BIOLOGICAL PSYCHIATRY - ORIGINAL PAPER Sleep disturbance, circadian preference and symptoms of adult attention deficit hyperactivity disorder (ADHD) Bogdan Ioan Voinescu • Aurora Szentagotai • Daniel David Received: 1 February 2012 / Accepted: 30 June 2012 / Published online: 20 July 2012 Ó Springer-Verlag 2012 Abstract Inattention is a core symptom of attention deficit hyperactivity disorder (ADHD) and one of the main impairments resulting from insomnia disorders. These dis- orders have also been reported to be linked with disturbances in circadian rhythms and with increased eveningness. To explore these associations, more than 550 adults were sur- veyed across Romania. Using self-reported questionnaires, the presence and severity of ADHD and insomnia symptoms were determined, together with sleep and circadian typology parameters. ADHD symptoms were more frequent and severe among younger individuals. Subjects with probable ADHD complained more frequently of sleep disturbance of the insomnia type (more than 50 %) and reported shorter sleep durations and longer sleep latencies and more frequent unwanted awakenings. Individuals likely to suffer from ADHD and/or insomnia disorder were significantly more evening oriented than controls. Inattention was associated with both insomnia and eveningness, while impulsivity was associated with poor sleep. Hyperactivity and sleep timing were associated with poor sleep only in probable insomnia group. These findings highlight the reciprocal links between ADHD symptoms, sleep and diurnal preference. Keywords Insomnia Á Self-report Á Eveningness Introduction Attention Deficit Hyperactivity Disorder (ADHD) is one of the most common mental disorders in childhood, with 5.29 % being affected worldwide (reviewed by Polanczyk et al. 2007). Despite initial beliefs that ADHD is rare in adulthood (Hill and Schoener 1996), more recent meta- analyses revealed that at the age of 25 it persists in between 15 and 60 % of those with the childhood condition, depending on the used criteria (Faraone et al. 2006), giving an estimated prevalence of around 2.5 % (Simon et al. 2009). Insomnia is a common diagnostic criterion for many psychiatric disorders and may cause several functional impairments such as inattention, one of the core symptoms of ADHD. Despite the possibility of an association between sleep disturbance and ADHD symptoms, there is little research on this relationship. In non-clinical samples, inattention was associated with insomnia (Kass et al. 2003) or difficulties falling asleep, longer times in bed and less efficient sleep, while hyperactivity was associated with decreased sleep duration (Gau et al. 2007). Decreased sleep duration, increased sleep latency and more disturbed sleep were also linked with hyperactivity in non-medicated adults suffering from ADHD (Mahajan et al. 2010), while longer sleep latencies, low sleep quality and daytime sleepiness were reported by adult ADHD patients (Bijlenga et al. 2011; Schredl et al. 2007; Surman et al. 2009). Shorter and later sleep were found to be linked with hyperactivity (Bijlenga et al. 2011). Polysomnography and actigraphy studies in adults diagnosed with ADHD also revealed reduced sleep efficiency, as well as alterations in other sleep parameters (Boonstra et al. 2007; Kooij et al. 2001; Sobanski et al. 2008; Van Veen et al. 2010). Eveningness, a psychometric parameter describing the preference of an individual for later bed and wake times, as well as patterns of alertness and activity associated with later times during the day, has also been found to be linked with inattention (Bae et al. 2010; Caci et al. 2009; Rybak et al. 2007) and hyperactivity (Bae et al. 2010). Recent B. I. Voinescu (&) Á A. Szentagotai Á D. David Department of Clinical Psychology and Psychotherapy, Babes ¸-Bolyai University, Cluj-Napoca, Romania e-mail: [email protected]123 J Neural Transm (2012) 119:1195–1204 DOI 10.1007/s00702-012-0862-3
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Sleep disturbance, circadian preference and symptoms of adult attention deficit hyperactivity disorder (ADHD)
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Sleep disturbance, circadian preference and symptoms of adult attention deficit hyperactivity disorder (ADHD) Bogdan Ioan Voinescu • Aurora Szentagotai • Daniel David Received: 1 February 2012 / Accepted: 30 June 2012 / Published online: 20 July 2012 Springer-Verlag 2012 hyperactivity disorder (ADHD) and one of the main impairments resulting from insomnia disorders. These dis- orders have also been reported to be linked with disturbances in circadian rhythms and with increased eveningness. To explore these associations, more than 550 adults were sur- veyed across Romania. Using self-reported questionnaires, the presence and severity of ADHD and insomnia symptoms were determined, together with sleep and circadian typology parameters. ADHD symptoms were more frequent and severe among younger individuals. Subjects with probable ADHD complained more frequently of sleep disturbance of the insomnia type (more than 50 %) and reported shorter sleep durations and longer sleep latencies and more frequent unwanted awakenings. Individuals likely to suffer from ADHD and/or insomnia disorder were significantly more evening oriented than controls. Inattention was associated with both insomnia and eveningness, while impulsivity was associated with poor sleep. Hyperactivity and sleep timing were associated with poor sleep only in probable insomnia group. These findings highlight the reciprocal links between ADHD symptoms, sleep and diurnal preference. Keywords Insomnia Self-report Eveningness 5.29 % being affected worldwide (reviewed by Polanczyk et al. 2007). Despite initial beliefs that ADHD is rare in adulthood (Hill and Schoener 1996), more recent meta- analyses revealed that at the age of 25 it persists in between 15 and 60 % of those with the childhood condition, depending on the used criteria (Faraone et al. 2006), giving an estimated prevalence of around 2.5 % (Simon et al. 2009). Insomnia is a common diagnostic criterion for many psychiatric disorders and may cause several functional impairments such as inattention, one of the core symptoms of ADHD. Despite the possibility of an association between sleep disturbance and ADHD symptoms, there is little research on this relationship. In non-clinical samples, inattention was associated with insomnia (Kass et al. 2003) or difficulties falling asleep, longer times in bed and less efficient sleep, while hyperactivity was associated with decreased sleep duration (Gau et al. 2007). Decreased sleep duration, increased sleep latency and more disturbed sleep were also linked with hyperactivity in non-medicated adults suffering from ADHD (Mahajan et al. 2010), while longer sleep latencies, low sleep quality and daytime sleepiness were reported by adult ADHD patients (Bijlenga et al. 2011; Schredl et al. 2007; Surman et al. 2009). Shorter and later sleep were found to be linked with hyperactivity (Bijlenga et al. 2011). Polysomnography and actigraphy studies in adults diagnosed with ADHD also revealed reduced sleep efficiency, as well as alterations in other sleep parameters (Boonstra et al. 2007; Kooij et al. 2001; Sobanski et al. 2008; Van Veen et al. 2010). Eveningness, a psychometric parameter describing the preference of an individual for later bed and wake times, as well as patterns of alertness and activity associated with later times during the day, has also been found to be linked with inattention (Bae et al. 2010; Caci et al. 2009; Rybak et al. 2007) and hyperactivity (Bae et al. 2010). Recent B. I. Voinescu (&) A. Szentagotai D. David Department of Clinical Psychology and Psychotherapy, Babes-Bolyai University, Cluj-Napoca, Romania DOI 10.1007/s00702-012-0862-3 preference are associated with changes in circadian rhythms at both hormonal (Baird et al. 2011; Van Veen et al. 2010) and molecular levels (Baird et al. 2011). There are two main groups of adults with ADHD: those with a known diagnosis in childhood and who still have symptoms, and those who do not have a pre-existing diag- nosis. As ADHD in adults has only been relatively recently recognized in many European countries, many individuals may have never been identified with the disorder as a child. Moreover, as the comorbidity with other psychiatric disor- der s is high, the risk of being misdiagnosed or for remaining undiagnosed and consequently mis- or untreated is considerable. To better understand the associations between sleep disturbance, diurnal preference and ADHD in adults, we conducted an exploratory research on young adults. This population is at a higher risk to display ADHD symptomatology, is generally physically healthy and may represent an ideal population to examine relationships between self-reported adult ADHD symptomatology, sleep timings, circadian type, sleep quality and insomnia severity (Sample 1). Then, we broadened our research by including older adults and recruited participants from across Romania (Sample 2). In our opinion, this gave us a glimpse on the current situation of adult ADHD and chronic insomnia symptoms in the general community, as well as the opportunity to better understand the links between circadian typology, sleep quality and timings on ADHD in adults. Methods only (Sample 1) and one in general population (Sample 2). Along with providing demographic data, they all com- pleted a battery of tests translated into Romanian that was filled in via Surveygizmo platform. The studies had been approved by the ‘‘Babes-Bolyai’’ University Ethics Committee. Participants was 21.82 (standard deviation (SD) 2.52). No other demographic data were collected. were women (N = 176, 70.4 %). Mean age was 38.61 (SD 12.40). More than a half completed undergraduate educa- tion (N = 134; 53.6 %) and 33.2 % postgraduate one (N = 83). The o majority were employed (N = 218, 87.2 %) and 6.0 % (N = 15) were retired. Seven people (2.8 %) declared they were unemployed. More than a half (N = 144, 57.6 %) reported incomes of less than 1,500 RON (about €350) and being married (N = 140, 56.0 %). The respondents were from all over Romania, but around a third were from the cities of Baia Mare and Cluj-Napoca only (33.2 %, N = 83). The Adult Self-Report Scales (ASRS) Symptom Checklist is the official instrument of the WHO (Kessler et al. 2005) and is available in many languages.1 It has two forms: a standard version, which contains eighteen DSM-IV items, and a shorter one, the ASRS Screener, that has four inat- tention items and two hyperactivity items. It is generally accepted to detect self-report pathology in adults (Rosler et al. 2010). The items can be scaled from 0 to 4. Internal consistency reliability of the ASRS Screener was 0.678 and of the whole scale 0.909, which is comparable to available data (Kessler et al. 2007; Adler et al. 2006). The Barkley Adult ADHD Rating Scale-IV (BAARS- IV): Current Symptoms is a new behavior rating scale for adult ADHD symptoms that consists of the 18 DSM-IV symptoms (9 for inattention, 5 for hyperactivity and 4 for impulsivity) together with 9 additional items for evaluating the symptoms of sluggish cognitive tempo (SCT), a pos- sible distinct type of ADHD (Barkley 2011). As in the case of ASRS, it has also a shorter version: the Quick Screen. The items are scaled from 1 to 4. Internal consistency was 0.777 for the screener, 0.914 for total score, 0.870 for Inattention, 0.754 for the Hyperactivity, 0.807 for the Impulsivity and 0.852 for SCT subscales, respectively. Sleep disturbance report categorical questionnaire, which evaluates the presence of insomnia according to the DSM-IV and ICSD- R criteria (Violani et al. 2004). It allows respondents’ classification into three categories: good sleep, chronic insomnia and sub-threshold insomnia. In this paper, we used the term ‘‘chronic insomnia’’ for the sleep disturbance that was reported as being present three or more nights per week, which lasted for more than 1 month and caused significant impairment in social, occupational or cognitive 1 downloadable from http://www.hcp.med.harvard.edu/ncs/asrs.php. daytime functioning. Sub-threshold insomnia was defined as above in terms of duration and impairment, but had to be reported for 2–3 nights per week instead of more than three nights per week. The term ‘‘acute insomnia’’ was used when insomnia had been present for less than a month, for at least 3 days in a week, and had caused significant impairment in at least one area of daytime functioning. The Sleep Condition Indicator (SCI) is a new insomnia self-report instrument (Espie 2011) that consists of eight items, scored on a Likert scale from 0 (Not at all) to 4 (Very much) that gathers information on sleep pattern in the last month (minutes needed for falling asleep, minutes being awake during the night, number of problem nights in a week), sleep quality, impact of poor sleep, level of concern about poor sleep and history of poor sleep. It is based on proposed DSM-5 criteria. Internal consistency was 0.862. Diurnal preference used instrument for determining circadian typology (mor- ningness/eveningness) and is available in several lan- guages. It contains 13 questions, most of them having four choices, with a Likert-type response format and total scores range from 13 (extreme eveningness) to 55 (extreme morningness) (Smith et al. 1989). We used authors’ rec- ommendations and calculated the cut off scores for the sample using the 10/90 percentile (higher than 42 for morningness, lower than 24 for eveningness). The Sleep Timing Questionnaire (STQ) is an alternative to a sleep journal and contains 16 questions regarding sleep timings and their variability for work and rest nights, as well as 2 items for ‘‘unwanted wakefulness’’ (Monk et al. 2003). Procedure Psychology at ‘‘Alexandru Ioan Cuza’’ University in Iasi and at ‘‘Babes-Bolyai’’ University in Cluj-Napoca, Romania, to participate in an online survey. They were given a web link with the description of the study and offered extra credit for participating in the research. Col- lection took place during the first and second semesters of 2011. Participants for Sample 2 were recruited from adults from the general community via a dedicated website, online adverts posted on health-related sites, as well as via adverts in local mass media in Cluj-Napoca, Romania. Participation was unpaid and all respondents received a brief interpretation of their scores on the completion of the questionnaires, as well as the possibility of a free basic clinical assessment if it was the case. Data collection took place during the second semester of 2011. Data analysis sub-total scores. T tests or ANOVAs were used to compare the differences between means and the Chi-Square test for differences between frequencies among various groups, respectively, with p \ 0.05 considered significant. Pearson R or Spearman q was used for calculating correlations between different variables. FUZZY extension2 was used to match participants. Data analysis was performed with IBM SPSS Statistics 20.0.0. We first examined differences in age and scores in ADHD scales that could be related to gender and found that men scored significantly higher in BAARS Hyperactivity sub- scale in Sample 2. There were significant differences for the total morningness and sluggish cognitive tempo scores between Samples 1 and 2, As seen in Table 1, the differ- ence in diurnal preference was obvious as about a third in Sample 2 were morning types (compared to less than 10 % in Sample 1), as might be expected due to the different age profiles of the samples. Using ASRS and BAARS-IV and the proposed cut-off points (Barkley 2011; Gau et al. 2007), we identified 46 (8.3 %) participants (aged 26.93 (10.14), most of them women (N = 32, 69.6 %)), who were likely to meet the DSM-IV criteria for ADHD. The majority were from Sample 1 (N = 30, 9.9 % of the total), while the remaining third came from Sample 2 (N = 16, 6.4 % of the total). Based on responses in SDQ, 73 (13.24 %) participants met the criteria for chronic insomnia, while 327 (59.3 %) reported sleeping soundly. A minority (N = 35, 6.4 %) complained of acute symptoms, while the rest of the sleep disturbance that did not meet the DSM or ICSD criteria for acute or chronic insomnia (‘‘sub-threshold’’ insomnia). Chronic insomnia had a prevalence of 11.3 % in Sample 1 and 15.6 % in Sample 2. From those likely to suffer from ADHD, 21.7 % (N = 10) met the criteria for chronic insomnia, another ten (21.7 %) for sub-threshold insomnia and six more (13.0 %) for acute insomnia, meaning that 2 available for download at http://www.ibm.com/developerworks/ spssdevcentral. Sleep disturbance, circadian preference and symptoms of adult ADHD 1197 54.5 %). We eliminated those selected for being highly likely to suffer from ADHD or from chronic insomnia and randomly matched the ADHD-likely participants by age and sex with 46 ‘‘healthy controls’’ (mean age 27.00 ± 10.34, 30.4 % men, N = 14). Evening typology was significantly more frequent in the ADHD group (23.9 %, N = 11) than in the control one (4.3 %; N = 2), while there were significantly fewer morning types (10.9 %, N = 5 in ADHD group, 19.6 %, N = 9 in Non-ADHD one). Comparisons revealed significant differences in sleep quality and morningness score, with the ADHD-likely group sleeping worse, and displaying more evening orientation, as indicated by higher SCI scores and lower CSM scores, respectively (Table 2). We also compared these same parameters in those of the remaining sixty-three participants complaining of chronic insomnia (after exclusion of the ten ADHD-likely sub- jects), as matching by age and sex could not be performed. Significant differences were found in sleep quality score and in all ADHD scales, with insomnia suspects scoring higher in SCI and lower in ADHD scales (Table 2). Compared to the control group, those likely to suffer from chronic insomnia scored higher in all ADHD scales, particularly in the SCT. Chronotype distribution did not differ significantly between the groups. When analyzing the differences in sleep timings (going to/going out of bed times, both in workdays and rest days), we found that ADHD-likely individuals went to bed later than the healthy controls, particularly before a rest day, and also got out of bed at a later time (Table 3). Regarding sleep duration and latency, ADHD-likely respondents reported significantly less time being asleep and more time needed to fall asleep (19.6 %, N = 9 reported needing more than 45 min com- paring to none among controls); when comparing these to insomnia participants, they slept less, although the differ- ences were not significant; nevertheless, 34.9 % (N = 22) in the insomnia group reported needing more than 45 min for falling asleep and 38.1 % (N = 24) being awake for more than the same amount of time, compared to only 8.7 %, N = 4 in ADHD group. In the ADHD-likely sample, we found that latest waking up time during rest days was moderately correlated with SCI (Spearman q = 0.348, p = 0.03) but not correlated with ADHD symptoms. Also, SCT scores had a large association with SCI (q = 0.659, p \ 0.001), and moder- ately so with impulsivity (q = -0.410, p = 0.006) and inattention (q = 0.488, p = 0.001). Morningness score was moderately linked with SCI (q = -0.328, p = 0.026) and inattention (q = -0.360, p = 0.018). Among the insomnia group, habitual bed time (q = -0.304, p = 0.028) and rising time at weekends (q = -0.329, Table 1 Summary of the descriptive data for samples 1 and 2 Sample 1 Sample 2 Females Males Total Females Males Total N (%) 255 (84.7) 46 (15.3) 301 176 (70.4) 74 (29.6) 250 Age (SD) 21.78 (2.55) 22.00 (2.39) 21.82 (2.52) 37.80 (12.10) 40.53 (12.95) 38.61 (12.4) ASRS (SD) Inattention (SD) 14.50 (6.18) 16.33 (5.54) 14.81 (6.10) 21.04 (3.85)a 22.00 (5.94)a 21.26 (4.28) Hyperactivity/impulsivity (SD) 12.13 (5.88) 14.30 (6.43) 12.50 (6.01) 17.38 (5.85)a 14.86 (4.74)a 16.81 (5.64) BAARS-IV Inattention (SD) 15.26 (4.55) 16.37 (4.89) 15.43 (4.61) 14.46 (4.23) 15.09 (4.53) 14.64 (4.32) Hyperactivity (SD) 7.42 (2.41) 7.94 (3.04) 7.49 (2.51) 6.82 (2.13) 7.90 (2.42) 7.12 (2.26) Impulsivity (SD) 6.88 (2.46) 7.10 (3.04) 6.91 (2.54) 6.46 (2.14) 7.07 (2.25) 6.63 (2.18) Sluggish cognitive tempo (SD) 17.24 (4.88) 17.58 (5.38) 17.29 (4.94) 15.50 (4.24) 16.41 (4.41) 15.76 (4.30) CSM (SD) 33.24 (6.59) 32.32 (6.82) 33.1 (6.54) 37.42 (7.90) 36.53 (8.03) 37.15 (7.93) SCI (SD) 11.96 (6.31) 11.30 (6.06) 11.86 (6.27) 11.85 (7.83) 11.21 (6.79) 11.66 (7.53) ADHD likely N (%) 22 (73.3) 8 (26.6) 30 (9.9) 10 (62.5) 6 (37.5) 16 (6.4) Chronic insomnia N (%) 31 (91.1) 3 (8.9) 34 (11.3) 27 (69.2) 12 (30.8) 39 (15.6) Circadian typology Morning (%) 26 (10.2) 2 (4.3) 28 (9.3) 64 (36.4) 18 (24.3) 82 (32.8) Indifferent (%) 201 (78.8) 36 (78.3) 237 (78.7) 100 (56.8) 48 (64.9) 148 (59.2) Evening (%) 28 (11.0) 8 (17.4) 36 (12.0) 12 (6.8) 8 (10.8) 20 (8.0) a Scores were calculated only for those who screened positive in the ASRS screener (N = 31) 1198 B. I. Voinescu et al. 123 p = 0.021) were associated with SCI scores. Hyperactivity scores were significantly, but weakly associated with sleep duration (R = -0.177, p = 0.024) and sleep latency (R = 0.176, p = 0.024) in the whole sample, but not in the ADHD group. during childhood significantly more frequently than con- trols (N = 8, X = 6.03, p = 0.014), as well as more cur- rent sleep problems (onset and maintenance insomnia, non- refreshing sleep) and daytime sleepiness (Table 4). Other analyses quality, while hyperactivity showed a small magnitude association. A small negative association of inattention with total morningness score was detected in Sample 1 and a larger one in Sample 2 (Table 5). When examining differences between average scores on ADHD scales according to circadian typology and presence of insomnia, Table 2 Comparison of BAARS-IV ASRS Circadian typology Table 3 Sleep timings for ADHD-likely, non ADHD and Rest days Good morning time (SD) Rest days Sleep duration (SD) 5.64 (1.39) 7.18 (1.23)** 6.17 (1.55) Sleep latency (SD) 32.71 (24.77) 15.18 (7.36)** 41.79 (36.02) Sleep disturbance, circadian preference and symptoms of adult ADHD 1199 123 we found significant differences (Table 6). As we had a large number of morning types when using the authors’ criteria (Smith et al. 1989), we calculated the cut-off points by three different age groups and 10/90 percentiles. According to the new criteria, 54 (9.8 %) participants were evening types (compared with 56 initially) and 58 (10.5 %) morning types (110 initially). ANOVA revealed significant differences across the different circadian preferences or insomnia in Inattention, Hyperactivity, SCT and SCI scores, but not in Impulsivity (Table 6). Post hoc tests showed that the differences were significant when com- paring insomnia subtypes to no insomnia (but not between insomnia subtypes) and between chronotypes (evening types scored higher). ADHD and insomnia symptoms, sleep and circadian typology. Our study protocol allowed us to gather and compare data from two different populations: young adults (students) and an older cohort from the general population. We found that ADHD symptoms were more severe in younger adults and that eveningness was more frequent both among ADHD and chronic insomnia suspected indi- viduals, while inattention was strongly linked with dis- turbed sleep. Sleep disturbance, but not ADHD symptoms, was linked with some of the sleep timings, and was reported by more than a half of the ADHD-likely group (summarized in Fig. 1). the hyperactivity scale compared to women, across all ages, and that this was more pronounced in older subjects. Also, the young adult sample revealed significant lower morningness scores compared to the older sample, with a likely explanation being the effect of age on chronotype (Paine et al. 2006; Park et al. 1998). ADHD-likely indi- viduals were likely to be younger, probably as symptoms reduce in severity during lifetime, while insomnia was more prevalent in the general population sample, sleep becoming more superficial and shorter in duration with advancing age. ing up too early or non-refreshing sleep, (the core symp- toms of insomnia disorder) were reported by more than a half of the probable-ADHD group, with slightly less than a quarter of this group complaining of these symptoms…