Abstract
Introduction
Sleep difficulties in childhood ADHD have been documented by numerous studies and meta-analyses (Corkum, Tannock, & Moldofsky, 1998; Cortese, Farone, Konofal, & Lecendreux, 2009). Studies examining sleep in adult ADHD are less numerous than in childhood ADHD but document similar pattern and prevalence of sleep problems as in children. Questionnaire studies examining subjective sleep measures consistently report sleep onset problems, restless and nonrestorative sleep, and increased daytime sleepiness in up to 80% of adult ADHD patients (Schredl, Alm, & Sobanski, 2007; Surman et al., 2009; Yoon, Jain, & Shapiro, 2013), and recent studies report a circadian preference toward eveningness (Baird, Coogan, Siddiqui, Donev, & Thome, 2012; Rybak, McNeely, Mackenzie, Jain, & Levitan, 2007). Studies assessing objective sleep parameters by polysomnography (PSG) or actigraphy report reduced sleep efficiency, longer sleep onset latencies, more nocturnal awakenings, and increased nocturnal activity in adult ADHD compared with healthy controls (Kooij, Middelkoop, van Gils, & Buitelaar, 2001; Philipsen et al., 2005; Sobanski, Schredl, Kettler, & Alm, 2008). Studies assessing objective daytime sleepiness in ADHD are still relatively sparse. To date, there are three studies that used the multiple sleep latency test (MSLT) in school-aged children with ADHD, which have yielded mixed results. Two studies report decreased sleep latency (SL) in ADHD compared with controls (Golan, Shahar, Ravid, & Pillar, 2004; Lecendreux, Konofal, Bouvard, Falissard, & Mouren-Simeoni, 2000), while a recent study failed to find any difference in mean MSLT-SL in ADHD compared with controls (Prihodova et al., 2010). To the best of our knowledge, MSLT studies in adults with ADHD are still lacking. This is a crucial evidence gap, as results from MSLT studies in children cannot be transferred directly to adult ADHD, because sleep characteristics including duration of sustained wakefulness during the day and the need of daytime naps are related to developmental level and age. For scientific reasons, it is useful to extend the still inconsistent data on daytime sleepiness in ADHD as there is some evidence that pathophysiologic mechanisms underlying attention deficits in ADHD involve dysregulation of arousal (Benikos & Johnstone, 2009). A Consensus Working Group on ADHD and sleep recently identified hypoarousal and daytime sleepiness in ADHD as one of six future major key research areas (Owens et al., 2013).
The primary aim of the present study is to assess objective and subjective daytime sleepiness by MSLT-SL and by the self-rated questionnaire Epworth Sleepiness Scale (ESS) in adult patients with ADHD compared with healthy controls. Secondary aims of the study are to analyze the interplay of MSLT-SL and ESS scores, and the association of both sleep measures with current and childhood ADHD symptom severity and ADHD subtype according to Diagnostic and Statistical Manual of Mental Disorders (4th ed.; DSM-IV; American Psychiatric Association [APA], 1994) criteria.
Method
Participants
The study was approved by the local ethics committees. All participants gave written informed consent before participating in the study. Patients with ADHD were recruited from consecutive referrals at the Adult ADHD Outpatient Clinic at the Central Institute of Mental Health (CIMH), Mannheim, Germany. MSLT and other sleep parameters were assessed within a polysomnographic study evaluating the influence of methylphenidate treatment on sleep in adult patients with ADHD (Sobanski et al., 2008). Healthy controls were recruited by personal contact at the Departments for Sleep Medicine at the CIMH and at the Psychiatric University Hospital in Freiburg, Germany. MSLT in healthy controls was carried out at the Department for Sleep Medicine at the University of Freiburg within studies assessing the impact of psychopharmacological treatment on nocturnal sleep and daytime sleepiness (Doerr et al., 2010; Möller & Riemann, 2002).
Patients and controls underwent a comprehensive semi-structured clinical interview in which information about current psychiatric status and symptoms, sleep disturbances and disorders, medical status, and psychiatric and medical history was assessed. All interviews were performed by experienced clinicians. In addition, we performed a physical examination along with an evaluation of laboratory parameters for hematology, biochemistry, and thyroid parameters, as well as a urine drug test. For inclusion, all participants had to be 18 to 55 years old. Patients had to be diagnosed with ADHD according to DSM-IV criteria (APA, 1994) and according to expert consensus (E.S., B.A.). Childhood ADHD and chronic course of ADHD symptoms from childhood to adulthood were confirmed by collateral information (e.g., interviewing the patients’ parents, school reports) whenever possible. Clinical diagnosis of ADHD in patients was validated by standardized instruments. To be included, patients had to be rated with ≥15 points in the ADHD–Diagnostic Checklist (ADHD-DC; Rösler et al., 2004) and ≥30 points in the validated German Wender–Utah Rating Scale, Short Version (WURS-k; Retz-Junginger et al., 2003). Patients were further required to have an IQ > 85 to exclude psychosocial impairment due to reduced intelligence level. Exclusion criteria for all participants were an apnea index > 5 during polysomnographic recording, obstructive snoring or working night shift, intake of any medication within 4 weeks including methylphenidate before the start of the study, any unstable psychiatric and medical condition, current substance abuse, more than 10 points in the Beck Depression Scale and/or clinically significant abnormal laboratory values, or a positive urinary drug screen.
Assessments
Sleep Assessments
ESS
The ESS is a self-rated questionnaire used to determine the level of daytime sleepiness (Johns, 1991, 2000). It is widely used for clinical and research purpose (Geisler et al., 2006; Neu et al., 2008; Yoon et al., 2013) due to its ability to measure sleep propensity in different situations of daily living and to provide a reflection of general characteristic of sleepiness in daily life. Participants are asked to rate their propensity to doze off or fall asleep for eight different situations of daily living on a scale of increasing probability with a range from 0 to 3. Scores higher than 10 are indicative of clinically relevant daytime sleepiness.
MSLT
Before MSLT, patients and controls spent a night in sleep laboratory for polysomnography (PSG). PSG encompassed electroencephalogram (EEG) (C3-A2, C4-A1), assessment of horizontal and vertical eye movements, submental and leg electromyogram, electrocardiogram, and assessment of respiration (oral and nasal air flow, thoracoabdominal respiratory movements, and oxygen saturation). All recordings were carried out from 11:00 p.m. (lights out) to 7:00 a.m. (lights on) and scored in 30-s epochs, according to Rechtschaffen and Kales’s (1968) criteria.
MSLT was performed the day following PSG in 13 patients with ADHD and in 26 healthy controls. The same MSLT-protocol was used for ADHD and control participants. Most participants were given five opportunities to fall asleep every 2 hr. In 18 participants, MSLT recording comprised four assessments. MSLT recording times were 9:00 a.m., 11:00 a.m., 1:00 p.m., and 3:00 p.m., and for those with five recordings, 5:00 p.m., with every nap opportunity lasting 20 min. For each nap, participants were requested to lie in bed in a dark, quiet, and comfortable room, with no external stimulation and were asked to fall asleep. SL for each trial was measured from the time of lights out to the first epoch of sleep. The time taken to fall asleep (SL) and sleep stages attained are recorded by PSG. Standard methods were used for MLST evaluation where the occurrence of one epoch of sleep of any stage was rated as sleep onset. If participants did not fall asleep after 20 min, the nap was terminated, and SL for that nap was assigned a value of 20 min. If participants fell asleep during the nap, they were allowed to sleep for 15 min.
Clinical Assessments
ADHD-DC
The ADHD-DC comprises 18 observer-rated items and assesses age-adapted ADHD symptoms according to DSM-IV and ICD-10 (International Classification of Diseases)research criteria. The diagnostic cutoff score is 15 points and provides a sensitivity of 77% and a specificity of 75% (Rösler et al., 2004).
WURS-k
The validated German version of the WURS-k is a 25-item self-rated instrument that assesses childhood ADHD symptoms retrospectively. The cutoff score is 30 points and provides a sensitivity of 85% and a specificity of 76% (Retz-Junginger et al., 2003).
BDI
The Beck Depression Inventory (BDI; Beck, 1988) is the most commonly used self-rating instrument to assess severity of depressive symptoms. It consists of 21 items that are rated from 0 to 3 according to severity. Psychometric properties of the validated German BDI version are satisfactory (Hautzinger, Bailer, Worall, & Keller, 1994).
Multiple Choice Vocabulary Test
The Multiple Choice Vocabulary Test (MWTB; Lehrl, 1997) is an instrument widely used in Germany for assessment of verbal IQ.
Statistics
Statistical analyses were carried out with SAS for Windows (Version 8.02) software package. T tests and Fisher Exact Test were used to analyze participants’ characteristics. Because patients and controls differed in mean age and gender distribution, ANCOVAs were computed to control for age and gender effects on ESS scores and for age on sleep latency in MSLT. Chi-square tests were used to analyze number of naps. Significance level was set to p < .05.
Results
Participants’ Characteristics
Thirteen patients with ADHD (9 ADHD DSM-IV combined type, 4 DSM-IV ADHD primarily inattentive type [APA, 1994]; 10 males, 3 females) with a mean age of 33.5 ± 9.4 years and 26 healthy male controls with a mean age of 26.7 ± 4.1 years underwent MSLT (age: t = 2.5, p < .05; gender: Fisher Exact Test, p < .1). None of the controls and two patients suffered from comorbid axis-I-disorders, namely, motoric tics and social phobia. None of the comorbid disorders required a priori clinical intervention, and both were regarded as mild. Mean BDI score was 9.2 ± 3.8 in ADHD patients and 1.9 ± 1.6 in controls (t = 7.0, p < .0001). Although the difference in means was statistically significant, in both groups, it was below 10 points indicating no clinically significant depressive symptoms (Beck, 1988). Mean patients’ WURS-k score was 42.4 ± 12.2 points; mean ADHD-DC score was 28.9 ± 7.2 points. Detailed participants’ characteristics are shown in Table 1.
Personal and Clinical Characteristics of ADHD Patients (n = 13) and Healthy Controls (n = 27) Participating in MSLT.
Note. MSLT = multiple sleep latency test; ADHD-DC = ADHD–Diagnostic Checklist; WURS-k = Wender–Utah Rating Scale, Short Version; BDI = Beck Depression Inventory. T Test, Fisher Exact Test.
ESS was assessed in 27 patients with ADHD (19 males, 8 females) with a mean age of 34.2 ± 9.0 years and in 182 healthy controls (69 males, 113 females) with a mean age of 30.8 ± 12.2 years (age: t = −1.4, p < .1; gender: χ2 = 10.2, p < .005).
Sleep Measures
MSLT
In the baseline night of PSG, ADHD and control group differed in age-corrected sleep efficiency (83% ± 11.0% vs. 90.5% ± 6.4%, F = 4.2, p < .05) and in age-corrected SLs by trend (22.5 ± 12.8 min vs. 16.0 ± 15.4 min, F = 2.5, p < .1). Full results of the PSG assessments have been published elsewhere (Sobanski et al., 2008). MSLT-SL and sleep efficiency in PSG were not correlated. Neither mean age-corrected MSLT-SL (ADHD: 10.6 ± 4.8, range: 4.6-20 min; controls: 12.2 ± 4.2, range 4.9-20 min; F = 0.9, n.s.) nor single MSLT-SLs at the first, second, third, fourth, and fifth assessments differed in ADHD and controls. Percentage of patients and controls falling asleep did not differ during Naps 1 to 3. During the fifth nap, more ADHD patients than controls (70% vs. 27.3%; χ2 = 3.8, p < .05) and during the fourth nap, more patients than controls (92.3% vs. 69.2%; χ2 = 2.6, p < .1) fell asleep by trend. For details, see Figure 1 and Table 2.

Percentage of patients with ADHD and controls falling asleep during MSLT assessments 1 to 5. At 5:00 p.m., MSLT was applied in 10 ADHD patients and 11 controls. Chi-square test.
Sleep Onset Latencies in Minutes During MSLT in ADHD Patients and Controls.
Note. p values ANCOVAs with age partialized out. MSLT = multiple sleep latency test; SL = sleep latency.
ESS
Mean age- and gender-corrected ESS score was higher in ADHD than controls (9.3 ± 4.9 vs. 6.9 ± 3.4 points; F = 9.0, p < .005), and 40.7% of the ADHD group had ESS scores >10 points, indicating clinically significant daytime sleepiness. ESS scores and MSLT-SL were inversely correlated by trend (r = −.45, p < .1), indicating that patients who complained about higher daytime tiredness by self-report also fell faster asleep during MSLT. We found no correlation of ESS scores and MSLT-SL in controls.
Correlation of SL in MSLT and Subjective Daytime Sleepiness With ADHD Symptoms and Subtype
We found no correlation between subjective and objective parameters of daytime tiredness (MSLT-SL, ESS scores) with current and childhood ADHD symptom severity (ADHD-DC, WURS-k) or current ADHD subtype according to DSM-IV criteria.
Discussion
Recently, hypoarousal and daytime sleepiness in ADHD were identified as one major key research area by a Consensus Working Group on ADHD and sleep (Owens et al., 2013). Arousal dysregulation is discussed as a possible mechanism involved in the pathophysiology of the inattentive symptom cluster of ADHD, as deficits in arousal modulation has been found to be related to deficits in cognitive performance in ADHD (Benikos & Johnstone, 2009). However, our results of comparable mean MSLT-SL in ADHD and healthy controls do not suggest increased objective daytime sleepiness in adults with ADHD. Mean SL in our controls was 12.2 ± 4.2 min corresponding to a mean SL in healthy controls of 11.5 ± 5.1 min (Johns, 2000) and 11.1 ± 4.6 min (Steinberg, Schonberg, Weess, Schneider, & Pritzel, 1996) reported by other studies. Our finding confirms the result of the most recent of three MSLT studies in children that also found comparable MSLT-SL in school-aged children with ADHD and controls (Prihodova et al., 2010). As these two negative results are contrasted by two other MSLT studies that report increased daytime sleepiness in children with ADHD (Lecendreux et al., 2000), further studies and meta-analyses are needed to broaden the evidence on objective daytime sleepiness in adults with ADHD. Our finding of similar MSLT-SL in ADHD and controls also contrasts to the self-reported increase of subjective daytime sleepiness with a mean ESS score of 9.3 ± 4.9 points in our ADHD patients compared with controls. Mean ESS score in healthy controls was 6.9 ± 3.4 points and corresponds to ESS means between 3.5 ± 2.2 and 7.5 ± 3.9 points in healthy controls reported by other studies (Geisler et al., 2006; Johns & Hocking, 1997; Neu et al., 2008). We found a moderate, negative correlation of ESS scores and MSLT-SL, indicating that patients, who experience subjective higher daytime sleepiness, also fell asleep faster during MSLT. Our finding of increased subjective daytime sleepiness in ADHD corresponds to the recently published results of Yoon et al. (2013) who report a mean ESS score of 9.7 ± 4.5 points in their ADHD sample compared with 9.3 ± 4.9 points in our patients. This argues for the validity of these findings and a subjective feeling of increased daytime sleepiness in adults with ADHD. We observed that more patients with ADHD than controls fell asleep at the latest assessment at 5:00 p.m. However, this is not clear to interpret, as it may be induced by a sharp decrease in controls falling asleep at that time point and not by increase of sleeping in ADHD patients. We failed to find an association of measures of daytime sleepiness with childhood or current severity of ADHD symptoms. This was also reported by one childhood study (Prihodova et al., 2010), whereas another childhood MSLT study reports a correlation of sleep onset latency with ADHD symptoms (Lecendreux et al., 2000).
Some limitations of our study must be considered. An important limitation of the study is the small sample size that may have been too small to detect differences in SLs between ADHD patients and controls. Although ADHD patients were recruited from unselected consecutive referrals to the CIMH Adult ADHD Outpatient Department, one cannot exclude the possibility that study participation was preferentially accepted by those suffering from sleep disturbances or daytime sleepiness, which would imply a selection bias toward patients with sleep problems. However, our results argue against that conclusion as we found no difference in MSLT-SL in ADHD patients and controls despite increased subjective daytime sleepiness in the ADHD group. Increased subjective daytime sleepiness was also reported in an unselected adult ADHD sample not participating in a PSG and MSLT assessment by Yoon et al., 2013 and also in a precedent questionnaire study conducted by our group (Schredl et al., 2007). Controls did not undergo an assessment of ADHD, which may have resulted in overlooking ADHD. However, with a mean prevalence for adult ADHD of 3% to 4% in the general population, there is a statistical probability of, at the most, one individual suffering from ADHD out of the 26 controls who underwent MSLT. Psychiatric disorders in ADHD patients and healthy controls were assessed by experienced psychiatrists with a semi-structured clinical interview. However, we did not use a highly standardized instrument like e. g. the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I), and thus, a risk of overlooking comorbid psychiatric conditions cannot be completely ruled out.
We also did not use an adaptation night for PSG recording, which may be of relevance as a first-night effect with reduced sleep efficiency in ADHD patients has been reported (Prihodova et al., 2010). Thus, a possible first-night effect on sleep efficiency cannot be ruled out. However, as MSLT-SL did not differ in ADHD and controls despite reduced sleep efficiency in ADHD patients during PSG, this argues for the validity of the MSLT findings. Furthermore, MSLT may not be the appropriate method to measure objective daytime sleepiness in adults with ADHD. Eventually, a more naturalistic approach and assessment of daytime sleepiness in daily living by electronic diaries or multiple wake tests and pupillography would be more suitable methods. As recent studies have shown that adult ADHD is associated with alterations in circadian rhythms (Baird et al., 2012; Van Veen, Kooij, Boonstra, Gordijn, & Van Someren, 2010), future studies should also include the assessment of circadian rhythms and its complex interplay with sleep and sleep disturbances in ADHD.
Footnotes
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Esther Sobanski: Phase III studies, investigator-initiated trails, lectures, travel support, advisory boards: Medice, Novartis, Eli Lilly, Federal Ministry of Education and Research; Barbara Alm: Phase III studies, lectures, travel support, advisory boards: Medice, Eli Lilly, Novartis; Oliver Hennig: lectures, travel support: Medice, Eli Lilly; Dieter Riemann: Advisory boards; Abbvie Bernd Feige: None; Michael Schredl: Phase III studies, research studies: Merck Sharp & Dohme GmbH Sharp & Dohme GmbH, Dream Science Foundation Correct.
