Eur J Pediatr DOI 10.1007/s00431-013-2090-8

ORIGINAL ARTICLE

The effect of a weight management program on postural balance in obese children Nili Steinberg & Alon Eliakim & Michal Pantanowitz & Reuven Kohen-Raz & Aviva Zeev & Dan Nemet

Received: 28 February 2013 / Accepted: 28 June 2013 # Springer-Verlag Berlin Heidelberg 2013

Abstract The present study aimed to investigate whether obese children improve their balance and postural performance following a 6-month-weight management program. Twenty-nine obese children aged 6–14 years were examined posturographically before and after participation in weight management program. The interactive balance system evaluated the stability index, Fourier spectral analysis, weight distribution index, and falling index. The performance was evaluated for eight positions requiring closure of eyes, standing on pillows, as well as head turns. Anthropometric measurements (e.g., weight, height, BMI, and BMI percentiles) were also determined before and after the intervention. We found significant increase in height and significant decreased in BMI percentile following the intervention program (p<.05). Pre-intervention BMI percentile was found to be correlated with stability index in most of the positions measured (e.g., normal open position=.464; p=.011). Following the intervention program, an interaction was found between BMI percentile differences (pre- versus post-interventional) and balance (stability index and F2–F4 frequencies of most standing positions). Furthermore, a correlation was found between general stability and the falling index (.446; p=.015). Regression analysis showed that only initial weight

N. Steinberg (*) : A. Zeev Zinman College of Physical Education and Sport Sciences, Wingate Institute, Netanya, Israel e-mail: [email protected] A. Eliakim : M. Pantanowitz : D. Nemet Child Health and Sports Center, Department of Pediatrics, Meir Medical Center, Sackler School of Medicine, Tel-Aviv University, Kfar-Saba, Israel R. Kohen-Raz School of Education, Hebrew University, Jerusalem, Israel

distribution index and post-intervention BMI entered the equation as predictors of post-intervention weight distribution index. Conclusion: Weight management program for childhood obesity improved stability, reduced potential vestibular stress/disturbances, and decreased falling probability of the participants. Further longitudinal studies are needed to verify the relationship between physical activity, weight loss, and reduction of subsequent injuries in obese children. Keywords Childhood obesity . Physical activity . Postural stability . Weight distribution . Falling index Abbreviations F1 Frequencies between 0.01 and 0.10 Hz appear to express “higher level” visual–labyrinthine central nervous system control F2–F4 Deviations of 0.10 to 0.50 Hz reflect vestibular stress and vestibular disturbances F5–F6 Frequencies between 0.50 and 1.00 Hz reflect somatosensory feedback F7–F8 Frequencies between 1.00 and 3.00 Hz are signs of postural tremor or other possible neuropathology

Introduction Childhood obesity has gained epidemic proportions worldwide [4]. Along with many health- and psychosocialassociated co-morbidities, childhood obesity is also associated with alterations in bone mineral density, balance control [10], and increased risk of fractures [36]. Several studies have suggested that overweight and especially obesity impose significant constraints on balance control. Colne et al. [3] and Deforche and colleagues [6] found that the

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general stability among obese children was lower than normal weight children when comparing the sway area of foot pressure (on a Balance Master) and balance skills. McGraw and colleagues [19] found that obese children have greater sway area in the medial/lateral direction and greater instability and that their stability was more influenced by the visual system, compared with non-obese children. Pau and colleagues [26] suggested existence of different postural strategies and reduced balance capabilities among overweight children, and Goulding et al. [10] found that heavier boys were less stable than leaner boys on a balance beam (standing on one leg). Steinberg and colleagues [35] reported that the general stability of obese children deviated from that of the normal weight controls, emphasizing the fact that obese children without associated disorders (such as ADHD and clumsiness) manifested similar balance abilities as the non-obese controls. Maintaining a stable posture is essential for many daily activities, as well as for injury prevention. Poor balance of obese children, in particularly when combined with reduced bone mineral density [10, 11], may lead to a higher risk of falling and fractures compared to leaner children [12, 36, 39]. This may be especially important when obese children join exercise training programs or increase physical activity in an effort to maintain or reduce body weight. If their balance differs from normal weight children, and they are more susceptible to falls and injuries, then one of the main initial goals of childhood obesity exercise programs should be improvement of balance in order to minimize the risk of falls. Very few studies examined the influence of physical activity and weight reduction on postural balance among school age overweight/obese children. Physical activity as part of weight management intervention for obese children and adolescents was associated with significant decrease in BMI and body fat, increased physical fitness, and improved movement’s skills [23, 34, 40]. However, all these previous studies assessed balance indirectly by physical fitness or skill performance tests. Therefore, the aim of the present study was to investigate the effect of 6 months of a combined physical activity– nutritional intervention on postural balance, measured by posturographic records, among obese children, of different ages and of both genders. The main hypotheses of the current study were: (a) participation of obese children in a weight management program will improve their postural balance; (b) since economy of movement improves with age, a greater influence on balance would be seen in older obese participants; and (c) no gender differences would be demonstrated in intervention-related improvement of balance ability.

Material and methods Participants Twenty-nine children (17 girls—58.6 % and 12 boys—41.4 %; BMI%, 96.9±2.3 %), aged 6 to 14 years

(9.0±2.1), completed the 6-month-multidisciplinary childhood obesity treatment program at Meir Medical Center Kfar-Saba, Tel-Aviv University, Israel. The drop-out rate in our program is 20 % mainly due to transportation difficulties to our training facility and to relocation [23]. The study was approved by the institutional review board of the Meir Medical Center. Subjects were examined using IBS. The children’s posturographic records were taken before and after the 6 months weight management program. Dietary intervention The participants met with the dietitian six times during the program. The appointments were dedicated for acquaintance, learning the reasons for childhood obesity, receiving information about food choices, dietary and cooking habits, understanding the motivation for weight loss, as well as trying to enroll the whole family to the “battle” against overweight and nutritional education. In addition, children received dietary information and received a balanced hypocaloric diet [23]. Exercise program All intervention subjects participated in a twice-weekly training sessions (1 h each). Training was directed by professional youth coaches at the Child Health and Sports Center training center. The intervention was designed to mimic the type and intensity of exercise that elementary and high school children normally perform. Each session started with a warm up, followed by stretching and flexibility exercises. Strengthening exercises for different muscle groups (e.g., abdominal, shoulder girdle, and lower extremity muscles), balance exercises, agility exercises, and coordination exercises were followed by distance running to improve their aerobic endurance. The activities varied in duration and intensity throughout the program and were designed primarily as games to encourage enthusiasm and participation of the subjects. Endurance-type activities accounted for most of the time spent in training (∼50 % team sports and 50 % running games), with attention given, as noted, to coordination and flexibility skills. To encourage personal responsibility among the participants, subjects were instructed to add an extra 30 to 45 min of walking or other weight-bearing sport activities at least once per week. These activities were reported to the coach each week at the end of the last training session. Subjects were encouraged throughout the program, by the staff, to reduce sedentary activities (e.g., to reduce television viewing and video game use, to use stairs instead of elevators, and to play outside instead of inside) [23]. Anthropometric measurements Anthropometric measurements (weight, height) were taken by standard scales, and stadiometer and BMI were calculated. Since BMI changes with age, BMI-for-age percentiles were calculated according to the Centers for Disease Control and Prevention growth charts [18].

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Posturographic assessment In order to investigate the postural control among the obese children, a posturographic assessment was performed using a tetraataxiometric device called Tetrax (IBS; Tetrax Inc., Ramat Gan, Israel) [15]. Posturography is a diagnostic system which analyzes a subject’s balance and the mechanisms employed to maintain balance. This method of posturography is based on the assessment of the vertical pressure fluctuations on four independent force plates, each placed beneath the two heels and toe parts of the subject while he/she stands in an upright position [1]. The Tetrax plates (dimensions: length 25 cm, width 13 cm, height 8 cm each) are equipped with a strain gauge, which output consists of fluctuations of voltage. This output is transformed by an A–D device into a digital signal, which is analyzed by the tetrax software. The weight of the examinee is automatically controlled by the software while height does not interfere with the Tetrax parameters, as shown by systemic examinations [32]. The Tetrax device’s data include normative data. For each age cohort (by year of age), 30 boys and 30 girls from different European countries were tested. The norms were based on healthy, normalweight children who did not receive any medications and had no previous diagnosis of developmental or congenital problems. The software compares the assessment of each participant to age- and sex-matched controls [35]. The program computes the following parameters [1, 9, 25]: a) Stability index: The total amount of sway from the four footplates (right and left heels, right and left toes) is totaled and then divided by the subject’s weight (the amplitude of the indices of postural sway is affected by vertical pressure, and therefore, the division of the postural sway indices by the subject’s weight is used in posturographic methodology to cancel out the positive correlation of weight to the amplitude) [16]. That parameter was calculated as the square root of the sum of squared differences between adjacent pressure fluctuation signals, transmitted by the A–D device and sampled at a rate of 32 Hz for each of the four platforms. A higher score indicates greater sway and higher instability [9, 15, 16, 25, 30, 31]. b) Fourier spectral analysis: Pattern of sway intensities at different frequency ranges are shown by the Fourier analysis of the postural sway waves. Eight frequency band ranges (F1–F8; in Hz) were computed for easier clinical evaluation of the power–frequency pattern (F1=low, F2– F4=low–medium, F5–F6=medium–high, and F7–F8=high frequencies of the Fourier band). It was shown in a number of studies that the different frequency ranges of the postural Fourier spectrum are sensitive to disturbance of the postural control [5, 9, 14, 15]. F1=frequencies between 0.01 and 0.10 Hz appear to express “higher level” visual–labyrinthine central nervous system control;

F2–F4=deviations of 0.10 to 0.50 Hz reflect vestibular stress and vestibular disturbances; F5–F6=frequencies between 0.50 and 1.00 Hz reflect somatosensory feedback; and F7–F8=frequencies between 1.00 and 3.00 Hz are signs of postural tremor or other possible neuropathology [17, 22, 24, 29]. c) Weight distribution index: This is the standing deviation of the four weight distribution scores from an invariant mean of 25 %. This parameter reflects the amount of unevenness or discrepancy of the weight distribution. Weight distribution scores reflect the percentage of weight placed on each of the four platforms. This parameter is based on synchronization obtained by combining four separate body oscillation indications, produced by the two heel and toe plates of the Tetrax system (heel and toe of each foot; the two heels; the two toes; the diagonals-heel and contralateral toe part). d) Falling index: Falling index used to reevaluate the data. Its algorithm is based on the addition of standard deviation scores, which are obtained when calculating by how many standard deviations the performance of an examinee deviates from the mean of the normative database provided by the IBS software. Adding the standard scores for stability, Fourier intensities of ∼0.3 and ∼1.00 Hz, and synchronizations, a fall index is obtained with three numerical ranges 0 to 36, 37 to 40, and >41, indicating low, moderate, or high risk of falling, respectively, among young population. The index has been validated by clinical observations in geriatric clinics and hospitals in Israel and Austria [1, 9, 15, 25, 30, 35].

Procedure Subjects were asked to stand erect and focus as much as they could on a sticker placed 3 m in front of them. Each recording session lasted 32 s, in 8 test conditions, 7 of which were designed to impair the input from 1 of the 3 basic sensory systems regulating postural control [31]: (a) normal open position: standing straight with eyes open (unimpaired sensory input); (b) normal closed position: standing straight with eyes closed (stresses mainly the somatosensory and the vestibular systems); (c) pillows open: standing on pillows, with eyes open (reducing the somatosensory feedback from the lower extremity); (d) pillows closed: standing on pillows, with eyes closed (the vestibular system is the only unimpaired sensory information); (e) head right: standing with the head turned right and eyes closed (stresses the somatosensory system); (f) head left: standing with the head turned left and eyes closed (stresses the somatosensory system); (g) head back: standing with head tilted backward at a 30degree angle, with eyes closed (stresses the somatosensory system); and (h) head forward: standing with head tilted forward about 30 degrees, with eyes closed (stresses the somatosensory system).

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Previous studies demonstrated a fair reliability of the Tetrax device [9, 14]. Furthermore, validation between Tetrax positions and the four Romberg test positions manifested significant correlation between the two balance tests [15]. Data analysis Means and STD for pre- and postanthropometric parameters by age cohorts were measured by two-way ANOVA with repeated measures; Pearson correlation between pre-intervention BMI percentile, age, and gender to balance parameters were calculated; analysis of variance with repeated measures (pre–post) was performed for stability variables, with age, gender, and BMI percentile difference as independent variables; stepwise regression analysis was performed with post-interventional stability variables as dependent variable and pre-interventional stability variables, BMI, height, BMI percentile, weight, and falling index, as independent variables. Statistical significance was taken at p<0.05.

Results Pre- and post-anthropometric parameters of the obese children by age cohorts appear in Table 1. Significant increase in height and significant decrease in BMI percentile were found between pre- and post-intervention program (p<.05). Interactions were found between pre- to post-height, weight, and BMI with age; between pre- to post-weight and BMI percentile for each gender; and pre- to post-height and BMI with age and gender (p<.05). Pre-intervention results Based on the pre-intervention BMI percentile, correlation was found between pre-intervention BMI percentile and stability index in most of the positions measured (e.g., normal open position=.464; p=.011, pillow close position=.424; p=.022). Considering the age of participants, inverse correlation was found between the age and the stability index in most of

the positions measured (e.g., normal close position=−.643; p=.001, pillow open position=−.571; p=.001). In view of gender differences, inverse correlation was found between age and stability index in most of the positions measured for both genders (e.g., normal close position: males=−.703; p=.011, and females=−.787; p=.001). Nevertheless, correlation between BMI percentile and stability index in most positions was found for female only (e.g., normal close position: males = .225, p = .482 and females = .650, p=.005). Post-intervention results Following the intervention program, an interaction was found between BMI percentile differences (pre- to post-intervention program) and balance (stability index and F2–F4 frequencies of most standing positions), indicating improved post-intervention balance and reduced vestibular stress/disturbances with BMI percentile reduction (Fig. 1). Considering the age of participants, an interaction was found between BMI percentile differences (pre- to postintervention program), age, and balance (stability index and F2–F4 frequencies of most standing position). This might indicate an improved post-intervention balance and reduced vestibular stress/disturbances with BMI reduction and with increasing age (p<.05; Fig. 2). In consideration of gender differences, among the female group, an interaction was found between BMI percentile differences (pre- to post-intervention program) and balance (for weight distribution Index, F5–F6 frequencies and F7–F8 frequencies in normal close position and in head back position; p<.05). This might indicate improved weight distribution, improved somatosensory feedback and reduced tremor (cerebellar function) in the female group following the intervention. The male group manifested an interaction between BMI percentile differences (pre- to post-intervention program) and balance (for stability index, F5–F6 frequencies and F7–F8 frequencies in normal close position; p<.05) that might indicate improved post-intervention balance, improved somatosensory feedback, and reduced tremor in the male group as well (Fig. 3).

Table 1 Anthropometric parameters by sex and age cohorts Gender

F

M

N

10 5 2 4 4 4

Age

6-9 10-11 ≥12 6-9 10-11 ≥12

Height (cm)*, **, ****

Weight (kg)**, ***

BMI**, ****

BMI percentile*, ***

Pre

Post

Pre

Post

Pre

Post

Pre

Post

127.9±12.0 140.7±8.2 159.2±8.8 126.4±6.4 140.7±3.9 151.3±3.9

133.0±11.8 146.9±8.5 163.0±4.2 130.8±7.4 144.3±2.7 154.9±3.5

38.7±8.2 45.4±5.0 64.4±4.0 35.2±4.8 48.7±7.0 66.1±8.9

40.1±8.7 48.4±5.5 63.9±9.8 36.4±8.1 48.3±5.4 71.6±9.1

23.4±2.6 22.9±0.7 25.4±1.2 21.9±0.9 24.5±2.2 28.8±2.5

22.4±2.6 22.4±1.0 24.0±2.4 21.0±2.6 23.2±1.9 29.8±2.6

97.5±2.3 94.6±0.6 93.5±4.8 98.1±1.0 97.4±1.3 98.3±0.9

94.3±7.6 90.2±4.4 88.5±3.7 94.9±3.0 94.8±2.4 98.3±0.7

*p<.05, significant differences between pre- and post-intervention program; **p<.05, interaction between pre-post parameter and age cohorts; ***p<.05, interaction between pre-post parameter and gender; ****p<.05, interaction between pre-post parameter, age cohorts, and gender

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Fig. 1 Pre and post intervention F4 (reflect vestibular stress) in normal close position

Significant intervention-related improvements were found for falling index (p<.05). Correlation was found between stability index and falling index in the normal open position (.446; p=.015). Regression analysis for post-intervention weight distribution index showed that the variables that entered into the equation as predictors of post-intervention weight distribution index were the initial weight distribution index and postintervention BMI, explaining 55 % of the variance.

Discussion The aim of the present study was to examine the effect of 6 months combined physical activity–nutritional intervention on postural balance in obese children. Consistent with our hypotheses, obese children participating in the intervention improved their postural balance; older obese children demonstrated a greater improvement of postural balance, but greater improvement of balance ability in male participants. In the Tetrax software, there is an age- and gender-matched comparison to normal values collected from healthy, nonobese European children. In the previous paper, we already showed that balance indices of obese Israeli children were reduced compared to non-obese Israeli children [35]. Interestingly, following the intervention of the present study, the

Fig. 2 Pre- and post-intervention stability index in normal close position

Fig. 3 Pre and post intervention Weight Distribution Index in head back position for girls* and boys** (*=<.05; **=>.05)

balance indices of the obese children were still reduced from non-obese. We assume that a greater BMI reduction or a longer intervention may be required to possibly induce changes in balance at this age. Most previous studies support our finding that a benefit of physical activity intervention program for obese children is BMI reduction. For example, Poeta et al. [27] found that physical exercise and nutritional guidance program was effective in BMI reducing; Monzavi et al. [21] using 12 weeks of physical exercises with recreational activities and nutritional guidance intervention showed significant BMI reductions in obese children; and Zlatohlavek et al. [41] found weight loss and body mass reduction after 1-month lifestyle intervention in overweight/obese children. All those studies emphasized the relationship between improved anthropometric parameters (like BMI) and reduction of associated childhood obesity comorbidities. Trying to evaluate the clinical outcomes of a weight management intervention program on obese youth, with no physical activity management, manifested that an overweight youth who completed the program shows only modest change in weight status [13]. Very few studies examined the effect of weight management interventions on postural balance in obese children. That question is important, as previous studies already found reduced postural balance in obese children compared to lean age matched controls. D’Hondt et al. [7] investigated fine motor control in overweight and obese children compared to normal-weight peers in two different postural conditions: sitting and standing in a tandem stance on a balance beam. The overweight or obese children manifested decreased fine motor skill performance when standing on balance beam. The authors suggested that obese children might suffer from underlying perceptual–motor coordination difficulties compared to their age-matched controls. Obese children often manifest greater impairment of mobility and difficulties in sustaining high-intensity physical activity, which may result in decreased bone quality, increased bone fragility, and increase possibility of imbalance problems [33, 38, 39]. Goulding and colleagues [10] found that heavier boys were

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less stable than leaner boys on the balance beam (standing on one leg). The authors suggested that the balance deficiency resulted probably from decreased muscle tissue relative to the increased body weight (and not due to proprioceptive or sensory problems), and speculated that the decreased balance may increase falling risk. McGraw and colleagues [19] claimed that obese children were more influenced by the visual system to maintain stability, compared to non-obese children. Other studies demonstrated reduced center-of-foot pressure displacement, decreased velocity of gait, and longer duration of gait cycle in double support among obese children [3, 19]. These adaptive strategies could be related to limited muscular force or to efforts to compensate for the underlying postural instability by slowing themselves in order to prevent falling [3, 19]. In contrast, Deforche et al. [6] found that overweight and normal weight children have similar rates of falling. The direct influence of weight management intervention on balance was measured only in adult obese participants. Sartorio et al. [29] studied 230 obese adults (>18 years) before and after a 3-week-weight reduction program. Obese participants increased their one-leg standing balance test time by 20.5 %, as an indication of significant improvements in motor control. Moreover, weight loss was strongly correlated with improvement in balance control in obese adults [37]. The main finding of the present study was that 6 months of weight reduction intervention in obese children was associated with improved postural stability, reduced potential vestibular stress/disturbances, and decreased falling probability of the participants. We previously demonstrated [35] using a greater sample size of obese children an inferior baseline falling index of obese children compared to normal weight children (with 28 % of the children demonstrated a moderate falling index and 12 % exhibited severe deviation from the norm). Comparing our results to other published data is limited as the literature regarding intervention programs among obese children, aimed mostly to increase physical activity, reinforce healthy nutrition and eating habits, and reduce media use. Improving motor abilities (such as balance) was aimed as secondary outcomes only [24]. Indeed, a similar childhood obesity program was associated with significantly increased habitual physical activity (∼100 %) and endurance time (∼25 %) among participants [23]. Reviewing of the literature for leaner age-matched children participating in a balance exercise program, Puder and colleagues [28] reported correlations between physical activity and fitness including agility, balance, and aerobic fitness in young healthy children. Their pre-intervention results indicated sex- and age-adjusted positive associations between physical activity and balance. Nevertheless, following the intervention program, no relationship was found between physical

activity and balance. Considering the age of participants, previous studies in normal weight children found that the mean stability score measured by posturography improved progressively with increasing age (from 6 to 14 years old), and that 8-year-old children displayed significantly greater sway than the older children [2, 8, 20]. That supports our findings of greater intervention-related improvement in postural stability with increasing age, suggesting that the combined dietary–physical activity intervention was more effective in pubertal participants with stability impairment. When comparing postural balance between genders, we found that although at baseline the stability index correlated with BMI percentiles only among females suggesting reduced balance, following the intervention, the males improved their stability whereas females improved only their weight distribution. Mickle et al. [20] reported that when comparing postural stability of young children, boys displayed greater postural sway than girls in all movement skills performed. The authors suggested the concept of greater intervention-related effects in participants with greater stability impairment. The main limitations of the present study is the lack of follow-up measures to evaluate the long-term efficiency of the intervention on postural balance of obese children, and the absence of functional falling testing of the participants. In addition, the lack of control groups (obese children participating in a weight management program without physical exercise, or obese children who increase their physical activity and improve fitness despite no change in BMI percentiles) precludes a possibility to determine the isolated or relative effect of weight reduction, exercise, and growth on the balance change of the participants. Therefore, whether the intervention-associated effect on stability was related to reduced body weight per se, or to changes in movement patterns or physical fitness, or if mere growing up had an effect, or any combination of factors, cannot be determined from the present study.

Conclusions We found evidence to support beneficial effects of a combined dietary–physical activity intervention on postural stability, on potential vestibular stress/disturbances and on falling probability of obese children. The results suggest the concept of greater improvement in male participants, and in older adolescent participants. The prevalence of childhood obesity increases worldwide. The reduced balance of obese children, in particularly when combined with reduced bone mineral density may predispose them to a higher risk of falling and fractures when joining exercise training programs in an effort to reduce body weight. Thus, it is important that childhood obesity exercise

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programs would focus on balance improvement in early stages in order to minimize the risk of falls. Future research should determine the specific role of weight reduction and changes in physical fitness on obese children’s improvements in postural balance and on specific consideration to obese children with severe forms of balance disturbances.

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