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Static standing balance in adolescents with Down syndrome
Research in Developmental Disabilities 33 (2012) 1294–1300
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Research in Developmental Disabilities
Static standing balance in adolescents with Down syndrome M. Adoracio´n Villarroya a,b,*, Alejandro Gonza´lez-Agu¨ero a,c,d, Teresa Moros-Garcı´a b, Mario de la Flor Marı´n e, Luis A. Moreno a,b, Jose´ A. Casaju´s a,b,c a
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University School of Health Sciences (EUCS), University of Zaragoza, Zaragoza, Spain Department of Physiatry and Nursing, University of Zaragoza, Spain c Faculty of Health and Sport Sciences (FCSD), Huesca, University of Zaragoza, Spain d Department of Musical, Plastic and Corporal Expression, University of Zaragoza, Spain e Hospital Clı´nico Universitario Lozano Blesa, Zaragoza, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 February 2012 Accepted 20 February 2012 Available online 29 March 2012
Aim: To analyse static-standing-balance of adolescents with Down syndrome (DS). Methods: Thirty-two adolescents with DS aged 10–19 years (DSG); 33 adolescents, age/ sex-matched, without DS (CG). Static-standing-balance under four conditions (C1: openeyes/fixed-foot-support; C2: closed-eyes/fixed-foot-support; C3: open-eyes/compliantfoot-support; closed-eyes/compliant-foot-support) was examined by means of time and frequency Postural-Parameters (PPs). To evaluate the contribution of each sensory system influencing postural control ratios among the four conditions were calculated. Mean values of all PPs were higher in the DSG than in the CG. Mean values of time PPs were higher in both groups on compliant-foot-support (with open and closed eyes) than on fixed-foot-support. Ratios C2/C1 were significantly lower in DSG than in CG; ratios C3/C1 presented higher values in DSG than in CG, with significant differences in length path and RMS-velocity; there were no differences in ratios C4/C1. Conclusions: In our group of DS adolescents the shift from visual to multimodal control of stance had occurred and they showed similar postural control patterns than non-DS. Even though, they presented worse static balance than their peers without DS and they had more problems with altered somasosensory input. An adequate rehabilitation program insisting on somatosensory input could be a useful measure to improve balance. ß 2012 Elsevier Ltd. All rights reserved.
Keywords: Postural control Stabilometry Down’s syndrome Multimodal control
1. Introduction Static standing balance is defined as a state, in a quiet stance, of maintaining or controlling the position and momentum of the whole body center mass within the base of support without falling (Cherng, Lee, & Su, 2003). It is essential for upright posture and for most of the functional activities (Tanaka, Takeda, Izumi, Ino, & Ifukube, 1997) whose performance can be seriously limited by postural instability (Baker, Newstead, Mossberg, & Nicodemus, 1998). The most current measures for assessing the postural sway are related to the excursion of the center of pressure (COP) (Hof, Gazendam, & Sinke, 2005; Prieto, Myklebust, Hoffmann, Lovett, & Myklebust, 1996), which has been widely used in the literature (Deitz, Richardson, Crowe, & Westcott, 1996; Murray, Seireg, & Sepic, 1975; Winter, 2009; Wrisley & Whitney, 2004). Several postural parameters (PPs) in the time and/or frequency domains have been reported according to the COP
* Corresponding author at: Facultad de Medicina, Aulario B, C/Domingo Miral s/n, 50009 Zaragoza, Spain. Tel.: +34 976761000; fax: +34 976761720. E-mail addresses: [email protected] (M.A. Villarroya), [email protected] (A. Gonza´lez-Agu¨ero), [email protected] (T. Moros-Garcı´a), [email protected] (L.A. Moreno), [email protected] (J.A. Casaju´s). 0891-4222/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2012.02.017
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excursion (Cherng et al., 2003; Wolff et al., 1998). PPs in the time domain have been used extensively to quantify postural stability (Baloh et al., 1994; Ledin & Odkvist, 1993; McGraw, McClenaghan, Williams, Dickerson, & Ward, 2000). The main PPs of the COP excursion in the time domain include: maximum displacement (range) both in anterior–posterior (A/P) and medial–lateral (M/L) directions, total length of its trajectory, sway area, and peak and average velocities (Abrahamova & Hlavacka, 2008; Galli et al., 2008). The range of COP displacement represents the difference between the maximum and minimum values; thus, it uses only two points that are thought to represent the changes occurring in an entire trial of data (Palmieri, Ingersoll, Stone, & Krause, 2002). Others researches use the root mean square (RMS) of this displacement (Berg, Maki, Williams, Holliday, & Wood-Dauphinee, 1992; Geurts, Ribbers, Knoop, & van Limbeek, 1996; Niam, Cheung, Sullivan, Kent, & Gu, 1999). The RMS of COP displacement measures the average absolute displacement around the mean COP. In regards to the PPs in the frequency domain, a Fast Fourier Transform (FFT) is used to quantify the frequency composition of the signals of COP displacement. Two PPs from the frequency spectra are commonly used: mean and median frequencies (in both the A/P and M/L directions) (Cherng et al., 2003; Nolan, Grigorenko, & Thorstensson, 2005). Rigoldi, Galli, Mainardi, Crivellini, and Albertini (2011) insisted on the importance of carrying out a complete analysis, both in time and frequency domains, because computing parameters only in the time domain could sometimes lead to an erroneous interpretation of the data. These authors indicated that a decrease in time PPs values linked to an increase in frequency PPs values does not always mean a better posture control but it could be due to an increase in oscillations. Postural control requires two different processes: the sensory organizational process, in which multimodal sensory systems, including the visual, somatosensory and vestibular ones, are involved and integrated within the central nervous system (CNS); and the motor adjustment process, involved in executing coordinated and properly scaled musculoskeletal responses (Hirabayashi & Iwasaki, 1995; Nashner & Peters, 1990; Wrisley & Whitney, 2004). By the age of 6–7 years, a shift ˆ , 2001; from visual dependence to multimodal control occurs (Shumway-Cook & Woollacott, 1985; Vuillerme, Marin, & Debu Woollacott & Shumway-Cook, 1990), but it is not well established when patterns are comparable to those in adults. Some authors (Shumway-Cook & Woollacott, 1985; Wolff et al., 1998) indicated that the response patterns become comparable to those in adults at the age of 7–10 years, suggesting that, by this age, maturation of organizational processes, required to integrate sensory input, have occurred. However, Nolan et al. (2005) suggest that some aspects of postural control still appear to be developing after 9–10 years of age, and Hirabayashi and Iwasaki (1995) observed that the maturation process continued throughout childhood and had not reached the adult level at the age of 14–15 years. It is known that subjects with Down syndrome (DS) often show deficits in maintaining static standing balance (Galli et al., 2008). Many studies about balance in the DS population have been carried out in children under 10 years of age (Butterworth & Cichetti, 1978; Woollacott & Schumway-Cook, 1986). These studies showed that the development of postural control is particularly delayed in young children with DS (Block, 1991; Galli et al., 2008; Henderson, Morris, & Frith, 1981; Woollacott & Schumway-Cook, 1986). Wade, Van Emmerick, and Kernozek (2000) determined that the shift from visual to multimodal control of stance had not yet taken place in their sample of children with DS aged 10 years. Other studies analyzed postural control in adults with DS (Cabeza-Ruiz et al., 2011; Galli et al., 2008). However, to our knowledge, only two studies assessed postural control in adolescents with DS. Rigoldi et al. (2011) analyzed balance with open and closed eyes in 3 groups of age with and without DS: children, adolescents and adults. Vuillerme et al. (2001) compared balance, under different conditions related to vision and support, in 13 DS and 11 non-DS adolescents. Both of them showed that the DS adolescents presented a worse balance than their control couterparts. The worse static standing balance of persons with DS could partially explain some common functional balance problems in this population, and its knowledge may be useful for the planning of rehabilitation programs (Galli et al., 2008). We considered it of interest to increase our knowledge of postural control in a large group of adolescents with DS (analysing not only the time PPs, including the RMS of the COP displacement, but also the frequency PPs) under different conditions related to vision and support and to compare all these PPs with those of a control group. Furthermore, it is important to know how these conditions impact on DS and control groups, in order to have a deeper knowledge of the sensory organizational process, and to compare the impacts on the two groups. Therefore, the aims of this study were: (1) to compare the static standing balance between two groups of adolescents, with and without DS, by means of time and frequency PPs; (2) to analyze the contribution of visual and somatosensory input and to compare this contribution between both groups. 2. Materials and methods 2.1. Participants A sample of 32 children and adolescents (15 females/17 males aged 10–19 years) with DS were recruited from different schools and institutions of Arago´n (Spain). An age- and sex-matched control group (CG) composed of 33 participants (14 females/ 19 males) without DS were also recruited. Inclusion criteria for the DS group (DSG) subjects were: the presence of trisomy 21; the absence of any gross visual or organic defect and independence in stance and ambulation. All participants without DS were healthy, without signs of any orthopedic or neurological disorders, impairment of somatosensory activity, hearing, vestibular or uncorrected visual functions and free of medications for at least 3 months before the beginning of the study. Full clinical history, including illnesses or surgical interventions and stays in a hospital, was collected for all individuals. Both parents and children were informed about the aims and procedures, as well as possible risks and benefits, of the study. Written informed consent was obtained from all the subjects included and from their parents or guardians. The study was
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performed in accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the Research Ethics Committee of the Government of Aragon (CEICA, Spain). 2.2. Balance assessment A pressure distribution platform (Loran Engineering SrL, Italy. Software ‘‘FootChecker’’ 4.0.) with 2304 resistive sensors and a sampling frequency of 30 Hz was used to collect COP data. Subjects were instructed to maintain an upright standing position on the pressure platform, barefoot with arms hanging by the sides and feet positioned in a natural position (forming 308 relative to each other and heels 5 cm apart) for 30 s. Each participant performed 2 trials under four balance testing conditions, generally used in clinical tests of sensory interaction on balance (Lin, Lee, Chen, Lee, & Kuo, 2006; Wrisley & Whitney, 2004). The conditions were: (C1) open-eyes, fixed-foot-support, (C2) closed-eyes, fixed-foot-support, (C3) openeyes, compliant-foot-support, (C4) closed-eyes, compliant-foot-support. With open-eyes, subjects were asked to look at a 1.5 m-distant black target, adjustable in height according to the eye level of each subject. The pressure platform served as the fixed-foot-support. In the compliant-foot-support condition, a medium density foam mat was placed under the subjects’ feet. The order of trials with open or closed eyes was balanced among subjects to control any effects associated with repeated testing. One practice trial prior to testing was allowed to familiarize participants with the procedure. Standardized verbal cues of encouragement were given to each subject. Testing was conducted in a quiet room to limit external influences. The subjects were permitted to have short breaks between trials and between tests. The independent variables were gender and condition (DS and non-DS). Dependent variables were (1) the different PPs based on COP sway (under the four studied conditions related to vision and support), calculated using the raw data supplied by the system, and (2) the ratios of these PPs among the four studied conditions related to vision and support. To obtain the PPs, COP sway data were analyzed using two different methods: (1) calculation of time PPs from COP coordinates; and (2) analysis of PPs in the frequency domain. The time PPs were: the RMS of COP excursion (RMS-ROM; mm) in the A/P and M/L directions; the length of the sway path (sway path; mm); and the RMS of the COP velocity (RMS-velocity; mm/s). A Fast Fourier Transform was used to analyze PPs in the frequency domain and the median frequencies (Hz) were calculated in both the A/P and M/L directions. To evaluate the contribution of each sensory system influencing postural control, as previously described by Hirabayashi and Iwasaki (1995), some ratios between the four conditions were calculated: (A) ratios between condition 2/ condition 1 (C2/C1). These ratios represent the effect of closing the eyes on stability stance. (B) Ratios between condition 3/ condition 1 (C3/C1). These ratios represent the effect of somatosensory input on the stability. (C) Ratios between condition 4/condition 1 (C4/C1). These ratios represent the effect both of visual and somatosensory input on the stability stance. For each of the above mentioned variables and for each condition, the average of two trials was used in the statistical analysis. 2.3. Statistical analyses In order to avoid the influence of the subject’s height, all time PPs were normalized to the subject’s height. The SPSS 15.0 software for Windows (SPSS Inc. Chicago, IL) was used for the analyses and the significance level was 5%. Mean and standard deviations were calculated for the description of dependent variables (by gender). All data were tested for normality by using the Kolmogorov–Smirnov test. Dependent variables were compared between boys and girls (in both groups), by using the independent t-test, when the data distribution was normal, and the Mann Whitney test, when the data distribution was not normal. A general linear model with repeated measures, followed by Bonferroni post hoc test, was used: the within-subjects were vision (open and closed eyes) and the surface (firm and compliant); the between-subjects factors were the two groups (CG and DSG). To establish differences in the influence of different conditions between CG and DSG, a comparison of the different ratios was carried out by using the independent t-test or the Mann–Whitney test, according to the data distribution. These entire tests were applied in boys and girls independently and in the whole group. 3. Results The general features of the participants of both groups are shown in Table 1. As no differences between genders were found for any of the reported variables, results are showed as a group. Table 2 shows mean values and standard deviations of time and frequency variables. Higher mean values in all PPs were observed between the two groups (all p < 0.05), except in RMS-ROM M/L (p: 0.064). Table 3 shows differences among conditions within groups. In regards to C1 and C2, no differences were found in DSG, but in CG there were significant higher values of RMS-ROM A/P in C2 (with closed eyes) (p < 0.05). In regards to the differences between C1 and C3, significant higher values of all time PPs on the latter (on compliant-foot-support) were found in both groups (all p < 0.05). Comparison between C1 and C4 also showed significant higher values of all time PPs on the latter, with closed eyes on compliant-foot-support (all p < 0.05). Table 4 displays mean values and standard deviations of the different ratios of the analyzed variables. No differences in ratios of frequency PPs between both groups were found but there were some differences in ratios of time PPs: ratios C2/C1
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Table 1 General features of the participants of both groups. Boys (n: 36)
p DS group, n = 17
Control group, n = 19
Age (years) Weight (kg) Height (m) BMI (kg/m2)
Girls (n: 29)
Mean
sd
Mean
sd
13.95 55.28 1.65 19.83
2.51 12.62 0.13 2.75
14.54 46.43 1.48 20.61
2.65 11.16 0.11 2.75
0.499 0.033 <0.0001 0.402
p
Control group, n = 14
DS group, n = 15
Mean
sd
Mean
sd
13.75 52.6 1.55 21.36
2.87 16.64 0.14 4.36
13.85 42.58 1.37 22.06
3.27 13.01 0.10 4.33
0.937 0.081 0.001 0.670
DS, Down syndrome; BMI, Body Mass Index.
Table 2 Mean values and standard deviation of the studied posturographic parameters. C1: FIX-SUP/OE.
RMS-ROM AP (mm) RMS-ROM ML (mm) Sway path (mm) RMS-Velocity (mm/s) Median Freq. AP (Hz) Median Freq. ML (Hz)
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
C2: FIX-SUP/CE
CG
DSG
p
CG
DSG
0.710 0.418 1.197 0.549 16.355 14.849 1.055 1.002 0.24 0.27 0.17 0.16
1.549 1.297 2.520 1.761 43.762 31.788 3.069 2.519 0.42 0.50 0.47 0.52
<0.001
0.885 0.556 1.732 1.106 20.424 12.421 1.346 0.860 0.20 0.21 0.22 0.24
1.501 1.261 2.630 2.498 47.247 32.155 3.369 2.627 0.47 0.51 0.74 0.81
<0.001 <0.0001 <0.0001 0.047 <0.031
p 0.050 0.064 <0.0001 <0.0001 0.012 <0.001
C3: COMPLIANT-SUP/OE
C4: COMPLIANT-SUP/CE
CG
DSG
CG
DSG
1.614 0.891 2.471 1.732 20.277 10.822 1.353 0.828 0.19 0.20 0.16 0.25
2.568 1.836 5.229 2.528 67.888 39.015 4.744 2.875 0.33 0.20 0.50 0.27
1.424 0.833 2.653 1.454 30.480 17.297 1.974 1.171 0.20 0.27 0.19 0.24
3.019 3.485 5.744 3.018 93.806 59.622 6.689 4.406 0.40 0.45 0.66 0.32
p 0.045 <0.0001 <0.0001 <0.0001 0.049 0.017
p 0.005 <0.0001 <0.0001 <0.0001 0.041 0.026
p: Signification of the comparison between control group (CG) and Down syndrome group (DSG) (FIX-SUP, fixed-foot-support; COMPLIANT-SUP, compliantfoot-support; OE, open-eyes; CE, closed-eyes; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velolcity; Freq, frequency). Bold means statistically significant differences.
Table 3 Comparisons among the different conditions analyzed in Down syndrome and control groups.
RMS-ROM AP RM-ROM ML Length path RMS-velocity Median Freq. AP Median Freq. ML
DSG CG DSG CG DSG CG DSG CG DSG CG DSG CG
Between C2 and C1
Between C3 and C1
Between C4 and C1
1.000 0.021 1.000 0.059 0.606 0.062 0.477 0.062 1.000 1.000 1.000 0.188
0.006 <0.0001 <0.0001 0.002 <0.0001 0.424 <0.0001 0.003 1.000 1.000 1.000 1.000
0.021 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 1.000 1.000 1.000 1.000
C1, Condition1; C2, Condition2; C3, Condition3; C4, Condition4; CG, control group; DSG, Down syndrome group; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velolcity; Freq, frequency. Bold means statistically significant differences.
were significantly lower in DSG than in CG; ratios C3/C1 presented higher values in DSG than in CG, with significant differences in length path and RMS-velocity; there were no differences in ratios C4/C1.
4. Discussion A shift from visual to multimodal control of stance in our group of DS adolescents and a COP which traveled faster, farther, and with substantially different spectral features than in their peers without DS was noted. In addition, DSG was more influenced by alteration of somatosensory input.
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Table 4 Mean values and standard deviation of the analyzed ratios. Ratio C2/C1
RMS-ROM.AP RMS-ROM ML Length path RMS-velocity Median Freq. AP Median Freq. ML
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
Ratio C3/C1
Ratio C4/C1
CG
DSG
p
CG
DSG
p
CG
DSG
p
134.70 63.76 175.12 125.19 142.45 41.35 150.44 49.57 96.72 119.79 181.24 325.33
117.39 93.61 117.15 78.21 113.86 36.55 120.40 64.68 247.89 615.91 422.48 344.88
0.039
282.83 166.67 261.97 265.12 145.94 47.48 151.51 50.18 108.95 162.17 254.73 242.13
250.97 221.44 285.32 179.96 184.18 89.38 196.88 105.32 168.32 502.19 191.55 391.70
0.151
254.46 170.63 303.42 299.92 215.63 81.57 226.18 104.27 103.78 66.25 134.34 113.03
300.50 367.80 287.43 161.43 266.07 180.91 288.07 215.27 165.41 214.28 117.01 98.29
0.485
0.054 0.004 0.039 0.267 0.351
0.682 0.037 0.032 0.693 0.939
0.193 0.778 0.334 0.217 0.405
p: Signification of the comparison between control group (CG) and Down syndrome group (DSG) (C1, Condition1; C2, Condition2; C3, Condition3; C4, Condition4; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velocity; Freq, frequency). Bold means statistically significant differences.
4.1. Differences in postural parameters between groups There are large variations in all the studied PPs among subjects in both groups. This variability has been attributed to individual differences in the maturation of elements of the postural control processes (Baker et al., 1998; Figura, Cama, Capranica, Guidetti, & Pulejo, 1991; Riach & Hayes, 1987) and to the way people use the information from the different systems (visual, somatosensory, vestibular) (Shumway-Cook & Woollacott, 1985; Winter, Patla, & Frank, 1990). Almost all the studied PPs under the four sensory conditions showed significant differences between CG and DSG, with higher values in the last; thus, there was a worse balance in DSG. Adolescents with DS presented larger COP displacements, in both the A/P and M/L directions, a greater COP sway path and, to balance, they exhibited higher COP velocity and median frequency. Vuillerme et al. (2001) found results similar to ours in the time PPs they studied. They indicated that by the age of 14–18 years, people affected by DS presented an evident worse balance than the non-DS ones. Rigoldi et al. (2011) found greater values in DS adolescents group than in control group in the A/P COP displacement and in the center frequencies. In a previous study (Galli et al., 2008), it was showed, under two different conditions (open and closed eyes), larger COP sway path and larger COP oscillations in the M/L direction in subjects with DS, without significant differences in the A/P direction. However, with regard to frequency domain, subjects with DS in that study were characterized by a higher frequency, not only in the M/L direction, but also in A/P. In our study, the median frequency was also significantly greater in the DSG which confirmed their altered balance. Imperfect stance stability requires DS adolescents to correct their COP at a faster rate than their CG peers. 4.2. Contribution of visual and somatosensory input Postural control, as mentioned above, is a particularly complex system that involves the integration of various motor and sensory components (Isableu & Vuillerme, 2006). The motor process must be developed in early childhood, but the resolution of intersensory conflicts in maintaining standing balance increases with age (Cherng et al., 2003; Riach & Hayes, 1987). Young children are more influenced by visual input than adults (Woollacott & Shumway-Cook, 1990). Higher susceptibility to deprivation of visual information is due to poorer information from somatosensory input in young children than in adults. By the age of 6–7 years, a shift from visual dependence to multimodal control has been suggested (ShumwayCook & Woollacott, 1985) and postural sway during quiet standing is reduced. From this age, the fundamental source of postural stability should be somatosensorial (Uyanik & Kayihan, 2012). As far as the contribution of individual sensory input is concerned, some differences were found in this study between the two groups. The CG presented higher values for C2 than for C1 in the time PPs, but differences were significant only in the RMS-ROM A/P. No changes were observed between these two conditions in DSG which indicates that our group of adolescents with DS with privation of vision relied on somatosensory input; thus, the shift from visual to multimodal control of stance had occurred. Wade et al. (2000) did not observe this shift in their population with DS by the age of 10 years, but Vuillerme et al. (2001) obtained the same conclusion as we did in their group of adolescents with DS. However, these last authors found a similar behavior in their two groups of adolescents, with and without DS, under both conditions: no differences in the COP range, although a higher COP mean velocity with closed eyes. Galli et al. (2008) did not report any differences between open and closed eyes, either in their group of young adults with DS (mean age-18.7 years) or in their CG. When comparing ratios C2–C1 to assess how the suppression of visual information affected the two groups, no differences were found in the frequency PPs ratios but a significantly lower value of the time PPs ratios, except in M/L COP displacement, was appreciated in DSG. These results suggest a high reliance on somatosensory input in DSG than in CG. One
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of the reasons for this greater influence of the somatosensory system could be the higher number of receptors, the greater plantar surface being due to the flatfeet this population usually presents (Lin et al., 2006). Comparisons between C1 and C3 showed that the alteration of somatosensory input did not significantly affect the frequency PPs, probably due to the large variability of these parameters, but affected almost every PPs in both groups, with increases in their values. However, comparison of ratios C3–C1 between CG and DSG showed significant higher values in the DSG in the COP length path and velocity; thus, there was a greater influence of somatosensory input on the adolescents with DS. The greater instability in this group, with altered somatosensory input, could be due to the loss of the greater amount of receptors due to their flatfeet, but also to the greater difficulty in the DSG shifting from the use of somatosensory to visual input when the former was altered, as described in younger children (Shumway-Cook & Woollacott, 1985; Woollacott, Debu, & Mowatt, 1987). Vuillerme et al. (2001) also described, under conditions of deteriorated somatosensory input, that adolescents with DS made greater efforts to control balance. Gomes and Barela (2007) found that when an additional sensory information was provided to their group of DS adults, they took a great advantage of it decreasing body sway. They indicated that it might be the reason why these subjects needed a longer period of practice than subjects without DS in order to successfully use sensory input. Comparisons of ratios C4–C1 between DSG and CG showed no differences; both of them had similar behavior with closed eyes on a compliant-foot-support. In this case, leaving only vestibular input to aid in balance, both groups had greater sway paths and surface of their COP oscillations, with higher COP displacement velocities. The differences in the contribution of individual sensory input between the two groups do not seem the only responsible for the evidently worse balance DS adolescents present. As Vuillerme et al. (2001) described in DS adolescents and Gomes and Barela (2007) in DS adults, our group of DS adolescents seem to have similar postural control patterns than non-DS, but with qualitative differences. The ability to control balance of the body is an important prerequisite to functional activities (Figura et al., 1991; Shumway-Cook & Woollacott, 1985) and failure in this control can seriously limit performance (Baker et al., 1998). Thus, it is necessary to improve the precarious balance of the adolescents with DS. Their condition generally led them to an inactivity which contributes to an even worse postural control (Cabeza-Ruiz et al., 2011). Therefore, adapted training programs could improve balance in these adolescents. From our results, these programs should insist on somatosensory input. We must not forget that postural control involves not only the sensory system but also the motor system, responsible of executing coordinated musculoskeletal responses (Davis & Kelso, 1982). It is known that problems in the motor system in DS population (reduced strength (Cioni et al., 1994), low levels of lean mass (Gonza´lez-Agu¨ero, Ara, Moreno, Vicente-Rodrı´guez, & Casaju´s, 2011), ligament laxity and hypotonia (Connolly & Michael, 1986; Rigoldi et al., 2011)) can also contribute to their precarious balance. Therefore, these programs should also insist on strength and muscular coordination (Gonza´lez-Agu¨ero, Vicente-Rodrı´guez, et al., 2011; Rigoldi et al., 2011). 5. Conclusions In conclusion, in DS adolescents the shift from visual to multimodal control of stance had occurred and they showed similar postural control patterns than non-DS. Even though, they presented worse static balance than their peers without DS and they had more problems with altered somasosensory input. Conflict of interest There are no conflicts of interest or financial disclosures for any author of this manuscript. None of the authors have any financial interest. Acknowledgments The authors want to thank all the children and their parents that participated in the study for their understanding and dedication to the project. Special thanks are given to Fundacio´n Down Zaragoza and Special Olympics Aragon for their support. This study is being supported by Spanish ‘Ministry of Innovation and Science’ (Project DEP2009-09183). There are no potential conflicts of interest that may affect the contents of this work. References Abrahamova, D., & Hlavacka, F. (2008). Age-related changes of human balance during quiet stance. Physiological Research, 57, 957–964. Baker, C. P., Newstead, A. H., Mossberg, K. A., & Nicodemus, C. L. (1998). Reliability of static standing balance in nondisabled children: Comparison of two methods of measurement. Pediatric Rehabilitation, 2, 15–20. Baloh, R. W., Fife, T. D., Zwerling, L., Socotch, T., Jacobson, K., Bell, T., & Beykirch, K. (1994). Comparison of static and dynamic posturography in young and older normal people. Journal of the American Geriatrics Society, 42, 405–412. Berg, K. O., Maki, B. E., Williams, J. I., Holliday, P. J., & Wood-Dauphinee, S. L. (1992). Clinical and laboratory measures of postural balance in an elderly population. 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Contents lists available at SciVerse ScienceDirect
Research in Developmental Disabilities
Static standing balance in adolescents with Down syndrome M. Adoracio´n Villarroya a,b,*, Alejandro Gonza´lez-Agu¨ero a,c,d, Teresa Moros-Garcı´a b, Mario de la Flor Marı´n e, Luis A. Moreno a,b, Jose´ A. Casaju´s a,b,c a
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University School of Health Sciences (EUCS), University of Zaragoza, Zaragoza, Spain Department of Physiatry and Nursing, University of Zaragoza, Spain c Faculty of Health and Sport Sciences (FCSD), Huesca, University of Zaragoza, Spain d Department of Musical, Plastic and Corporal Expression, University of Zaragoza, Spain e Hospital Clı´nico Universitario Lozano Blesa, Zaragoza, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 February 2012 Accepted 20 February 2012 Available online 29 March 2012
Aim: To analyse static-standing-balance of adolescents with Down syndrome (DS). Methods: Thirty-two adolescents with DS aged 10–19 years (DSG); 33 adolescents, age/ sex-matched, without DS (CG). Static-standing-balance under four conditions (C1: openeyes/fixed-foot-support; C2: closed-eyes/fixed-foot-support; C3: open-eyes/compliantfoot-support; closed-eyes/compliant-foot-support) was examined by means of time and frequency Postural-Parameters (PPs). To evaluate the contribution of each sensory system influencing postural control ratios among the four conditions were calculated. Mean values of all PPs were higher in the DSG than in the CG. Mean values of time PPs were higher in both groups on compliant-foot-support (with open and closed eyes) than on fixed-foot-support. Ratios C2/C1 were significantly lower in DSG than in CG; ratios C3/C1 presented higher values in DSG than in CG, with significant differences in length path and RMS-velocity; there were no differences in ratios C4/C1. Conclusions: In our group of DS adolescents the shift from visual to multimodal control of stance had occurred and they showed similar postural control patterns than non-DS. Even though, they presented worse static balance than their peers without DS and they had more problems with altered somasosensory input. An adequate rehabilitation program insisting on somatosensory input could be a useful measure to improve balance. ß 2012 Elsevier Ltd. All rights reserved.
Keywords: Postural control Stabilometry Down’s syndrome Multimodal control
1. Introduction Static standing balance is defined as a state, in a quiet stance, of maintaining or controlling the position and momentum of the whole body center mass within the base of support without falling (Cherng, Lee, & Su, 2003). It is essential for upright posture and for most of the functional activities (Tanaka, Takeda, Izumi, Ino, & Ifukube, 1997) whose performance can be seriously limited by postural instability (Baker, Newstead, Mossberg, & Nicodemus, 1998). The most current measures for assessing the postural sway are related to the excursion of the center of pressure (COP) (Hof, Gazendam, & Sinke, 2005; Prieto, Myklebust, Hoffmann, Lovett, & Myklebust, 1996), which has been widely used in the literature (Deitz, Richardson, Crowe, & Westcott, 1996; Murray, Seireg, & Sepic, 1975; Winter, 2009; Wrisley & Whitney, 2004). Several postural parameters (PPs) in the time and/or frequency domains have been reported according to the COP
* Corresponding author at: Facultad de Medicina, Aulario B, C/Domingo Miral s/n, 50009 Zaragoza, Spain. Tel.: +34 976761000; fax: +34 976761720. E-mail addresses: [email protected] (M.A. Villarroya), [email protected] (A. Gonza´lez-Agu¨ero), [email protected] (T. Moros-Garcı´a), [email protected] (L.A. Moreno), [email protected] (J.A. Casaju´s). 0891-4222/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2012.02.017
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excursion (Cherng et al., 2003; Wolff et al., 1998). PPs in the time domain have been used extensively to quantify postural stability (Baloh et al., 1994; Ledin & Odkvist, 1993; McGraw, McClenaghan, Williams, Dickerson, & Ward, 2000). The main PPs of the COP excursion in the time domain include: maximum displacement (range) both in anterior–posterior (A/P) and medial–lateral (M/L) directions, total length of its trajectory, sway area, and peak and average velocities (Abrahamova & Hlavacka, 2008; Galli et al., 2008). The range of COP displacement represents the difference between the maximum and minimum values; thus, it uses only two points that are thought to represent the changes occurring in an entire trial of data (Palmieri, Ingersoll, Stone, & Krause, 2002). Others researches use the root mean square (RMS) of this displacement (Berg, Maki, Williams, Holliday, & Wood-Dauphinee, 1992; Geurts, Ribbers, Knoop, & van Limbeek, 1996; Niam, Cheung, Sullivan, Kent, & Gu, 1999). The RMS of COP displacement measures the average absolute displacement around the mean COP. In regards to the PPs in the frequency domain, a Fast Fourier Transform (FFT) is used to quantify the frequency composition of the signals of COP displacement. Two PPs from the frequency spectra are commonly used: mean and median frequencies (in both the A/P and M/L directions) (Cherng et al., 2003; Nolan, Grigorenko, & Thorstensson, 2005). Rigoldi, Galli, Mainardi, Crivellini, and Albertini (2011) insisted on the importance of carrying out a complete analysis, both in time and frequency domains, because computing parameters only in the time domain could sometimes lead to an erroneous interpretation of the data. These authors indicated that a decrease in time PPs values linked to an increase in frequency PPs values does not always mean a better posture control but it could be due to an increase in oscillations. Postural control requires two different processes: the sensory organizational process, in which multimodal sensory systems, including the visual, somatosensory and vestibular ones, are involved and integrated within the central nervous system (CNS); and the motor adjustment process, involved in executing coordinated and properly scaled musculoskeletal responses (Hirabayashi & Iwasaki, 1995; Nashner & Peters, 1990; Wrisley & Whitney, 2004). By the age of 6–7 years, a shift ˆ , 2001; from visual dependence to multimodal control occurs (Shumway-Cook & Woollacott, 1985; Vuillerme, Marin, & Debu Woollacott & Shumway-Cook, 1990), but it is not well established when patterns are comparable to those in adults. Some authors (Shumway-Cook & Woollacott, 1985; Wolff et al., 1998) indicated that the response patterns become comparable to those in adults at the age of 7–10 years, suggesting that, by this age, maturation of organizational processes, required to integrate sensory input, have occurred. However, Nolan et al. (2005) suggest that some aspects of postural control still appear to be developing after 9–10 years of age, and Hirabayashi and Iwasaki (1995) observed that the maturation process continued throughout childhood and had not reached the adult level at the age of 14–15 years. It is known that subjects with Down syndrome (DS) often show deficits in maintaining static standing balance (Galli et al., 2008). Many studies about balance in the DS population have been carried out in children under 10 years of age (Butterworth & Cichetti, 1978; Woollacott & Schumway-Cook, 1986). These studies showed that the development of postural control is particularly delayed in young children with DS (Block, 1991; Galli et al., 2008; Henderson, Morris, & Frith, 1981; Woollacott & Schumway-Cook, 1986). Wade, Van Emmerick, and Kernozek (2000) determined that the shift from visual to multimodal control of stance had not yet taken place in their sample of children with DS aged 10 years. Other studies analyzed postural control in adults with DS (Cabeza-Ruiz et al., 2011; Galli et al., 2008). However, to our knowledge, only two studies assessed postural control in adolescents with DS. Rigoldi et al. (2011) analyzed balance with open and closed eyes in 3 groups of age with and without DS: children, adolescents and adults. Vuillerme et al. (2001) compared balance, under different conditions related to vision and support, in 13 DS and 11 non-DS adolescents. Both of them showed that the DS adolescents presented a worse balance than their control couterparts. The worse static standing balance of persons with DS could partially explain some common functional balance problems in this population, and its knowledge may be useful for the planning of rehabilitation programs (Galli et al., 2008). We considered it of interest to increase our knowledge of postural control in a large group of adolescents with DS (analysing not only the time PPs, including the RMS of the COP displacement, but also the frequency PPs) under different conditions related to vision and support and to compare all these PPs with those of a control group. Furthermore, it is important to know how these conditions impact on DS and control groups, in order to have a deeper knowledge of the sensory organizational process, and to compare the impacts on the two groups. Therefore, the aims of this study were: (1) to compare the static standing balance between two groups of adolescents, with and without DS, by means of time and frequency PPs; (2) to analyze the contribution of visual and somatosensory input and to compare this contribution between both groups. 2. Materials and methods 2.1. Participants A sample of 32 children and adolescents (15 females/17 males aged 10–19 years) with DS were recruited from different schools and institutions of Arago´n (Spain). An age- and sex-matched control group (CG) composed of 33 participants (14 females/ 19 males) without DS were also recruited. Inclusion criteria for the DS group (DSG) subjects were: the presence of trisomy 21; the absence of any gross visual or organic defect and independence in stance and ambulation. All participants without DS were healthy, without signs of any orthopedic or neurological disorders, impairment of somatosensory activity, hearing, vestibular or uncorrected visual functions and free of medications for at least 3 months before the beginning of the study. Full clinical history, including illnesses or surgical interventions and stays in a hospital, was collected for all individuals. Both parents and children were informed about the aims and procedures, as well as possible risks and benefits, of the study. Written informed consent was obtained from all the subjects included and from their parents or guardians. The study was
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performed in accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the Research Ethics Committee of the Government of Aragon (CEICA, Spain). 2.2. Balance assessment A pressure distribution platform (Loran Engineering SrL, Italy. Software ‘‘FootChecker’’ 4.0.) with 2304 resistive sensors and a sampling frequency of 30 Hz was used to collect COP data. Subjects were instructed to maintain an upright standing position on the pressure platform, barefoot with arms hanging by the sides and feet positioned in a natural position (forming 308 relative to each other and heels 5 cm apart) for 30 s. Each participant performed 2 trials under four balance testing conditions, generally used in clinical tests of sensory interaction on balance (Lin, Lee, Chen, Lee, & Kuo, 2006; Wrisley & Whitney, 2004). The conditions were: (C1) open-eyes, fixed-foot-support, (C2) closed-eyes, fixed-foot-support, (C3) openeyes, compliant-foot-support, (C4) closed-eyes, compliant-foot-support. With open-eyes, subjects were asked to look at a 1.5 m-distant black target, adjustable in height according to the eye level of each subject. The pressure platform served as the fixed-foot-support. In the compliant-foot-support condition, a medium density foam mat was placed under the subjects’ feet. The order of trials with open or closed eyes was balanced among subjects to control any effects associated with repeated testing. One practice trial prior to testing was allowed to familiarize participants with the procedure. Standardized verbal cues of encouragement were given to each subject. Testing was conducted in a quiet room to limit external influences. The subjects were permitted to have short breaks between trials and between tests. The independent variables were gender and condition (DS and non-DS). Dependent variables were (1) the different PPs based on COP sway (under the four studied conditions related to vision and support), calculated using the raw data supplied by the system, and (2) the ratios of these PPs among the four studied conditions related to vision and support. To obtain the PPs, COP sway data were analyzed using two different methods: (1) calculation of time PPs from COP coordinates; and (2) analysis of PPs in the frequency domain. The time PPs were: the RMS of COP excursion (RMS-ROM; mm) in the A/P and M/L directions; the length of the sway path (sway path; mm); and the RMS of the COP velocity (RMS-velocity; mm/s). A Fast Fourier Transform was used to analyze PPs in the frequency domain and the median frequencies (Hz) were calculated in both the A/P and M/L directions. To evaluate the contribution of each sensory system influencing postural control, as previously described by Hirabayashi and Iwasaki (1995), some ratios between the four conditions were calculated: (A) ratios between condition 2/ condition 1 (C2/C1). These ratios represent the effect of closing the eyes on stability stance. (B) Ratios between condition 3/ condition 1 (C3/C1). These ratios represent the effect of somatosensory input on the stability. (C) Ratios between condition 4/condition 1 (C4/C1). These ratios represent the effect both of visual and somatosensory input on the stability stance. For each of the above mentioned variables and for each condition, the average of two trials was used in the statistical analysis. 2.3. Statistical analyses In order to avoid the influence of the subject’s height, all time PPs were normalized to the subject’s height. The SPSS 15.0 software for Windows (SPSS Inc. Chicago, IL) was used for the analyses and the significance level was 5%. Mean and standard deviations were calculated for the description of dependent variables (by gender). All data were tested for normality by using the Kolmogorov–Smirnov test. Dependent variables were compared between boys and girls (in both groups), by using the independent t-test, when the data distribution was normal, and the Mann Whitney test, when the data distribution was not normal. A general linear model with repeated measures, followed by Bonferroni post hoc test, was used: the within-subjects were vision (open and closed eyes) and the surface (firm and compliant); the between-subjects factors were the two groups (CG and DSG). To establish differences in the influence of different conditions between CG and DSG, a comparison of the different ratios was carried out by using the independent t-test or the Mann–Whitney test, according to the data distribution. These entire tests were applied in boys and girls independently and in the whole group. 3. Results The general features of the participants of both groups are shown in Table 1. As no differences between genders were found for any of the reported variables, results are showed as a group. Table 2 shows mean values and standard deviations of time and frequency variables. Higher mean values in all PPs were observed between the two groups (all p < 0.05), except in RMS-ROM M/L (p: 0.064). Table 3 shows differences among conditions within groups. In regards to C1 and C2, no differences were found in DSG, but in CG there were significant higher values of RMS-ROM A/P in C2 (with closed eyes) (p < 0.05). In regards to the differences between C1 and C3, significant higher values of all time PPs on the latter (on compliant-foot-support) were found in both groups (all p < 0.05). Comparison between C1 and C4 also showed significant higher values of all time PPs on the latter, with closed eyes on compliant-foot-support (all p < 0.05). Table 4 displays mean values and standard deviations of the different ratios of the analyzed variables. No differences in ratios of frequency PPs between both groups were found but there were some differences in ratios of time PPs: ratios C2/C1
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Table 1 General features of the participants of both groups. Boys (n: 36)
p DS group, n = 17
Control group, n = 19
Age (years) Weight (kg) Height (m) BMI (kg/m2)
Girls (n: 29)
Mean
sd
Mean
sd
13.95 55.28 1.65 19.83
2.51 12.62 0.13 2.75
14.54 46.43 1.48 20.61
2.65 11.16 0.11 2.75
0.499 0.033 <0.0001 0.402
p
Control group, n = 14
DS group, n = 15
Mean
sd
Mean
sd
13.75 52.6 1.55 21.36
2.87 16.64 0.14 4.36
13.85 42.58 1.37 22.06
3.27 13.01 0.10 4.33
0.937 0.081 0.001 0.670
DS, Down syndrome; BMI, Body Mass Index.
Table 2 Mean values and standard deviation of the studied posturographic parameters. C1: FIX-SUP/OE.
RMS-ROM AP (mm) RMS-ROM ML (mm) Sway path (mm) RMS-Velocity (mm/s) Median Freq. AP (Hz) Median Freq. ML (Hz)
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
C2: FIX-SUP/CE
CG
DSG
p
CG
DSG
0.710 0.418 1.197 0.549 16.355 14.849 1.055 1.002 0.24 0.27 0.17 0.16
1.549 1.297 2.520 1.761 43.762 31.788 3.069 2.519 0.42 0.50 0.47 0.52
<0.001
0.885 0.556 1.732 1.106 20.424 12.421 1.346 0.860 0.20 0.21 0.22 0.24
1.501 1.261 2.630 2.498 47.247 32.155 3.369 2.627 0.47 0.51 0.74 0.81
<0.001 <0.0001 <0.0001 0.047 <0.031
p 0.050 0.064 <0.0001 <0.0001 0.012 <0.001
C3: COMPLIANT-SUP/OE
C4: COMPLIANT-SUP/CE
CG
DSG
CG
DSG
1.614 0.891 2.471 1.732 20.277 10.822 1.353 0.828 0.19 0.20 0.16 0.25
2.568 1.836 5.229 2.528 67.888 39.015 4.744 2.875 0.33 0.20 0.50 0.27
1.424 0.833 2.653 1.454 30.480 17.297 1.974 1.171 0.20 0.27 0.19 0.24
3.019 3.485 5.744 3.018 93.806 59.622 6.689 4.406 0.40 0.45 0.66 0.32
p 0.045 <0.0001 <0.0001 <0.0001 0.049 0.017
p 0.005 <0.0001 <0.0001 <0.0001 0.041 0.026
p: Signification of the comparison between control group (CG) and Down syndrome group (DSG) (FIX-SUP, fixed-foot-support; COMPLIANT-SUP, compliantfoot-support; OE, open-eyes; CE, closed-eyes; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velolcity; Freq, frequency). Bold means statistically significant differences.
Table 3 Comparisons among the different conditions analyzed in Down syndrome and control groups.
RMS-ROM AP RM-ROM ML Length path RMS-velocity Median Freq. AP Median Freq. ML
DSG CG DSG CG DSG CG DSG CG DSG CG DSG CG
Between C2 and C1
Between C3 and C1
Between C4 and C1
1.000 0.021 1.000 0.059 0.606 0.062 0.477 0.062 1.000 1.000 1.000 0.188
0.006 <0.0001 <0.0001 0.002 <0.0001 0.424 <0.0001 0.003 1.000 1.000 1.000 1.000
0.021 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 1.000 1.000 1.000 1.000
C1, Condition1; C2, Condition2; C3, Condition3; C4, Condition4; CG, control group; DSG, Down syndrome group; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velolcity; Freq, frequency. Bold means statistically significant differences.
were significantly lower in DSG than in CG; ratios C3/C1 presented higher values in DSG than in CG, with significant differences in length path and RMS-velocity; there were no differences in ratios C4/C1.
4. Discussion A shift from visual to multimodal control of stance in our group of DS adolescents and a COP which traveled faster, farther, and with substantially different spectral features than in their peers without DS was noted. In addition, DSG was more influenced by alteration of somatosensory input.
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Table 4 Mean values and standard deviation of the analyzed ratios. Ratio C2/C1
RMS-ROM.AP RMS-ROM ML Length path RMS-velocity Median Freq. AP Median Freq. ML
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
Ratio C3/C1
Ratio C4/C1
CG
DSG
p
CG
DSG
p
CG
DSG
p
134.70 63.76 175.12 125.19 142.45 41.35 150.44 49.57 96.72 119.79 181.24 325.33
117.39 93.61 117.15 78.21 113.86 36.55 120.40 64.68 247.89 615.91 422.48 344.88
0.039
282.83 166.67 261.97 265.12 145.94 47.48 151.51 50.18 108.95 162.17 254.73 242.13
250.97 221.44 285.32 179.96 184.18 89.38 196.88 105.32 168.32 502.19 191.55 391.70
0.151
254.46 170.63 303.42 299.92 215.63 81.57 226.18 104.27 103.78 66.25 134.34 113.03
300.50 367.80 287.43 161.43 266.07 180.91 288.07 215.27 165.41 214.28 117.01 98.29
0.485
0.054 0.004 0.039 0.267 0.351
0.682 0.037 0.032 0.693 0.939
0.193 0.778 0.334 0.217 0.405
p: Signification of the comparison between control group (CG) and Down syndrome group (DSG) (C1, Condition1; C2, Condition2; C3, Condition3; C4, Condition4; RMS-ROM, root mean square of COP excursion; AP, anterior–posterior; ML, medial–lateral; RMS-velocity, root mean square of COP velocity; Freq, frequency). Bold means statistically significant differences.
4.1. Differences in postural parameters between groups There are large variations in all the studied PPs among subjects in both groups. This variability has been attributed to individual differences in the maturation of elements of the postural control processes (Baker et al., 1998; Figura, Cama, Capranica, Guidetti, & Pulejo, 1991; Riach & Hayes, 1987) and to the way people use the information from the different systems (visual, somatosensory, vestibular) (Shumway-Cook & Woollacott, 1985; Winter, Patla, & Frank, 1990). Almost all the studied PPs under the four sensory conditions showed significant differences between CG and DSG, with higher values in the last; thus, there was a worse balance in DSG. Adolescents with DS presented larger COP displacements, in both the A/P and M/L directions, a greater COP sway path and, to balance, they exhibited higher COP velocity and median frequency. Vuillerme et al. (2001) found results similar to ours in the time PPs they studied. They indicated that by the age of 14–18 years, people affected by DS presented an evident worse balance than the non-DS ones. Rigoldi et al. (2011) found greater values in DS adolescents group than in control group in the A/P COP displacement and in the center frequencies. In a previous study (Galli et al., 2008), it was showed, under two different conditions (open and closed eyes), larger COP sway path and larger COP oscillations in the M/L direction in subjects with DS, without significant differences in the A/P direction. However, with regard to frequency domain, subjects with DS in that study were characterized by a higher frequency, not only in the M/L direction, but also in A/P. In our study, the median frequency was also significantly greater in the DSG which confirmed their altered balance. Imperfect stance stability requires DS adolescents to correct their COP at a faster rate than their CG peers. 4.2. Contribution of visual and somatosensory input Postural control, as mentioned above, is a particularly complex system that involves the integration of various motor and sensory components (Isableu & Vuillerme, 2006). The motor process must be developed in early childhood, but the resolution of intersensory conflicts in maintaining standing balance increases with age (Cherng et al., 2003; Riach & Hayes, 1987). Young children are more influenced by visual input than adults (Woollacott & Shumway-Cook, 1990). Higher susceptibility to deprivation of visual information is due to poorer information from somatosensory input in young children than in adults. By the age of 6–7 years, a shift from visual dependence to multimodal control has been suggested (ShumwayCook & Woollacott, 1985) and postural sway during quiet standing is reduced. From this age, the fundamental source of postural stability should be somatosensorial (Uyanik & Kayihan, 2012). As far as the contribution of individual sensory input is concerned, some differences were found in this study between the two groups. The CG presented higher values for C2 than for C1 in the time PPs, but differences were significant only in the RMS-ROM A/P. No changes were observed between these two conditions in DSG which indicates that our group of adolescents with DS with privation of vision relied on somatosensory input; thus, the shift from visual to multimodal control of stance had occurred. Wade et al. (2000) did not observe this shift in their population with DS by the age of 10 years, but Vuillerme et al. (2001) obtained the same conclusion as we did in their group of adolescents with DS. However, these last authors found a similar behavior in their two groups of adolescents, with and without DS, under both conditions: no differences in the COP range, although a higher COP mean velocity with closed eyes. Galli et al. (2008) did not report any differences between open and closed eyes, either in their group of young adults with DS (mean age-18.7 years) or in their CG. When comparing ratios C2–C1 to assess how the suppression of visual information affected the two groups, no differences were found in the frequency PPs ratios but a significantly lower value of the time PPs ratios, except in M/L COP displacement, was appreciated in DSG. These results suggest a high reliance on somatosensory input in DSG than in CG. One
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of the reasons for this greater influence of the somatosensory system could be the higher number of receptors, the greater plantar surface being due to the flatfeet this population usually presents (Lin et al., 2006). Comparisons between C1 and C3 showed that the alteration of somatosensory input did not significantly affect the frequency PPs, probably due to the large variability of these parameters, but affected almost every PPs in both groups, with increases in their values. However, comparison of ratios C3–C1 between CG and DSG showed significant higher values in the DSG in the COP length path and velocity; thus, there was a greater influence of somatosensory input on the adolescents with DS. The greater instability in this group, with altered somatosensory input, could be due to the loss of the greater amount of receptors due to their flatfeet, but also to the greater difficulty in the DSG shifting from the use of somatosensory to visual input when the former was altered, as described in younger children (Shumway-Cook & Woollacott, 1985; Woollacott, Debu, & Mowatt, 1987). Vuillerme et al. (2001) also described, under conditions of deteriorated somatosensory input, that adolescents with DS made greater efforts to control balance. Gomes and Barela (2007) found that when an additional sensory information was provided to their group of DS adults, they took a great advantage of it decreasing body sway. They indicated that it might be the reason why these subjects needed a longer period of practice than subjects without DS in order to successfully use sensory input. Comparisons of ratios C4–C1 between DSG and CG showed no differences; both of them had similar behavior with closed eyes on a compliant-foot-support. In this case, leaving only vestibular input to aid in balance, both groups had greater sway paths and surface of their COP oscillations, with higher COP displacement velocities. The differences in the contribution of individual sensory input between the two groups do not seem the only responsible for the evidently worse balance DS adolescents present. As Vuillerme et al. (2001) described in DS adolescents and Gomes and Barela (2007) in DS adults, our group of DS adolescents seem to have similar postural control patterns than non-DS, but with qualitative differences. The ability to control balance of the body is an important prerequisite to functional activities (Figura et al., 1991; Shumway-Cook & Woollacott, 1985) and failure in this control can seriously limit performance (Baker et al., 1998). Thus, it is necessary to improve the precarious balance of the adolescents with DS. Their condition generally led them to an inactivity which contributes to an even worse postural control (Cabeza-Ruiz et al., 2011). Therefore, adapted training programs could improve balance in these adolescents. From our results, these programs should insist on somatosensory input. We must not forget that postural control involves not only the sensory system but also the motor system, responsible of executing coordinated musculoskeletal responses (Davis & Kelso, 1982). It is known that problems in the motor system in DS population (reduced strength (Cioni et al., 1994), low levels of lean mass (Gonza´lez-Agu¨ero, Ara, Moreno, Vicente-Rodrı´guez, & Casaju´s, 2011), ligament laxity and hypotonia (Connolly & Michael, 1986; Rigoldi et al., 2011)) can also contribute to their precarious balance. Therefore, these programs should also insist on strength and muscular coordination (Gonza´lez-Agu¨ero, Vicente-Rodrı´guez, et al., 2011; Rigoldi et al., 2011). 5. Conclusions In conclusion, in DS adolescents the shift from visual to multimodal control of stance had occurred and they showed similar postural control patterns than non-DS. Even though, they presented worse static balance than their peers without DS and they had more problems with altered somasosensory input. Conflict of interest There are no conflicts of interest or financial disclosures for any author of this manuscript. None of the authors have any financial interest. Acknowledgments The authors want to thank all the children and their parents that participated in the study for their understanding and dedication to the project. Special thanks are given to Fundacio´n Down Zaragoza and Special Olympics Aragon for their support. 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