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Volume 14 No. 06
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Scientific Investigations

The Differential Effects of Regular Shift Work and Obstructive Sleep Apnea on Sleepiness, Mood and Neurocognitive Function

Jennifer M. Cori, PhD1; Melinda L. Jackson, PhD1,2; Maree Barnes, MBBS1,3; Justine Westlake, BA/BAppSci (Hons)1; Paul Emerson, BSocSc1; Jacen Lee, DPsych1,4; Rosa Galante, DPsych1,5; Amie Hayley, PhD1,6,7; Nicholas Wilsmore, MBBS (Hons)1,8; Gerard A. Kennedy, PhD1,2; Mark Howard, MBBS, PhD1,3
1Institute for Breathing and Sleep and Austin Health, Heidelberg, Victoria, Australia; 2School of Health & Biomedical Sciences, RMIT University, Bundoora, Victoria, Australia; 3Department of Medicine, University of Melbourne, Parkville, Victoria, Australia; 4Hong Kong Clinical Neuropsychology Service, Hong Kong SAR, China; 5Department of Psychology, Victoria University, St. Albans, Victoria, Australia; 6Centre for Human Psychopharmacology, Faculty of Health Arts and Design, Swinburne University of Technology, Hawthorn, Victoria, Australia; 7School of Clinical Sciences at Monash Health, Faculty of Medicine Nursing and Health Sciences, Monash University, Clayton, Victoria, Australia; 8Department of Respiratory and Sleep Medicine, Eastern Health, Melbourne, Victoria, Australia

ABSTRACT

Study Objectives:

To assess whether poor sleep quality experienced by regular shift workers and individuals with obstructive sleep apnea (OSA) affects neurobehavioral function similarly, or whether the different etiologies have distinct patterns of impairment.

Methods:

Thirty-seven shift workers (> 24 hours after their last shift), 36 untreated patients with OSA, and 39 healthy controls underwent assessment of sleepiness (Epworth Sleepiness Scale [ESS]), mood (Beck Depression Index, State Trait Anxiety Inventory [STAI], Profile of Mood States), vigilance (Psychomotor Vigilance Task [PVT], Oxford Sleep Resistance Test [OSLER], driving simulation), neurocognitive function (Logical Memory, Trails Making Task, Digit Span Task, Victoria Stroop Test) and polysomnography.

Results:

Sleepiness (ESS score; median, interquartile range) did not differ between the OSA (10.5, 6.3–14) and shift work (7, 5–11.5) groups, but both had significantly elevated scores relative to the control group (5, 3–6). State anxiety (STAI-S) was the only mood variable that differed significantly between the OSA (35, 29–43) and shift work (30, 24–33.5) groups, however both demonstrated several mood deficits relative to the control group. The shift work and control groups performed similarly on neurobehavioral tasks (simulated driving, PVT, OSLER and neurocognitive tests), whereas the OSA group performed worse. On the PVT, lapses were significantly greater for the OSA group (3, 2–6) than both the shift work (2, 0–3.5) and control (1, 0–4) groups.

Conclusions:

Shift workers and patients with OSA had similar sleepiness and mood deficits relative to healthy individuals. However, only the patients with OSA showed deficits on vigilance and neurocognitive function relative to healthy individuals. These findings suggest that distinct causes of sleep disturbance likely result in different patterns of neurobehavioral dysfunction.

Citation:

Cori JM, Jackson ML, Barnes M, Westlake J, Emerson P, Lee J, Galante R, Hayley A, Wilsmore N, Kennedy GA, Howard M. The differential effects of regular shift work and obstructive sleep apnea on sleepiness, mood and neurocognitive function. J Clin Sleep Med. 2018;14(6):941–951.


BRIEF SUMMARY

Current Knowledge/Study Rationale: Shift work and obstructive sleep apnea (OSA) both impair sleep quality and quantity. Although similar symptomology has been described for shift work and OSA, their effect on sleepiness, mood, vigilance, and neurocognitive function has not been directly compared.

Study Impact: Patients with OSA had sleepiness and mood similar to that of regular shift workers but performed significantly worse on vigilance and neurocognitive measures. These findings suggest that the facets of sleepiness, mood, vigilance, and neurocognitive function are not uniformly affected by poor quality sleep, and that specific impairments across these domains are likely dependent on the nature of the underlying sleep disturbance.

INTRODUCTION

Regular, good-quality sleep of 7 to 9 h/night is recommended for optimal health.1 Insufficient and/or poor-quality sleep is associated with excessive daytime sleepiness, physical and psychological illness, decreased neurocognitive performance, and increased risk for occupational and motor vehicle accidents.25 The adverse effects of insufficient and/or poor-quality sleep have been widely reported in two distinct populations with different causal mechanisms, shift workers and individuals with obstructive sleep apnea (OSA). Despite similar symptomology, these groups have not been directly compared and thus it is not known whether the differing pathophysiology results in distinct patterns of neurobehavioral impairment.

Sleep impairment in shift workers is primarily the result of circadian rhythm misalignment with the daily cycles of light and dark. Shift workers often work when the circadian rhythms promote sleep, and attempt sleep during the day when the circadian rhythms promote wakefulness. During these daytime sleep periods, shift workers may experience difficulty initiating and maintaining sleep, resulting in both reduced sleep quality and quantity.6,7

Sleep impairment in patients with OSA is a consequence of repeated episodes of upper airway collapse during sleep. During upper airway collapse, there is a reduction or cessation in airflow that results in hypoxia and hypercapnia. Upper airway patency is generally restored with an arousal from sleep; however, upon return to sleep further upper airway collapse typically occurs. Thus, sleep in OSA is highly fragmented and may include intermittent hypoxemia/reoxygenation, both of which are considered responsible for the adverse consequences of OSA.4,8

Excessive sleepiness is a common consequence of poor quality sleep, and is reported in approximately 30% of patients with OSA (Epworth Sleepiness Scale [ESS] score > 11),9 and in approximately 35% of rotating shift workers and approximately 45% of night shift workers (ESS score ≥ 10).10 Increased risk for motor vehicle accidents is also common in these groups, with patients with OSA 1.2–4.9 times more likely to have an accident.4 Among motor vehicle crash survivors, shift work is the most common sleep-related factor associated with crash occurrence.11 In regard to neurocognitive function, OSA has been associated with attention, memory, and executive function impairments,8,12,13 with similar findings demonstrated in shift workers immediately following night shift,14 where acute sleep deprivation is the likely catalyst for poor performance. However, long-term neurocognitive deficits have also been reported for shift workers in respect to general cognitive function, attention, immediate memory, and cognitive speed.15,16 Disturbed mood is also common in both groups, with depression and anxiety prevalence higher in patients with OSA than in healthy individuals.17,18 For shift workers, depressed mood symptoms are elevated compared to regular day workers.19,20

In summary, the consequences of poor-quality sleep appear to overlap in patients with OSA and shift workers. This study aimed to determine whether these consequences are indeed similar or distinct, by directly comparing regular shift workers to patients with untreated OSA. To minimize the acute effects of sleep restriction, shift workers had at least 24 hours recovery from their last night shift, so that the chronic effects of shift work could be examined. It was hypothesized that both the shift worker and OSA groups would experience excessive sleepiness and deficits in mood, vigilance, and neurocognitive function relative to a healthy control group.

METHODS

Participants

A total of 112 participants were recruited to three groups; shift workers (n = 37), patients with OSA (n = 36), and healthy controls (n = 39). The shift work and control participants were recruited via newspapers, newsletters, and trade union publications. Patients with OSA were recruited via the Austin Health Sleep Laboratory Clinic.

General inclusion criteria were age 18 through 65 years, a current Australian driver's license and fluency in English. Exclusion criteria were visual acuity impairments (not corrected by glasses), respiratory disorders (other than OSA), chronic medical comorbidities (including neurological and psychiatric disorders), and regular sedative use.

Shift work participant specific inclusion criteria were employment in regular rotating shifts (day, afternoon, and night) on a weekly basis for the previous 3 months, with no more than 4 days recovery between shift types. Permanent night shift workers were eligible if, on nonworking days, they engaged in activities during daytime hours as this was considered to disrupt circadian sleep-wake patterns similar to rotating shifts. Further shift work specific inclusion criteria was a score ≤ 0.5 on the Multivariate Apnea Prediction Index (MAPI)21 to ensure low probability of OSA.

OSA participant specific inclusion criterion was untreated, previously diagnosed moderate to severe OSA as defined by an apnea hypopnea index (AHI) ≥ 15 events/h.

Healthy control participant specific inclusion criteria were a MAPI score ≤ 0.5 and an ESS score < 10 to ensure normal sleepiness. Healthy control specific exclusion criteria were rotating or night shift work.

Participants provided written informed consent. The study was approved by the Austin Health Research Ethics Committee.

Procedure

Participants attended the sleep laboratory at 1:00 pm for a single session of neurobehavioral testing. On the day of testing participants were instructed to avoid caffeine, stimulant medication, and alcohol. For shift workers, the testing was at least 24 hours following their last shift. Upon arrival they completed a general demographics and driving questionnaire, as well as the MAPI and ESS (see Figure 1 for a schematic of study protocol). Following the questionnaires, if eligible, the participants practiced the driving simulator task before completing an approximate 3.5-hour test battery, which comprised the following tasks in this order: Wechsler Memory Scales III Logical Memory I (LM I), Trail Making Test (TMT), Digit Span Forward (DSF), Digit Span Backward (DSB), Victoria Stroop Test (VST), Beck Depression Inventory (BDI), Profile of Mood States-short form (POMSSF), State Trait Anxiety Inventory (STAI), Wechsler Memory Scales III Logical Memory II (LM II), Oxford Sleep Resistance Test (OSLER 1 - 40 minutes), AusEd driving simulation task (30 minutes), Psychomotor Vigilance Task (PVT - 10 minutes), and a second Oxford Sleep Resistance Test (OSLER 2 - 40 minutes). On the night of testing, all shift work and healthy control participants underwent an ambulatory, in-home polysomnography (PSG). The patients with OSA underwent a clinical in-laboratory diagnostic PSG, prior to the current study; hence, AHI and sleep parameters were already known and PSG was not repeated in this group. In-laboratory and ambulatory PSG measures included electroencephalography (C4-A1), electrooculography (left-right), submental electromyography, anterior tibialis piezo movement sensors, electrocardiography, nasal pressure using a cannula, naso-oral airflow using a thermistor, respiratory effort using chest and abdomen piezoelectric bands, body position, heart rate, and oxygen saturation using pulse oximetry. Ambulatory recordings were via Compumedics Somte (Abbottsford, Victoria, Australia) and in-laboratory recordings were via Compumedics E-series (Abbottsford, Victoria, Australia). Sleep and arousals were staged and scored according to standard laboratory procedures.22,23 Respiratory events were scored according to the criteria published by the American Academy of Sleep Medicine.24

Schematic of study protocol.

Recruitment criteria and study protocol for the OSA, shift work, and control groups. All groups completed the neurobehavioral testing but only the shift work and control groups completed the overnight ambulatory polysomnography. AHI = apnea-hypopnea index, BDI = Beck Depression Index, DSB = Digit Span Backward, DSF = Digit Span Forward, ESS = Epworth Sleepiness Scale, LM I = Logical Memory I, LM II = Logical Memory II, MAPI = Multivariate Apnea Prediction Index, OSA = obstructive sleep apnea, OSLER = Oxford Sleepiness Resistance Test, POMS-SF = Profile of Mood States-short form, PSG = polysomnography, PVT = Psychomotor Vigilance Task, STAI = State Trait Anxiety Inventory, VST = Victoria Stroop Test.

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Figure 1

Schematic of study protocol.

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Materials

Simulated Driving Performance

The AusEd task assessed simulated driving performance.25 Participants were seated at a computer, with a steering wheel and pedals for braking and acceleration. The 30-minute simulation comprised night driving on a two-lane country road with both straights and bends. Participants were instructed to maintain their speed between 60–80 kilometers per hour (km/h), stay in the middle of the left lane, and to brake immediately when a truck intermittently appeared in the lane ahead. To minimize learning effects participants underwent a 10-minute practice drive. The first 6 minutes of the actual drive were removed from the analysis. Lane deviations (cm), speed deviations (km/h), braking reaction times (ms), and crash occurrence (off-road and truck collisions) were assessed as they are sensitive to the effects of OSA and restricted sleep.25,26

Psychomotor Vigilance Task

A 10-minute PVT assessed reaction time and vigilance. The PVT is free of aptitude and learning effects and is sensitive to performance variation due to sleepiness.27 Median reaction time, the slowest 10% of reaction times, and number of lapses were recorded.

Neurocognitive Tests

Logical Memory: The LM I and LM II assessed immediate and delayed recall.28 For LM I, two short stories (A and B) were presented orally, with story B presented twice. Immediately following each story presentation, the participants had to retell the story. For LM II the participants had to retell story A and B following a 30-minute delay. Recall scores were out of 25 for each story; thus, the total scoring was out of 75 for LM I and 50 for LM II.

Trail Making Test: Participants were administered TMT to assess attention (Trail A) and executive function (Trail B).29 The trails comprised 25 numbered circles. For Trail A the participant had to connect the circles by drawing a continuous line in ascending order from 1 to 25. For Trail B the circles were numbered 1–13 and lettered A–L. The participants had to draw a continuous line in an ascending pattern alternating between the numbers and letters (ie, 1-A, 2-B, 3-C, etc.).

Digit Span Task: The DSF assessed attention and short-term memory whereas DSB assessed executive function.30 For DSF, the participants had to recall number sequences in their presentation order. Participants had two trials for each number sequence. A number was added to the sequence if it was correctly recalled. The task terminated when the participant reached 8 consecutive numbers sequences or they were unable to repeat a sequence two trials in a row. For the DSB the participant recalled the number sequences (maximum of 7) in backward order. Scores were out of 16 for DSF and 14 for DSB. DSF and DSB scores were combined to form the Digit Span Total (DST) scores of out 30.

The Victoria Stroop Test: The VST assessed selective attention and inhibitory control. The test consists of 3 cards. The first contains colored dots (card D). The second contains common words printed in colors (card W). The third contains color words (eg, red) that are incongruent with the color in which they are printed (card C). For each card, the participant must name the printed color (green, blue, yellow, red) moving from left to right as quickly as possible. To assess executive function the time taken to complete cards C and D was calculated (C/D).31

Mood Questionnaires

Mood questionnaires included the BDI,32 the STAI,33 and the POMS-SF.34

Objective Sleepiness/Alertness

The OSLER assessed ability to maintain wakefulness.35 The participant was seated upright in a quiet, dimly lit room and instructed to remain awake and respond on a portable hand-held device each time a dim light (1 second in duration) illuminated at 3-second intervals. The testing was terminated if the participant failed to respond to 7 consecutive illuminations, indicating sleep onset latency, otherwise the testing continued for 40 minutes. Participants completed two sessions; OSLER 1 commenced at approximately 2:00 pm and OSLER 2 at approximately 3:50 pm.

Ocular Measures

The Optalert Drowsiness Measurement System (ODMS) recorded ocular measures during the driving, PVT, and OSLER tasks. ODMS utilizes a lens-free glasses frame that contains a light-emitting diode, positioned in front of and just below the eye, that emits brief infrared pulses at 500 Hz.36 A phototransistor detects light that reflects off the eyeball and eyelid. ODMS parameters were averaged over 60-second epochs. The following ODMS parameters were analyzed as they have been shown to be sensitive to restricted sleep:

  1. Negative interevent duration (IED): time between maximum velocity of the eyelid closing to the maximum velocity of the eyelid reopening.

  2. Negative amplitude velocity ratio (AVR): ratio between the maximum amplitude to the maximum velocity for the eye reopening on all eye blinks. A larger ratio indicates slower eye reopening.

  3. % long eye closures: % of time where eyelid is completely shut for > 10 ms.

Statistical Analysis

Data were analyzed using IBM SPSS Statistics version 24.0 (IBM Corp., Armonk, New York, United States). Nonparametric Kruskal-Wallis and paired Dunn tests assessed group differences. A chi-square test of homogeneity was used with a pairwise Z-test of two proportions (Bonferroni corrected) where appropriate. Not all participants contributed to each analysis for reasons including equipment failure, task withdrawal, and the addition of the neurocognitive and OSLER tasks following study commencement. Result tables list the number of participants who contributed to each analysis.

RESULTS

The participants with OSA were older and more obese than the shift workers and the control group (Table 1). The ESS score did not significantly differ between the OSA and shift work groups, but both groups had elevated scores relative to the control group. The participants with OSA worked more days per week than the shift workers, but total hours worked per week did not differ between any of the groups. On their working days, those in the OSA and shift work groups slept fewer hours than those in the control group. On their nonworking days, the participants with OSA also slept less than those in the control group, but did not differ significantly from the shift workers.

Demographics.

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Table 1

Demographics.

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As expected, the OSA group was significantly different from the shift work and control groups with respect to AHI, arousal index, minimum oxygen desaturation (SpO2), and sleep efficiency (Table 2). There were no differences between the control and shift work groups with respect to the sleep variables.

Sleep parameters.

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Table 2

Sleep parameters.

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The OSA group had poorer performance on most of the vigilance and neurocognitive assessments relative to the other groups, whereas the shift work group was generally similar to the control group (Table 3). For driving performance, the participant groups did not differ with respect to lane deviations and braking reaction time (Table 3). However, for speed deviations outside the 60- to 80-km zone and number of crashes, the OSA group performed significantly worse than the shift work group. The proportion of participants with crashes during the driving simulation was 46.9%, 18.9%, and 21.1% for the OSA, shift work, and control groups respectively (χ2(2) = 8.07, P = .02). Post hoc pairwise comparisons using the Z-test of two proportions revealed that the OSA group had a higher proportion of crash occurrence than the shift work group (P < .05) but not the control group, and the latter pair did not differ significantly (P > .05).

Neurobehavioral performance.

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Table 3

Neurobehavioral performance.

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PVT median reaction time did not differ between the groups (Table 3). In contrast, the total number of PVT lapses was significantly increased in the OSA group compared to the shift work and control groups.

Similarly, the OSA group had an increased number of signal misses compared to the control group on OSLER 1 (Table 3). There were no other differences between groups for OSLER 1 and 2 sleep latency and OSLER 2 signal misses.

For the neurocognitive tests, the OSA group performed worse than the shift work group on all tasks except the Trail A and the DSB (Table 3). Compared to the control group, the OSA group performed worse on LM I, LM II, DSF, and DST. To assess for the confounding effects of age, additional analysis was conducted on LM I, LM II, and DSF as these variables satisfied the assumptions of analysis of covariance. After controlling for age, significant group effects were present for LM I (F2,86 = 5.6, P < .01), LM II (F2,86 = 8.7, P < .01), and DSF (F2,86 = 6.3, P < .01). Paired comparisons (means ± standard error) with Bonferroni adjustments revealed that the OSA group had significantly lower (P < .05) LM I scores (34.7 ± 1.7) compared to both the shift work (42.1 ± 1.6) and control (41.5 ± 1.6) groups. Similarly, the OSA group had significantly lower (P < .01) scores for LM II (18.4 ± 1.5) compared to both the shift work (26.0 ± 1.3) and control groups (26.0 ± 1.3). DSF scores were also significantly lower (P < .05) for the OSA group (9.2 ± 0.4) compared to both the shift work (11.2 ± 0.4) and control (11.0 ± 0.4) groups.

The OSA group demonstrated impaired mood in a range of areas compared to the control group, whereas the shift work group demonstrated impaired mood on select measures only (Figure 2). The OSA group had a significantly higher BDI score (12.0, 8.0–17.8) than the control group (4.0, 2.0–9.0) but not the shift work group (7.0, 4.5–14.0). The shift work group had a trend toward higher BDI than the control group but this did not reach significance (P = .054). The portions of participants in the OSA, shift work, and control groups who had a BDI score > 13 (at minimum mild depressive scores) was 36.1%, 24.3%, and 12.8%, respectively (χ2(2) = 5.055, P = .06). In respect to state-related anxiety (STAI-S), the OSA group scored significantly higher than the shift work group but not the control group. There were no differences between the groups for trait anxiety (STAI-T). For POMS-SF, the participant groups did not differ for the tension/anxiety, depression/dejection, and anger/hostility subscales. For the vigor/activity, fatigue/inertia, confusion/bewilderment, and total mood disturbance sub-scales, the OSA group scored worse than the control group, but were not different from the shift work group. The shift work group also scored significantly worse than the control group on the vigor/activity and the fatigue/inertia subscales.

Mood scales scores.

Bars above figure demonstrate significant differences between groups using pairwise Dunn tests with Bonferroni corrections. Asterisks indicates statistical significance: * = P < .05, ** = P < .01, *** = P < .001. Values of P with a trend toward significance are also displayed. Circles and stars within boxplots show outliers and extreme outliers respectively. A/H = anger/hostility, BDI = Beck Depression Inventory, C = healthy control group, C/B = confusion/bewilderment, D/D = dejection/depression, F/I = fatigue/inertia, OSA = obstructive sleep apnea group, POMS = Profile of Mood State, STAI-S = State Trait Anxiety Index-State, STAI-T = State Trait Anxiety Index-Trait, SW = shift work group, T/A = tension-anxiety, TMD = total mood disturbance, V/A = vigor/activity.

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Figure 2

Mood scales scores.

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Ocular measures of alertness are shown in Table 4. The OSA group demonstrated reduced alertness, particularly during the PVT and OSLER 1 and 2 tests. For driving performance, maximum negative AVR was significantly greater for the OSA group than the control group, whereas the other ocular measures did not vary between groups. Shift workers demonstrated some reduced alertness compared to the control group on the OSLER 1 and 2 but only in respect to the percentage of long eye closures.

Ocular parameters.

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Table 4

Ocular parameters.

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DISCUSSION

The aim of this study was to compare the effects of regular shift work and OSA on sleepiness, mood, vigilance, driving performance, and neurocognitive function. The OSA group and shift work group were similar in respect to mood and sleepiness, but vigilance and neurocognitive performance were worse for the OSA group. Relative to healthy individuals, the OSA group had greater sleepiness, impaired mood, and reduced vigilance and neurocognitive function. The shift work group had greater subjective sleepiness and some altered mood relative to healthy individuals, but performed just as well as the control group on the vigilance and neurocognitive measures following 24 hours of recovery from their last shift. This suggests that for shift workers, sleepiness and some altered mood may persist, even though other aspects of neurocognitive function and vigilance have likely recovered.

Subjective Measures of Sleepiness and Mood

Consistent with previous literature, both the shift work and OSA groups reported higher levels of sleepiness than the healthy control group.9,10 In part, this is likely attributable to sleep restriction as both groups self-reported sleeping less than the control group. For the OSA group, sleep fragmentation is a likely additional mechanism that contributes to excessive daytime sleepiness.37 For shift workers, sleeping out of phase is a likely important additional mechanism. For the OSA group, the average ESS score (10.5) was outside the normal range (< 10), whereas for the shift workers, the average ESS score (7) was within the normal range (< 10).38 It is possible that shift workers have lower ESS scores than anticipated, because of the “healthy worker effect,” whereby only fit and healthy individuals self-select into and remain in shift work.19

The OSA group self-reported deficits on all mood measures (BDI, STAI, and POMS-SF) relative to the control group, consistent with previous reports of elevated symptoms of anxiety and depression in OSA.17,18 The association between psychological symptoms and OSA is not well understood. Sleep fragmentation is often considered the main catalyst,18 as it is believed to be responsible for excessive daytime sleepiness, which is associated with depressive symptoms in patients with OSA.17 The shift work group also experienced mood deficits relative to the control group on the vigor and fatigue POMS-SF subscales and had a trend toward a lower BDI score. These findings are concordant with prior reports of increased fatigue and mood disturbance in shift workers.19,20 It has been theorized that mood deterioration occurs because shift work disrupts sleep quality and duration, reduces natural light exposure, disturbs the melatonin circadian rhythm, impairs relationships, and interrupts leisure activities.20

Objective Measures of Vigilance

With regard to simulated driving, the OSA group had a greater speed variation and a higher crash incidence than the shift work group. However, unlike prior work, there were no differences observed between the OSA and control groups.26 The test duration (30 minutes) may have been a limitation, as Vakulin et al. demonstrated differences among patients with OSA and healthy individuals during a 90-minute drive, that were not present in the first 30 minutes.26 In the current study, the shift work group showed no impairment on simulated driving following at least 24 hours of recovery after their last shift. Although shift work has been demonstrated to increase lane deviation, speed deviation and crash occurrence on both simulated and on-road driving at the beginning39 and immediately following a night shift,40 there is little research examining driving following a recovery period. One study that simulated two cycles of 5 consecutive night shifts in healthy individuals separated by a 34-hour rest break, demonstrated that simulated driving was no worse on day 1 of week 2 (preceded by 5 night shifts and a 34-hour recovery period) compared to day 1 of week 1 (preceded by no shift work and normal sleep).41 Together these findings suggest that a 24- to 34-hour recovery is sufficient to restore driving performance to normal in shift workers. However, both laboratory studies assessed driving performance on a 30-minute simulator. Longer duration on-road drives may have differential effects.

For the stimulus response tasks (PVT and OSLER), the OSA group registered more lapses than the control and shift work groups. This is consistent with prior work in populations with OSA that demonstrate impairment on the PVT42 and OSLER.43 In those with OSA it has been shown that PVT response time is closely related to sleepiness, whereas inaccurate responding is closely related to hypoxemia, AHI, and sleep fragmentation.42 In the current study the shift work group performed similarly to the control group, suggesting there is no lag effect of shift work on vigilance following a recovery period. This was unexpected because there are clear cumulative effects of chronic partial sleep deprivation on vigilance.27 For instance, sleep restriction of 4 to 6 hours of time in bed each night has been shown to linearly increase PVT lapses, such that at the end of 1 week the deficit is similar to 48 hours of total sleep deprivation.27 How much time is necessary to recover the performance deficit is unclear. Banks et al.44 demonstrated that a single recovery sleep of 10 hours of time in bed was not sufficient to return PVT lapses to baseline following 5 consecutive nights of 4 hours of time in bed. Other studies have demonstrated a lack of full recovery following chronic partial sleep deprivation even when multiple recovery days are permitted.45 Thus, it is somewhat surprising that the shift workers in the current study, who likely accumulated sleep debt across their shift schedules, performed comparably to healthy controls with no apparent sleep-related impairment. Previous sleep restriction studies have used non–shift-worker groups; thus, a potential explanation for this discrepancy is the aforementioned “healthy worker effect.”19 This suggests that shift workers may represent a population of workers who are more resilient to sleep disruption.

The OSA group demonstrated impairment on almost all ocular measures of alertness during the PVT and OSLER test. The OSA group generally had longer eyelid closure duration, larger amplitude-velocity ratios, and a greater percentage of time with eyes closed. These measures are sensitive to both circadian modulation and increased homeostatic drive46 and predict failure to respond on both PVT and OSLER with high accuracy.47 Thus, impairment for the participants with OSA in the current study likely reflects reduced vigilance secondary to sleep fragmentation. Interestingly, ocular measures were similar between groups during the simulated driving task, with the exception that the OSA group had larger amplitude-velocity ratios than the control group. The deficits observed suggest that ocular measures may be a useful tool for assessing alertness in OSA. For the shift workers, there were no differences in ocular measures when compared to the healthy individuals, except during OSLER when the percentage of long eye closures was greater for shift workers. That ocular measures were mostly similar between the shift work and OSA groups is consistent with the finding of no performance deficits between these groups on these tasks.

Neurocognitive Tasks

The participants with OSA showed deficits on a range of neurocognitive assessments relative to the shift workers and controls. For the attention (assessed via DSF and Trail A) and long-term verbal memory (LM I and LM II) tasks, the OSA group performed worse than both the shift work and control groups. For executive function tasks (DSB, VST, and Trail B) the participants with OSA were generally impaired but only relative to the shift workers. These findings add to the current body of literature, which is inconclusive due to mixed findings regarding the effect of OSA on long-term memory8 and executive function.8,13 However, the effects of OSA on attention are more conclusive, with consistent deficits demonstrated for patients with severe OSA, mixed deficits for moderate patients and no deficits for mild patients.12 Because our OSA sample consisted of moderate to severe patients it was unsurprising that attention deficits were found in the current study. Although we did not assess the mechanisms for the neurocognitive deficits observed in patients with OSA, they have previously been attributed to sleep disruption and/or neuronal damage relating to hypoxemia.8

Shift workers were not impaired on the neurocognitive measures relative to controls. The prior literature concerning the chronic effects of shift work on neurocognitive function is mixed. A study of more than 3,000 employees demonstrated an association between shift work and poor cognitive efficiency in males.15 A longitudinal follow-up of this cohort revealed that shift work was associated with cognitive impairment in both males and females. Impairment was most evident in those who engaged in shift work for > 10 years, and was equivalent to the cognitive decline shown with 6.5 years of aging in the non–shift-work cohort. The cognitive domain most severely affected was memory.16 Another longitudinal study of more than 15,000 nurses found no association between shift-work history and cognitive decline assessed via general cognitive and verbal memory48; however, this study only assessed women who performed shift work at midlife between the ages of 58 to 68 years. Although the current study suggests there are no chronic effects of shift work on neurocognitive function, the shift workers only had to be engaged in shift work for more than 3 months to be considered eligible, which may not have been sufficient time for chronic effects to become apparent. Future studies are required to clarify the chronic effect of shift work on cognitive function.

Limitations

Several limitations should be considered. Although all shift workers had a break of at least 24 hours since their last shift, some may have had longer recovery times that may have caused washout effects. However, the primary aim was to assess long-term shift-work effects rather than acute effects. The study was performed in controlled laboratory conditions, and thus caution must be applied when generalizing to the real world. Driving simulators have been shown to predict on-road driving incidents reasonably; however, the driving task is monotonous compared to real-world driving and thus effects may be exaggerated.49 Despite this, only small effects were demonstrated in participants with OSA for simulated driving. The current study was not limited to a particular shift schedule (eg, night shift, forward rotating, or backward rotating). It is possible that specific shift schedules may have more severe long-term effects. A further limitation was that the OSA group was significantly older than the shift work and control groups. Age is known to affect neurocognitive ability and therefore the deficits observed in the OSA group may be attributed to age. However, additional analyses for LM I, LM II, and DSF revealed that the group differences were still present even when controlling for age. Another limitation was that the OSA group had a significantly higher body mass index than the shift work and control groups. While this was expected, as there is a close relationship between obesity and OSA,50 it is possible that some of the differences observed between groups may be attributable to the effects of obesity independent of OSA. Further, the OSA group had in-laboratory PSG prior to study entry whereas the shift work and control groups had ambulatory in-home PSG, although the parameters analyzed were otherwise identical. Finally, overnight PSG revealed that some of the shift work and control participants had OSA, despite efforts to screen them out using the MAPI questionnaire.

Implications

These findings suggest that shift work affects subjective ratings of mood and sleepiness, but does not impair neurocognitive performance when assessed following a recovery period. In contrast, the OSA group was impaired both on subjective ratings of mood and sleepiness as well as objective measures of neurocognitive performance. This suggests that the sequelae of OSA (sleep fragmentation and hypoxia) have a greater effect on neurocognitive performance than the sequelae of shift work (chronic sleep restriction and circadian phase disruption) after allowing for a 24-hour recovery. That there are residual effects of shift work on subjective sleepiness and mood suggest that adequate support and coping strategies need to be made available to ensure optimal mental health of shift workers. Further, performance deficits were not evident following at least 24 hours of recovery, suggesting that the neurocognitive impairment generally observed following sleep restriction is potentially reversible following a recovery period in shift workers. Future studies should determine the minimum amount of recovery time necessary to return performance back to normal, as this would improve workplace performance as well as minimize occupational accidents and errors.

CONCLUSIONS

Patients with OSA had elevated sleepiness, altered mood, and neurocognitive function deficits. Regular shift workers had no neurocognitive impairment, but had altered mood and elevated sleepiness, suggesting that these adverse effects may be chronic in shift workers while the neurocognitive effect may recover. The observed differences in sleepiness, mood, and neurocognitive function between the patients with OSA and the shift workers suggest that the underlying causes of the sleep disturbance in these populations has differential effects on neurobehavioral function.

DISCLOSURE STATEMENT

All authors have seen and approved the final manuscript. Work for this study was performed at the Institute for Breathing and Sleep and Austin Health, Heidelberg, Victoria, Australia. The authors report no conflicts of interest.

ABBREVIATIONS

AHI

apnea-hypopnea index

AVR

amplitude velocity ratio

BDI

Beck Depression Index

DSB

Digit Span Backward

DSF

Digit Span Forward

DST

Digit Span Total

ESS

Epworth Sleepiness Scale

IED

inter-event duration

LM I

Logical Memory I

LM II

Logical Memory II

MAPI

Multivariate Apnea Prediction Index

ODMS

Optalert Drowsiness Measurement System

OSA

obstructive sleep apnea

OSLER

Oxford Sleepiness Resistance Test

POMS-SF

Profile of Mood States-short form

PSG

polysomnography

PVT

Psychomotor Vigilance Task

SpO2

oxygen desaturation

STAI

State Trait Anxiety Inventory

STAI-S

State Trait Anxiety Inventory-State

STAI-T

State Trait Anxiety Inventory-Trait

TMT

Trail Making Test

VST

Victoria Stroop Test

REFERENCES

1 

Watson NF, Badr MS, Belenk G, et al. Recommended amount of sleep for a healthy adult: A joint consensus statement of the American Academy of Sleep Medicine and Sleep Research Society. Sleep. 2015;38(6):843–844. [PubMed Central][PubMed]

2 

Ferrara M, Gennaro L De. How much sleep do we need? Sleep Med Rev. 2001;5(2):155–179. [PubMed]

3 

Rosekind MR, Gregory KB, Mallis MM, Brandt SL, Seal B, Lerner D. The cost of poor sleep: Workplace productivity loss and associated costs. J Occup Environ Med. 2010;52(1):91–98. [PubMed]

4 

Tregear S, Reston J, Schoelles K, Phillips B. Obstructive sleep apnea and risk of motor vehicle crash: systematic review and meta-analysis. J Clin Sleep Med. 2009;5(6):573–581. [PubMed Central][PubMed]

5 

Akerstedt T, Fredlund P, Gillberg M, Jansson B. A prospective study of fatal occupational accidents - relationship to sleeping difficulties and occupational factors. J Sleep Res. 2002;11(1):69–71. [PubMed]

6 

Sallinen M, Härmä M, Mutanen P, Ranta R, Virkkala J, Müller K. Sleep-wake rhythm in an irregular shift system. J Sleep Res. 2003;12(2):103–112. [PubMed]

7 

Ohayon MM, Lemoine P, Arnaud-Briant V, Dreyfus M. Prevalence and consequences of sleep disorders in a shift worker population. J Psychosom Res. 2002;53(1):577–583. [PubMed]

8 

Bucks RS, Olaithe M, Eastwood P. Neurocognitive function in obstructive sleep apnoea: A meta-review. Respirology. 2013;18(1):61–70. [PubMed]

9 

Gottlieb DJ, Whitney CW, Bonekat WH, et al. Relation of sleepiness to respiratory disturbance index: The sleep heart health study. Am J Respir Crit Care Med. 1999;159(2):502–507. [PubMed]

10 

Drake CL, Roehrs T, Richardson G, Walsh JK, Roth T. Shift work sleep disorder: Prevalence and consequences beyond that of symptomatic day workers. Sleep. 2004;27(8):1453–1462. [PubMed]

11 

Crummy F, Cameron PA, Swann P, Kossmann T, Naughton MT. Prevalence of sleepiness in surviving drivers of motor vehicle collisions. Intern Med J. 2008;38(10):769–775. [PubMed]

12 

Jackson ML, Howard ME, Barnes M. Cognition and daytime functioning in sleep-related breathing disorders. Prog Brain Res. 2011;190:53–68. [PubMed]

13 

Twigg GL, Papaioannou I, Jackson M, et al. Obstructive sleep apnea syndrome is associated with deficits in verbal but not visual memory. Am J Respir Crit Care Med. 2010;182(1):98–103. [PubMed Central][PubMed]

14 

Özdemir PG, Selvi Y, Özkol H, et al. The influence of shift work on cognitive functions and oxidative stress. Psychiatry Res. 2013;210(3):1219–1225. [PubMed]

15 

Rouch I, Wild P, Ansiau D, Marquié J-C. Shiftwork experience, age and cognitive performance. Ergonomics. 2005;48(10):1282–1293. [PubMed]

16 

Marquie JC, Tucker P, Folkard S, Gentil C, Ansiau D. Chronic effects of shift work on cognition: findings from the VISAT longitudinal study. Occup Environ Med. 2015;72(4):258–264. [PubMed]

17 

Ishman SL, Cavey RM, Mettel TL, Gourin CG. Depression, sleepiness, and disease severity in patients with obstructive sleep apnea. Laryngoscope. 2010;120(11):2331–2335. [PubMed]

18 

Yue W, Hao W, Liu P, Liu T, Ni M, Guo Q. A case-control study on psychological symptoms in sleep apnea-hypopnea syndrome. Can J Psychiatry. 2003;48(5):318–323. [PubMed]

19 

Driesen K, Jansen NWH, van Amelsvoort LGPM, Kant I. The mutual relationship between shift work and depressive complaints - a prospective cohort study. Scand J Work Environ Heal. 2011;37(5):402–410. [PubMed]

20 

Driesen K, Jansen NW, Kant I, Mohren DC, Van Amelsvoort LG. Depressed mood in the working population: associations with work schedules and working hours. Chronobiol Int. 2010;27(5):1062–1079. [PubMed]

21 

Maislin G, Pack AI, Kribbs NB, et al. A survey screen for prediction of apnea. Sleep. 1995;18(3):158–166. [PubMed]

22 

Iber C, Ancoli-Israel S, Chesson AL Jr, Quan SF; for the American Academy of Sleep Medicine. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. 1st ed. Westchester, IL: American Academy of Sleep Medicine; 2007.

23 

Rechtschaffen A, Kales A. A Manual of Standardized Terminology, Techniques and Scoring System of Sleep Stages in Human Subjects. Los Angeles, CA: Brain Information Service/Brain Research Institute, University of California; 1968.

24 

Berry RB, Budhiraja R, Gottlieb DJ, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. J Clin Sleep Med. 2012;8(5):597–619. [PubMed Central][PubMed]

25 

Desai AV, Wilsmore B, Bartlett D, et al. The utility of the AusEd driving simulator in the clinical assessment of driver fatigue. Behav Res Methods. 2007;39(3):673–681. [PubMed]

26 

Vakulin A, Catcheside PG, Baulk SD, et al. Individual variability and predictors of driving simulator impairment in patients with obstructive sleep apnea. J Clin Sleep Med. 2014;10(6):647–655. [PubMed Central][PubMed]

27 

Van Dongen HP, Maislin G, Mullington JM, Dinges DF. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep. 2003;26(2):117–126. [PubMed]

28 

Drozdick L, Holdnack J, Weiss L, Zhou X. Overview of the WAIS-IV, WMS-IV and ACS. In: Holdnack J, Drozdick L, Weiss L, Iverson G, eds. WAIS-IV, WMS-IV, and ACS. 1st ed. Oxford, UK: Elsevier Science; 2013:1–73.

29 

Lamar M, Raz A. Neuropsychological assessment of attention and executive function. In: Ayers S, Baum A, McManus C, et al., eds. Cambridge Handbook of Psychology, Health and Medicine. Cambridge, UK: Cambridge University Press; 2007:290–297.

30 

Sattler JM, Ryan JJ. Chapter 3. WAIS-IV subtests. In: Assessment with the WAIS-IV. San Diego, CA: Jerome M. Sattler, Publisher Inc.; 2009:90–94.

31 

Strauss E, Sherman EMS, Spreen O. Executive Functions - Stroop Test. In: A Compendium of Neuropsychological Tests: Administration, Norms and Commentary. 5th ed. New York, NY: Oxford University Press; 2006:477–499.

32 

Beck AT, Steer RA. Internal consistencies of the original and revised beck depression inventory. J Clin Psychol. 1984;40(6):1365–1367. [PubMed]

33 

Spielberger C, Gorsuch R, Lushene R, Vagg P, Jacobs G. State-Trait Anxiety Inventory: Bibliography. 2nd ed. Palo Alto, CA: Consulting Psychologists Press; 1983.

34 

Shacham S. A Shortened Version of the Profile of Mood States. J Pers Assess. 1983;47(3):305–306. [PubMed]

35 

Bennett LS, Stradling JR, Davies RJ. A behavioural test to assess daytime sleepiness in obstructive sleep apnoea. J Sleep Res. 1997;6(2):142–145. [PubMed]

36 

Johns MW, Tucker A, Chapman R, Crowley K, Michael N. Monitoring eye and eyelid movements by infrared reflectance oculography to measure drowsiness in drivers. Somnologie. 2007;11(4):234–242.

37 

Colt HG, Haas H, Rich GB. Hypoxemia vs sleep fragmentation as cause of excessive daytime sleepiness in obstructive sleep apnea. Chest. 1991;100(6):1542–1548. [PubMed]

38 

Johns M, Hocking B. Daytime sleepiness and sleep habits of Australian workers. Sleep. 1997;20(10):844–849. [PubMed]

39 

Howard ME, Radford L, Jackson ML, Swann P, Kennedy GA. The effects of a 30-minute napping opportunity during an actual night shift on performance and sleepiness in shift workers. Biol Rhythm Res. 2010;41(2):137–148.

40 

Lee ML, Howard ME, Horrey WJ, et al. High risk of near-crash driving events following night-shift work. Proc Natl Acad Sci U S A. 2016;113(1):176–181. [PubMed]

41 

Van Dongen HP, Belenky G, Vila BJ. The efficacy of a restart break for recycling with optimal performance depends critically on circadian timing. Sleep. 2011;34(7):917–929. [PubMed Central][PubMed]

42 

Sforza E, Haba-Rubio J, De Bilbao F, Rochat T, Ibanez V. Performance vigilance task and sleepiness in patients with sleep-disordered breathing. Eur Respir J. 2004;24(2):279–285. [PubMed]

43 

Mazza S, Pepin JL, Deschaux C, Naegele B, Levy P. Analysis of error profiles occurring during the OSLER test: A sensitive mean of detecting fluctuations in vigilance in patients with obstructive sleep apnea syndrome. Am J Respir Crit Care Med. 2002;166(4):474–478. [PubMed]

44 

Banks S, Van Dongen HPA, Maislin G, Dinges DF. Neurobehavioral dynamics following chronic sleep restriction: dose-response effects of one night for recovery. Sleep. 2010;33(8):1013–1026. [PubMed Central][PubMed]

45 

Rupp TL, Wesensten NJ, Bliese PD, Balkin TJ. Banking sleep: realization of benefits during subsequent sleep restriction and recovery. Sleep. 2009;32(3):311–321. [PubMed Central][PubMed]

46 

Anderson C, Chang AM, Sullivan JP, Ronda JM, Czeisler CA. Assessment of drowsiness based on ocular parameters detected by infrared reflectance oculography. J Clin Sleep Med. 2013;9(9):907–920. [PubMed Central][PubMed]

47 

Wilkinson VE, Jackson ML, Westlake J, et al. The accuracy of eyelid movement parameters for drowsiness detection. J Clin Sleep Med. 2013;9(12):1315–1324. [PubMed Central][PubMed]

48 

Devore EE, Grodstein F, Schernhammer ES. Shift work and cognition in the nurses' health study. Am J Epidemiol. 2013;178(8):1296–1300. [PubMed Central][PubMed]

49 

Philip P, Sagaspe P, Taillard J, et al. Fatigue, sleepiness, and performance in simulated versus real driving conditions. Sleep. 2005;28(12):1511–1516. [PubMed]

50 

Shah N, Roux F. The relationship of obesity and obstructive sleep apnea. Clin Chest Med. 2009;30(3):455–465. [PubMed]