Research in Developmental Disabilities 34 (2013) 2185–2190

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Research in Developmental Disabilities

Effects of treadmill inclination on the gait of children with

Down syndrome

Thayse L.M. Rodenbusch a, Tatiana S. Ribeiro a,*, Camila R. Simao a,Heloisa M.J.S. Britto a, Eloisa Tudella b, Ana R. Lindquist a

a Department of Physical Therapy, Federal University of Rio Grande do Norte (UFRN), Natal, Rio Grande do Norte, Av. Senador Salgado Filho,

3000, Post Office Box: 1524, Zip Code: 59072-970, Brazilb Department of Physical Therapy, Federal University of Sao Carlos (UFSCAR), Sao Carlos, Sao Paulo, Via Washington Luiz, km 235,

Post Office Box: 676, Zip Code: 13565-905, Brazil

A R T I C L E I N F O

Article history:

Received 7 September 2012

Received in revised form 6 February 2013

Accepted 8 February 2013

Available online 30 April 2013

Keywords:

Down syndrome

Gait

Inclination

A B S T R A C T

The goal of this study was to analyze the effects of upward treadmill inclination on the gait

of children with Down syndrome (DS). Sixteen children with a mean age 8.43 � 2.25 years,

classified at level I of the Gross Motor Function Classification System (GMFCS) and able to walk

without personal assistance and/or assistive devices/orthosis were evaluated. Spatial-

temporal variables were observed as well as the angular variation of hip, knee and ankle

in the sagittal plane, while children walked on the treadmill carried out on 0% and 10% upward

inclination. The results showed that children with DS presented changes in spatio-temporal

variables (reduced cadence and increased cycle time and swing time) and in angular variables

(increased hip, knee and ankle angles at initial contact; increased maximum hip flexion and

maximum stance dorsiflexion; and reduced plantarflexion at pre-swing). Treadmill

inclination seemed to act positively on the angular and spatio-temporal characteristics of

gait in children with DS, demonstrating a possible benefit from the use of this type of surface in

the gait rehabilitation of this population.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Down syndrome (DS) is an encephalopathy caused by irregular cell division process that leads, among other disorders, tocognitive impairments and delayed motor development, due to neurological, physiological and biomechanical factors(Anson, 1992; Shumway-Cook & Woollacott, 1985).

Biomechanical alterations, such as hypermobility, hypotony and ligament laxity are primarily responsible for the delayedacquisition of motor development milestones (Rigoldi et al., 2012). Consequently, children with DS start the sequence ofacquiring motor skills (such as rolling, sitting and crawling) at later age, starting to walk, on average, one year after normalchildren. This in turn restricts their opportunities to interact with the environment and hinders development in the motor,social and cognitive domains (Tudella, Pereira, Basso, & Savelsbergh, 2011; Ulrich, Ulrich, Angulo-Kinzler, & Yun, 2001).

Although this pathology may not progress, there are resultant physical impairments and functional limitations thatcan change with development. According to the dynamic systems approach, motor skills are multidimensional and emergefrom interaction between several subsystems of intrinsic properties such as genetic, biomechanical and physiological

* Corresponding author at: Federal University of Rio Grande do Norte, Department of Physical Therapy – Av. Senador Salgado Filho, 3000,

Post Office Box: 1524, Zip Code: 59072-97, Brazil. Tel./fax: +55 84 3342 2010.

E-mail addresses: tatalucena@gmail.com (Thayse L.M. Rodenbusch), tathy_souza@hotmail.com (T.S. Ribeiro), camila.simao@gmail.com (C.R. Simao),

fsthelobritto@gmail.com (Heloisa M.J.S. Britto), tudella@terra.com.br (E. Tudella), araquel@ufrnet.br (A.R. Lindquist).

0891-4222/$ – see front matter � 2013 Elsevier Ltd. All rights reserved.

http://dx.doi.org/10.1016/j.ridd.2013.02.014

T.L.M. Rodenbusch et al. / Research in Developmental Disabilities 34 (2013) 2185–21902186

characteristics and of extrinsic properties, notably, the environment. Changes in one or more subsystems may lead to thereorganization of an individual’s movement patterns (Thelen & Fisher, 1982; Thelen, 1984, 1986) and consequent acquisitionof a new motor skill or readjustment of this ability (Stein & Daniels-McQueen, 2002).

Considering this, modifying context, by selecting disturbances that alter behavior in a desired manner, becomes a keyfactor to improve the motor repertoire of a child (Thelen & Ulrich, 1991). In relation to gait, training on inclined surfaces hasbeen suggested due to inclination is an environmental disturbance that exerts a profound effect on the locomotionmechanism, given that gait patterns continuously change to satisfy kinematic limitations (Prentice, Hasler, Groves, & Frank,2004). Although the effects of gait training on inclined surfaces (upward and downward) have been studied in otherpopulations (Lay, Hass, & Gregor, 2006; Leroux, Fung, & Barbeau, 2002; Leroux, Fung, & Barbeau, 2006; Moreno, Mendes, &Lindquist, 2011; Stansfield & Nicol, 2002), there is yet little research direct to examination of how pathological gait patternsare modified in these circumstances, and particularly, no studies demonstrating the effects of this type of environmentaldisturbance on the kinematic gait parameters of children with DS.

Thus, the aim of this study was to assess the effects of upward electric treadmill inclination (10%) on the kinematicparameters of gait in children with DS. Our hypothesis is that treadmill inclination produces changes to angular and spatio-temporal parameters, such as an increase in the incursion of the hip, knee and ankle, and a longer duration of the gait cycle,which could improve the functionality of this population.

2. Material and methods

2.1. Participants

The sample was composed of 23 children with DS, aged 5–11 years. These children were non-probabilistically chosenfrom two rehabilitation centers (The Association of Parents and Friends of Exceptional Children – APAE – and The Associationto Assist Disabled People – ADOTE), both located in Natal City, in Rio Grande do Norte State, Brazil. All children wereaccompanied by physical therapists since birth.

Inclusion criteria were as follows: children classified at level I of the Gross Motor Function Classification System (GMFCS;Palisano, Rosenbaum, Stephen, Russel, Wood, & Galapi, 1997) and able to walk without personal assistance and/or assistivedevices/orthesis; did not exhibit any other neurological alterations, or associated respiratory or osteomyoarticularpathologies (not due to DS); and exhibited capacity to understand and obey simple verbal commands. Were excluded fromthe study those children who did not followed correctly the instructions given by the therapist, i.e., that refused to cooperatewith the therapist (even after several attempts).

The study was approved by the Research Ethics Committee and all parents or legal guardians signed an informed consentform, authorizing their children to participate of the study.

2.2. Measuring instruments

The gross motor function was classified by the GMFCS, which provides a standardized system of classifying the grossmotor function of children into five levels (level I the least severe to level V the most severe). The GMFCS has been found to bevalid and reliable for this proposal (Palisano, Rosenbaun, Bartlett, & Livingston, 2008) and was translated and adapted for theBrazilian population (Hiratuka, Matzukura, & Pfeifer, 2012). To evaluate balance, we used the Berg Balance Scale (BBS; Berg,Wood-Dauphinee, Williams, & Maki, 1992) –, which assesses functional balance performance based on 14 items common todaily life. The maximum score that can be reached is 56 and each item possesses an ordinal scale of five alternatives rangingfrom 0 to 4 points (Miyamoto, Lombardi, Berg, Ramos, & Natour, 2004).

Gait analysis was obtained using the Qualisys Motion Capture System,1 a video-based photogrammetric system thatallows the reconstruction of a three-dimensional (3D) biomechanical model, using passive reflective markers positioned onspecific bone prominences. Three cameras (Qualysis ProReflex MCU-240) light reflected by the passive markers were used.The data were captured at a frequency of 120 Hz by Qualisys Track Manager 1.6 (QTM) acquisition software and weresubsequently exported to Visual 3D processing software,2 which provided for the construction of the biomechanical modelfor analysis of spatio-temporal and angular gait variables.

2.3. Evaluation procedure

After obtaining anthropometric measurements, patient identification, clinical diagnosis, medications used and relatedinformation, clinical evaluations (using GMFCS and BBS) and kinematic gait analysis were performed.

Kinematic assessments of the children’s gaits were performed in two stages: static and dynamic collection. For theseassessments, passive markers were positioned on the following anatomic marks of the lower limb: greater trochanter ofthe femur, medial and lateral epicondyle of the femur, medial and lateral malleolus, calcaneus, heads of the 1st and5th metatarsal. A set of four markers, called tracking markers, were also placed on each segment, to define its trajectory

1 Qualisys Medical AB, Packhusgatan 6, 411 13 Gothenburg, Sweden.2 C-Motion Inc, 20030 Century Blvd, Ste 104A, Germantown, MD 20874.

T.L.M. Rodenbusch et al. / Research in Developmental Disabilities 34 (2013) 2185–2190 2187

during movement. All the markers were placed on right leg, for standardization; on the left leg, markers were placed only onthe calcaneous and 1st metatarsal head of feet (Moreno et al., 2011).

In static collection, individuals remained in the orthostatic position (position of reference) with their feet aligned alongthe x and y axes, in order to provide data for the future creation of their biomechanical model. The data were collected for 5 s.

In dynamic collections, gait was evaluated while the subjects walked on the Gait Trainer System 2 treadmill.3 On thetreadmill, the participants walked at a comfortable speed for two minutes in each experimental condition: 0% and 10%treadmill incline. After this adaptation period, in which the examiner was positioned beside the treadmill to orient the childduring the procedure, data were captured for 30 s in each condition. To avoid fatigue, a 1-minute rest period was givenbetween the different experimental conditions (Moreno et al., 2011).

2.4. Data reduction

Data were processed by Visual 3D software, which, based on the positions of the anatomical markers captured by QTM,creates a system of coordinates for each segment and determines the positions and instantaneous orientations of eachsegment. Using anatomical and tracking markers, we built a biometric model for each participant composed of the pelvis,thigh, leg and foot. Angular displacements of each joint were obtained according to the angle sequence proposed by Cardan(Cole, Nigg, Ronsky, & Yeadon, 1993).

Ten gait cycles were analyzed for each study participant. The following spatio-temporal parameters were analyzed:cadence, stride length, cycle time, double-support time, stance time and swing time. With respect to angular variables, theangular displacements and range of motion (ROM), in degrees, of the hip, knee, and ankle in the sagittal plane wereinvestigated. ROM was obtained by subtracting the minimum from the maximum value reached. Hip, knee and ankle jointswere also assessed to determine angles at initial contact, maximum stance extension and maximum swing flexion (for thehip and knee), maximum plantarflexion at pre-swing and maximum stance dorsiflexion (for the ankle).

2.5. Data analysis

Data analysis was carried out using Bioestat 5.0 software,4 at a significance level less than 5% for all statistical tests.Descriptive analysis was conducted using measures of central tendency and standard deviation. Data normality was verifiedusing the D’Agostino test, and then the paired t-test was applied to identify the existence of significant differences in theangular and spatio-temporal variables between the two experimental conditions. Finally, an analysis of the effect size ofinclination on the some spatio-temporal and angular variables also carried out.

3. Results

3.1. Clinical assessment

Seven children were excluded from the sample for not collaborating during data collection. The final sample wascomposed of 16 children: 11 (68.75%) boys and 5 (31.25%) girls. The remaining characteristics are illustrated in Table 1.

3.2. Spatio-temporal variables

Analysis of spatio-temporal variables revealed that upward treadmill inclination caused a reduction in cadence (P < .04),and an increase in both cycle time (P = .03) and in swing time (P < .001), as shown in Table 2.

3.3. Angular variables

Angular gait variables showed an increase at the hip joint (P < .0001), in both the angle at initial contact and maximumflexion angle during inclined treadmill walking. The knee joint exhibited similar behavior to that observed in the hip, with anincrease in the angle at initial contact (P < .0001). However, there was no difference in maximum flexion and extension. Theankle joint followed the same pattern, with an increase at initial contact on an inclined surface (P < .0001). A reduction inmaximum plantarflexion at pre-swing (P < .0004) and an increase in maximum dorsiflexion in stance (P < .0009) was foundbetween treadmill walking at 0% and 10% incline (Table 3).

3.4. Effect size

Effect size of inclination can be found in Table 4. Inclination had a slight effect on spatio-temporal variables, with indicesranging between 0.2 and 0.4 and a large effect on angular variables, with indices between 0.2 and 1.51. Values below 0.2 were

3 Biodex Medical Systems Inc, 20 Ramsay Rd, Shirley, NY 11967-4704.4 Institute for Sustainable Development, Mamiraua/IDSM/MCT/CNPq, Bexiga Road 2.584, Fonte Boa, 69470-000 – Tefe, AM, Brazil.

Table 2

Spatio-temporal variables during treadmill walking without inclination (0%) and with inclination (10%).

Variables 0% 10%

Cadence (steps/min) 108.92 (39.07)a 99.11 (27.51)a

Stride length (m) 0.30 (0.10) 0.32 (0.10)

Cycle time (s) 1.24 (0.27)b 1.36 (0.34)b

Double-support time (s) 0.51 (0.17) 0.55 (0.18)

Stance time (s) 1.54 (0.34) 1.75 (0.58)

Swing time (s) 0.77 (0.15)c 0.82 (0.18)c

Note: values are presented as mean (standard deviation).a P < .04b P = .03c P < .001.

Table 3

Angular variables during treadmill walking without inclination (0%) and with inclination (10%).

Variables 0% 10%

Hip at IC (8) 12.23 (4.63)a 18.49 (5.17)a

Max. hip extension (8) �6.7 (6.2) �5.35 (5.4)

Max. hip flexion (8) 12.96 (4.32)a 19.50 (4.51)a

ROM (8) 6.16 (11.14)b 14.06 (8.12)b

Knee at IC (8) 15.59 (6.71)a 21.63 (6.84)a

Max. knee extension (8) 43.09 (6.26) 43.80 (5.82)

Max. knee flexion (8) 7.00 (6.32) 6.89 (5.12)

ROM (8) 18.85 (10.88) 18.57 (10.72)

Ankle at IC (8) �2.79 (9.8)a 2.25 (8.79)a

Max. plantarflexion at PS (8) �6.33 (8.77)c �2.69 (8.62)c

Max. stance dorsiflexion (8) 4.41 (10.07)b 7.13 (11.58)b

ROM (8) �1.57 (5.47) 2.23 (4.91)

Note: Values are presented as mean (standard deviation).

Abbreviations: IC, initial contact; Max, maximum; ROM, range of motion; PS, pre-swing.a P < .0001.b P < .0009.c P < .0004.

Table 1

Clinical and demographic characteristics of participants (n = 16).

Characteristics Mean (SD)

Age (years) 8.43 (2.25)

Body mass (kg) 32.25 (12.00)

Height (m) 1.25 (0.14)

Speed (m/s) 0.24 (0.04)

BBS score 51.87 (4.60)

Abbreviation: BBS, Berg balance scale.

Table 4

Effect size of the inclination on spatio-temporal and angular gait variables.

Variables Effect size

Cadence (steps/min) 0.2

Cycle time (s) 0.4

Swing time (s) 0.3

Hip at IC (8) 1.35

Max. hip flexion (8) 1.51

Knee at IC (8) 0.9

Ankle at IC (8) 0.5

Max. plantarflexion at PS (8) 0.4

Max. dorsiflexion (8) 0.2

Abbreviations: IC, initial contact; Max, maximum; PS, pre-swing.

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considered to have no effect, between 0.2 and 0.5 a slight effect, between 0.5 and 0.8 a medium effect and above 0.8 a largeeffect.

4. Discussion

This study showed that upward treadmill inclination at 10% caused changes on the following angular and spatio-temporal gait parameters: cadence, cycle time and swing time, as well as in hip, knee and ankle angles at initial contact,maximum hip flexion, maximum dorsiflexion and maximum plantarflexion at pre-swing.

It is known that children with DS present with hypotony, reduced muscle strength and cerebellar alterations that affectbalance and postural control, leading to less stability during gait. These characteristics cause them to take smaller stepswhile walking in addition to increasing cadence. According to Vogt and Banzer (1999), the typical response to increasedinclination is to walk slower and take smaller steps. Considering this, the children with DS in our study, seem to havedeveloped similar adaptations in cadence to those of typical children, when faced with a new context.

An increase in cycle time was also observed, differing from findings obtained by Vogt and Banzer (1999) and Leroux, Fung,and Barbeau (1999), who found no significant alterations in this variable in healthy subjects and in individuals with spinalcord injury. It is believed that the increase in time cycle was due to the biomechanical adaptation that individuals exhibitedwhile walking on the inclined treadmill, since they showed reduced cadence. Moreover, a significant increase in swing time wasobserved, which probably contributed to increase the cycle time. An increased swing time is an important finding, because it isrelated to the greater capacity of individual to maintain unipodal stance and facilitate walking. This implies an improvement inindividual’s adaptation to daily obstacles, reinforcing the idea that the inclination is an interesting tool for this purpose.

The angular gait variables of hip, knee and ankle joints showed statistically significant differences between the twoexperimental conditions. The hip joint showed a significant increase in the mean flexion angles at initial contact andmaximum flexion in the swing phase. These findings corroborate those ones obtained by Prentice et al. (2004) and Lerouxet al. (1999), who observed an increase in hip flexion during gait on an inclined surface in healthy subjects, but differ fromthose of Leroux et al. (2002), who found no significant alterations in hip flexion angles in patients with medullary lesion.Thus, it can be observed that treadmill inclination results in children with DS acquiring similar gait patterns to those ofindividuals with typical motor development. Furthermore, increased hip flexion angles are associated with the need to liftthe lower limb higher during the swing phase on an inclined treadmill, so that it does not drag on the surface. This results ingreater hip excursion during this phase (Felıcio, Gava, Zanella, & Pereira, 2008; Leroux et al., 1999).

The knee joint, in turn, showed a statistically significant difference only in the angle at initial contact. According to Lerouxet al. (1999), normal subjects use the same hip-knee coordination pattern in uphill walking as in level walking, whichinvolves a progressive increase in hip flexion and a simultaneous decrease in knee extension toward the end of swing to footcontact. Children with DS generally present with stiff, hyperextended knees, hindering their flexion in the next gait phase(loading response), thus contributing to worst impact on this joint (Copetti, Mota, Graup, Menezes, & Venturini, 2007; Lerouxet al., 2002; Van Hedel, 2009). The inclination favored knee flexion at initial contact, which may have led to a more functionalgait with better shock absorption in the knee joint.

The ankle joint showed an increase in initial contact angle and in maximum stance dorsiflexion, with reduction inmaximum plantarflexion at pre-swing. Similar findings were found in other studies conducted with healthy individuals(Prentice et al., 2004; Stoquart, Detrembleur, & Lejeune, 2008); however, different results were obtained in a study ofpatients with medullary lesion (Leroux et al., 1999). Considering the trend of children with DS walk with atypical gait(Copetti et al., 2007), the findings of present study indicate a decrease in plantarflexion posture after the use of inclination,with an adoption of adaptation strategies similar to those individuals with typical motor development instead of resemblingthe behavior exhibited by individuals with other pathologies, such as medullary lesion.

According to Thelen and Ulrich (1991), new forms of behavior emerge from both cooperation among differentcomponents and the context of the task. When disturbances that facilitate this interaction are imposed, motor skills becomemore functional. In the specific case of gait, for the limb to move in harmony and enable the individual to walk, hip flexionmust increase and knee extension decrease for the ankle to move adequately (Leroux et al., 1999). The inclination showed tohave a large effect on the angular gait variables in the present study, suggesting that the use of inclined surfaces allowsconcurrent activity of the three lower limb joints. This favors the development of a harmonious movement pattern inchildren with DS that resembles as closely as possible to that of children with normal motor development.

The results of this study demonstrate that inclination acts as a constructive environmental disturbance for the gait ofchildren with DS, given that it causes positive alterations in the angular and spatio-temporal gait parameters of the studypopulation. This indicates a possible benefit from the use of a 10% electric incline treadmill for the gait rehabilitation of thispopulation. We suggest, however, that further studies about the effects of inclination on the gait of children with DS,involving larger samples and electromyographic assessment of gait, for example, should be performed in order to allowcomparisons and greater generalizations of the findings.

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