a neurometabolic cascade and release of neurotransmitters that are involved in the regulation of sleep–wake circuits as well as being implicated in co-morbidities to include psychiatric symptoms. Of symptoms and complaints that are most evident following concussion of all aetiologies, sleep disturbances are described subjectively as one of the most common factors. A challenge in interpreting prevalence data is that many of the studies included the entire spectrum of traumatic brain injury from mild (concussions) to moderate–severe. Furthermore, studies have evaluated subjective complaints of sleep following TBI, as well as objective tests to include polysomnogram (PSG), multiple sleep latency testing (MSLT), advanced electroencephalogram (EEG) techniques and circadian rhythm markers. Common complaints include excessive daytime somnolence, insomnia and unusual behaviours during sleep or transition stages (parasomnias). Prevalence studies based on subjective report estimate the presence of any sleep disturbance following TBI of any severity as ranging from 42–70% [24, 25]. Several studies also exist which evaluate sleep disturbance following TBI with objective measures through the use of PSG and MSLT. Objective evaluation of sleep complaints following TBI has several limitations and challenges, including the inherent limitations to polysomnographic studies, such as the first night effect observed in sleep laboratories which may not accurately reflect the quality of
DOI: 10.3109/02699052.2014.983978
sleep in a patient’s home environment. Another limitation is the effects of medications that may be used for concurrent conditions such as headaches and depression. An additional limitation is that, if a disorder is seen on a diagnostic test, it is difficult to determine if the disorder is pre-morbid or a result of the traumatic injury. Finally, there is inconsistency in the medical literature in which sleep disorder diagnoses are made solely on the basis of results of diagnostic tests as opposed to those diagnosed with clinical correlation of sleep lab findings. Diagnostic evaluations conducted 3 months after TBI show abnormalities in polysomnography (PSG) in 47% of patients and abnormal multiple sleep latency test (MSLT) in 25% of patients [26].
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
Insomnia Within the TBI population the most common subjective sleep complaints include excessive daytime somnolence (EDS) and insomnia [27]. These symptoms are not always distinguished from one another [27]. Insomnia following traumatic brain injury is self-reported in 33% of patients [27]. Of the patients who reported insomnia, approximately half have sleep onset insomnia associated with increased latency and approximately half report sleep maintenance insomnia associated with increased awakenings during the night. Patients with sleep onset insomnia had higher anxiety scores, while patients with sleep maintenance insomnia had higher depression scores [27]. On subjective reports, mild TBI is more associated with insomnia than more severe forms of TBI. Insomnia can be reported acutely or chronically (greater than 3 months after injury). A higher acute post-concussive symptom load tends to predict a higher risk for persistent insomnia complaints [28]. When post-concussive insomnia is evaluated with objective parameters, the severity of subjectively reported insomnia appears to be over-estimated [29]. Insomnia can be associated with states of increased arousal, which may adversely affect one’s self-perception of insomnia symptoms and severity. There are some theories regarding the pathophysiology and explanation for insomnia being reported more often in mild TBI than with more severe injuries. One theory involves the role of awareness. Patients with more severe injuries may not have as much awareness of their sleep difficulty. Conversely, those with concussions may have hyper-awareness as a function of hyper-arousal or other contributing post-concussive symptoms such as anxiety. Some hypothesize that more diffuse injuries (i.e. diffuse axonal injury) that occur in mild TBI lead to higher impairment in global functioning such as arousal than more severe or focal traumatic injuries [30]. Another theory is that there is dysregulation of shifting between sleep states or sleep state maintenance [31].
Excessive daytime sleepiness and hypersomnia Excessive daytime somnolence is reported in 50% of patients [27]. A clinical challenge is determining whether the excessive daytime sleepiness may have contributions from other sleep disorders such as insomnia or a disturbance in circadian rhythms or whether the excessive daytime sleepiness is due to an underlying hypersomnolence syndrome.
Sleep disturbances in athletic concussion
223
The entity of post-traumatic hypersomnia receives attention and consideration in patients following TBI who report excessive daytime sleepiness. In one study, 25% of chronic TBI patients demonstrated a mean sleep latency of 10 minutes or less via Multiple Sleep Latency Test (MSLT), the standard evaluation for hypersomnolence syndromes [27]. However, this study also illustrates no correlation between subjective sleepiness reporting on the Epworth Sleepiness Scale and objective MSLT results. This implies there may be a lack of awareness of sleepiness. There are some analytical challenges with studies such as these. Analyses of trauma patients 1 month after injury illustrate that problems of hypersomnia are more prominent with injuries involving the head than in injuries not involving the head. Hypersomnolence improves in many trauma patients, but 25% may have persistent symptoms at 1 year post-injury [27]. In patients with TBI, studies demonstrate a correlation between injury severity and both the degree of hypersomnia and its persistence. Following a severe TBI, 98% of patients report excessive daytime somnolence 15 months after TBI [32]. A diagnosis of narcolepsy is made in 6% of patients. The problem of hypersomnolence following severe TBI has been hypothesized to be due to injury to the posterolateral hypothalamus whose cells synthesize hypocretin-1, which is important in maintaining the wakefulness state. Low CSF levels of hypocretin-1 have been reported in 95% of patients following moderate–severe injury [33]. Many patients with TBI are thought to normalize their hypocretin levels within 6 months post-injury. Although mild TBI has higher subjective reports of sleep disturbance, when post-traumatic sleep data is analysed by severity of injury, objective evidence of hypersomnia is equivocal. It is important to not confuse the complaint of excessive daytime sleepiness with a manifestation of a circadian disruption.
TBI and circadian disruption Sleep disturbance following TBI may be associated with alterations in timing and rhythm of sleep. This can result in a mismatch between the biological sleep–wake schedule and the desired 24-hour environmental and social schedule. Such mismatches are associated with altered rhythm and timing of melatonin secretion and body temperature. Studies show a reduction in the evening production of melatonin following traumatic brain injury [34]. The most commonly described circadian rhythm disturbance following traumatic brain injury is delayed sleep phase syndrome. This is a condition in which an individual’s normal sleep cycle is shifted such that their biological rhythm is disrupted and they cannot fall asleep until late at night and, thus, have a later morning wake time. Often the requirements of work or school schedule result in insufficient sleep for these individuals. Delayed sleep phase syndrome can be often misinterpreted as insomnia. One study evaluating patients with mild TBI and insomnia revealed that 15 of 42 patients (36%) were more properly diagnosed with delayed sleep phase syndrome [35]. This correlates with the study describing decreased melatonin
224
M. S. Jaffee et al.
release in patients following mild TBI [34]. For comparison, a circadian rhythm disorder was found in the context of subjective insomnia in 7–10% of the general population. An additional challenge of interpretation in sports concussion is one of epidemiology. There are studies illustrating that teenagers and young adults have a baseline biological predilection for a delayed circadian phase [36]. As many athletic concussions occur in this age demographic, it is a challenge to determine if this finding is pre-morbid or found as a result of injury. It is possible that injury may exacerbate such a premorbid tendency. Head trauma with concomitant eye injuries can be associated with a free-running circadian rhythm in which the sleep and wake times gradually shift forward around the clock each day due to the loss of the ability for light to entrain the circadian rhythm [37].
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
Other disorders of sleep It is unclear if the diagnoses of obstructive sleep apnea and restless legs syndrome/periodic limb movements of sleep and parasomnias represent a result of injury or represent a previously unrecognized primary sleep disorder or possibly exacerbation of a pre-existing condition. If these conditions are pre-existing, it raises the question as to whether they may have either contributed to sub-optimal athletic performance or were a risk factor in sustaining the concussion. Parasomnias Parasomnias are noted in 25% of patients [27]. The most commonly reported parasomnia is REM Behaviour Disorder in which individuals lose their normal physiological paralysis of skeletal muscles during REM sleep and, therefore, have dream enactment behaviours. The theory is that this indicates damage or dysfunction of the brainstem mechanisms responsible for inhibiting spinal motor neurons during REM sleep [27]. Another challenge of evaluation in the concussion population is that this symptom can sometimes be provoked by medications such as antidepressants that may be used in the treatment of other post-concussive symptoms. Sleep-disordered breathing Observational studies from PSG and MSLT following TBI led to abnormal findings and diagnoses based on sleep study criteria in 46% of patients [26]. Obstructive sleep apnea was observed in 23% of patients following TBI in the general population. This is compared to a clinical report of 4–9% in the general population without TBI and is noted to occur in more obese patients. Abnormal leg movements Periodic limb movements of sleep have been reported in 17% of patients following TBI [38]. This is compared to a reported prevalence of 5% in the general population. Periodic limb movements of sleep can correlate with Restless Legs Syndrome, which has a strong familial and genetic predisposition. Some cases of periodic limb movements following injury are transient. Some medications that may be used in the management of other post-concussive symptoms such as
Brain Inj, 2015; 29(2): 221–227
antidepressants are correlated as being an iatrogenic aetiology of Restless Legs Syndrome and Periodic Limb Movements of sleep. In some cases, the periodic limb movements may adversely affect sleep quality.
Considerations of co-morbidities and other post-concussive symptoms Cognitive neuropsychological deficits following concussion with associated sleep dysfunction can be a challenge to analyse. Some objective studies in non-TBI patients with sleep deprivation or a primary sleep disorder such as obstructive sleep apnea, where cognitive deficits in attention, memory and processing speed are noted [39]. In addition, there are well-described cognitive deficits in attention, memory and processing speed that can be seen as part of a post-concussive syndrome. With such overlapping profiles, it may be difficult to attribute residual cognitive deficits following concussion to the injury itself or sleep deprivation. Sideline assessments with computer based tests in sports concussion have demonstrated deficits in reaction time. Bloomfield et al. [40] demonstrated that sleep disruption also contributes to poor testing on reaction time and divided attention in patients with moderate–severe TBI. These computer-based tests are sometimes used to inform returnto-play decisions and the effects of sleep disruption on reaction time and divided attention in sports concussion may be contributing to the results and return-to-play decisions as well as effects on performance. There are other co-morbid conditions such as psychiatric syndromes following concussion that can further complicate sleep. During the first 3 months following injury, an acute post-TBI anxiety disorder was considered the most significant risk factor associated with worsening sleep [40]. In addition, it has been shown that patients with mild TBI and psychiatric syndromes have a higher prevalence for reporting post-concussive symptoms such as sleep disturbance than do patients with mild TBI or a psychiatric syndrome independently [41, 42]. Furthermore, there may be an independent relationship between TBI and/or psychiatric syndromes to obstructive sleep apnea. Despite the challenge of co-morbidities, the symptom of sleep disturbance remains a target symptom in the overall management plan. In addition to direct treatment, there may be a role for incorporating considerations of adverse effects of sleep disturbance on school and academic performance, regardless of aetiology [43].
Treatment issues Treatment of sleep complaints follows a target symptom approach using similar approaches as those used in the nonTBI population. There is limited literature on the efficacy of insomnia treatment in the TBI or concussion population. For insomnia, recommended treatment modalities include pharmacological therapy and non-pharmacological behavioural interventions. Non-pharmacological behavioural interventions include Cognitive Behavioural Therapy for Insomnia (CBT-i). CBTi interventions include stimulus control, sleep restriction to improve consolidation, cognitive restructuring, fatigue management and sleep hygiene education. Sleep
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
DOI: 10.3109/02699052.2014.983978
hygiene alone has not been shown to be effective in insomnia populations. Successful use of CBTi treatment was reported in a TBI case report [44]. Management of insomnia with medications (prescription and over-the-counter) remain the most common and accessible. A pharmacological trial showed efficacy of both melatonin and low dose amitriptyline with improvements in alertness, sleep duration, sleep latency, and sleep quality in patients with post-TBI and insomnia [45]. Another review recommended the use of Zopiclone and Lorazepam, while Melatonin, Amitriptyline and Sertraline were not recommended [46]. There are Clinical Practice Guidelines specifically for mild TBI that include management recommendations for sleep disturbances. These include the VA/DoD Clinical Practice Guidelines, the American Association of Neuroscience Nurses/Association of Rehabilitation Nurses Clinical Practice Guidelines, and the Ontario Neurotrauma Foundation Guidelines. Each of the guidelines emphasizes cognitive and behavioural management [47]. The VA/DoD Clinical Practice Guidelines and the Ontario Neurotrauma Foundation Guidelines recommend pharmacotherapy acutely with limitations [48, 49]. Agents recommended are selective alpha-1 Benzodiazepine receptor agonist or selective serotonin reuptake inhibitors. The Ontario Neurotrauma Foundation Guideline recommends limiting pharmacotherapy to 7 days, while the VA/DoD Clinical Practice Guideline for TBI recommend limiting the duration of Ambien usage to a maximum of 10 days. When using pharmacotherapy, it is important to consider the potential effects on cognitive recovery following concussion, especially for agents that may have anti-cholinergic sideeffects. Furthermore, certain antidepressant medications may lower seizure threshold. The use of Benzodiazepines is discouraged. This class of medications is thought to have an adverse effect on both cognition and neuroplasticity. Agents that bind more specifically to the alpha-1 complex of the GABA receptor are thought to not have as persistent adverse effects. Examples of these medications include Zolpidem and Zaleplon. There is general consensus that pharmacological therapy is suggested for acute but not chronic insomnia. Combination therapies for insomnia with pharmacotherapy acutely combined with CBTi interventions over a longer term have not been adequately studied and would be of interest in the sports concussion population. There have been associated reports of sleep improvement in mild TBI when other associated symptoms have been targeted. When symptoms of post-traumatic stress have been managed with Prazosin in a TBI population, there has been improvement in sleep [50]. There is also a case report of hyperbaric oxygen (HBO) therapy improving sleep in two patients being treated for posttraumatic headaches [51]. Circadian rhythm disorders are treated with exogenous melatonin and phototherapy. Hypersomnia can be managed with Modafinil or Armodafanil as a first-line therapy with consideration of usage of stimulant medications with more severe cases. Conditions of sleep-disordered breathing can be managed with the appropriate positive
Sleep disturbances in athletic concussion
225
airway pressure therapy such as CPAP (continuous positive airway pressure). Treatment of sleep disorders following TBI may result in polysomnographic resolution without change in subjective sleepiness or neuropsychological function [52]. This phenomenon requires further investigation. A possible theory for this phenomenon may be derived from a recent study which demonstrated that, in subjects with mild TBI who were 2 weeks or less post-injury, there were abnormalities on sleep electroencephalogram power spectra as compared to controls, while both populations had normal polysomnograms [30]. This suggests a possibility that there may be more subtle brain electrical changes on power spectral analyses that are first to present and last to resolve.
Research and clinical directions Sleep disturbances following concussion have traditionally been viewed as a post-concussive symptom that needs to be targeted and managed for relief similar to the way posttraumatic headaches are regarded. There are evolving paradigms that focus on the pathophysiology of concussion and the underlying pathophysiology of sleep. Current understanding of pathophysiology of concussion describes an initial metabolic storm and subsequent neurometabolic energy mismatch between brain glucose supply and demand. Sleep pathophysiology is thought to be restorative to brain energy patterns. Synaptic activity returns to baseline during sleep as compared to wake when synaptic activity consumes 80% of the brain’s energy [53]. This implies that adequate sleep duration, quality, and timing may be important for neuroplastic recovery following concussion. This paradigm shifts sleep as a target symptom to be managed to a neurorestorative process to be utilized. Newer treatments are being developed to address sleep complaints such as insomnia. These include a variety of devices and novel pharmacological approaches to include Hypocretin antagonists. It is not clear what effect these agents may have on neuroplastic recovery and if there may be a potential application in the management of sports concussion. More information is emerging regarding the role of recurrent concussions in athletes and the increased risk of chronic traumatic encephalopathy (CTE). A key feature of this entity is cognitive disturbances. The interface of sleep disruption and the physiological cascades that trigger these changes has yet to be fully elucidated. Key points regarding sleep dysfunction and traumatic brain injury include: Sleep issues and TBI are very intertwined and complicated by co-morbidities that have their own sleep dysfunction. Disturbances in sleep either prior to concussion or following concussion can affect athletic performance. Mild TBI patients tend to have more subjective sleep complaints, with the most common complaints being excessive daytime somnolence and insomnia. Delayed Circadian Phase can present as insomnia. Prevalence of post-injury hypersomnia, which is likely related to decreased hypocretin, is more of an issue in moderate–severe TBI.
226
M. S. Jaffee et al.
Consider sleep screening in TBI patients with sleep complaints. More research is needed to further guide evaluation and management and to harness potential plastic recovery processes of sleep.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
References 1. Gosselin N, Lassonde M, Petit D, et al. Sleep following sports related concussion. Sleep Medicine 2009;10:35–46. 2. Gosselin N, Tellier M. Patients with traumatic brain injury are at high risk of developing chronic sleep-wake disturbances. Journal of Neurology, Neurosurgery & Psychiatry 2010;81:1297. 3. McCrory P, Meuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: The 4th international conference on concussion in sport held in Zurich, 2012. British Journal of Sports Medicine 2013;47:250–258. 4. Oliver SJ, Costa RJ, Laing SJ, Bilzon JL, Walsh NP. One night of sleep deprivation decreases treadmill endurance performance. European Journal of Applied Physiology 2009;107: 155–156. 5. Dinges DF, Pack F, Williams K, et al. Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 1997; 20:267–277. 6. Belenky G, Wesensten N, Thorne D, et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: A sleep dose-response study. Journal of Sleep Research 2003;12:1–12. 7. Mah CD, Mah KE, Kezirian EJ, Dement WC. The effects of sleep extension on the athletic performance of collegiate basketball players. Sleep 2011;34:943–950. 8. Mah CD, Mah KE, Dement WC. Extended sleep and the effects on mood and athletic performance in college swimmers. Sleep 2008; 31:128. 9. Taub JM, Globus GG, Phoebus E, Drury R. Extended sleep and performance. Nature 1971;233:142–143. 10. Sassin JF, Parker DC, Mace JW, Gotlin RW, Johnson LC, Rossman LG. Human growth hormone release: Relation to slow-wave sleep and sleep-walking cycles. Science 1969;165:513–515. 11. Van Cauter E. Slow wave sleep and release of growth hormone. Journal of the American Medical Association 2000; 284:2717. 12. George CF, Kab V, Kab P, Villa JJ, Levy AM. Sleep and breathing in professional football players. Journal of Clinical Sleep Medicine 2003;4:317–325. 13. Schreiber S, Barkai G, Gur-Hartman T, et al. Long-lasting sleep patterns of adult patients with mild traumatic brain injury (mTBI) and non-mTBI subjects. Sleep Medicine 2008;9: 481–487. 14. Kaufman Y, Tzischinsky O, Epstein R, et al. Long-term sleep disturbaces in adolescents after minor head injury. Pediatric Neurology 2001;24:129–134. 15. Winget CM, DeRoshia CW, Holley DC. Circadian rhythms and athletic performance. Medicine & Science in Sports & Exercise 1985;17:498–516. 16. Atkinson G, Coldwells A, Reilly T, et al. The influence of age on diurnal variations in competitive cycling performances. Journal of Sport Science 1994;12:127–128. 17. Smith RS, Jamieson M, Dement WC. A comparison of peak performance, competition, and training times in elite athletes. Sleep Research 1996;25:574. 18. Rice TB, Dunn RE, Lincoln AE, et al. Sleep-disordered breathing in the National Football League. Sleep 2010;33:819–812. 19. Recht LD, Lew RA, Schwartz WJ. Baseball teams beaten by jet lag. Nature 1995;377:583.
Brain Inj, 2015; 29(2): 221–227
20. Winter WC, Hammond WR, Green NH, Zhang Z, Bliwise DL. Measuring circadian advantage in Major League Baseball: A 10-year retrospective study. International Journal of Sports Physiology & Performance 2009;4:394–401. 21. Mihalik JP, Lengas E, Register-Mihalik JK, Oyama S, Begalle RL, Guskiewicz KM. The effects of sleep quality and sleep quantity on concussion baseline assessment. Clinical Journal of Sport Medicine 2013;23:343–348. 22. Halstead ME, Walter KD; Council on Sports Medicine and Fitness. American Academy of Pediatrics. Clinical report – sports-related concussion in children and adolescents. Pediatrics 2010;126: 871–881. 23. Carskadon MA, Wolfson AR, Acebo C, Tzischinsky O, Seifer R. Adolesent sleep patterns, circadian timing, and sleepiness at a transition to early school days. Sleep 1998;21:871–881. 24. Fichtenberg NL, Zafonte RD, Putnam S, et al. Insomnia in a psotacute brain injury sample. Brain Injury 2002;16:197–206. 25. Makley MJ, English JB, Drubach DA, et al. Prevalence of sleep disturbance in closed head injury patients in a rehabilitation unit. Neurorehabilitation & Neural Repair 2008;22:341–347. 26. Castriotta RJ, Wilde MC, Lai JM, et al. Prevalence and consequences of sleep disorder s in traumatic brain injury. Journal of Clinical Sleep Medicine 2007;3:349–356. 27. Verma A, Anand V, Verma NP. Sleep disorders in chronic traumatic brain injury. Journal of Clinical Sleep Medicine 2007;3: 357–362. 28. Lundin A, de Boussard C, Edman G, Borg J. Symptoms and disability until 3 months after mild TBI. Brain Injury 2006;20: 799–806. 29. Ouellet MC, Morin CM. Subjective and objective measures of insomnia in the context of traumatic brain injury: A preliminary study. Sleep Medicine 2006;7:486–497. 30. Rao V, Bergey A, Hill H, et al. Sleep disturbance after mild traumatic brain injury: Indicator of injury? Journal of Neuropsychiatry & Clinical Neurosciences 2011;23:201–205. 31. Murillo-Rodrı´guez E, Arias-Carrio´n O, Sanguino-Rodrı´guez K, et al. Mechanisms of sleep-wake cycle modulation. CNS & Neurological Disorders - Drug Targets 2009;8:245–253. 32. Guilleminault C, Yuen KM, Gulevich MG, et al. Hypersomnia after head-neck trauma: A medicolegal dilemma. Neurology 2000;54: 653–659. 33. Baumann CR, Stocker R, Imhof HG, et al. Hypocretin-1 (Orexin A) deficiency in acute traumatic brain injury. Neurology 2005;65: 147–149. 34. Shekelton JA, Parcell DL, Redman JR, et al. Sleep disturbance and melatonin levels following traumatic brain injury. Neurology 2000; 74:1732–1738. 35. Ayalon L, Borodkin K, Dishon L, et al. Circadian rhythm sleep disorders following mild traumatic brain injury. Neurology 2007; 68:1136–1140. 36. Gruber R, Sheshko D. Circadian sleep disorders in children and adolescents. In: Ivanenko A, editors. Sleep and psychiatric disorders in children and adolescents. USA: Informa Healthcare; 2008. pp 61–78. 37. Carter KA, Lettieri CJ, Pena JM. An unusual case of insomnia following IED-induced traumatic brain injury. Journal of Clinical Sleep Medicine 2010;6:205–206. 38. Masel BE, Scheibel RS, Kimbark T, et al. Excessive daytime sleepiness in adults with brain injuries. Archives of Physical Medicine & Rehabilitation 2001;82:1526–1532. 39. Yaffe K, Laftan AM, Harrison SL, et al. Sleep-disordered breathing, hypoxia, and risk of mild cognitive impairment and dementia in older women. Journal of the American Medical Association 2011;306:613–619. 40. Rao V, Spiro J, Vashnavi S, et al. Prevalence and types of sleep disturbances acutely after traumatic brain injury. Brain Injury 2008; 22:381–386. 41. Brenner LA, Ivins BJ, Schwab K, et al. Traumatic brain injury, posttraumatic stress disorder, and postconcussive symptom reporting among troops returning from Iraq. Journal of Head Trauma Rehabilitation 2010;25:307–312. 42. Defense Centers of Excellence for Psychological Health and Traumatic Brain Injuries Webinar. Treating sleep problems in Post-traumatic Stress Disorder (PTSD) and Traumatic Brain Injury (TBI). 2012.
DOI: 10.3109/02699052.2014.983978
Brain Inj Downloaded from informahealthcare.com by Kainan University on 04/12/15 For personal use only.
43. Dewald JF, Meijer AM, Oort FJ, et al. The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: A meta-analytic review. Sleep Medicine Reviews 2010;14:179–189. 44. Oulette MC, Morin CM. Efficacy of cognitive-behavioral therapy for insomnia associated with traumatic brain injury: A single-case experimental design. Archives of Physical Medicine & Rehabilitation 2007;88:1581–1592. 45. Kemp S, Biswas R, et al. The value of melatonin for sleep disorders occurring in post-head injury. A pilot RCT. Brain Injury 2014;18: 911–919. 46. Zeltzer JM, Friedman L, Ohara R. Insomnia in the context of traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:827–836. 47. West TA, Bergman K, Biggins MS, et al. Care of the patient with mild traumatic brain injury. AANN and ARN clinical practice guideline series. Silver Spring, MD: Defense and Veterans Brain Injury Center; 2011. pp 1–35. 48. Management of Concussion/mTBI Working Group. VA/DoD clinical practice guideline for management of concussion/mild traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:CP1–68.
Sleep disturbances in athletic concussion
227
49. Ontario Neurotrauma Foundation. Guidelines for mild traumatic brain injury and persistent symptoms. Ontario, Canada: Guideline Development Team; 2011. 50. Ruff RL, Ruff SS, Wang XF. Improving sleep: Initial headache treatment in OIF/OEF veterans with blast-induced mild traumatic brain injury. Journal of Rehabilitation Research & Development 2009;46:1071–1084. 51. Wright JK, Zant E, Groom K, et al. Case report: Treatment of mild traumatic brain injury with hyperbaric oxygen. Undersea & Hyperbaric Medical Society 2009;36: 391–399. 52. Castriotta RJ, Atanasov S, Wilde MC, et al. Treatment of sleep disorders after traumatic brain injury. Journal of Clinical Sleep Medicine 2009;5:137–144. 53. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscience 2008;11:200–208. 54. Bloomfield IL, Espie CA, Evans JJ. Do sleep difficulties exacerbate deficits in sustained attention following traumatic brain injury? Journal of the International Neuropsychological Society 2010;16: 17–25.
