PAPER Overweight and obesity in children with Attention-Deficit - Nature

International Journal of Obesity (2004) 28, 685–689 & 2004 Nature Publishing Group All rights reserved 0307-0565/04 $25.00 www.nature.com/ijo

PAPER Overweight and obesity in children with Attention-Deficit/Hyperactivity Disorder ¨ ller1, N Heussen2, S Herpertz3, B Herpertz-Dahlmann1 and K Holtkamp1*, K Konrad1, B Mu 4 J Hebebrand 1

Department of Child and Adolescent Psychiatry and Psychotherapy, Technical University of Aachen, Germany; Department of Medical Statistics, Aachen University, Germany; 3Department of Psychiatry and Psychotherapy, University of Rostock, Germany; and 4Department of Child and Adolescent Psychiatry and Psychotherapy, University of Marburg, Germany 2

OBJECTIVE: Epidemiological studies suggest that adiposity in children may be associated with a reduced level of physical activity. Children with Attention-Deficit/Hyperactivity Disorder (ADHD) are physically hyperactive as of early childhood and have been shown to exhibit higher levels of motor activity than normal. The aim of our study was to assess if the prevalence of overweight and obesity is lower in a population of boys with ADHD in comparison with the German healthy male reference population of the same age. DESIGN: Patients were investigated from 1999 until 2001 upon referral to the inpatient and outpatient unit of the Department of Child and Adolescent Psychiatry of the University of Aachen. SUBJECTS: A total of 97 male patients (mean age 1072 y) with a diagnosis of ADHD according the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV), who were free of potentially orexigenic medication and who had no further comorbid diagnosis apart from conduct disorder. MEASUREMENTS: BMI standard deviation scores (BMI-SDS) were calculated and compared to age-adapted reference value of the German population. RESULTS: Patients’ mean BMI–SDS was significantly higher than the age-adapted reference values of the German population (P ¼ 0.038). Our sample included significantly more subjects than expected with a BMI Z90th percentile (19.6%, Po0.001) and Z97th percentile (7.2%, P ¼ 0.007). CONCLUSION: Surprisingly, being ‘hyperactive’ in the sense of the DSM-IV diagnosis of ADHD does not prevent the development or persistence of overweight and obesity in children. The examination of these children might be a helpful approach in the investigation of the relationship between obesity and its contributing psychological and behavioural factors. International Journal of Obesity (2004) 28, 685–689. doi:10.1038/sj.ijo.0802623 Published online 16 March 2004 Keywords: attention deficit; obesity; physical activity; children

Introduction Overweight and obesity result from a prolonged positive energy balance. Since physical activity is an important component of energy expenditure, it is often assumed that a low level of physical activity is involved in the aetiology of obesity and overweight. However, the relationship between physical activity and fatness is not as clear as might be

*Correspondence: Dr K Holtkamp, Department of Child and Adolescent Psychiatry, University of Aachen, Neuenhofer Weg 21, Aachen 52064, Germany. E-mail: [email protected] Received 30 July 2003; revised 16 December 2003; accepted 2 February 2004

expected. Evidence for an influence of childhood activity on the development of obesity is inconsistent, with studies roughly divided between finding either no effect.1–4 or a protective effect of activity.5–7 Indeed, there are a lot of methodological problems measuring physical activity, especially in children. Many studies so far have used questionnaires focusing on only few dimensions of activity that are believed to be easily recalled by children and their parents. However, questionnaires may be appropriate for assessing planned and vigorous activity like aerobic exercise, but are unlikely to be reliable in measuring daily living activity. Since activity of children is often sporadic and spontaneous in nature, and not particularly controlled by cognitions and because daily living activity may be more important than

Overweight and obesity in children withADHD K Holtkamp et al

686 aerobic exercise to prevent obesity,8–11 the use of activity questionnaires in children may lead to false negative results. In this regard, the examination of a population of children who naturally express a high level of lifestyle activity may represent an interesting alternative approach. According to the fourth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV;12), children with Attention-Deficit/Hyperactivity Disorder (ADHD) are physically hyperactive per definition. ADHD represents a neuropsychiatric disorder in which physical hyperactivity is present from early childhood on13,14 and must have caused impairment before the age of 7 y.12 According to the DSM-IV criteria, the following symptoms of hyperactivity have persisted for at least 6 months to a degree that is maladaptive and inconsistent with developmental level: (1) often fidgets with hands or feet or squirms in seat; (2) often leaves seat in classroom or in other situations in which remaining seated is expected; (3) often runs about or climbs excessively in situations in which it is inappropriate; (4) often has difficulty playing or engaging in leisure activities quietly; (5) is often ‘on the go’ or often acts as if ‘driven by a motor’. Porrino et al15 measured physical activity of ADHD children and controls by an acceleration-sensitive device placed at the trunk. Motor activity was automatically and continuously recorded for seven days, 24 h a day. They found that ADHD children were significantly more physically active than controls regardless of the time of day (P ¼ 0.02). As they placed the devise at the trunk, they recorded real body movements and not only fidgetiness. Therefore, it is reasonable to assume that boys with ADHD express a comparably high grade of lifestyle activity as of their early childhood. Thus, we hypothesized that the prevalence of overweight and obesity is lower in a population of boys with ADHD than in the German reference population of the same age.

Methods A clinical sample of 97 boys with the ADHD diagnosis of the combined type (combination of the inattentive and hyperactive-impulsive types; DSM-IV 314.01) aged between 5.5 and 14.7 y (mean 1072 y) admitted to the in-patient and outpatient units of the Department of Child and Adolescent Psychiatry of the University of Aachen from 1999 until 2001 were included in the study. These patients were originally recruited for a previous study assessing psychophysiological responses in ADHD boys with and without conduct disorder.16 Conduct disorder was defined according DSM-IV (312.8). Patients with ADHD and oppositional defiant disorder (DSM-IV 313.8) were excluded in that study and therefore were not part of the current investigation. A total of 14 patients received methylphenidate medication (mean duration: 5 months, mean dosage 0.5 mg/kg/day); all others were medication-naı¨ve. All children were diagnosed according to DSM-IV criteria by an experienced child and adolescent psychiatrist and a child psychologist. DSM-IV International Journal of Obesity

diagnose of ADHD and of conduct disorder were additionally assessed by the Diagnostic System for Psychiatric Disorders in Childhood and Adolescence (DISYPS;17). Only if both clinicians’ diagnoses were concordant with the DISYPS diagnosis, patients were included into the study. Parent and Teacher Rating Scales18 were obtained for all children as well (to be included in the study children had to have the following criteria: a minimal parent or teacher score of 15 and a minimal sum score of 30). The mean IQ as assessed by the German version of the Wechsler Intelligence Scale for Children (HAWIK-III,19) was 96710. Exclusion criteria were simple attention deficit disorder without hyperactivity (predominantely inattentive subtype, DSM-IV 314.00), IQ below 85 on both Verbal and Performance Scale of the HAWIK-III and an additional mental disorder (eg pervasive developmental disorder, psychosis, tics or a clinically significant anxiety or mood disorder). Clinically relevant somatic disorders and neurological disorders (eg epilepsy and traumatic head injuries) were excluded by medical history, physical examination and EEG. A routine blood test including TSH, T3 and T4 was only performed if there was any doubt on the medical diagnosis. Psychiatric exclusion criteria were assessed with the Diagnostic Interview for Psychiatric Disorders in Childhood and Adolescence (KinderDIPS,20), which is a standardized psychiatric interview. Children and their parents gave written informed consent after receiving a comprehensive description of the study. The Ethics Committee of the University of Aachen approved the study. Height was measured by stadiometry. Standard deviation scores (SDS) and percentiles were calculated according to age-adapted reference values of the German population (Kromeyer-Hausschild et al,21 http://www.mybmi.de). This reference BMI data set was compiled of 17 different studies including 17 147 boys and 17 275 girls aged 0–18 y. In line with the definition of the European Childhood Obesity Group22 and the practice guidelines of the German Obesity Society,23 children with a BMI Z90th percentile were classified as overweight and with a BMI Z97th percentile as obese. The w2 test was used to define if the occurrence of overweight and obese subjects was different in patients with ADHD compared to those with both ADHD and conduct disorder. One-sample t-test was used to compare SDS of patients to the mean reference value of 0. Binominal test was used to examine if the proportions of patients with BMI Zthe 90th and 97th percentile, respectively, were significantly higher than expected.

Results A total of 41 patients received a diagnosis of ADHD and 56 of ADHD in combination with conduct disorder. Anthropometric data of the whole sample are given in Table 1. Both groups showed no significant differences in the relative number of overweight (w2: 2.46; P ¼ 0.118) and obese subjects (w2: 2.42; P ¼ 0.122) nor in mean SDS of height


687 Table 1

Anthropometric data of 97 patients with ADMD Mean7SD

Age (y) Weight (kg) Weight-percentile Height (cm) Height-percentile BMI (kg/m2) BMI-percentile % of subjects with BMI Z90 percentile % of subjects with BMI Z97 percentile

1072 38712 54730 142712 49726 18.373.5 57730 19.6 7.2

(ADHD vs ADHD þ CD: 0.0570.93 vs 0.0570.87; P ¼ 0.98), weight (0.1670.87 vs 0.1771.25; P ¼ 0.99) and BMI (0.2770.92 vs 0.2371.34; P ¼ 0.88). Medicated and medication-naive patients did not significantly differ in height-SDS (0.1170.77 vs 0.0470.91; P ¼ 0.79), weightSDS (0.0671.22 vs 0.2071.09; P ¼ 0.39) and BMI-SDS (0.1071.42 vs 0.3171.13; P ¼ 0.22). Therefore, further statistics were performed for the whole sample. Patients’ mean BMI-SDS was 0.2571.2 and thus significantly higher than the mean reference value of 0 (P ¼ 0.038; Figure 1). The mean height-SDS (0.0670.9; P ¼ 0.67) did not significantly differ from 0. The proportions of overweight (19.6%; P ¼ 0.0008) and obese (7.2%; P ¼ 0.0075) subjects were significantly higher than expected.

Discussion To our knowledge this is the first study to assess the prevalences of overweight and obesity in ADHD patients. In contrast to our hypothesis, our ADHD sample had a significantly higher BMI-SDS and included significantly more overweight and obese subjects than the German population of the same age range. Therefore, our results argue against a protective influence of high levels of physical activity on the development and persistence of overweight and obesity in ADHD boys. Our results are in line with the studies of Robinson et al24 and of Maffeis et al,2 who found that higher activity levels of children were not associated with a decreased risk of later fatness. Nevertheless, since we did not directly measured physical activity (eg with accelerometry) and since we relied on the assumption that physical activity levels relevant for energy expenditure are increased in ADHD children, we can only hypothesize that increased physical activity levels does not provide a protective effect in our patient sample. Therefore, future studies should include objective measurements of physical activity to address this issue. We can only speculate on factors underlying the unexpected high prevalence of overweight and obesity in our patient group. Our study sample only includes subjects without significant comorbid medical and psychiatric disorders (especially depression) and without potentially orexi-

Figure 1 BMI standard devision scores (BMI-SDS) of 97 boys with attention deficit hyperactivity disorder (ADHD) in relation to reference values of the German population (grey dots ¼ MPH treated subjects, black dots ¼ treatment-naı¨ve subjects).

genic medication that might have contributed to the development of increased rates of overweight and obesity in medicated ADHD children. Methylphenidate often has anorexigenic side effects leading to weight loss.25 However, although we included 14 patients who received methylphenidate for a mean of 5 months, we still found a high prevalence of overweight and obesity in the whole study sample, and mean BMI-SDS of patients with or without methylphenidate medication did not differ significantly. Only few studies have addressed potential psychological or behavioural factors on food intake in the development of obesity in childhood. Moreover, mechanisms by which such factors might disturb energy balance appear largely untested.11 We have previously assessed BMI of children and adolescents with two other psychiatric disorders: obsessivecompulsive disorder26 and Asperger’s syndrome.27 In contrast to the current study, these two psychiatric conditions were characterized by predominance of children with BMI in the low percentile range. Pine et al28 reported a potentially relevant correlation between symptoms of conduct disorders during adolescence and obesity in early adulthood, attributed to common mechanisms underlying ‘impulsive aggression’ and dysregulation of body weight. Another study by Altfas29 reported a high prevalence of ADHD in obese bariatric adults, which was related to a poor treatment outcome. Altfas hypothesized that impulsivity might be involved in the onset or persistence of obesity. Consistently, Agranat et al30 reported that the prevalence of ADHD among International Journal of Obesity


688 morbidly obese children was significantly higher than in the population at large. In contrast, Mustillo et al31 demonstrated that in a general population sample, chronically obese children were not significantly more likely than nonobese children to have conduct disorder or ADHD. Nevertheless, the authors found chronic obesity to be associated with oppositional defiant disorder. Moreover, Lumeng et al32 found clinically meaningful behaviour problems in 8–11-y-old children independently associated with an increased risk of concurrent overweight and becoming overweight in previously normal-weight children. In sum, theses studies imply that at least in a subgroup of obese patients behavioural problems may be involved in the development or maintenance of overweight and obesity. Impulsive behaviour is a symptom of ADHD, conduct disorder and oppositional defiant disorder and as such may play a role in the development of obesity in ADHD children. Animal, genetic and neuroimaging studies suggest that the dopaminergic system plays a role in both the neurobiology of ADHD (for a review, see Biederman and Faraone33) as well as in the reward system of food-seeking behaviour (for a review, see Salamone et al34). Therefore, one may hypothesize that factors that are believed to contribute to children’s ADHD symptoms also affect their reward system for food and therefore change the appetizing value of certain food stimuli resulting in an increased food intake. The following limitations apply to our study: elevated mean BMI-SDS and rates of overweight and obesity in our ADHD children could be due to the fact that the reference population was assessed prior to our cases, implying that a secular trend might explain the observed results. Nevertheless, we have recently shown that the mean BMI of 6-yold children in the city of Aachen (where our department is situated) in the year 2002 was nearly completely concordant (51th percentile) with the 50th percentile of the reference population we have used in the current paper (Lamerz et al, in revision). Therefore, it seems to be unlikely that our results are due to the secular trend. Generalizability of conclusions based on our data is limited by the use of a clinical sample of ADHD boys only, which may not be representative of the general ADHD population. For this reason, our results need to be confirmed in nonclinical samples of both male and female subjects. Samples of children with conduct disorder often include a higher proportion of subjects with low socioeconomic status, which may account for an increased rate of overweight and obesity. Nevertheless, in our study, there were no differences in the relative number of overweight and obese subjects nor in mean SDS of height and BMI in children with ADHD in combination with conduct disorder in comparison to children with ADHD alone. However, future studies of obesity in ADHD children should control for known risk factors of obesity like socioeconomic status and BMI of the parents, which were not assessed in the current study. In sum, ADHD children may represent a population that expresses both higher rates of lifestyle activity and obesity. International Journal of Obesity

We hypothesize that further examination of these children will help to investigate the relationship between obesity and contributing psychological or behavioural factors.

Acknowledgements We thank the patients for their participation. This research was supported by the German Federal Ministry for Education and Research (NeuroNet Marburg, NGFN; 01 GS 0168 and 01 GS 0118).

References 1 Muller MJ, Grund A, Krause H, Siewers M, Bosy-Westphal A, Rieckert H. Determinants of fat mass in prepubertal children. Br J Nutr 2002; 88: 545–554. 2 Maffeis C, Talamini G, Tato L. Influence of diet, physical activity and parents’ obesity on children’s adiposity: a four-year longitudinal study. Int J Obes Relat Metab Disord 1998; 22: 758–764. 3 Treuth MS, Figueroa-Colon R, Hunter GR, Weinsier RL, Butte NF, Goran MI. Energy expenditure and physical fitness in overweight vs non-overweight prepubertal girls. Int J Obes Relat Metab Disord 1998; 22: 440–447. 4 Bandini LG, Schoeller DA, Dietz WH. Energy expenditure in obese and nonobese adolescents. Pediatr Res 1990; 27: 198–203. 5 Moore LL, Gao D, Bradlee ML, Cupples LA, Sundarajan-Ramamurti A, Proctor MH, Hood MY, Singer MR, Ellison RC. Does early physical activity predict body fat change throughout childhood? Prev Med 2003; 37: 10–17. 6 Lazzer S, Boirie Y, Bitar A, Montaurier C, Vernet J, Meyer M, Vermorel M. Assessment of energy expenditure associated with physical activities in free-living obese and nonobese adolescents. Am J Clin Nutr 2003; 78: 471–479. 7 Trost SG, Sirard JR, Dowda M, Pfeiffer KA, Pate RR. Physical activity in overweight and nonoverweight preschool children. Int J Obes Relat Metab Disord 2003; 27: 834–839. 8 Krebs NF, Jacobson MS. American Academy of Pediatrics Committee on Nutrition. Prevention of pediatric overweight and obesity. Pediatrics 2003; 112: 424–430. 9 Hill JO, Wyatt HR, Reed GW, Peters JC. Obesity and the environment: where do we go from here? Science 2003; 299: 853–855. 10 Epstein LH, Valoski A, Wing RR, McCurley J. Ten-year outcomes of behavioral family-based treatment for childhood obesity. Health Psychol 1994; 13/5: 373–383. 11 Parsons TJ, Power C, Logan S, Summerbell CD. Childhood predictors of adult obesity: a systematic review. Int J Obes Relat Metab Disord Suppl 1999; 23/8: 1–107. 12 American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association: Washington, DC; 1994. 13 Barley RA, Jackson T. Hyperkinesis autonomic nervous system activity and stimulant drug effects. J Child Psychol Psychiat 1977; 18: 247–258. 14 Kendall P, Brophy C. Activity and attentional correlates of teacher ratings of hyperactivity. J Pediatr Psychol 1981; 6: 451–458. 15 Porrino LJ, Rapoport JL, Behar D, Sceery W, Ismond DR, Bunney Jr WE. A naturalistic assessment of the motor activity of hyperactive boys. I. Comparison with normal controls. Arch Gen Psychiatry 1983; 40/6: 681–687. 16 Herpertz SC, Wenning B, Mueller B, Qunaibi M, Sass H, HerpertzDahlmann B. Psychophysiological responses in ADHD boys with and without conduct disorder: implications for adult antisocial behavior. J Am Acad Child Adolesc Psychiatry 2001; 40/10: 1222– 1230.


689 17 Doepfner M, Lehmkuhl G. Diagnostic system for mental disorders in child and adolescence according to ICD-10 and DSM-IV (DISYPS-KJ). Huber: Bern, Switzerland; 1998. 18 Conners CK. Rating scales for use in drug studies with children. Psychopharmacol Bull 1973; 9: 24–84. 19 Tewes U, Rossmann P, Schallberger U. Wechsler intelligence test for children, HAWIK-III, 3rd edn. Huber: Bern, Switzerland; 1999. 20 Unnewehr S, Schneider S, Margraf J. Diagnostic interview for psychiatric disorders in childhood and adolescence. Springer: Berlin, Germany; 1995. 21 Kromeyer-Hauschild K, Wabitsch M, Kunze D, Geller F, Gei HC, Hesse V, von Hippel A, Jaeger U, Johnsen D, Korte W, Menner K, ¨ ller G, Mu ¨ ller JM, Niemann-Pilatus A, Remer T, Schaefer F, Mu Wittchen H-U, Zabransky S, Zellner K, Ziegler A, Hebebrand J. Percentiles of body mass index in children and adolescents evaluated from different regional German studies. Monatsschr Kinderheilk 2001; 149: 807–818. 22 Poskitt EM. Defining childhood obesity: the relative body mass index (BMI). European Childhood Obesity group. Acta Paediatr 1995; 84: 961–963. 23 Wabitsch M, Kunze D. D 4 adipositas. In: Reinhardt D (ed). Leitlinien Kinderheilkunde und Jugendmedizin. Urban Fischer: ¨ nchen; 2002. pp 1–36. Mu 24 Robinson TN, Hammer LD, Killen JD, Kraemer HC, Wilson DM, Hayward C, Taylor CB. Does television viewing increase obesity and reduce physical activity? Cross-sectional and longitudinal analyses among adolescent girls. Pediatrics 1993; 91/2: 273–280. 25 Schertz M, Adesman AR, Alfieri NE, Bienkowski RS. Predictors of weight loss in children with attention deficit hyperactivity disorder treated with stimulant medication. Pediatrics 1996; 98: 763–769.

26 Henninghausen K, Rischmuller B, Heseker H, Remschmidt H, Hebebrand J. Low body mass indices in adolescents with obsessive-compulsive disorder. Acta Psychiatr Scand 1999; 99/4: 267–273. 27 Hebebrand J, Henninghausen K, Nau S, Himmelmann GW, Schulz E, Schafer H, Remschmidt H. Low body weight in male children and adolescents with schizoid personality disorder or Asperger’s disorder. Acta Psychiatr Scand 1997; 96/1: 64–67. 28 Pine DS, Cohen P, Brook J, Coplan JD. Psychiatric symptoms in adolescence as predictors of obesity in early adulthood: a longitudinal study. Am J Public Health 1997; 87/8: 1303–1310. 29 Altfas JR. Prevalence of attention deficit/hyperactivity disorder among adults in obesity treatment. BMC Psychiatry 2002; 13/2: 9. 30 Agranat AN Oral representation at the 50th Anniversary Meeting of the American Academy of Child and Adolescent Psychiatry in October 2003. 31 Mustillo S, Worthman C, Erkanli A, Keeler G, Angold A, Costello EJ. Obesity and psychiatric disorder: developmental trajectories. Pediatrics 2003; 111: 851–859. 32 Lumeng JC, Gannon K, Cabral HJ, Frank DA, Zuckerman B. Association between clinically meaningful behavior problems and overweight in children. Pediatrics 2003; 112: 1138–1145. 33 Biederman J, Faraone SV. Current concepts on the neurobiology of Attention-Deficit/Hyperactivity. J Atten Disord Suppl 2002; 6/1: 7–16. 34 Salamone JD, Correa M, Mingote S, Weber SM. Nucleus accumbens dopamine and the regulation of effort in foodseeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 2003; 305/1: 1–8.

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