ADHD symptoms and maturity a study in primary school children

Acta Pædiatrica ISSN 0803–5253 REGULAR ARTICLE ADHD symptoms and maturity – a study in primary school children P Gustafsson ([email protected]....
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Acta Pædiatrica ISSN 0803–5253

REGULAR ARTICLE

ADHD symptoms and maturity – a study in primary school children P Gustafsson ([email protected])1 , G Thernlund1 , J Besjakov2 , MK Karlsson3,4 , I Ericsson5 , CG Svedin6 1.Department of Child and Adolescent Psychiatry, Lund University, Lund, Sweden 2.Department of Radiology, Malmo¨ University Hospital, Malmo, ¨ Sweden 3.Clinical and Molecular Osteoporosis Research Unit, Department of Clinical Science, Lund University, Lund, Sweden 4.Department of Orthopaedics, Malmo¨ University Hospital, Malmo, ¨ Sweden 5.School of Education, Malmo¨ University, Malmo, ¨ Sweden 6.Division of Child and Adolescent Psychiatry, IMK, Faculty of Health Sciences, Linkoping ¨ University, Linkoping, ¨ Sweden

Keywords ADHD-symptoms, Biological maturity, Maturational-lag, Motor function Correspondence P Gustafsson, Department of Child and Adolescent Psychiatry, Malmo University Hospital, SE-205 02 Malmo, Sweden. Tel: +4646174436 | Fax: +4646133324 | Email: [email protected] Received 24 June 2007; revised 23 August 2007; accepted 29 October 2007. DOI:10.1111/j.1651-2227.2007.00608.x

Abstract Aim: To study if age and non-behavioural measures of biological maturity have any associations with attention deficit hyperactivity disorder (ADHD). Methods: Two hundred fifty-one children 7 to 9 years of age in a Swedish school were screened for ADHD-symptom. ADHD-symptoms were estimated by Conners Abbreviated Questionnaire by both parents and teachers. Motor function, body weight and body height were measured. Skeletal age was estimated through hand radiographs. Results: Height, weight and skeletal bone-age did correlate significantly with age (rs = 0.44–0.69, p < 0.001) but not with ADHD symptom scores. Motor dysfunction had a weak negative correlation with age (rs = −0.21, p < 0.05). Parent and teacher scores of ADHD-symptoms did not correlate with age. Conclusion: This study showed that the variables measuring general biological maturity had a strong association with age, whereas motor dysfunction and ADHD symptoms had no significant association with age. ADHD symptoms did not correlate with the variables measuring general biological maturity. These results do not support the hypothesis that a general biological immaturity is an important etiologic factor for ADHD symptomatology.

INTRODUCTION Attention deficit hyperactivity disorder (ADHD) is defined by difficulties in sustaining attention and/or hyperactivity impulsivity. These symptoms have important developmental aspects and change considerably over time (1,2). Children with ADHD perform like younger children in tests of executive functions (3). About 50% of children with ADHD have been described as having developmental coordination disorder (DCD), which also has a developmental aspect (4,5). Thus, the idea of a maturational-lag as an underlying cause of ADHD has been proposed by some researchers (6,7) while others have opposed this idea and have claimed that children with ADHD have deficits in brain functioning (8–10). ElSayed and Steffensson (11,12) propose that ADHD in some cases may be due to a relatively slower rate of mental maturation with the possibility of a catch-up occurring later. The concept of maturational-lag or a slower pace of development is intriguing. The difference between grown-ups and children is supposed to be that the pace of development is much faster in children and that some aspects of development end at some point e.g. increase in height. If some more slowly developing children are to catch up, they either will have to show a sudden leap in development or a longer time period will have to elapse until the development begins to slow down or cease. Children with mental retardation have both a slower pace of development and less complex devel-

opmental stages. They cannot be expected to catch up completely, as their development supposedly begins to cease at about the same age as it does for normal children. For premature children a catch-up in length is expected, but a catch-up is not expected for children who are short due to a genetic disposition. Children with motor dysfunction might improve with increasing age, but some will continue to have motor problems in adulthood and others may have subclinical degrees of motor dysfunction (13). Denckla postulates that Fog’s test and ‘mirror movements’ significantly distinguish children with hyperactivity from normal controls, that is hyperactive children had overflow-movements like younger children, which she contributes to an anomalous maturation of inhibitory function (14). Over-activity has been shown to decrease with age so that only one in two school children will meet full criteria for over-activity at 22 years of age (13). The diagnosis of ADHD is difficult to make in young children, as many normal preschool children are more hyperactive and impulsive and have shorter attention span than majority of the older children, a fact which could support the idea of a maturational-lag. There is also a sex difference in both activity level and attention. The aim of this study was to test the theory put forward by El Sayed and Steffensson that ADHD in children in some cases may be due to a slow biological speed of maturation, that is a maturational-lag (12). To examine this theory, we proposed the following questions:

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1. Is there a marked decline of ADHD symptoms with age that will possibly be determined by comparing school children from grade one, two and three in elementary school, a decline that could support the theory of maturationallag? 2. Is there an association between ADHD symptoms and biological measures of maturity, like skeletal bone-age, height, weight and motor function? SUBJECTS AND METHODS All children from grade one, two and three in an elementary school in Malmo, ¨ Sweden (n = 251) participating in a study of the effect of additional physical exercise on skeletal bone density as well as motor functioning and learning (15,16), were screened for ADHD symptoms by parental and teacher self-report questionnaires before the exercise intervention was initiated. In the total population, the internal drop-out frequency concerning skeletal bone-age was 50 children (20%), and for height and weight 40 children (16%). The internal drop-out was 18 children (7.2%) for the parent Conners ratings, 3 children (1.2%) for the teacher Conners ratings and 6 children (2.3%) for the motor examination. When comparing examined children (for bone-age, height and weight) and drop-outs, there were no significant differences between the two groups concerning Conners ratings (according to both parents and teachers). Methods ADHD symptoms The Conners Abbreviated Questionnaire, including 10 questions, was used to define ADHD-symptoms (17). The questionnaires were filled in by both the parents and the teachers. Every item is scored on a 0–3 scale. The total score is the sum of the individual items and ranges between 0 and 30, with higher scores indicating more clinical problems. The reliability has been studied by Goyette et al. (18). Pearson correlations of inter-parent agreement were found to be 0.55 and parent–teacher agreement 0.49 (in the present study 0.44). In the present study, internal consistency, measured by Cronbach’s alpha, was found to be 0.76 for parent ratings (n = 233) and 0.92 for teacher ratings (n = 248). Motor function The physical education teacher performed a standardised motor examination called ‘motor development as a basis for learning’ (MUGI) (16), see Appendix I. Each item is scored on a scale 0–2. The total score is the sum of the individual items and ranges between 0 and 32, with higher scores indicating poor function. The tests were performed by three trained examiners. The internal consistency in this study, estimated by Cronbach’s alpha, was found to be 0.80. The inter-rater reliability between the three examiners was found to have a mean correlation of 0.75. The MUGI examination has been constructed according to theories of children’s normal motor development and has items similar to other examinations like those described by Kadesjo¨ and Gillberg (19), Holle et al. (20) and Bille et al. (21). Normative data for

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Swedish children has previously been reported by Ericsson (22). Body height, body weight, skeletal bone-age and diff. bone age, defined as the difference between the child’s chronological age and the child’s skeletal bone-age in months The height in centimetres was measured for all children by using a wall tapered height meter. The weight in kilograms was measured by using an electronic scale. The standardized height and standardized weight measures were calculated and expressed in z-scores, that is number of standard deviations from the mean for sex and age in the Swedish population. The children underwent a radiographic anterioposterior X-ray examination of the hand, from which the skeletal bone-age was assessed by an experienced skeletal radiologist (JB) according to the Greulich method and Pyle method (23). The difference between the child’s chronological age and the child’s skeletal bone-age in months (which we will refer to as the diff. bone-age) was then calculated. Chronological age The chronological age of the child in months was registered at the examination when height, weight and skeletal boneage also were measured. Statistics The Spearman correlation equation was used to compare the measures of age, ADHD symptoms, height, weight, skeletal bone-age and motor function. The Mann–Whitney test was used to compare diff. bone-age in children with high and low Conners scores. One-sided statistical power estimates were made by using the correlation coefficient calculator from the UCLA department of statistics (updated May 2002). Ethical considerations The study was approved by the Ethical Committee at the Medical Faculty, Lund University, LU 330-99 and the Radiographic Committee at Malmo¨ University Hospital, and all parents of participating children gave their written consent. The study was conducted according to the declaration of Helsinki 2000 and the Swedish Data Inspection Board approved the data collection and the database. RESULTS Table 1 shows basic information for all children. Table 2 shows correlations between age and estimates of maturity as body height, body weight, skeletal bone-age, motor function according to the MUGI-examination and Conners parent and teacher scores. Height, weight and skeletal bone-age did correlate significantly with age (Table 2). Motor dysfunction had a weak negative correlation with age (not significant after correction for multiple comparisons). Conners parent and teacher scores did not correlate with age, standardized height, standardized weight, skeletal bone-age or diff bone-age. Motor function did not correlate significantly

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Table 1 Median, inter-quartile range, maximum and minimum values for different variables Grade 1, 2, 3 (n = 251) Item

n

Median

Range

Minimum

Maximum

Height (cm) All 210 Girls 91 Boys 119

131.8 131.1 132.5

127.6–137.3 127.7–137.1 127.2–137.5

111.1 111.1 112.3

151.5 146.6 151.5

Weight (kg) All 210 Girls 91 Boys 119

28.6 29.0 28.3

25.2–33.6 24.9–33.3 25.3–34.1

16.0 17.8 16.0

58.0 53.5 58.0

Standardized height (SD) All 210 0.4 Girls 91 0.5 Boys 119 0.2

−0.3–1.0 −0.06–1.0 −0.5–1.1

−2.1 −2.0 −2.1

3.1 2.4 3.1

Standardized weight (SD) All 210 0.6 Girls 91 0.6 Boys 119 0.6

−0.3–1.6 −0.4–1.6 −0.2–1.6

−3.0 −3.0 −2.2

7.0 6.0 7.0

Skeletal bone-age (months) All 203 96.0 Girls 88 94.0 Boys 115 96.0

84.0–96.0 94.0–106.0 84.0–108.0

50.0 50.0 60.0

138.0 132.0 138.0

Diff. bone-age (months) All 203 −2.0 Girls 88 −1.0 Boys 115 −3.0 Conners parents (points) All 233 2.0 Girls 104 1.0 Boys 129 3.0

−10.0–4.0 −9.0–6.0 −12.0–4.0

−31.0 −24.0 −31.0

33.0 33.0 32.0

0.0–5.0 0.0–4.0 0.0–5.5

0.0 0.0 0.0

24.0 15.0 24.0

Conners teachers (points) All 248 1.0 Girls 110 0.0 Boys 138 1.0

0.0–3.0 0.0–1.0 0.0–6.0

0.0 0.0 0.0

29.0 28.0 29.0

MUGI (points) All 245 Girls 110 Boys 135

2.0 2.0 3.0

1.0–6.0 0.0–4.0 1.0–7.0

0.0 0.0 0.0

30.0 19.0 30.0

Age (months All 208 Girls 89 Boys 119

101.0 100.0 101.0

91.0–106.0 90.0–106.0 92.0–106.0

71.0 71.0 81.0

118.0 118.0 116.0

with standardized height, standardized weight or diff. boneage but did correlate significantly with both Conners parent and teacher scores (Table 2). There are some important methodological problems to consider in this kind of analysis. One is that many children got a score of zero according to the parents (29.2%) and the teachers (49.2%) creating a floor-effect. Another question is whether some children without ADHD have a few ADHD-symptoms and if these can be regarded as indicting the same kinds of problems as the ones seen in children with a diagnosis. Furthermore, four items in the Conners questionnaire are not specific to ADHD but are associated with more general disruptive be-

haviour. To deal with these methodological problems, we performed an analysis with children scoring over the 90th percentile on the Conners parents questionnaire (Table 3). This analysis gave very similar results to the first with no correlations between the Conners scores and standardized height, standardized weight, skeletal bone-age and diff boneage. For age and Conners parent scores, there was a weak correlation that was no longer significant after correction for multiple comparisons. The weak correlation between motor function and age disappeared in the second analysis (Table 3). Motor function did have a weak correlation with Conners parent and Conners teacher scores, but did not correlate with standardized height, standardized weight or diff. bone-age. When children with Conners parent scores above the 90th percentile were compared with children below the 90th percentile, we found no significant difference in diff. bone-age. We also studied children who got scores over the 90th percentile according to the Conners teacher ratings, and this analysis gave results similar to the parent ratings. DISCUSSION This study showed only a weak non-significant correlation between age and ADHD-symptoms while there was a strong correlation between age and biological measures such as body height, body weight and skeletal bone-age. The data give no direct support to the hypothesis that ADHD symptoms are a function of general immaturity with a decreasing severity of symptoms with advancing age. Great caution must be taken when interpreting the results. The time frame of three years (more than 6 and less than 10 years of age) might be too short to study a decrease in ADHD symptoms, if the decline in symptoms occurs at a much slower rate than for changes in height, weight and skeletal bone-age. There could also be a bias so that the older children might have had different means and distribution of important variables when they were the same age as the younger children. To control these kinds of problems a longitudinal rather than a cross-sectional design should be employed, and we have been considering a follow-up study. No correlations were found between ADHD-symptoms and the biological measures standardized height, standardized weight, skeletal bone-age and diff. bone-age, thus contradicting the second hypothesis that there is an association between ADHD symptoms and general biological measures of maturity. The statistical power of detecting a correlation of 0.20 between the Conners scores and standardized height, standardized weight and diff.bone-age, when p < 0.05 was used as the significance level, was calculated to 80%. There are, of course, some problems in analysing variables such as height and weight. Weight and especially height are to a great deal genetically determined and individuals will have very different height and weight when they have grown up. Thus, height and weight only measure maturity to a certain degree, although somewhat better before than after the onset of adolescence. Because of these problems we have been especially interested in the results obtained by using skeletal bone-age as a measure of maturity. All

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Table 2 Spearman correlations between age and maturity dependent variables

Age (months) Skeletal bone-age Height Weight Conners parents Conners teachers MUGI

Age (months)

Skeletal bone-age

Height

Weight

Conners parents

Conners teachers

MUGI

1.000 n = 207 0.689∗∗∗ n = 199 0.667∗∗∗ n = 202 0.439∗∗∗ n = 202 −0.010 n = 201 −0.043 n = 205 −0.209∗ n = 203

1.000 n = 200 0.692∗∗∗ n = 199 0.550∗∗∗ n = 199 −0.005 n = 195 −0.047 n = 199 −0.100 n = 197

1.000 n = 210 0.771∗∗∗ n = 210 −0.003 n = 202 −0.076 n = 208 −0.132 n = 206

1.000 n = 210 −0.054 n = 202 −0.032 n = 208 −0.048 n = 206

1.000 n = 233 0.327∗∗∗ n = 231 0.208∗∗ n = 230

1.000 n = 248 0.277∗∗∗ n = 244

1.000 n = 245

Significance levels: ∗ = p < 0.05, ∗∗ = p < 0.01, ∗∗∗ = p < 0.001.

Table 3 Spearman correlation between age and maturity dependent variables for children scoring over the 90th percentile on the parent Conners questionnaire

Age (months) Skeletal bone-age Height Weight Conners parents Conners teachers MUGI

Age (months)

Skeletal bone-age

Height

Weight

Conners parents

Conners teachers

MUGI

1.000 n = 27 0.877∗∗∗ n = 26 0.667∗∗∗ n = 26 0.484∗ n = 26 −0.398∗ n = 27 −0.219 n = 26 −0.366 n = 26

1.000 n = 26 0.737∗∗∗ n = 26 0.504∗∗ n = 26 −0.351 n = 26 −0.069 n = 25 −0.225 n = 25

1.000 n = 26 0.859∗∗∗ n = 26 −0.264 n = 26 0.011 n = 25 −0.196 n = 25

1.000 n = 26 −0.216 n = 26 0.063 n = 25 −0.195 n = 25

1.000 n = 28 0.454∗ n = 27 0.481∗ n = 27

1.000 n = 27 0.396∗ n = 27

1.000 n = 27

Significance levels: ∗ = p < 0.05, ∗∗ = p < 0.01, ∗∗∗ = p < 0.001.

children will eventually mature so that the skeletal growth zones will close, which makes this measure more reliable as a true measure of maturity. If ADHD-symptoms can be regarded as associated with a slow rate of general biological maturation, children with ADHD ought to have lower skeletal bone-age than children without ADHD, but this was not what we found. Not unexpectedly, we found an association between ADHD symptoms and poor motor function in accordance with the concept of ‘deficits in attention, motor control and perception’ (DAMP) formulated by Gillberg and Gillberg (13,24,25). The reason we wanted to study motor dysfunction was not to show an association between ADHD and motor function, which has already been shown by several researchers (13), but rather to study patterns of development over time compared with ADHD-symptoms and the other variables used as measures of general biological maturation. Motor dysfunction did not show any association with our non-neurological measures of maturity.

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El Sayed et al. (11) reported motor dysfunction as a sign of immaturity, but they measured the motor function of their subjects only in order to exclude children with neurological disorders and DCD. Thus, our two neurological measures, ADHD-symptoms and motor function, had an association with each other but not with our more general biological measures height, weight and, most important, skeletal bone-age. There is of course a possibility that there may be a maturational-lag affecting only the development of the brain or of a part of it, with a slow catch-up so that we could not catch it with our limited time span of 3 years. El Sayed and Steffensson (11,12) argue that children with ADHD have patterns of EEG reminiscent of patterns in younger children with more low frequency components, thus supporting the theory that at least some children with ADHD have a slow CNS-maturation that will eventually catch up. Many researchers in the field have proposed that children with ADHD have a different brain function

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compared to normal controls. Some researchers have recently described qualitative differences between children with ADHD and younger normally developed children in patterns of processing of perceptual information and motor planning when studying event related potentials as well as in reaction-time patterns in tasks requiring inhibitory control and modulation of attention (26–28). Biederman et al. (29) have performed a longitudinal study of boys with ADHD that seems to indicate that most individuals with ADHD in childhood continue to have problems in adulthood, even those who no longer fulfil criteria for an ADHD-diagnosis. Castellanos et al. (30) have described decreased total brain volume for children and adolescents with ADHD, where developmental trajectories for all brain structures except the caudate nucleus remain roughly parallel for patients and controls showing no tendency of catchup. In adult ADHD patients, inhibition deficits as well as a slower reaction time and enhanced variability have been described (5), indicating that these deficits persist until adulthood. In our study, we found no support for the theory of a general biological immaturity, where the child shows signs of biological immaturity of the kind a normal younger child would show, as an important etiologic factor for ADHD symptomatology. To determine if there is a true ‘catch-up’ in an immature group of children with ADHD, a study is needed where children with ADHD who are also classified as immature are followed into adulthood.

ADHD symptoms and maturity

8. 9.

10.

11.

12.

13.

14. 15. 16.

17.

ACKNOWLEDGEMENTS This study was supported by the Lindhaga Foundation, Bror Gadelius minnesfond, The Council for Research in Health and Clinical Care in Southern Sweden, The Swedish Psychiatry Foundation, The Lindgren Foundation, Skanska, the Sven Jerring Foundation, the Konig-S oderstr omska ¨ ¨ ¨ Sjukhemmet Foundation and the Region of Skane (FoUU). ˚

18.

19.

20.

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Appendix I Items on the MUGI-examination performed by the physical education teacher in the school study • • • • • • •

• •

Track of gymnastics Imitating movements Alternating jumping left–right foot forward Walking with toes pointing outwards Standing on one leg, right and left Hopping on one leg, right and left Skip Jump (jumping two times forward with one foot in front of the other and then changing to keeping the other foot in front of the first and jumping two times forward and then continuing in the same way jumping two times before changing foot) Bouncing with a ball with one hand, both right and left Throwing and catching a ball

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