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Association of Sleep and Co-Occurring Psychological Conditions at 1 Year After Traumatic Brain Injury

      Abstract

      Fogelberg DJ, Hoffman JM, Dikmen S, Temkin NR, Bell KR. Association of sleep and co-occurring psychological conditions at 1 year after traumatic brain injury.

      Objectives

      To compare individuals' sleep 1 year after traumatic brain injury (TBI) with that of a healthy comparison group, and examine the relationship between sleep, co-occurring conditions, and functional status in those with TBI.

      Design

      Longitudinal assessment of a prospectively studied sample of individuals with moderate to severe TBI. Assessment of sleep occurred at 1 year after TBI.

      Setting

      Inpatient acute rehabilitation for TBI and community follow-up at 1 year postinjury.

      Participants

      Individuals with TBI (N=174) were recruited from consecutive admissions to an inpatient rehabilitation unit and enrolled into the TBI Model Systems study. Participant mean age was 38, and mean Glasgow Coma Scale score on admission was 9.3. Seventy-eight percent of the sample were men.

      Interventions

      None.

      Main Outcome Measures

      Sleep was assessed with the Pittsburgh Sleep Quality Index (PSQI). Depression, anxiety, and pain were measured with the Patient Health Questionnaire-9, the Generalized Anxiety Disorder-7 Scale, and an analog pain rating scale, respectively.

      Results

      Participants with TBI reported significantly greater sleep difficulties than the healthy comparison group. Forty-four percent of participants with TBI reported significant sleep problems (PSQI>5). Participants with 1 or more co-occurring conditions (depression, pain, or anxiety) had significantly worse sleep than those without such a condition. The highest level of sleep problems was reported by participants with multiple co-occurring conditions. Sleep problems were also associated with poor functional status.

      Conclusions

      Sleep difficulties are a frequent problem at 1 year after TBI, and often co-occur with depression, anxiety, and pain. Assessment and treatment of sleep difficulties should be included in clinical practice. Future research on the potential causal relationship among co-occurring conditions may assist in additional intervention planning.

      Key Words

      List of Abbreviations:

      DRS (Disability Rating Scale), GAD-7 (Generalized Anxiety Disorder-7 Scale), GCS (Glasgow Coma Scale), PHQ-9 (Patient Health Questionnaire-9), PSQI (Pittsburgh Sleep Quality Index), SWLS (Satisfaction With Life Scale), TBI (traumatic brain injury), TBIMS (Traumatic Brain Injury Model Systems)
      SLEEP DISTURBANCES are commonly recognized yet poorly understood sequelae of traumatic brain injury (TBI). While an estimated 10% to 17% of the general population experience sleep disturbance,
      • Johnson E.O.
      • Roehrs T.
      • Roth T.
      • Breslau N.
      Epidemiology of alcohol and medication as aids to sleep in early adulthood.
      • Nowell P.D.
      • Mazumdar S.
      • Buysse D.J.
      • Dew M.A.
      • Reynolds C.F.
      • Kupfer D.J.
      Benzodiazepines and zolpidem for chronic insomnia: a meta-analysis of treatment efficacy.
      research indicates that the phenomenon is far more prevalent among individuals who have sustained a TBI.
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Orff H.J.
      • Ayalon L.
      • Drummond S.P.
      Traumatic brain injury and sleep disturbance: a review of current research.
      • Ouellet M.C.
      • Savard J.
      • Morin C.M.
      Insomnia following traumatic brain injury: a review.
      Makley et al
      • Makley M.J.
      • English J.B.
      • Drubach D.A.
      • Kreuz A.J.
      • Celnik P.A.
      • Tarwater P.M.
      Prevalence of sleep disturbance in closed head injury patients in a rehabilitation unit.
      found that 68% of patients with a closed head injury on a rehabilitation unit experienced disrupted nighttime sleep. In the first 3 months after a TBI, Rao et al
      • Rao V.
      • Spiro J.
      • Vaishnavi S.
      • et al.
      Prevalence and types of sleep disturbances acutely after traumatic brain injury.
      found that individuals had difficulty in sleep initiation, maintenance, quality, adequacy, and somnolence. Sleep disturbances are not confined to the newly injured, but are an enduring problem for a significant number of individuals with TBI. In a survey of individuals who were between 15 and 24 years postinjury, Colantonio et al
      • Colantonio A.
      • Ratcliff G.
      • Chase S.
      • Vernich L.
      Aging with traumatic brain injury: long-term health conditions.
      found that sleep problems continued to affect 27% of the sample.
      Although the body of literature examining sleep disturbance among adults with TBI has grown in recent years, the picture remains unclear and fragmented. The diversity of findings is evident in a survey of studies of disrupted sleep after TBI by Zeitzer et al,
      • Zeitzer J.M.
      • Friedman L.
      • O'Hara R.
      Insomnia in the context of traumatic brain injury.
      who reported prevalence rates ranging between 3% and 84%. Most studies have included small sample sizes, and those with larger sample sizes contain a wide range of injury severity and enrollment at many different times postinjury.
      • Ouellet M.C.
      • Savard J.
      • Morin C.M.
      Insomnia following traumatic brain injury: a review.
      The picture is further complicated by the various forms of sleep disturbance measured. Additionally, there is little consistency in the methods used to measure sleep disturbance; these have ranged from endorsement of a single item on a questionnaire to full polysomnographic assessment.
      • Ouellet M.C.
      • Savard J.
      • Morin C.M.
      Insomnia following traumatic brain injury: a review.
      There are multiple reasons to suspect that sleep disturbance in its various forms could be associated with poor functional status. Within the general population, the consequences of sleep disturbance can be severe, and even relatively short periods of sleep disturbance can potentially impair cognitive functioning, in particular, executive functions including decision-making and judgment of risk.
      • Harrison Y.
      • Horne J.A.
      The impact of sleep deprivation on decision making: a review.
      • Pilcher J.J.
      • Huffcutt A.J.
      Effects of sleep deprivation on performance: a meta-analysis.
      • Venkatraman V.
      • Chuah Y.
      • Huettel S.A.
      • Chee M.
      Sleep deprivation elevates expectation of gains and attenuates response to losses following risky decisions.
      Given the direct impact TBI can have on these functions, the potential of sleep disturbance, which can further compromise them, is of concern. Furthermore, disorders of sleep may be associated with various co-occurring conditions seen in individuals with TBI. For example, sleep deprived individuals experience greater levels of fatigue and sleepiness,
      • Vgontzas A.
      • Zoumakis E.
      • Bixler E.
      • et al.
      Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines.
      both conditions affecting a significant number of those with TBI.
      • Cantor J.B.
      • Ashman T.
      • Gordon W.
      • et al.
      Fatigue after traumatic brain injury and its impact on participation and quality of life.
      The direction of this relationship is unclear, because Ouellet et al
      • Ouellet M.C.
      • Savard J.
      • Morin C.M.
      Insomnia following traumatic brain injury: a review.
      have suggested that fatigue may not only result from sleep disturbance, but may actually contribute to long-term insomnia by encouraging irregular sleep habits. Chronic pain, a condition found in up to 76% of individuals up to 1 year after TBI, interferes with sleep.
      • Haack M.
      • Sanchez E.
      • Mullington J.M.
      Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers.
      • Lautenbacher S.
      • Kundermann B.
      • Krieg J.C.
      Sleep deprivation and pain perception.
      • Smith M.
      • Haythornthwaite J.
      How do sleep disturbance and chronic pain inter-relate? Insights from the longitudinal and cognitive-behavioral clinical trials literature.
      However, research has also indicated that sleep disturbance can exacerbate the experience of pain,
      • Smith M.
      • Edwards R.
      • McCann U.
      The effects of sleep deprivation on pain inhibition and spontaneous pain in women.
      • Roehrs T.
      • Hyde M.
      • Blaisdell B.
      • Greenwald M.
      • Roth T.
      Sleep loss and REM sleep loss are hyperalgesic.
      potentially creating a feedback loop. Depression has been more extensively studied with rates of depression as high as 53% within the first year after TBI.
      • Bombardier C.H.
      • Fann J.R.
      • Temkin N.R.
      • Esselman P.C.
      • Barber J.
      • Dikmen S.S.
      Rates of major depressive disorder and clinical outcomes following traumatic brain injury.
      Results of studies done to examine the relationship between depression and sleep suggest that sleep disturbance may be both a consequence and an exacerbating factor of depression.
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      • Shekleton J.A.
      • Parcell D.L.
      • Redman J.R.
      • Phipps-Nelson J.
      • Ponsford J.L.
      • Rajaratnam S.M.
      Sleep disturbance and melatonin levels following traumatic brain injury.
      • Parcell D.L.
      • Ponsford J.L.
      • Rajaratnam S.M.
      • Redman J.R.
      Self-reported changes to nighttime sleep after traumatic brain injury.
      Anxiety has been found to frequently co-occur with TBI, with rates as high as 28%.
      • Ashman T.A.
      • Spielman L.A.
      • Hibbard M.R.
      • Silver J.M.
      • Chandna T.
      • Gordon W.A.
      Psychiatric challenges in the first 6 years after traumatic brain injury: cross-sequential analyses of axis I disorders.
      The relationship between many of these conditions and sleep has not been well studied in individuals with TBI, and most of the studies conducted have had relatively small sample sizes.
      The goals of the current study were to examine sleep difficulties in individuals with TBI compared with a healthy comparison group, and to examine the relationship between sleep difficulties and common co-occurring disorders including depression, anxiety, and pain at 1 year postinjury. Our sample included adults with TBI enrolled at the time of acute rehabilitation care and longitudinally followed and tested at 1 year after injury. In addition, we examined the relationship between sleep problems and functional status at 1 year after injury.

      Methods

      Participants

      Participants were a subset of individuals with a TBI, who were recruited from consecutive admissions to a single inpatient rehabilitation unit and were enrolled into the Traumatic Brain Injury Model Systems (TBIMS) and followed at 1 year after injury. The TBIMS is a longitudinal database and research program sponsored by the National Institute on Disability and Rehabilitation Research. Inclusion criteria were the same as for the TBIMS: (1) a diagnosis of TBI with at least 1 of the following: Glasgow Coma Scale (GCS) score <13 on emergency department admission not due to intubation, sedation, or intoxication; loss of consciousness >30 minutes; posttraumatic amnesia >24 hours; or intracranial abnormality on neuroimaging; (2) at least 16 years of age; (3) arrival to the system's acute hospital within 72 hours of acute injury; and (4) received both acute medical and rehabilitation care within the same system. Over 90% of eligible subjects with TBI admitted to rehabilitation consented to participate in the TBIMS. Of the 174 individuals who were consecutively enrolled between August 2004 and October 2007, a total of 157 (90%) were followed at 1 year after injury. In addition to assessments specific to the TBIMS, additional questionnaires were given to assess sleep and mood. For this study, we examined the 129 who completed the Pittsburgh Sleep Quality Index (PSQI)
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      at their scheduled 1-year follow-up. A comparison of the 129 who completed the PSQI with the 45 who were enrolled but did not complete the measure showed no difference on age, sex, cause of injury, or injury severity. The 2 groups did differ significantly on race such that those who were not followed had fewer individuals who endorsed being white (64% vs 84%, P<.001). The primary reason that participants did not complete this measure was insufficient time for administration during telephone follow-up. The TBIMS study and the additional measures were approved by the Human Subjects Division of the University of Washington.

      Measures

      Demographic and injury data

      Data were gathered through medical chart review and interviews conducted with the subject or their family and included age, sex, race/ethnicity (white, black, Asian/Pacific Islander, Native American, and Hispanic), cause of injury (vehicular, violence, sports, fall, pedestrian, and other), and GCS score
      • Wilson J.T.
      • Pettigrew L.E.
      • Teasdale G.M.
      Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use.
      at admission to the hospital.

      Sleep disturbance

      Sleep disturbance was measured by the PSQI.
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      This is a 19-item questionnaire, which yields scores for 7 components of sleep (subjective sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of sleep medication, and daytime dysfunction), each of which has a range of 0 to 3, with higher scores indicating more problematic sleep. These scores can be summed to produce a global score that has a range of 0 to 21. The PSQI's global score has been shown to differentiate between good sleepers (≤5) and poor sleepers (>5) in the general population,
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      and the PSQI has been validated in patients with TBI.
      • Fichtenberg N.
      • Putnam S.
      • Mann N.
      • Zafonte R.
      • Millard A.
      Insomnia screening in postacute traumatic brain injury—utility and validity of the Pittsburgh Sleep Quality Index.

      Co-Occurring Conditions

      Depression was measured with the Patient Health Questionnaire-9 (PHQ-9).
      • Kroenke K.
      • Spitzer R.L.
      • Williams J.B.
      The PHQ-9: validity of a brief depression severity measure.
      Total scores on this 9-item module indicate the presence and severity of depressive symptoms. A total score ≥10 strongly suggests a clinically significant depressive episode.
      • Kroenke K.
      • Spitzer R.L.
      • Williams J.B.
      The PHQ-9: validity of a brief depression severity measure.
      The PHQ-9 is used frequently in assessment of individuals with TBI,
      • Bombardier C.H.
      • Fann J.R.
      • Temkin N.R.
      • Esselman P.C.
      • Barber J.
      • Dikmen S.S.
      Rates of major depressive disorder and clinical outcomes following traumatic brain injury.
      • Harch P.
      • Andrews S.R.
      • Fogarty E.
      • et al.
      A phase I study of low pressure hyperbaric oxygen therapy for blast-induced post concussion syndrome and post traumatic stress disorder.
      • Hart T.
      • Brenner L.
      • Clark A.N.
      • et al.
      Major and minor depression after traumatic brain injury.
      and is currently part of the National Institute on Disability and Rehabilitation Research-funded TBIMS National Database. Anxiety was measured by the Generalized Anxiety Disorder-7 Scale (GAD-7).
      • Spitzer R.L.
      • Kroenke K.
      • Williams J.B.
      • Lowe B.
      A brief measure for assessing generalized anxiety disorder.
      Scores on this 7-item measure range from 0 to 21, with a score of 10 or higher indicating anxiety. Pain scores were based on participant report of the average intensity of their overall pain during the past week. This average is reported on an analog scale ranging from 0 (no pain) to 10 (pain as bad as can be). The 0 to 10 numerical rating scale has consistently shown its validity as a measure of pain intensity through its strong association with other measures of pain intensity, as well as its sensitivity to detect changes in pain associated with pain treatments.
      • Jensen M.
      • Karoly P.
      Self-report scales and procedures for assessing pain in adults.

      Functional Status Measures

      Disability Rating Scale (DRS)
      • Rappaport M.
      • Hall K.M.
      • Hopkins K.
      • Belleza T.
      • Cope D.N.
      Disability rating scale for severe head trauma: coma to community.
      scores were used to measure functional outcomes and have been collected as part of the TBIMS National Database since 1994. Scores on this measure range from 0 to 29, with higher scores indicating a greater degree of functional impairment. This is not a true interval measure, and its sensitivity decreases at the lower end of the scale.
      • Wright J.
      The Disability Rating Scale The Center for Outcome Measurement in Brain Injury.
      It has been shown to have good interrater reliability and validity in individuals with TBI.
      • Rappaport M.
      • Hall K.M.
      • Hopkins K.
      • Belleza T.
      • Cope D.N.
      Disability rating scale for severe head trauma: coma to community.
      Scores on the FIM
      • Hamilton B.B.
      • Granger C.V.
      • Sherwin F.S.
      • Zielezny M.
      • Tashman J.S.
      Uniform national data system for medical rehabilitation.
      were also used to indicate subjects' functional outcomes. This measure includes items assessing both physical and cognitive abilities, and is widely used in rehabilitation. Total scores range from 18 to 126, with lower scores indicating a greater level of care needed for the individual. Life satisfaction, a third outcome, was measured using the Satisfaction With Life Scale (SWLS).
      • Diener E.
      • Emmons R.A.
      • Larsen R.J.
      The Satisfaction With Life Scale.
      Total scores on this 5-item measure range from 5 to 35, with higher scores indicating a greater degree of life satisfaction. This measure has been found to have good reliability and construct validity.
      • Corrigan J.
      Satisfaction With Life Scale.

      Statistical Analyses

      Simple descriptive statistics were used to describe the population. Mann-Whitney U tests and Fisher exact tests were used to compare those with TBI with and without sleep disturbance on demographics, co-occurring disorders, and functional status. Independent sample t tests were used to compare the study population with the results from Buysse et al.
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      Buysse presented mean and SDs on all subscale and global scores for 52 healthy individuals without identified sleep disorders. The 52 healthy comparison subjects included 40 men and 12 women with an average age of 59.9 years (range, 24–83y). Correlations were calculated among the global sleep score and the measures of co-occurring conditions, in order to further examine the relationship among these variables. Independent sample t tests compared those with and without co-occurring conditions with each other and with the healthy comparison subjects. Given the number of comparisons conducted, P<.001 was considered significant. All other P values between .05 and .001 were considered potential trends.

      Results

      Demographics and Injury Data

      Demographic and injury data collected during inpatient rehabilitation are included in table 1.
      Table 1Demographic and Injury Data Comparison for Those With and Without Disordered Sleep
      MeasureOverall (n=129)PSQI ≤5 (n=72)PSQI >5 (n=57)P
      Demographic and injury variables
       Age (mean [SD])37.1 (15.4)37.6 (16.7)36.5 (13.9).694
       Male (sample size [%])100 (78)58 (81)42 (74).399
      Indicates values are from the Fisher exact test.
       White (sample size [%])107 (84)64 (89)43 (75)<.001
      Indicates values are from the Fisher exact test.
       Cause.301
      Indicates values are from the Fisher exact test.
        Vehicular (sample size [%])70 (55)43 (60)27 (47)
        Fall/objects (sample size [%])33 (26)18 (25)15 (26)
        Other (sample size [%])25 (20)11 (15)14 (25)
       Admission GCS (mean [SD])9.7 (4.5)9.2 (4.7)10.3 (4.1).293
       FIM at discharge (mean [SD])103 (15)102 (15)107 (13).136
      Co-occurring disorders at year 1
       PHQ-9 (mean [SD])6.1 (6.2)2.8 (3.3)10.2 (6.6)<.001
       GAD-7 (mean [SD])3.3 (4.3)1.2 (2.2)6.0 (4.8)<.001
       Pain average (mean [SD])2.8 (2.6)1.6 (1.7)4.3 (2.8)<.001
      Outcomes at year 1
       DRS (mean [SD])1.5 (1.4)1.3 (1.5)1.9 (1.2)<.001
       Satisfaction with life (mean [SD])20.6 (8.3)23.8 (7.1)16.5 (8.1)<.001
       FIM (mean [SD])115 (10)118 (10)113 (10)<.001
      NOTE. P values are from the Mann-Whitney U test, unless otherwise noted.
      low asterisk Indicates values are from the Fisher exact test.

      Differences Between Individuals With and Without Sleep Disturbance

      Table 1 also contains comparisons between participants with and without sleep disturbance. At 1 year after TBI, 44% of the participants had global PSQI scores greater than 5, indicating the presence of a clinically significant sleep disturbance.
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      Those participants who were classified as poor sleepers were more likely to be nonwhite and have significant levels of depression, anxiety, or pain. In addition, they also had significantly worse scores on all 3 functional status measures (FIM, DRS, and SWLS).

      Sleep Disturbance at 1 Year After TBI

      Mean scores for each of the sleep components and the global score of the PSQI are shown in table 2. The mean global score was 5.54, which indicates a significant sleep problem. Significant differences between the current sample and the healthy comparison group were found in 4 of the 7 sleep components measured by the PSQI, as well as for the global scores. Specifically, participants with TBI took significantly longer to fall asleep (sleep latency), used more sleep medications (medication use), and reported worse effects on daytime functioning (daytime dysfunction) compared with the healthy comparison group. The participants rated the overall quality of their sleep (subjective sleep quality) lower than the comparison group in the Buysse et al study.
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      There was a trend toward those with TBI reporting sleep more disturbed by awakening during the night, respiratory problems, pain, or being too hot or too cold than the healthy comparison group. No significant differences were found in number of hours slept (sleep duration) and the ratio of hours slept to hours spent in bed (habitual sleep efficiency).
      Table 2Comparison of PSQI for TBI and Healthy Group
      P<.01;
      Sleep ComponentsTBIHealthy Comparison
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      t test
      nMean ± SDnMean ± SD
      Sleep quality1300.83 ± 0.86520.35 ± 0.483.78
      P<.001;
      Latency1241.32 ± 1.14520.56 ± 0.734.46
      P<.001;
      Duration1290.43 ± 0.78520.29 ± 0.501.23
      Efficiency1260.29 ± 0.70520.10 ± 0.301.91
      Disturbances1251.23 ± 0.71521.00 ± 0.402.22
      P<.05.
      Medication use1300.55 ± 1.09520.04 ± 0.283.34
      P<.001;
      Daytime dysfunction1290.74 ± 0.77520.35 ± 0.483.38
      P<.001;
      Global score1155.54 ± 3.94522.67 ± 1.705.04
      P<.001;
      low asterisk P<.01;
      P<.001;
      P<.05.

      Association of Sleep Disturbance With Co-Occurring Conditions

      In this sample, global sleep scores, depression, anxiety, and pain were all highly correlated (r=.72, .39, and .56 between sleep and depression, anxiety, and pain, respectively; P≤.001 for each). In order to better understand the relationship between sleep and these co-occurring conditions, the sample was divided into groups based on co-occurring conditions: no co-occurring conditions (n=79), a single co-occurring condition (anxiety n=1, depression n=6, pain n=13), and 2 or more co-occurring conditions (depression and pain, n=6; n of other 2 pairings was 0, all 3 n=16). Nine participants with missing data on 1 or more variables were not included in this analysis. Total PSQI scores for each of the groups represented within the sample are depicted in figure 1. Those participants with 2 or 3 co-occurring conditions reported the worst sleep.
      Figure thumbnail gr1
      Fig 1Global sleep problems by number of co-occurring conditions.
      A series of independent sample t tests were conducted comparing subjects with 1 or more of the co-occurring disorders with subjects without any of these disorders (table 3). These 2 groups differed significantly on 5 of the dimensions (latency, disturbance, daytime dysfunction, quality, and medication use), as well as the global score, with a trend toward difference in duration.
      Table 3Sleep Dimensions by Co-Occurring Disorder
      Sleep ComponentsTBI With 1 or More Co-Occurring Conditions (n=42)TBI With No Co-Occurring Condition (n=79)Healthy Comparison Group
      • Ashman T.A.
      • Spielman L.A.
      • Hibbard M.R.
      • Silver J.M.
      • Chandna T.
      • Gordon W.A.
      Psychiatric challenges in the first 6 years after traumatic brain injury: cross-sequential analyses of axis I disorders.
      (n=52)
      t Test (TBI with vs without co-occurring condition)t Test (TBI with co-occurring condition vs healthy comparison)t Test (TBI without co-occurring condition vs healthy comparison)
      Sleep quality1.4 (0.9)0.5 (0.6)0.35 (0.48)6.57
      P<.001;
      7.24
      P<.001;
      1.51
      Latency2.0 (1.1)1.0 (1.0)0.56 (0.73)5.06
      P<.001;
      7.60
      P<.001;
      2.73
      P<.01;
      Duration0.8 (1.1)0.4 (0.7)0.29 (0.50)2.44
      P<.05.
      2.99
      P<.01;
      0.98
      Efficiency0.7 (1.1)0.4 (0.9)0.10 (0.30)1.613.77
      P<.001;
      2.32
      P<.05.
      Disturbance1.5 (0.8)0.9 (0.5)1.00 (0.40)5.07
      P<.001;
      3.94
      P<.001;
      1.21
      Medication use1.1 (1.3)0.3 (0.8)0.04 (0.28)4.19
      P<.001;
      5.72
      P<.001;
      2.25
      P<.05.
      Daytime dysfunction1.3 (0.8)0.5 (0.6)0.35 (0.48)6.20
      P<.001;
      7.13
      P<.001;
      1.51
      Global score8.9 (3.9)3.8 (2.6)2.67 (1.70)8.59
      P<.001;
      10.37
      P<.001;
      2.77
      P<.01;
      NOTE. Values are mean (SD) or as otherwise indicated.
      low asterisk P<.001;
      P<.01;
      P<.05.
      We then compared each of these groups with the healthy comparison group reported by Buysse.
      • Buysse D.
      • Reynolds C.
      • Monk T.
      • Berman S.
      • Kupfer D.
      The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
      The differences between subjects with 1 or more co-occurring conditions and the healthy comparison group were significant (P<.001) on 6 of the dimensions. Those subjects with TBI and no co-occurring disorders had trends toward differences from the healthy comparison group on 3 dimensions (latency, habitual efficiency, and medication use), as well as the global score.

      Discussion

      The results of this study indicate that individuals with TBI have significantly more problems with sleep than previously published data on healthy individuals, a finding that is consistent with existing literature.
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Orff H.J.
      • Ayalon L.
      • Drummond S.P.
      Traumatic brain injury and sleep disturbance: a review of current research.
      • Ouellet M.C.
      • Savard J.
      • Morin C.M.
      Insomnia following traumatic brain injury: a review.
      • Zeitzer J.M.
      • Friedman L.
      • O'Hara R.
      Insomnia in the context of traumatic brain injury.
      Of the 7 components of sleep measured by the PSQI, those with TBI indicated worse functioning on 4 (sleep quality, latency, sleep medication use, and daytime dysfunction), as well as on the global score. Sleep problems were most pronounced among those subjects who reported significant levels of pain, depression, or anxiety, with the highest scores on the PSQI reported by those individuals who reported a combination of 2 or more of these conditions. There were no significant differences found between those subjects with TBI who had no co-occurring conditions and the healthy comparison group, but trends were observed for sleep latency, sleep efficiency, medication use, and the global score. Additionally, the functional status of individuals with and without sleep disturbance were significantly different, with those reporting sleep problems describing more functional limitations, higher reliance on others, and diminished satisfaction with their quality of life. Given that the healthy sample was older, which may increase the likelihood of sleep problems, the level of sleep disturbance in those with TBI may be underestimated. While we were unable to determine whether there is any causal link between these outcomes and sleep, the outcomes do suggest the need to address sleep difficulties, which may impact function.
      Five other studies have examined sleep disturbances in TBI
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Cantor J.B.
      • Ashman T.
      • Gordon W.
      • et al.
      Fatigue after traumatic brain injury and its impact on participation and quality of life.
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      • Fichtenberg N.
      • Zafonte R.
      • Putnam S.
      • Mann N.
      • Millard A.
      Insomnia in a post-acute brain injury sample.
      • Mahmood O.
      • Rapport L.J.
      • Hanks R.A.
      • Fichtenberg N.L.
      Neuropsychological performance and sleep disturbance following traumatic brain injury.
      and association between sleep disorders and co-occurring conditions using the PSQI.
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      Our results, consistent with prior work,
      • Fichtenberg N.
      • Zafonte R.
      • Putnam S.
      • Mann N.
      • Millard A.
      Insomnia in a post-acute brain injury sample.
      suggest that approximately 42% to 44% of those with TBI have sleep disturbance. However, a number of studies have reported higher rates,
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Cantor J.B.
      • Ashman T.
      • Gordon W.
      • et al.
      Fatigue after traumatic brain injury and its impact on participation and quality of life.
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      which are likely related to the samples studied. Our sample was limited to individuals who were admitted for rehabilitation services. However, by prospectively examining a group enrolled shortly after injury, we avoided the bias created by enrolling individuals presenting to outpatient clinics,
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Fichtenberg N.
      • Zafonte R.
      • Putnam S.
      • Mann N.
      • Millard A.
      Insomnia in a post-acute brain injury sample.
      • Mahmood O.
      • Rapport L.J.
      • Hanks R.A.
      • Fichtenberg N.L.
      Neuropsychological performance and sleep disturbance following traumatic brain injury.
      which includes those seeking follow-up care and may indicate more complicated recoveries. In addition, previous samples also varied with respect to severity and time from injury.
      • Englander J.
      • Bushnik T.
      • Oggins J.
      • Katznelson L.
      Fatigue after traumatic brain injury: association with neuroendocrine, sleep, depression and other factors.
      • Cantor J.B.
      • Ashman T.
      • Gordon W.
      • et al.
      Fatigue after traumatic brain injury and its impact on participation and quality of life.
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      Our study reports on the nature of the sleep difficulties (eg, sleep quality, latency, duration), which prior studies using the PSQI did not. Given the highly variable nature of sleep disturbances, this information provides clues for tailoring interventions to address the individual's specific sleep problem. The results of the current study also extend the work of Rao et al,
      • Rao V.
      • Spiro J.
      • Vaishnavi S.
      • et al.
      Prevalence and types of sleep disturbances acutely after traumatic brain injury.
      who found early difficulties in individuals with TBI in sleep initiation, maintenance, and quality, all of which we found at 1 year after injury. These findings suggest that the sleep difficulties are not temporary problems from which the person with TBI recovers. The ability to identify specific types of sleep difficulties may assist with more specific and effective treatment.
      Our results highlight the importance of evaluating the sleep quality of individuals with TBI. Similar to prior research, which has shown associations between chronic pain,
      • Haack M.
      • Sanchez E.
      • Mullington J.M.
      Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers.
      • Lautenbacher S.
      • Kundermann B.
      • Krieg J.C.
      Sleep deprivation and pain perception.
      • Smith M.T.
      • Haythornthwaite J.A.
      How do sleep disturbance and chronic pain inter-relate? Insights from the longitudinal and cognitive-behavioral clinical trials literature.
      depression, and sleep,
      • Parcell D.L.
      • Ponsford J.L.
      • Redman J.R.
      • Rajaratnam S.M.
      Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study.
      • Shekleton J.A.
      • Parcell D.L.
      • Redman J.R.
      • Phipps-Nelson J.
      • Ponsford J.L.
      • Rajaratnam S.M.
      Sleep disturbance and melatonin levels following traumatic brain injury.
      • Parcell D.L.
      • Ponsford J.L.
      • Rajaratnam S.M.
      • Redman J.R.
      Self-reported changes to nighttime sleep after traumatic brain injury.
      we also found that participants with 1 or more of these conditions had more difficulties with sleep. The strong relationship that was found between sleep disturbances and commonly co-occurring psychological disorders is interesting and raises the question of causal direction. Does the sleep disorder cause or contribute to mental health disorders? Do problems with mental health disrupt sleep? Or is there a reciprocal effect of each? These results indicate the need for not only comprehensive early evaluation to detect such conditions, but additional research to better understand the interactions of these conditions with each other and with sleep, which are likely to have implications with respect to the development of interventions and the ultimate success of those interventions.

      Study Limitations

      We did not measure sleep characteristics or parameters during inpatient rehabilitation early after injury. While no studies specifically address the association of sleep and functional outcomes during hospitalization after TBI, it is the observation of most clinicians that sleep disturbances are extremely common and associated with early behavioral disturbances and poorer cognitive functioning. It is interesting that poor sleepers have significantly worse function even at 1 year after injury. While we were able to consecutively enroll patients from inpatient rehabilitation, our results are limited, because we did not include those with TBI who were not admitted for rehabilitation. Future studies should examine sleep disturbances in more representative cases, as well as examine the predictive value of early sleep disturbances on later functioning and the development of mental health disorders.
      Although a significant difference was found between racial/ethnic groups in this study, this finding should be interpreted with caution, because the nonwhite groups were very small. It is also difficult to know the precise purpose for which medications were given to this group. Antidepressants and even neuroleptics are often used to treat sleep complaints as well as mental health disorders in this population.
      The data gathered through the PSQI are not detailed enough to allow differential diagnosis of sleep disorders. Also, the PSQI relies on self-report of sleep, and, like all self-report measures, is susceptible to inaccuracies because of poor recall or incorrect attribution. Polysomnographic studies have had conflicting results to date on whether self-reports actually correlate with sleep architecture disturbances.
      • Baker F.C.
      • Maloney S.
      • Driver H.S.
      A comparison of subjective estimates of sleep with objective polysomnographic data in healthy men and women.
      None of these studies to date have examined the presence of co-occurring disorders in the context of TBI. Ideally, improved means of documenting physiologic sleep parameters in a naturalistic setting will be available in the future to augment self-report, allowing for better understanding of the perception of sleep and the interaction with other disorders.
      The evaluation of sleep in a clinical setting should not only involve the use of validated sleep measures, which will improve the identification of sleep disorder types (eg, differentiating sleep latency disorders from circadian rhythm disturbances), but should also routinely include evaluations for commonly co-occurring mental health disorders and painful conditions. This might allow for more precise diagnosis and a more parsimonious use of medications, which may have potential detrimental effects on daytime cognitive functioning. A more detailed knowledge of the sleep disorder type would also enable the selection of appropriate nonpharmacologic treatments. For example, cognitive behavioral therapy has been shown to be effective in the treatment of insomnia
      • Espie C.A.
      • Inglis S.J.
      • Tessier S.
      • Harvey L.
      The clinical effectiveness of cognitive behaviour therapy for chronic insomnia: implementation and evaluation of a sleep clinic in general medical practice.
      and has been adapted successfully for use in TBI.
      • Ouellet M.C.
      • Morin C.M.
      Cognitive behavioral therapy for insomnia associated with traumatic brain injury: a single-case study.
      • Ouellet M.C.
      • Morin C.M.
      Efficacy of cognitive-behavioral therapy for insomnia associated with traumatic brain injury: a single-case experimental design.
      Other nonpharmacologic sleep treatments include behavioral therapy, phototherapy, and chronotherapy.
      • Rao V.
      • Rollings P.
      Sleep disturbances following traumatic brain injury.
      In addition, given the relationship between sleep difficulties and functional outcomes, it will be important for clinicians to consider sleep as a possible factor in any decline of function over time.

      Conclusions

      This study has demonstrated the common occurrence of sleep complaints in those with TBI, and the association of these complaints with other disorders such as depression, anxiety, and pain syndromes in people with TBI. Future studies are necessary to determine the causal relationships among these co-occurring disorders, their differential relationship with functional status, and response to treatment.

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