alertness problems and ADHD symptoms in a sample of obese adolescents

Journal of Psychosomatic Research 63 (2007) 587 – 590

Short communication

Parent reports of sleep/alertness problems and ADHD symptoms in a sample of obese adolescents Samuele Cortese a,b,⁎, Claudio Maffeis c , Eric Konofal b,d,e , Michel Lecendreux b,e , Erica Comencini a , Marco Angriman a , Brenda Vincenzi a , Franco Pajno-Ferrara a , Marie-Christine Mouren b , Bernardo Dalla Bernardina a a

Child Neuropsychiatry Unit, Department of Mother-Child and Biology-Genetics, G.B. Rossi Hospital, Verona University, Verona, Italy b Child and Adolescent Psychopathology Unit, Robert Debré Hospital, Paris VII University, Paris, France c Pediatrics Clinic, Department of Mother-Child and Biology-Genetics, G.B. Rossi Hospital, Verona University, Verona, Italy d Pediatric Sleep Disorder Center, Robert Debré Hospital, Paris VII University, Paris, France e Sleep Disorder Center, Pitié-Salpetrière Hospital, Paris, France Received 17 April 2007; received in revised form 9 August 2007; accepted 9 August 2007

Abstract Objective: Recent evidence suggests an association between obesity and Attention Deficit/Hyperactivity Disorder (ADHD) or ADHD traits. The characteristics of obese subjects with a higher probability of ADHD symptoms are still unclear. We explore the hypothesis that obese adolescents with sleep/alertness problems represent a subgroup at high risk for ADHD traits, independently from associated symptoms of anxiety/depression. The aim of this study was to assess the relationship between parent reports of sleep/alertness problems and ADHD traits in a clinical sample of obese adolescents, controlling for symptoms of anxiety/depression. Methods: Seventy obese subjects (age range, 10–16 years) were included. The parents filled out the Sleep Disturbance Scale for Children (SDSC), the Conners Parents Rating Scale-Revised (Short Version) (CPRS-R:S), and the Child Behavior Checklist (CBCL). The ADHD Rating Scale (ADHD-RS) was completed by

a child psychiatrist. Results: Using multiple regression models controlling for symptoms of anxiety/depression, scores of excessive daytime sleepiness on the SDSC were significantly associated with ADHD traits on the CPRS-R:S as well as on the ADHD-RS. Conclusions: Obese adolescents described as excessively sleepy by their parents may be at higher risk of ADHD symptoms, independently from symptoms of anxiety/depression. Although the clinician may overlook a potential diagnosis of ADHD in obese adolescents described as sleepy, the results of this study suggest to systematically look for symptoms of ADHD in this subgroup of obese patients. Further studies using objective methods to assess sleep/alertness disturbances are needed to gain insight into the relationship between sleep/alertness disturbances and ADHD in obese individuals. © 2007 Elsevier Inc. All rights reserved.

Keywords: Sleep; Alertness; Sleepiness; ADHD; Obesity; Adolescents

Introduction Recent evidence suggests an association between obesity and Attention Deficit/Hyperactivity Disorder (ADHD) (diagnosed according to standardized criteria) [1–3] or ADHD traits (i.e., ADHD symptoms without full ADHD criteria) ⁎ Correspondng author. Servizio di Neuropsichiatria infantile, Ospedale G.B. Rossi, P.le L. A. Scuro, 10, 37134 Verona, Italy. Tel.: +39 0458074398; fax: +39 045501118. E-mail address: [email protected] (S. Cortese). 0022-3999/07/$ – see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jpsychores.2007.08.005

[4,5]. However, the characteristics of obese subjects with a higher probability of ADHD symptoms are still unclear. We explore the hypothesis that obese adolescents with sleep/alertness problems represent a subgroup at high risk for ADHD traits. Available evidence supports a significant association between ADHD and excessive daytime sleepiness (EDS) (primary or determined by any sleep disorders) [6]. Several studies reported a significant association between obesity and sleep disturbances[7], including Sleep Disordered Breathing (SDB) [8,9], which may lead to EDS. Recent

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studies demonstrated that even obese patients without SDB may present higher EDS than controls, suggesting that, at least in some patients, EDS may be related to a metabolic and/or circadian abnormality associated with obesity more than being a consequence of SDB [10–12]. Given the relationship between sleep/alertness problems and ADHD traits, and considering the relevance as well as the peculiarities of sleep/alertness disturbances in obese subjects, we were interested in gaining insight into the relationship between sleep/alertness problems and ADHD traits in this specific population. In particular, in the present study we felt it would be interesting to focus on the parental perception of ADHD traits and sleep/alertness problems in obese adolescents. Given the role of the parents as informants during the clinical consultation, we believe that this aspect may be of interest in the clinical practice with obese children and adolescents. Therefore, the aim of the present study was to assess the relationship between parent reports of sleep/alertness problems and ADHD traits in a clinical sample of obese adolescents. Since inattention, hyperactivity, and impulsivity are common symptoms not only of ADHD but also of depression and anxiety [13], we felt it important to assess the relationship between sleep/alertness problems and ADHD traits controlling for symptoms of depression and anxiety.

Methods

Box–Cox transformation (LMS method) based on national norms [15]. During the first visit, parents were asked to fill out the following questionnaires: 1) The Sleep Disturbance Scale for Children (SDSC) [16]: it includes 26 items. The SDSC consists of six factors: difficulty in initiating and maintaining sleep (DIMS), sleep-breathing disorders (SBD), arousal disorders (DA), sleep-wake transition disorders (SWTD), disorders of excessive sleepiness (DOES), and sleep hyperhydrosis (SHY). The total score is the sum of the 26 items. 2) The Conners Parents Rating Scale-Revised (Short Version) (CPRS-R:S) [17]: this questionnaire consists of 27 items. The CPRS-R:S include four scales: oppositional, inattention, hyperactivity, and the ADHD index. The ADHD index provides a global measure of symptoms of inattention, hyperactivity, and impulsivity. The inattention and hyperactivity scores, as well as the ADHD index, were used in the statistical analysis; 3) The Child Behavior Checklist (CBCL) [18]: it is a standardized checklist which consists of eight symptom clusters (subscales): withdrawn, somatic complaints, anxious/depressed, social problem behaviors, thought problems, attention problems, delinquent behaviors, aggressive behaviors. The anxious/ depressed scores were used in the statistical analysis.

Subjects The study sample consisted of obese patients referred to the outpatient clinic of the Department of Pediatrics at the University Hospital in Verona, Italy. Criteria for the inclusion were (1) obesity [body mass index (BMI) N95th percentile for age and sex reference values] and (2) age range between 10 and 16 years. Exclusion criteria were (1) secondary causes of obesity, (2) use of medications which may impact sleep, and (3) parents of the patients unable to provide the requested information. The final study sample consisted of 70 obese subjects. The children and their parents gave their informed consent to the study. The protocol was approved by the Ethics Committee of the University of Verona. Procedure Demographic and clinical data were obtained from the subjects and their parents during an initial consultation. Each child underwent a physical examination, including height, weight, and puberty development on the basis of Tanner stages [14]. The BMI was calculated as weight (kilograms) divided by height (meters) squared. National BMI charts were used as the reference [15]. BMI values were standardized (BMI Z-score) using age- (to the nearest month) and sex-specific median, S.D., and power of the

ADHD traits were also evaluated using the ADHD Rating Scale (ADHD-RS) [19], which is an interview with the patient's parent(s), rated by the investigator. It consists of 18 items. The ADHD-RS includes two subscales (Inattention and Hyperactivity–Impulsivity) and provides three scores: Total, Inattention, and Hyperactivity–Impulsivity. Statistical analysis Demographic and clinical data were shown as means and S.D. or percentages. The relationship between parentally reported sleep problems, anxious/depressed symptoms, and ADHD traits was assessed using bivariate correlations and multiple regression models. A probability level of Pb.05 was used to indicate statistical significance. All statistical analyses were performed using the SPSS v. 13.0 software (SPSS, Chicago, IL, USA).

Results Table 1 shows the demographic and anthropometric characteristics of the subjects. Bivariate correlations showed that the inattention, hyperactivity, and ADHD index scores

S. Cortese et al. / Journal of Psychosomatic Research 63 (2007) 587–590 Table 1 Demographic and clinical characteristics of the subjects

n Age (y) Weight (kg) Height (cm) BMI (kg/m2) BMI Z-scores Race Caucasian Puberty stage 1 2 3 4 5

Females

Males

All patients

37 12.2 (1.3) 69.3 (16.4)* 152.2 (15.8) 30.9 (3.7) 2.3 (0.6)

33 13.1 (1.7) 82.2 (25.6) 157.5 (26.7) 34.5 (5.3) 2.5 (0.6)

70 12.6 (1.65) 75.9 (22.3) 154.9 (22.0) 32.7 (14.1) 2.4 (0.6)

37 (100)

33 (100)

70 (100)

7 (18.9) 6 (16.2) 6 (16.2) 4 (10.8) 14 (37.8)

6 (18.2) 6 (18.2) 9 (27.3) 4 (12.1) 8 (24.2)

13 (18.6) 12 (17.1) 15 (21.4) 8 (11.4) 21 (30.0)

Data are shown as mean and S.D. or percentage. Significant difference: *Pb.05.

on the CPRS-R:S as well as the Inattention scores on the ADHD-RS were significantly correlated with the SDSCDOES scores (respectively, r=0.442, P=.001; r=0.459, P=.001; r=0.468, P=.001; r=0.380, P=.008) as well as with the CBCL anxious/depressed scores (respectively, r=0.368, P=.008; r=0.424, P=.007; r=0.480, P=.005; r=0.268, P=.012). Using the SDSC–DOES scores and the CBCL anxious/depressed scores as independent variables in regression models, the associations between the CBCL anxious/depressed scores and the inattention, hyperactivity, ADHD index, and ADHD-RS Inattention scores were no more significant (Table 2). The Hyperactivity–Impulsivity as well as the Total scores on the ADHD-RS were significantly correlated with the DA, SWTD, DOES, total scores on the SDSC, and CBCL anxious/depressed scores (respectively, r=0.348, P=.005; r=0.423, P=.003; r=0.398, P=.05; r=0.482, P=.001; r=0.348, P=.005 for the Hyperactivity-Impulsivity scores and r=0.306, P=.035; r=0.299, P=.039; r=0.415, P=.003; r=0.405, P=.004; r=0.390, P=.004 for the ADHD-RS Total scores). Using the CBCL anxious/depressed scores and DA, SWTD, and DOES as independent variables in multiple regression models, DOES was the only variable significantly associated with the Hyperactivity–Impulsivity ADHD-RS and ADHD-RS Total scores (Table 2). Discussion This is the first study that specifically assessed the relationship between parentally reported sleep/alertness problems and ADHD traits in a sample of obese children and adolescents. The major finding of the present study was the significant association between parental reports of EDS and ADHD traits, even after controlling for symptoms of anxiety/ depression and for the other SDSC scores correlated to ADHD symptoms.

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Interestingly, EDS scores were significantly associated not only with symptoms of inattention but also with hyperactivity and impulsivity traits. This association may seem at first paradoxical. However, it may be explained considering the “hypoarousal theory” of ADHD, proposed by Weinberg and Harper [20]. According to this theory, children with ADHD/ADHD symptoms (or at least a subgroup of them) may actually be sleepier than controls and may use motor hyperactivity as a strategy to stay awake and alert in order to counteract the tendency to fall asleep [21]. Therefore, it is not surprising that a subset of parents in our study described their children as both sleepy and hyperactive. The results of our study also suggest that, in obese adolescents, parental reports of DIMS, SBD, DA, SWTD, and SHY do not seem to be a significant risk factor for

Table 2 Multiple regression analysis: final models

r2 Dependent variable: CPRS-I scores Independent variables DEOS AD Dependent variable: CPRS-H scores Independent variables DEOS AD Dependent variable: ADHD index Independent variables DEOS AD Dependent variable: ADHD-RS H-I scores Independent variables DEOS AD Dependent variable: ADHD-RS H-I scores Independent variables DEOS DA SWTD AD Dependent variable: ADHD-RS Total scores Independent variables DEOS DA SWTD AD

Standardized beta coefficients

S.E.

P

0.235 0.196

0.038 0.052

.046* .090

0.347 0.237

0.040 0.152

.036* .169

0.357 0.465

0.090 0.240

.012* .202

0.567 0.555

0.104 0.321

.010* .150

0.301 0.234 0.251 0.468

0.045 0.068 0.154 0.049

.047* .193 .092 .057

0.290 0.238 0.222 0.566

0.128 0.035 0.015 0.103

.037* .293 .553 .361

0.204

0.259

0.300

0.303

0.299

0.286

Significant association: *Pb.05. CPRS-I, Conners Parents Rating Scale-R inattention scores; CPRS-H, Conners Parents Rating Scale-R hyperactivity scores; ADHD index, ADHD index on the Conners Parents Rating Scale-R; AD, Child Behavior Checklist Anxiety/Depressed subscale; H-I, hyperactivity impulsivity.

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ADHD traits. Since our study was expressly designed to explore the parental perceptions, we cannot exclude that the severity of sleep disturbances evaluated using objective measures correlate significantly with ADHD traits in obese subjects. Some limitations of this study should be reported. First, the sample size was relatively small, and so, larger studies are needed to confirm our results. Second, no formal diagnosis of ADHD according to Diagnostic and Statistical Manual of Mental Disorders (DSM) criteria was conducted. However, we used the ADHD-RS which is based on DSM, Fourth Edition, Text Revision criteria. Moreover, given that even symptoms of ADHD not fulfilling full criteria may be socially impairing, we considered that it was noteworthy to explore the association between sleep problems and ADHD traits. Finally, the cross-sectional nature of the study makes it impossible to establish a relationship of causality between the variables. Notwithstanding these limitations, we believe that the results of our study may have important clinical implications. Parental reports of excessive daytime sleepiness may be considered by the clinician as an expression of the supposed “weak personality” of obese patients (i.e., laziness, inefficiency, etc.), and therefore, the clinician may overlook symptoms of hyperactivity and impulsivity in this subgroup of obese patients. Indeed, the results of our studies indicate that obese patients described as sleepy by their parents are also at risk for symptoms of hyperactivity and impulsivity. Therefore, we suggest to systematically look for symptoms of hyperactivity and impulsivity in obese patients described as sleepy. We also believe that the results of our study (based expressly on parents' reports) are of interest because they provide the basis for further studies using objective methodology in order to gain insight into the pathophysiology underlying the possible association between ADHD traits and sleep/alertness alterations in obese subjects. Given the significant personal, familial, and social burden associated with both obesity [22] and ADHD [23], research on the role of sleep/alertness disturbances as potential factors underlying the possible association between obesity and ADHD seems noteworthy and should be encouraged. References [1] Agranat-Meged AN, Deitcher C, Goldzweig G, Leibenson L, Stein M, Galili-Weisstub E. Childhood obesity and attention deficit/hyperactivity disorder: a newly described comorbidity in obese hospitalized children. Int J Eat Disord 2005;37:357–9. [2] Altfas JR. Prevalence of attention deficit/hyperactivity disorder among adults in obesity treatment. BMC Psychiatry 2002;2:9.

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