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Page 1: Balance in children with attention deficit hyperactivity disorder-combined type

Research in Developmental Disabilities 35 (2014) 1252–1258

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Balance in children with attention deficit hyperactivity

disorder-combined type

Hsun-Ying Mao a, Li-Chieh Kuo b, Ai-Lun Yang c, Chia-Ting Su d,*a Department of Physical Medicine & Rehabilitation, National Taiwan University Hospital Hsin-Chu Branch, Hsinchu, Taiwanb Department of Occupational Therapy, College of Medicine, National Cheng Kung University, Tainan, Taiwanc Graduate Institute of Exercise Science, University of Taipei, Taipei, Taiwand Department of Occupational Therapy, College of Medicine, Fu Jen Catholic University, New Taipei City, Taiwan

A R T I C L E I N F O

Article history:

Received 10 January 2014

Accepted 8 March 2014

Available online

Keywords:

Attention deficit hyperactivity disorder

(ADHD)

Balance ability

Dynamic sitting

Mechanical horseback riding

Motion analysis

A B S T R A C T

The balance ability in children with attention deficit hyperactivity disorder-combined

type (ADHD-C) has not been fully examined, particularly dynamic sitting balance.

Moreover, the findings of some published studies are contradictory. We examined the

static and dynamic sitting balance ability in 20 children with ADHD-C (mean age: 9 years 3

months; 18 boys, 2 girls) and 20 age-, sex-, height-, weight-, and IQ-matched healthy and

typically developing controls (mean age: 9 years 2 months; 18 boys, 2 girls). The balance

subtests of the Movement Assessment Battery for Children (MABC) and the Bruininks-

Oseretsky Test of Motor Proficiency (BOTMP) were used to compare the two groups, and a

mechanical horseback riding test was recorded using a motion-capture system. Compared

with the controls, children with ADHD-C had less-consistent patterns of movement, more

deviation of movement area, and less-effective balance strategies during mechanical

horseback riding. In addition, their performance on the balance subtests of the MABC and

BOTMP were not as well as those of the controls. Our findings suggest that balance ability

skill levels in children with ADHD-C were generally not as high as those of the controls in

various aspects, including static and dynamic balance.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Attention deficit hyperactivity disorder (ADHD) is one of the most common disorders in school-age children; theworldwide-pooled prevalence is 5.29% (Polanczyk, de Lima, Horta, Biederman, & Rohde, 2007). Some researchers have paidattention to the balance ability in children with ADHD (Piek, Pitcher, & Hay, 1999; Raberger & Wimmer, 2003; Schlee,Neubert, Worenz, & Milani, 2012; Tseng, Henderson, Chow, & Yao, 2004). Adequate balance ability is important for manydaily activities (Larkin & Hoare, 1992). Insufficient balance ability negatively affects not only children’s motor performancebut also the psychosocial aspect of their life (Shum & Pang, 2009; Simeonsson et al., 2003). Some studies (Piek et al., 1999;Shum & Pang, 2009; Tseng et al., 2004) on children with ADHD-combined type (ADHD-C) report that their balance issignificantly less proficient than that of matched controls without ADHD, but this finding was not consistent with otherreports (Pitcher, Piek, & Hay, 2003).

* Corresponding author at: Department of Occupational Therapy, College of Medicine, Fu Jen Catholic University, 510 Zhongzheng Road, Xinzhuang Dist.,

New Taipei City 24205, Taiwan. Tel.: +886 2 2905 2091; fax: +886 2 2904 6743.

E-mail addresses: [email protected], [email protected] (C.-T. Su).

http://dx.doi.org/10.1016/j.ridd.2014.03.020

0891-4222/� 2014 Elsevier Ltd. All rights reserved.

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1.1. ADHD and balance ability

Piek et al. (1999) used the Movement Assessment Battery for Children (MABC) to assess motor performance in 16 childrenwith ADHD-predominantly inattentive type (ADHD-PI), 16 children with ADHD-C, and a group of 16 age- and verbal-IQ-matched children without ADHD (controls). Their results showed that children with ADHD-PI ‘‘had significantly poorer finemotor skills. . . [and that those] with ADHD-C had significantly greater difficulty with gross motor skill’’ than did the controls.Consistently, Tseng et al. (2004) found that children with ADHD-C demonstrated poorer balance as measured by theBruininks-Oseretsky Test of Motor Proficiency (BOTMP). However, in another MABC-based study on balance in 104 boyswith ADHD and 39 controls without (Pitcher et al., 2003), they found no significant differences in the static and dynamicbalance subtest results. Thus, the question of balance ability in children with ADHD-C is still open.

1.2. ADHD and dynamic balance ability

Although the MABC and BOTMP balance subtests can tell us something about balance performance, they are lessinformative about dynamic balance performance and balance strategies (Hatzitaki, Zisi, Kollias, & Kioumourtzoglou, 2002).In daily life, dynamic balance ability is required for many tasks (Shumway-Cook & Woollacott, 2007). Because few studieshave investigated dynamic balance in children with ADHD, we used a (dynamic) mechanical horse and a motion analysissystem in our study.

1.3. Purposes of this study

The aim of our study was to examine the static and dynamic balance ability of children with ADHD-C. To our knowledge,this was the first study measuring dynamic balance ability in children with ADHD by using the objective motion analysis andmechanic horse. We hypothesized that children with ADHD-C would have static and dynamic balance performance levelsthat differed significantly from those of children without ADHD.

2. Methods

2.1. Participants

Forty children (age range: 6 years 8 months–12 years 4 months) were recruited from elementary schools in southernTaiwan. Twenty of them, 18 boys and 2 girls (mean age: 9 years 3 months [SD: 1 year 4 months]; age range: 7 years 7months–12 years 4 months), were diagnosed with ADHD-C by child psychiatrists using the criteria from the Diagnostic andStatistical Manual of Mental Disorders-4th edition (DSM-IV; American Psychiatric Association, 1994). The 20 controls, 18boys and 2 girls, were between 6 years 10 months and 11 years 4 months (mean age: 9 years 2 months [SD: 1 year 2 months]).There were no significant differences in age, height, or weight between the two groups. All participants met the age-equivalent score on the Similarities and Vocabulary subtests of the Wechsler Intelligence Scale for Children, 3rd edition(WISC-III). These two subtests were chosen because the combination of their results was viewed as one of the best indicatorsfor general cognitive ability (Sattler, 1992). The manual muscle test (MMT) was used to screen out children with abnormalmuscle strength that might affect the balance measurements; all the recruited children met the level of good or normalstrength. To confirm the grouping, a parental questionnaire to screen children with ADHD, Conners’ Parent Rating Scale-Revised Short Form, was used to assess all of the participants. The results supported the diagnosis of ADHD for each child inthe ADHD group, and indicated that none of the controls had the symptoms of ADHD.

2.2. Instruments

2.2.1. Qualisys motion capture system

The motion capture system (ProReflex-MCU 240; Qualisys Medical AB, Gothenburg, Sweden) used was a passive optoelectronickinematic analyzer with infrared cameras, a personal computer, and software. The camera unit used reflected infrared light todetect the position of each retro-reflective marker worn by participants. The motion data were captured at a sampling rate of100 Hz. A digital Butterworth filter with a cutoff frequency of 10 Hz was used to eliminate high-frequency noise. Forty-five retro-reflective markers 20-mm in diameter were attached at different body landmarks (Fig. 1) to estimate the movement ofparticipant’s center of mass (COM). Three markers were set on the mechanical horse (one on the front and two on the rear) toprovide a base when analyzing the motion during horseback riding. During data collection, a trial that contained four completecycles (i.e., four repetitions of motion) was considered sufficient for analysis. Three parameters of balance were drawn from thecollected data: (1) consistency of COM deviation in the four cycles: the more consistent the COM movement between cycles, themore stable the balance strategy; (2) deviation of COM area ratio: the ratio of the difference between the COM movement area ofthe horse and participant to the COM movement area of the horse (i.e., the absolute value of [COM movement of horse area� COMmovement of participant area]/[COM movement of horse area]): the larger the ratio, the less skilled the participant’s ability toadjust body movement based on how the mechanical horse moves; and (3) the largest COM differences in medial–lateral (ML) andanterior–posterior (AP) directions during movement, which is the largest length in the M–L and A–P minus the smallest length in

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[(Fig._1)TD$FIG]

Fig. 1. (A) Marker set (anterior view): twenty-eight circular markers were placed on the head, sternum, acromion (bilaterally), lateral elbow, wrist, anterior

superior iliac spine, medial ankle, foot (3rd metatarsal), and T-shaped markers for fixed 3D position were placed on both thighs and legs. (B) Marker set

(posterior view): seventeen markers placed on C7, L3, sacrum, and bilaterally on the medial elbow, medial metacarpal, lateral and medial knees, lateral

ankle, and heel. The medial elbow (upper arrows, B), knee (lower arrows, B), and ankle (arrows, A) were removed after the landmarks had been orientated.

H.-Y. Mao et al. / Research in Developmental Disabilities 35 (2014) 1252–12581254

the M–L and A–P directions of COM movement during mechanical horseback riding. The larger the value of this parameter, thelarger range of movement needed to maintain balance in that direction.

2.2.2. Mechanical horse

A mechanical horse (Joba EU-6441; Matsushita Electric Industrial Co., Ltd., Japan) designed based on the movementpattern of a real horse (i.e., a figure of eight) was used in our study. It includes nine levels of speed (range: 0.55–1.29 Hz). Theriders rely on their dynamic sitting balance ability to maintain their posture and prevent themselves from falling.

2.2.3. Movement Assessment Battery for Children (MABC)

The MABC is designed for assessing the motor competence of 4- to 12-year-old children. It contains four age bands, andincludes eight different items (three for manual dexterity, two for ball skills, and three for static and dynamic balance) ratedon a 6-point (0–5) scale. A higher score means greater motor impairment. The test has acceptable validity and reliability(Henderson & Sugden, 1992). We used the static and dynamic subtest to assess the balance ability of children, as did priorstudies (Piek et al., 1999; Pitcher et al., 2003; Raberger & Wimmer, 2003; Tseng et al., 2004).

2.2.4. Bruininks-Oseretsky Test of Motor Proficiency (BOTMP)

The BOTMP is designed to assess the gross and fine motor skills in children from 4 years 6 months to 14 years 6 monthsold. The battery composite is the sum of eight subtest scores: running speed and agility, balance, bilateral coordination,strength, upper-limb coordination, response speed, visual-motor control, and upper-limb speed and dexterity. Its validityand reliability were acceptable (Bruininks, 1978). We used its 8-item balance subtest to detect balance ability, as did Tsenget al., 2004.

2.3. Procedures

This study had ethical approval from the National Cheng Kung University Hospital Ethics Review Board (HumanExperiment and Ethics Committee). After obtaining the signed informed consent statements from all participants and their

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parents, the CPRS-R, MMT, and WISC-III Vocabulary and Similarities subtests were used to screen the participants for ourstudy. To minimize the effects of medication on the outcome measures, children with ADHD taking medication were asked todiscontinue their medication for 24–48 h before the tests. During the mechanical horseback riding, each participant wasinstructed to sit straight on the mechanical horse, look forward, and put both hands on the reins and both feet on thefootrests. A riding trial was performed for 10 s at a speed of 1.29 Hz (the maximum intensity of this mechanical horse). If thechildren moved their hands or feet from the supporter or if less than four cycles of movement were detected by our motionsystem, that trial was considered a failure. One or more trials were conducted until the required data were collected. All ofour participants were able to complete mechanical horseback riding without falling down and demonstrate one successfultrial. Following the evaluation of dynamic sitting balance during mechanical horseback riding, participants were tested byusing the balance subtests from the MABC and BOTMP. A total session of evaluation lasted for 70–90 min, and participantswere given 3- to 5-min breaks between tests.

2.4. Statistical analysis

SPSS 15 was used for all statistical analyses. The intraclass correlation coefficient (ICC) of the four cycles was calculated toassess the consistency of COM movement during the mechanical horseback riding for each group. Independent t tests wereused to compare differences between the two groups in the mean of the deviation of the COM area ratio during the fourcycles and in the largest COM difference of M–L and A–P direction, and to analyze differences in the balance ability scores onthe MABC and BOTMP balance subtests. Significance was set at p< 0.05.

3. Results

Examples of representative COM movement indicated that the child with ADHD-C demonstrated a pattern (Fig. 2A)different from that of the typically developing child (Fig. 2B). Specifically, the figure of movement was more unregulated andless similar to the figure of eight made by the mechanical horse (Fig. 2C) in the child with ADHD-C.

According to Rosner (2006), an ICC value smaller than 0.4 indicates poor reproducibility, and 0.4–0.75 means fair-to-goodreproducibility. During the mechanical horseback riding, the ICC value was low (0.09; p = 0.17) for the patterns in the fourcycles in the children with ADHD-C. In the control group, the ICC value was acceptable (0.67; p< 0.01) in all four cycles. Inaddition, the independent t test showed a significantly larger deviation of the COM area ratio (p< 0.05) and larger values forthe largest COM difference in the M–L (p< 0.01) and A–P (p< 0.01) directions for the ADHD-C group (Table 1).

Table 1

Differences in center of mass movement during mechanical horseback riding.

Measure Controls (n = 20) ADHD-C (n = 20) t p-Value

Mean SD Mean SD

Deviation of COM 0.39 0.20 0.64 0.36 2.34** 0.01

M–L direction 11.49 6.11 21.05 7.64 3.78** 0.00

A–P direction 15.57 9.18 29.81 18.43 2.68** 0.01

Controls, typically developing children; ADHD-C, attention deficit hyperactivity disorder-combined type; COM, center of mass; Deviation of COM

deviation of COM area ratio; M–L, medial–lateral; M–L direction, COM largest difference in M–L; A–P, anterior–posterior; A–P direction, COM larges

difference in A–P.

** p� 0.01.

[(Fig._2)TD$FIG]

C.B.A.

Horse_X (mm)

440.00420.00400.00380.00

Horse_Y

( mm)

260.00

240.00

220.00

200.00

180.00

COM M-L(mm)

0.00-20.00-40.00

COM

A-P(mm) 100.00

80.00

60.00

COM M-L(mm)

40.0020.000.00-20.00-40.00

COM

A-P(mm)

150.00

120.00

90.00

60.00

Fig. 2. (A) Movement pattern of a child with ADHD-C. (B) Movement pattern of a typically developing child. (C) Movement pattern of the mechanical horse.

The child with ADHD-C showed a more inconsistent movement pattern than did the matched control. COM, center of mass; M–L, medial–lateral; A–P,

anterior–posterior.

,

t

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Table 2

Differences in balance subtest scores for children with ADHD-C and typically developing children.

Measure Controls (n = 20) ADHD-C (n = 20) t p-Value

Mean SD Mean SD

BOTMP 15.80 4.41 10.15 5.03 �3.78** 0.00

MABC 0.55 1.15 3.75 3.27 4.13** 0.00

Controls, typically developing children; ADHD-C, attention deficit hyperactivity disorder-combined type; BOTMP, Bruininks-Oseretsky Test of Motor

Proficiency; MABC, Movement Assessment Battery for Children.

** p� 0.01.

H.-Y. Mao et al. / Research in Developmental Disabilities 35 (2014) 1252–12581256

Children with ADHD-C had significantly (p< 0.01) higher scores than did the controls on the static and dynamic balancesubtests of the MABC, and significantly (p< 0.01) lower scores on the balance subtest of the BOTMP (Table 2), which meansthat their balance performance was not as good.

4. Discussion

We found that, after the effects of ADHD medication had been adjusted for, the balance performances on the MABC,BOTMP, and mechanical horseback riding tests in typically developing children were significantly better than those inchildren with ADHD-C.

The current study appears to be the first to explore the dynamic sitting balance in children with ADHD-C while they areriding a mechanical horse. The finding of low consistency of COM movement in all four cycles during the mechanicalhorseback riding for children with ADHD-C indicated their unstable patterns of performance. This finding implies that [1]children with ADHD-C may have had difficulty finding the correct strategy for adjusting their movements while horsebackriding, and thus they continuously changed their patterns of movement in order to find a better strategy; or [2] they mighthave found the correct strategy, but were unable to maintain the same pattern of movement. The cerebellum is important formotor timing (Buderath et al., 2009) and correction errors (Bijsterbosch et al., 2011). Children with ADHD have a smallercerebellum volume than do typically developing children (Buderath et al., 2009; Durston, 2003), which may affect theirstrategies for maintaining dynamic balance. In addition, the control of dynamic balance is regulated by the neuromuscularsystem and related sensory systems: the somatosensory, vestibular, and visual systems (Hatzitaki et al., 2002). The brainneeds to organize different types of sensory information at the same time to perceive an individual’s orientation and tocoordinate the timing, direction, and force level of different limb segments to maintain balance during movement(Shumway-Cook & Woollacott, 2007). Some studies (Cheung & Siu, 2009; Engel-Yeger & Ziv-On, 2011; Lin, Yang, & Su, 2013;Mangeot et al., 2001; Miller, Nielsen, & Schoen, 2012) have reported that children with ADHD do not modulate sensory inputas well as do children without ADHD. This may contribute to their difficulties in finding the correct strategy for maintainingdynamic balance. Moreover, as dynamic balance ability is challenged, the related motor plan needs to be executed by thefeed-forward control of the musculoskeletal system to make postural adjustments (Hatzitaki et al., 2002). The motorperformance of children with ADHD is problematic (Tseng et al., 2004). The difficulty in sensory integration and motorperformance in children with ADHD may negatively affect their motor consistency in dynamic balance.

When riding the mechanical horse, children with ADHD-C showed a greater deviation of COM area ratio than did thecontrols. In addition, the irregular patterns of their COM movement were revealed. These indicated that children with ADHD-C had difficulties and used a larger area of movement to keep their body movement in accord with the movement of themechanical horse (i.e., the figure of 8). Furthermore, children with ADHD-C needed a larger range of movement in both theM–L and A–P directions to maintain their balance. These results may suggest that the children with ADHD-C needed a greaterrange of motion for the trial-and-error process of finding the right strategy to keep balance. Task constraints, maturity, andenvironmental demands influence the selection of appropriate balance strategies (Hatzitaki et al., 2002). Some researchers(Kalff et al., 2003) have reported that children with ADHD-C react less accurately and move less stably than do childrenwithout ADHD. During mechanical horseback riding, the whole body is in movement, and the base of support continuouslychanges position, as does the rider’s head. This challenges the sensory systems, especially the vestibular system, which isimportant for dynamic balance control (Shum & Pang, 2009). Because children with ADHD have difficulty with sensorymodulation (Cheung & Siu, 2009; Engel-Yeger & Ziv-On, 2011; Lin et al., 2013; Mangeot et al., 2001; Miller et al., 2012), theymay have to use more of a trial-and-error process than children without ADHD have to. Reaction time is also important fordynamic movement in the M–L plane (Hatzitaki et al., 2002). Shorter reaction times reduce the disturbance of the COM andthe preparation of postural adjustment for the task (Riach & Hayes, 1987). Therefore, perhaps because children with ADHDhave more difficulties to control their sensory modulation (Mangeot et al., 2001) and movement patterns (Kalff et al., 2003),and because they have longer reaction times (Rommelse et al., 2008; Sergeant & van der Meere, 1988) than do childrenwithout ADHD, children with ADHD are less able to maintain their dynamic balance during mechanical horseback riding.

Our results from both the MABC and the BOTMP balance subtests were in line with most other studies (Piek et al., 1999;Raberger & Wimmer, 2003; Rommelse et al., 2008; Tseng et al., 2004; Wang, Huang, & Lo, 2011). Some studies (Krain &Castellanos, 2006; Mackie et al., 2007) have reported that children with ADHD have smaller cerebellar hemispheric volumes,

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especially in the posterior inferior lobe of the cerebellum. Because the cerebellum is a motor coordination center, smallercerebellar hemispheric volumes may influence motor control and coordination, which might contribute to a less well-developed balance ability in children with ADHD. In addition, some researchers (Tseng et al., 2004; Wang et al., 2011;Yochman, Ornoy, & Parush, 2006) have said that sustained attention is an important predictive factor of motor performance.

Balance ability is essential for many daily activities. Balance dysfunctions may result in higher risk of injuries (DiScala,Lescohier, Barthel, & Li, 1998), especially in some situations that demand high-level balance ability, such as sports activities.The balance ability in children with ADHD should be of concern when setting up a treatment plan. For example, our findingssuggest that children with ADHD need more of a trial-and-error process to maintain their dynamic balance, which mayencourage us to provide some specific training to manage this difficulty.

This study has some limitations. Because our sample size was small, it may limit the generalization of our findings. Itwould also be interesting to explore dynamic balance using different perspectives of measurement and different types oftasks. For example, a force plate can be used to record precise quantitative data of kinetics, such as the body’s center ofpressure (COP). Schlee et al. (2012) used a force plate to measure COP in simple test situations and found that children withADHD showed levels of performance similar to those of children without ADHD. Mechanical horseback riding can be seen asa complex task for testing balance. Moreover, additional studies to explore the relationships of sensory processes withbalance ability should be beneficial for clarifying how to help children with ADHD.

5. Conclusion

This was the first study to show that children with ADHD-C have impaired dynamic balance during mechanical horsebackriding. Specifically, they had less-consistent patterns of movement and a more extended area for trial-and-error in theirattempt to maintain dynamic balance. In addition, children with ADHD did not score as well as children without ADHD onthe MABC and BOTMP balance subtests.

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