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Trunk and center of mass movements during gait in children with juvenile idiopathic arthritis
Human Movement Science 26 (2007) 296–305 www.elsevier.com/locate/humov
Trunk and center of mass movements during gait in children with juvenile idiopathic arthritis ˚ kerlind a, ¨ rtqvist a, Yvonne Haglund-A Eva Brostro¨m a,*, Maria O Stefan Hagelberg a, Elena Gutierrez-Farewik a,b a
Department of Woman and Child Health, Karolinska Institute, Sweden KTH Mechanics, Royal Institute of Technology, Stockholm, Sweden
b
Available online 6 March 2007
Abstract Motion of the body center of mass (CoM) can often indicate the overall effect of the strategy of forward progression used. In the present study, focus is placed on trunk movements in the sagittal, coronal, and transverse/rotation plane, as well as placement of the CoM, during gait in children with juvenile idiopathic arthritis (JIA). Seventeen children with JIA, all with polyarticular lower extremity involvement were examined before and approximately two weeks after treatment with intra-articular cortico-steroid injections. Movement was recorded with a 6-camera 3D motion analysis system in both the children with JIA and in 21 healthy controls. Trunk and center of mass movements were compared between JIA and controls, and effects of intra-articular cortico-steroid treatment were evaluated. Children with JIA were more posteriorly tilted in the trunk, contrary to the common clinical impression, and had their CoM placed more posterior and off-centred, which may have been a result of pain. With such knowledge, it might be possible to better understand the effects of their pain and involvement, and ultimately to plan a treatment strategy for improving their gait patterns. Ó 2007 Elsevier B.V. All rights reserved. PsycINFO classification: 3363 Keywords: Juvenile rheumatoid arthritis; 3D gait analysis; Centre of gravity
* Corresponding author. Present address: MotorikLab Q2:07 ALB, Karolinska University Hospital, 171 76 Stockholm, Sweden. Tel.: +46 8 517 77636. E-mail address: [email protected] (E. Brostro¨m).
0167-9457/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.humov.2007.01.007
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1. Introduction In normal walking the body functionally divides itself into two units, passenger (head, neck, trunk and arms) and locomotor (two lower limbs and pelvis). While there is motion and muscle action occurring in each, there is a difference between the two units. The passenger unit is responsible only for its own postural integrity, while the locomotor unit is a major determinant for muscle action within the locomotor system. During normal gait the head and trunk travel as a unit, with little apparent motion relative to the pelvis (Perry, 2002), but some studies report small arcs of displacement in both the sagittal and frontal planes (Krebs, Wong, Jevsevar, Riley, & Hodge, 1992; Perry, 2002; Thorstensson, Nilsson, Carlson, & Zomlefer, 1984). Small arcs of motion also occur in the pelvis (Perry, 2002). More recent studies verify these results; in normal populations of young females the trunk is more anteriorly flexed during walking than in standing, with small range of motion in the sagittal plane, and even smaller in the frontal plane (Frigo et al., 1996). The manifestations of juvenile idiopathic arthritis (JIA) include joint swelling, effusion, tenderness, painful limitation of joint movement, and a disturbance of gait (Cassidy & Petty, 2002). Previous studies of controlled quantitative gait assessment in JIA showed significant alterations from the normal in recorded kinematics and temporal data (Brostro¨m, Haglund-Akerlind, Hagelberg, & Cresswell, 2002; Fairburn et al., 2002; Frigo et al., 1996). Participants with JIA displayed excessive anterior tilt of the pelvis and decreased hip extension and ankle plantarflexion angle at toe-off (Lechner, McCarthy, & Holden, 1987). Later studies reported both kinematic and kinetic deviations (Brostro¨m, Hagelberg, & Haglund-Akerlind, 2004; Frigo et al., 1996). It has been shown that children with JIA walk more slowly, take shorter steps (Brostro¨m et al., 2002; Frigo et al., 1996; Gard, Miff, & Kuo, 2004; Lechner et al., 1987), and have a lower cadence (Lechner et al., 1987). While trunk movements have been reported in able-bodied populations (Frigo, Carabalona, Dalla, & Negrini, 2003; Van Emmerik, McDermott, Haddad, & Van Wegen, 2005), in idiopathic scoliosis (Engsberg, Lenke, Uhrich, Ross, & Bridwell, 2003; Kramers-de, Muller, Stacoff, Grob, & Stussi, 2004) and in myelomeningocele (Baker, 2001; Bartonek, Saraste, Eriksson, Knutson, & Cresswell, 2002; Gutierrez, Bartonek, Haglund-Akerlind, & Saraste, 2003b), among others, there are no studies focusing on trunk movements in children with JIA to our knowledge. Intra-articular corticosteroid injections (ICI) are a common and effective treatment in children with JIA (Huppertz, Tschammler, Horwitz, & Schwab, 1995; Padeh & Passwell, 1998). It is reported that this treatment is safe and provides continued anti-inflammatory effects on the synovium. In one study 82% of 300 joints that were injected demonstrated full clinical remission of the joint inflammation (Padeh & Passwell, 1998). There is also evidence that leg length discrepancy resulting from unilateral knee synovitis as well as joint deformity and joint damage may be prevented (Sherry, Stein, Reed, Schanberg, & Kredich, 1999). Long-term follow up with magnetic resonance imagining after repeated ICIs in knee of JIA patients showed preserved cartilage (Hagelberg, Magnusson, Jenner, & Andersson, 2000). Gait analysis is a common and objective method to verify and document a participant’s walking pattern. Gait is generally described in cycles for each side, beginning with foot contact of that side and ending with the next foot contact of the same foot, and further divided into two phases, stance and swing (Perry, 2002). The body center of mass (CoM) in a quiet standing position is located approximately anterior to the second sacral
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vertebra. To maintain a static position, the CoM must remain in balance over the base of support (Winter, 1995). The change in CoM motion during gait represents the overall result of joint and segment movements on the forward progression, and is of importance when describing pathological gait. It has been used to evaluate gait efficiency and strategy (Gutierrez, Bartonek, Haglund-Akerlind, & Saraste, 2003a). The CoM can either be measured as the centroid of a multi-body system (kinematic method) or from the ground reaction force, using a dynamic equilibrium calculation and integrating for the CoM displacement. Several studies have shown that the different measurement methods provide similar results (Eames, Cosgrove, & Baker, 1999; Gard et al., 2004; Gutierrez-Farewik, Bartonek, & Saraste, 2006). The goals of this study were to compare trunk and CoM motion in children with JIA and children without JIA and to detect alterations after ICI treatment. 2. Methods 2.1. Participants Seventeen children between 5 and 16 years of age (mean 11.4, SD 2.9 years, 14 females, 3 males) with JIA were diagnosed according to the criteria set by the Paediatric Standing Committee of International League of Associations for Rheumatology (ILAR, Table 1). All patients were treated regularly at the Department of Paediatric Rheumatology. They were all independent walkers, had lower extremity involvement in five or more joints (polyarticular), and were scheduled for treatment with ICI injections. The local research ethical committee approved the study. Participation was voluntary. Verbal and written information was given to the children and their parents. Twenty-one healthy children between 5 and 14 years of age (mean 10.4, SD 2.5 and 10 female, 11 male) were investigated with the same protocol (Table 1). Ages, weights and heights were approximately normal distributed in both groups, and no statistically significant differences were found in age, weight and height between the JIA and control groups using independent t-tests. 2.2. Treatment The participants with JIA were treated and injected with methylprednisolone acetate (Depo-medrolTM) in 1–10 joints in lower extremities for each participant (Table 2). The treatment policy is to inject joints that are active (with synovitis) at the time of evaluation. 2.3. Movement analysis Movement was recorded with a 6-camera 3D motion analysis system (Vicon Peak, Oxford, England) (Davis, Ounpuu, Tyberski, & Gage, 1991). Thirty-four reflective markers (25 mm) were attached bilaterally on the participant’s skin at the head, shoulders, trunk, arms, pelvis, legs and feet according to a common biomechanical gait model (Plug-in-Gait, Vicon Peak). The upper body model has been described previously (Gutierrez-Farewik et al., 2006). Children with JIA were evaluated a second time 8–17 days after treatment with ICI. The same examiner (EB) performed the clinical measurement and marker placement in children with JIA.
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Table 1 Descriptive information of the children with JIA (n = 17) and the control group (n = 21) Sex
Age (yrs)
Height (cm)
Weight (kg)
JIA (n = 17) J1 J2 J3 J4 J5 J6 J7 J8 J9 J10 J11 J12 J13 J14 J15 J16 J17
F F F F F M M F M F F F F F F F F
16.0 12.5 14.7 8.7 9.9 5.9 12.0 12.6 12.3 13.6 9.0 8.0 10.0 15.2 8.0 12.2 13.9
168.0 148.0 150.0 118.0 134.0 119.0 163.0 161.5 164.5 155.0 132.0 117.5 142.0 161.0 143.0 131.5 172.5
65.0 38.1 44.9 22.1 26.1 25.6 64.1 50.8 65.0 46.3 37.5 19.0 47.8 60.5 36.0 29.9 57.0
Controls (n = 21) C1 C2 C3 C4 C5 C6 C7 C8 C9 C10 C11 C12 C13 C14 C15 C16 C17 C18 C19 C20 C21
M F F F F M M M M M F F M F M M M F F M F
11.7 12.6 12.6 12.0 11.8 10.0 11.8 10.0 9.3 5.2 9.7 9.7 5.3 12.6 10.8 14.4 12.7 10.6 11.1 9.2 5.9
150.0 142.0 152.0 150.5 151.0 144.5 156.5 142.5 137.0 113.0 132.5 130.5 107.0 141.0 154.0 179.5 156.0 142.5 143.5 135.5 118.0
31.5 48.7 38.0 53.7 37.8 34.3 52.3 29.9 32.3 24.2 27.9 26.9 19.2 33.0 48.6 57.5 37.8 34.1 40.6 31.4 22.7
Table 2 Disease duration and injected joints for the children with JIA (n = 17) Disease duration (yrs)
Mean 3.5, SD 3.1
Injected joint Hip joint Knee joint Ankle and foot joints
Left 2 5 20
Right 4 6 22
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2.4. Data and statistical analysis To evaluate trunk kinematics, values of average, peak, and range of global trunk rotation in all three anatomical planes were calculated from five gait cycles beginning with the left foot strike and five gait cycles beginning with the right foot strike. For each participant, discrete parameters of trunk rotation (ex. range of trunk frontal rotation) was calculated for each side as the average value from the five gait cycles beginning with that side’s foot strike. Differences in trunk kinematics were evaluated in children with JIA between pre- and post-injection gait analyses using a Repeated Measures Analysis of Variance (ANOVA). Non-parametric statistical (Mann–Whitney) tests were used to determine differences between children with JIA before injection and controls, and between children with JIA after injection and controls. CoM data was calculated as the centroid of a multi-body system (kinematic method), which is based on a mass-proportionate anthropometrical model (Gutierrez-Farewik et al., 2006). CoM data was analyzed when kinematic data from all segments was available throughout a gait cycle, and was available in 14/17 participants with JIA and all 21 control participants. Trajectory of the CoM in all directions in global reference coordinates, 3D hip joint center locations in global reference coordinates, and pelvic rotation angles were imported as ASCII data into Matlab (Mathworks, USA). All data were normalized to 100 points throughout the gait cycle. The mean vertical CoM excursions for each participant were calculated from three gait cycles and normalized by each individual’s height. Differences were evaluated in children with JIA between pre- and post-injection gait analyses using a Wilcoxon Sign Rank test, between children with JIA before injection and controls, and between children with JIA after injection and controls, both using a Mann–Whitney test. To analyze CoM motion relative to the pelvis, the CoM position was determined relative to the midpoint between the hip joint centers, and then normalized to each individual’s inter-hip joint center distance as calculated by the model. This CoM trace was then rotated by the pelvic transverse rotation angle to a coordinate axis which was fixed on the hip joint centers, resulting in the CoM path relative to the pelvis in the transverse plane (Gutierrez et al., 2003a). Average fore-aft and left-right position of the CoM relative to the pelvis was calculated for each individual’s average CoM trace, and comparisons were made before and after ICI treatment (Wilcoxon Sign Rank test) and between participant groups (Mann–Whitney test). Commercially-available software was used for all statistical analyses (Statistica 7.0, StatSoft Inc., USA). Statistical significance was determined at the p < .05 level. Due to the relatively low number of participants, a ‘trend’ was defined at the p < .10 level.
3. Results 3.1. Trunk kinematics The children with JIA had a more posteriorly tilted trunk than the healthy controls (p = .01) before ICI treatment (Fig. 1). After ICI treatment in children with JIA, the lateral trunk sway, defined as the peak-to-peak range of lateral trunk deviation in a gait cycle, was reduced (p = .02), and the trunk was more posteriorly tilted than before
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8 Average Trunk Tilt (deg)
Ant
6 4 2 0 -2
.5
-4 -6
-8 Post -10
JIA
Control
Fig. 1. Average anterior trunk tilt throughout a gait cycle. Data points are shown for each participant in both JIA (pre-injection) and control groups.
treatment (p = .04). No differences were observed in transverse plane trunk rotation between participant groups or resulting from ICI treatment (Table 3). 3.2. CoM motion The children with JIA had a more lateral-deviating CoM movement than the controls (p < .001, Fig. 2) in this study. The CoM within the pelvis was more posterior and placed off-centered (more to the right side) in children with JIA than in controls (p < .001, Fig. 3). No differences in CoM movement or position were observed in CoM movement before and after ICI treatment in children with JIA (Table 3). Children with JIA showed a trend towards lower vertical CoM excursion before injection than the control group (2.05% height vs. 2.24% height, p = .08), but this result was not statistically significant. No difference was observed between vertical CoM excursion in pre- and post-injection gait analyses in the children with JIA (2.05% height in both cases).
Table 3 Averages of trunk kinematic parameters and CoM excursion before and after treatment with intra- articular corticosteroid injections in lower extremities in participants with JIA (n = 17, CoM n = 14) and in controls (n = 21) JIA before
JIA after
p (before vs. after ICI)
Controls
p (JIA-before ICI vs. control)
Trunk kinematics Lateral sway range (°) Average anterior tilt (°)
5 (2.1) 2 (2.1)
4 (1.2) 3 (2.3)
.02 .04
6 (3.0) 1 (3.6)
ns .001
CoM displacement Medio-lateral excursion (mm)
32.3 (23.3)
29.0 (19.3)
ns
19.0 (7.9)
<.001
The data are shown as mean (SD) and were calculated from five gait trials in each participant. A positive value of anterior trunk tilt implies anterior position, and a negative implies posterior. A p-value of ns implies p P .05.
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Fig. 2. CoM movement within the pelvis in the transverse plane in a representative child with JIA and a representative control participant. The data is scaled to each participant’s own inter-hip joint distance.
Fig. 3. Average CoM placement within the pelvis throughout a gait cycle in all JIA and control participants for whom such data was available. All data is scaled to each participant’s own inter-hip joint distance.
4. Discussion There are few studies investigating gait deviations in children with JIA, despite it being a common chronic disease which affects as many as 1500–1800 children in Sweden (Andersson et al., 1987). Contrary to the common clinical impression by rheumatologists and physiotherapists that children with JIA walk with an anteriorly flexed trunk, this study showed that they had essentially similar, if slightly more posterior trunk tilt than healthy controls. Even though significant differences existed in trunk displacement, the findings of differences of 1–2° are not considered clinically different. Upon visual observation of the gait analyses, children with JIA were also observed to flex their heads forward, as if looking down, and to have a noticeably large lumbar lordosis, though these specific parameters were not analyzed in the current study. The neck flexion can be attributed to both the need to look before stepping and to the common occurrence of pain and
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pathological involvement in the neck extensors. The posterior trunk position observed in children with JIA may be attributable to a need to increase their visual field due to the forward neck flexion and anterior pelvic tilt. It is hypothesized that the forward neck flexion can deceive the observer into believing that the trunk is also flexed anteriorly. Objective gait studies are crucial to confirm or refute such clinical impressions. Small differences were observed in the JIA group after treatment, but they are considered clinically negligible. Since the participants’ gait is visually improved after treatments and since the pain from a visual analog scale was reported as significantly reduced (Brostro¨m, Hagelberg, et al., 2004), we postulate that the post-treatment gait analyses in this study may have been performed too soon to detect larger changes in gait patterns. The gait compensation due to pain may not yet have diminished. The centers of mass in the JIA group were placed more posteriorly relative to the pelvis, confirming the findings of slightly posteriorly extended trunk position. The findings that the centers of mass in this group of children with JIA move asymmetrically within the pelvis and deviate more medio-laterally may be a result of pain, which is a common manifestation. Whether pain at the hips can lead to a gait compensatory mechanism to reduce hip abductor moment should be investigated, but such a mechanism may lead to greater medio-lateral CoM motion within the pelvis. The findings in the current study of increased laterally-deviating CoM correspond to findings of Gutierrez et al. (2003a), who analyzed gait in children with muscle weakness due to myelomeningocele, and who also had large laterally motion of the trunk. The lateral CoM deviation within the pelvis and the tendency to place the CoMs more on the right side in the group with JIA corresponds also to the injection sites, wherein a greater number of joints on the participants’ right sides were active (with synovitis) and treated. This implies that the participants leaned to favor the more active side. How gait is affected by the number of active and treated joints, as well as which joints (e.g., hip or knee or ankle) would require a much larger patient population and would be of great interest. It was, however, deemed that the trunk and the CoM movements in the present study represent the participants’ walking pattern as a whole, not the effect of injection at particular joints, and that the present method gives insight to the overall walking function. It has also been reported that participants with weak hip extensors have a more posterior placement of the CoM within the pelvis (Gutierrez et al., 2003a). Children with JIA are known to have reduced muscle strength in the plantarflexors (Brostro¨m, Nordlund, & Cresswell, 2004) but whether JIA can affect muscle strength at the other lower extremity joints is unknown. Future studies which compare lower limb muscle strength, as measured by a computerized dynamometer, to gait patterns will give better insight into the compensatory gait strategies in the studied population. Several other factors may influence the CoM movement, such as gender differences, according to Smith, Lelas, and Kerrigan (2002), who also showed that female participants had more frontal plane pelvic motion during gait then men. An increase in frontal plane pelvic motion may be advantageous from an energy conserving point (Saunders, Inman, & Eberhart, 1953) but it may also be associated with increased lumbo-sacral motion and lower back pain (Smith et al., 2002). To date, no known studies exist studying gender effects on pelvis-fixed CoM motion. Whether the differences observed are partly attributable to the high frequency of females in the JIA participant group is unknown. Cadence and walking speed can also affect the CoM movement. The group with JIA in the present study has been previously reported to have a normalized walking speed before ICI
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treatment of 0.79 s 1 (normalized to height), a step length of 0.53 m, and a cadence of 125 steps/min (Brostro¨m, Hagelberg, et al., 2004) and the group of controls, a normalized walking speed of 0.93 s 1, a step length of 0.61 m, and a cadence of 129 steps/min (Gutierrez, 2003). As such, some of the observed trend in CoM vertical displacement may be attributable to the difference in walking speed, where higher walking speed and/or step length was expected to be associated with higher vertical CoM excursions. In general, the overall similarity of upper body and CoM motion during gait between the participants with JIA and the control group was unexpected. The ICI treatment, while positively affecting the lower limb movements and kinetics (Brostro¨m, Hagelberg, et al., 2004), had no significant effect on the upper body kinematics, which were albeit similar to the control group. The studied group of children was heterogeneous with respect to the location and degree of affected joints, which may have affected the likelihood of finding significantly altered gait strategies in the upper body and CoM movements – each participant may be optimizing her gait according to her own experience of pain and impairment. The results of our study could have several implications in clinical practice. With the knowledge that children with JIA are more posteriorly tilted in the trunk, and place their centers of mass off-centered, it might be possible to understand better how children with JIA compensate for pain and involvement in their gait strategies, and ultimately to plan treatment to improving their gait. A thorough understanding of gait deviations and the resulting compensatory mechanisms helps clinicians treat the primary cause of gait deviation, instead of the secondary deviation. References Andersson, G. B., Fasth, A., Andersson, J., Berglund, G., Ekstrom, H., Eriksson, M., et al. (1987). Incidence and prevalence of juvenile chronic arthritis: A population survey. Annals of the Rheumatic Diseases, 46, 277–281. Baker, R. (2001). Pelvic angles: A mathematically rigorous definition which is consistent with a conventional clinical understanding of the terms. Gait and Posture, 13, 1–6. Bartonek, A., Saraste, H., Eriksson, M., Knutson, L., & Cresswell, A. G. (2002). Upper body movement during walking in children with lumbo-sacral myelomeningocele. Gait and Posture, 15, 120–129. Brostro¨m, E., Hagelberg, S., & Haglund-Akerlind, Y. (2004). Effect of joint injections in children with juvenile idiopathic arthritis: evaluation by 3D-gait analysis. Acta Paediatrica, 7, 906–910. Brostro¨m, E., Haglund-Akerlind, Y., Hagelberg, S., & Cresswell, A. G. (2002). Gait in children with juvenile chronic arthritis. Timing and force parameters. Scandinavian Journal of Rheumatology, 31, 317–323. Brostro¨m, E., Nordlund, M. M., & Cresswell, A. G. (2004). Plantar- and dorsiflexor strength in prepubertal girls with juvenile idiopathic arthritis. Archive Physical Medicine and Rehabilitation, 85, 1224–1230. Cassidy, J. T., & Petty, R. E. (2002). Textbook of pediatric rheumatology (2nd ed.). New York: Churchill Livingstone Inc. Davis, R. B., Ounpuu, S., Tyberski, D., & Gage, J. R. (1991). A gait analysis data collection and reduction technique. Human Movement Science, 10, 575–587. Eames, M. H. A., Cosgrove, A., & Baker, R. (1999). Comparing methods of estimating the total body centre of mass in three-dimensions in normal and pathological gaits. Human Movement Science, 18, 637–646. Engsberg, J. R., Lenke, L. G., Uhrich, M. L., Ross, S. A., & Bridwell, K. H. (2003). Prospective comparison of gait and trunk range of motion in adolescents with idiopathic thoracic scoliosis undergoing anterior or posterior spinal fusion. Spine, 28, 1993–2000. Fairburn, P. S., Panagamuwa, B., Falkonakis, A., Osborne, S., Palmer, R., Johnson, B., et al. (2002). The use of multidisciplinary assessment and scientific measurement in advanced juvenile idiopathic arthritis can categorise gait deviations to guide treatment. Archive Physical Medicine and Rehabilitation, 87, 160–165. Frigo, C., Bardare, M., Corona, F., Casnaghi, D., Cimaz, R., Naj Fovino, P., et al. (1996). Gait alteration in patients with Juvenile idiopathic arthritis: A computerized analysis. Journal of Orthopaedic Rheumatolgy, 9, 82–90.
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Frigo, C., Carabalona, R., Dalla, M. M., & Negrini, S. (2003). The upper body segmental movements during walking by young females. Clinical Biomechanics, 18, 419–425. Gard, S. A., Miff, S. C., & Kuo, A. D. (2004). Comparison of kinematic and kinetic methods for computing the vertical motion of the body center of mass during walking. Human Movement Science, 22, 597–610. Gutierrez, E. M. (2003). Gait strategy in myelomeningocele: Movements, mechanics and methods. Karolinska Institutet, Thesis. Gutierrez, E. M., Bartonek, A., Haglund-Akerlind, Y., & Saraste, H. (2003a). Centre of mass motion during gait in persons with myelomeningocele. Gait and Posture, 18, 37–46. Gutierrez, E. M., Bartonek, A., Haglund-Akerlind, Y., & Saraste, H. (2003b). Characteristic gait kinematics in persons with lumbosacral myelomeningocele. Gait and Posture, 18, 170–177. ˚ ., & Saraste, H. (2006). Comparison and evaluation of two common Gutierrez-Farewik, E. M., Bartonek, A methods to measure center of mass displacement in three dimensions during gait. Human Movement Science, 25, 238–256. Hagelberg, S., Magnusson, B., Jenner, G., & Andersson, U. (2000). Do frequent corticosteroid injections in the knee cause cartilage damage in juvenile chronic arthritis? Long-term follow-up with MRI. Journal of Rheumatology, 27(Suppl 58), 95. Huppertz, H. I., Tschammler, A., Horwitz, A. E., & Schwab, K. O. (1995). Intraarticular corticosteroids for chronic arthritis in children – efficacy and effects on cartilage and growth. Journal of Pediatrics, 127, 317–321. Kramers-de, Q. I., Muller, R., Stacoff, A., Grob, D., & Stussi, E. (2004). Gait analysis in patients with idiopathic scoliosis. Eurpean Spine Journal, 13, 449–456. Krebs, D. E., Wong, D., Jevsevar, D., Riley, P. O., & Hodge, W. A. (1992). Trunk kinematics during locomotor activities. Physical Therapy, 72, 505–514. Lechner, E. D., McCarthy, F. C., & Holden, M. K. (1987). Gait deviations in patients with juvenile rheumatoid arthritis. Physical Therapy, 67, 1335–1341. Padeh, S., & Passwell, J. H. (1998). Intraarticular corticosteroid injection in the management of children with chronic arthritis. Arthritis and Rheumatism, 41, 1210–1214. Perry, J. (2002). Gait analysis – normal and pathological function (1992 edn.). Thorafare: Slack. Saunders, J., Inman, V., & Eberhart, H. (1953). The major determinants in normal and patholigical gait. Journal of Bone and Joint Surgery America, 35, 543–558. Sherry, D. D., Stein, L. D., Reed, A. M., Schanberg, L. E., & Kredich, D. W. (1999). Prevention of leg length discrepancy in young children with particular juvenile rheumatoid arthritis by treatment with intraarticular steroids. Arthritis and Rheumatism, 42, 2330–2334. Smith, L. K., Lelas, J. L., & Kerrigan, D. C. (2002). Gender differences in pelvic motions and center of mass displacement during walking: Stereotypes quantified. Journal of Women’s Health and Gender-based Medicine, 11, 453–458. Thorstensson, A., Nilsson, J., Carlson, H., & Zomlefer, M. R. (1984). Trunk movements in human locomotion. Acta physiologica Scandinavica, 121, 9–22. Van Emmerik, R. E., McDermott, W. J., Haddad, J. M., & Van Wegen, E. E. (2005). Age-related changes in upper body adaptation to walking speed in human locomotion. Gait and Posture, 22, 233–239. Winter, D. A. (1995). Human balance and posture control during standing and walking. Gait and Posture, 3, 193–214.
Trunk and center of mass movements during gait in children with juvenile idiopathic arthritis ˚ kerlind a, ¨ rtqvist a, Yvonne Haglund-A Eva Brostro¨m a,*, Maria O Stefan Hagelberg a, Elena Gutierrez-Farewik a,b a
Department of Woman and Child Health, Karolinska Institute, Sweden KTH Mechanics, Royal Institute of Technology, Stockholm, Sweden
b
Available online 6 March 2007
Abstract Motion of the body center of mass (CoM) can often indicate the overall effect of the strategy of forward progression used. In the present study, focus is placed on trunk movements in the sagittal, coronal, and transverse/rotation plane, as well as placement of the CoM, during gait in children with juvenile idiopathic arthritis (JIA). Seventeen children with JIA, all with polyarticular lower extremity involvement were examined before and approximately two weeks after treatment with intra-articular cortico-steroid injections. Movement was recorded with a 6-camera 3D motion analysis system in both the children with JIA and in 21 healthy controls. Trunk and center of mass movements were compared between JIA and controls, and effects of intra-articular cortico-steroid treatment were evaluated. Children with JIA were more posteriorly tilted in the trunk, contrary to the common clinical impression, and had their CoM placed more posterior and off-centred, which may have been a result of pain. With such knowledge, it might be possible to better understand the effects of their pain and involvement, and ultimately to plan a treatment strategy for improving their gait patterns. Ó 2007 Elsevier B.V. All rights reserved. PsycINFO classification: 3363 Keywords: Juvenile rheumatoid arthritis; 3D gait analysis; Centre of gravity
* Corresponding author. Present address: MotorikLab Q2:07 ALB, Karolinska University Hospital, 171 76 Stockholm, Sweden. Tel.: +46 8 517 77636. E-mail address: [email protected] (E. Brostro¨m).
0167-9457/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.humov.2007.01.007
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1. Introduction In normal walking the body functionally divides itself into two units, passenger (head, neck, trunk and arms) and locomotor (two lower limbs and pelvis). While there is motion and muscle action occurring in each, there is a difference between the two units. The passenger unit is responsible only for its own postural integrity, while the locomotor unit is a major determinant for muscle action within the locomotor system. During normal gait the head and trunk travel as a unit, with little apparent motion relative to the pelvis (Perry, 2002), but some studies report small arcs of displacement in both the sagittal and frontal planes (Krebs, Wong, Jevsevar, Riley, & Hodge, 1992; Perry, 2002; Thorstensson, Nilsson, Carlson, & Zomlefer, 1984). Small arcs of motion also occur in the pelvis (Perry, 2002). More recent studies verify these results; in normal populations of young females the trunk is more anteriorly flexed during walking than in standing, with small range of motion in the sagittal plane, and even smaller in the frontal plane (Frigo et al., 1996). The manifestations of juvenile idiopathic arthritis (JIA) include joint swelling, effusion, tenderness, painful limitation of joint movement, and a disturbance of gait (Cassidy & Petty, 2002). Previous studies of controlled quantitative gait assessment in JIA showed significant alterations from the normal in recorded kinematics and temporal data (Brostro¨m, Haglund-Akerlind, Hagelberg, & Cresswell, 2002; Fairburn et al., 2002; Frigo et al., 1996). Participants with JIA displayed excessive anterior tilt of the pelvis and decreased hip extension and ankle plantarflexion angle at toe-off (Lechner, McCarthy, & Holden, 1987). Later studies reported both kinematic and kinetic deviations (Brostro¨m, Hagelberg, & Haglund-Akerlind, 2004; Frigo et al., 1996). It has been shown that children with JIA walk more slowly, take shorter steps (Brostro¨m et al., 2002; Frigo et al., 1996; Gard, Miff, & Kuo, 2004; Lechner et al., 1987), and have a lower cadence (Lechner et al., 1987). While trunk movements have been reported in able-bodied populations (Frigo, Carabalona, Dalla, & Negrini, 2003; Van Emmerik, McDermott, Haddad, & Van Wegen, 2005), in idiopathic scoliosis (Engsberg, Lenke, Uhrich, Ross, & Bridwell, 2003; Kramers-de, Muller, Stacoff, Grob, & Stussi, 2004) and in myelomeningocele (Baker, 2001; Bartonek, Saraste, Eriksson, Knutson, & Cresswell, 2002; Gutierrez, Bartonek, Haglund-Akerlind, & Saraste, 2003b), among others, there are no studies focusing on trunk movements in children with JIA to our knowledge. Intra-articular corticosteroid injections (ICI) are a common and effective treatment in children with JIA (Huppertz, Tschammler, Horwitz, & Schwab, 1995; Padeh & Passwell, 1998). It is reported that this treatment is safe and provides continued anti-inflammatory effects on the synovium. In one study 82% of 300 joints that were injected demonstrated full clinical remission of the joint inflammation (Padeh & Passwell, 1998). There is also evidence that leg length discrepancy resulting from unilateral knee synovitis as well as joint deformity and joint damage may be prevented (Sherry, Stein, Reed, Schanberg, & Kredich, 1999). Long-term follow up with magnetic resonance imagining after repeated ICIs in knee of JIA patients showed preserved cartilage (Hagelberg, Magnusson, Jenner, & Andersson, 2000). Gait analysis is a common and objective method to verify and document a participant’s walking pattern. Gait is generally described in cycles for each side, beginning with foot contact of that side and ending with the next foot contact of the same foot, and further divided into two phases, stance and swing (Perry, 2002). The body center of mass (CoM) in a quiet standing position is located approximately anterior to the second sacral
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vertebra. To maintain a static position, the CoM must remain in balance over the base of support (Winter, 1995). The change in CoM motion during gait represents the overall result of joint and segment movements on the forward progression, and is of importance when describing pathological gait. It has been used to evaluate gait efficiency and strategy (Gutierrez, Bartonek, Haglund-Akerlind, & Saraste, 2003a). The CoM can either be measured as the centroid of a multi-body system (kinematic method) or from the ground reaction force, using a dynamic equilibrium calculation and integrating for the CoM displacement. Several studies have shown that the different measurement methods provide similar results (Eames, Cosgrove, & Baker, 1999; Gard et al., 2004; Gutierrez-Farewik, Bartonek, & Saraste, 2006). The goals of this study were to compare trunk and CoM motion in children with JIA and children without JIA and to detect alterations after ICI treatment. 2. Methods 2.1. Participants Seventeen children between 5 and 16 years of age (mean 11.4, SD 2.9 years, 14 females, 3 males) with JIA were diagnosed according to the criteria set by the Paediatric Standing Committee of International League of Associations for Rheumatology (ILAR, Table 1). All patients were treated regularly at the Department of Paediatric Rheumatology. They were all independent walkers, had lower extremity involvement in five or more joints (polyarticular), and were scheduled for treatment with ICI injections. The local research ethical committee approved the study. Participation was voluntary. Verbal and written information was given to the children and their parents. Twenty-one healthy children between 5 and 14 years of age (mean 10.4, SD 2.5 and 10 female, 11 male) were investigated with the same protocol (Table 1). Ages, weights and heights were approximately normal distributed in both groups, and no statistically significant differences were found in age, weight and height between the JIA and control groups using independent t-tests. 2.2. Treatment The participants with JIA were treated and injected with methylprednisolone acetate (Depo-medrolTM) in 1–10 joints in lower extremities for each participant (Table 2). The treatment policy is to inject joints that are active (with synovitis) at the time of evaluation. 2.3. Movement analysis Movement was recorded with a 6-camera 3D motion analysis system (Vicon Peak, Oxford, England) (Davis, Ounpuu, Tyberski, & Gage, 1991). Thirty-four reflective markers (25 mm) were attached bilaterally on the participant’s skin at the head, shoulders, trunk, arms, pelvis, legs and feet according to a common biomechanical gait model (Plug-in-Gait, Vicon Peak). The upper body model has been described previously (Gutierrez-Farewik et al., 2006). Children with JIA were evaluated a second time 8–17 days after treatment with ICI. The same examiner (EB) performed the clinical measurement and marker placement in children with JIA.
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Table 1 Descriptive information of the children with JIA (n = 17) and the control group (n = 21) Sex
Age (yrs)
Height (cm)
Weight (kg)
JIA (n = 17) J1 J2 J3 J4 J5 J6 J7 J8 J9 J10 J11 J12 J13 J14 J15 J16 J17
F F F F F M M F M F F F F F F F F
16.0 12.5 14.7 8.7 9.9 5.9 12.0 12.6 12.3 13.6 9.0 8.0 10.0 15.2 8.0 12.2 13.9
168.0 148.0 150.0 118.0 134.0 119.0 163.0 161.5 164.5 155.0 132.0 117.5 142.0 161.0 143.0 131.5 172.5
65.0 38.1 44.9 22.1 26.1 25.6 64.1 50.8 65.0 46.3 37.5 19.0 47.8 60.5 36.0 29.9 57.0
Controls (n = 21) C1 C2 C3 C4 C5 C6 C7 C8 C9 C10 C11 C12 C13 C14 C15 C16 C17 C18 C19 C20 C21
M F F F F M M M M M F F M F M M M F F M F
11.7 12.6 12.6 12.0 11.8 10.0 11.8 10.0 9.3 5.2 9.7 9.7 5.3 12.6 10.8 14.4 12.7 10.6 11.1 9.2 5.9
150.0 142.0 152.0 150.5 151.0 144.5 156.5 142.5 137.0 113.0 132.5 130.5 107.0 141.0 154.0 179.5 156.0 142.5 143.5 135.5 118.0
31.5 48.7 38.0 53.7 37.8 34.3 52.3 29.9 32.3 24.2 27.9 26.9 19.2 33.0 48.6 57.5 37.8 34.1 40.6 31.4 22.7
Table 2 Disease duration and injected joints for the children with JIA (n = 17) Disease duration (yrs)
Mean 3.5, SD 3.1
Injected joint Hip joint Knee joint Ankle and foot joints
Left 2 5 20
Right 4 6 22
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2.4. Data and statistical analysis To evaluate trunk kinematics, values of average, peak, and range of global trunk rotation in all three anatomical planes were calculated from five gait cycles beginning with the left foot strike and five gait cycles beginning with the right foot strike. For each participant, discrete parameters of trunk rotation (ex. range of trunk frontal rotation) was calculated for each side as the average value from the five gait cycles beginning with that side’s foot strike. Differences in trunk kinematics were evaluated in children with JIA between pre- and post-injection gait analyses using a Repeated Measures Analysis of Variance (ANOVA). Non-parametric statistical (Mann–Whitney) tests were used to determine differences between children with JIA before injection and controls, and between children with JIA after injection and controls. CoM data was calculated as the centroid of a multi-body system (kinematic method), which is based on a mass-proportionate anthropometrical model (Gutierrez-Farewik et al., 2006). CoM data was analyzed when kinematic data from all segments was available throughout a gait cycle, and was available in 14/17 participants with JIA and all 21 control participants. Trajectory of the CoM in all directions in global reference coordinates, 3D hip joint center locations in global reference coordinates, and pelvic rotation angles were imported as ASCII data into Matlab (Mathworks, USA). All data were normalized to 100 points throughout the gait cycle. The mean vertical CoM excursions for each participant were calculated from three gait cycles and normalized by each individual’s height. Differences were evaluated in children with JIA between pre- and post-injection gait analyses using a Wilcoxon Sign Rank test, between children with JIA before injection and controls, and between children with JIA after injection and controls, both using a Mann–Whitney test. To analyze CoM motion relative to the pelvis, the CoM position was determined relative to the midpoint between the hip joint centers, and then normalized to each individual’s inter-hip joint center distance as calculated by the model. This CoM trace was then rotated by the pelvic transverse rotation angle to a coordinate axis which was fixed on the hip joint centers, resulting in the CoM path relative to the pelvis in the transverse plane (Gutierrez et al., 2003a). Average fore-aft and left-right position of the CoM relative to the pelvis was calculated for each individual’s average CoM trace, and comparisons were made before and after ICI treatment (Wilcoxon Sign Rank test) and between participant groups (Mann–Whitney test). Commercially-available software was used for all statistical analyses (Statistica 7.0, StatSoft Inc., USA). Statistical significance was determined at the p < .05 level. Due to the relatively low number of participants, a ‘trend’ was defined at the p < .10 level.
3. Results 3.1. Trunk kinematics The children with JIA had a more posteriorly tilted trunk than the healthy controls (p = .01) before ICI treatment (Fig. 1). After ICI treatment in children with JIA, the lateral trunk sway, defined as the peak-to-peak range of lateral trunk deviation in a gait cycle, was reduced (p = .02), and the trunk was more posteriorly tilted than before
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8 Average Trunk Tilt (deg)
Ant
6 4 2 0 -2
.5
-4 -6
-8 Post -10
JIA
Control
Fig. 1. Average anterior trunk tilt throughout a gait cycle. Data points are shown for each participant in both JIA (pre-injection) and control groups.
treatment (p = .04). No differences were observed in transverse plane trunk rotation between participant groups or resulting from ICI treatment (Table 3). 3.2. CoM motion The children with JIA had a more lateral-deviating CoM movement than the controls (p < .001, Fig. 2) in this study. The CoM within the pelvis was more posterior and placed off-centered (more to the right side) in children with JIA than in controls (p < .001, Fig. 3). No differences in CoM movement or position were observed in CoM movement before and after ICI treatment in children with JIA (Table 3). Children with JIA showed a trend towards lower vertical CoM excursion before injection than the control group (2.05% height vs. 2.24% height, p = .08), but this result was not statistically significant. No difference was observed between vertical CoM excursion in pre- and post-injection gait analyses in the children with JIA (2.05% height in both cases).
Table 3 Averages of trunk kinematic parameters and CoM excursion before and after treatment with intra- articular corticosteroid injections in lower extremities in participants with JIA (n = 17, CoM n = 14) and in controls (n = 21) JIA before
JIA after
p (before vs. after ICI)
Controls
p (JIA-before ICI vs. control)
Trunk kinematics Lateral sway range (°) Average anterior tilt (°)
5 (2.1) 2 (2.1)
4 (1.2) 3 (2.3)
.02 .04
6 (3.0) 1 (3.6)
ns .001
CoM displacement Medio-lateral excursion (mm)
32.3 (23.3)
29.0 (19.3)
ns
19.0 (7.9)
<.001
The data are shown as mean (SD) and were calculated from five gait trials in each participant. A positive value of anterior trunk tilt implies anterior position, and a negative implies posterior. A p-value of ns implies p P .05.
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Fig. 2. CoM movement within the pelvis in the transverse plane in a representative child with JIA and a representative control participant. The data is scaled to each participant’s own inter-hip joint distance.
Fig. 3. Average CoM placement within the pelvis throughout a gait cycle in all JIA and control participants for whom such data was available. All data is scaled to each participant’s own inter-hip joint distance.
4. Discussion There are few studies investigating gait deviations in children with JIA, despite it being a common chronic disease which affects as many as 1500–1800 children in Sweden (Andersson et al., 1987). Contrary to the common clinical impression by rheumatologists and physiotherapists that children with JIA walk with an anteriorly flexed trunk, this study showed that they had essentially similar, if slightly more posterior trunk tilt than healthy controls. Even though significant differences existed in trunk displacement, the findings of differences of 1–2° are not considered clinically different. Upon visual observation of the gait analyses, children with JIA were also observed to flex their heads forward, as if looking down, and to have a noticeably large lumbar lordosis, though these specific parameters were not analyzed in the current study. The neck flexion can be attributed to both the need to look before stepping and to the common occurrence of pain and
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pathological involvement in the neck extensors. The posterior trunk position observed in children with JIA may be attributable to a need to increase their visual field due to the forward neck flexion and anterior pelvic tilt. It is hypothesized that the forward neck flexion can deceive the observer into believing that the trunk is also flexed anteriorly. Objective gait studies are crucial to confirm or refute such clinical impressions. Small differences were observed in the JIA group after treatment, but they are considered clinically negligible. Since the participants’ gait is visually improved after treatments and since the pain from a visual analog scale was reported as significantly reduced (Brostro¨m, Hagelberg, et al., 2004), we postulate that the post-treatment gait analyses in this study may have been performed too soon to detect larger changes in gait patterns. The gait compensation due to pain may not yet have diminished. The centers of mass in the JIA group were placed more posteriorly relative to the pelvis, confirming the findings of slightly posteriorly extended trunk position. The findings that the centers of mass in this group of children with JIA move asymmetrically within the pelvis and deviate more medio-laterally may be a result of pain, which is a common manifestation. Whether pain at the hips can lead to a gait compensatory mechanism to reduce hip abductor moment should be investigated, but such a mechanism may lead to greater medio-lateral CoM motion within the pelvis. The findings in the current study of increased laterally-deviating CoM correspond to findings of Gutierrez et al. (2003a), who analyzed gait in children with muscle weakness due to myelomeningocele, and who also had large laterally motion of the trunk. The lateral CoM deviation within the pelvis and the tendency to place the CoMs more on the right side in the group with JIA corresponds also to the injection sites, wherein a greater number of joints on the participants’ right sides were active (with synovitis) and treated. This implies that the participants leaned to favor the more active side. How gait is affected by the number of active and treated joints, as well as which joints (e.g., hip or knee or ankle) would require a much larger patient population and would be of great interest. It was, however, deemed that the trunk and the CoM movements in the present study represent the participants’ walking pattern as a whole, not the effect of injection at particular joints, and that the present method gives insight to the overall walking function. It has also been reported that participants with weak hip extensors have a more posterior placement of the CoM within the pelvis (Gutierrez et al., 2003a). Children with JIA are known to have reduced muscle strength in the plantarflexors (Brostro¨m, Nordlund, & Cresswell, 2004) but whether JIA can affect muscle strength at the other lower extremity joints is unknown. Future studies which compare lower limb muscle strength, as measured by a computerized dynamometer, to gait patterns will give better insight into the compensatory gait strategies in the studied population. Several other factors may influence the CoM movement, such as gender differences, according to Smith, Lelas, and Kerrigan (2002), who also showed that female participants had more frontal plane pelvic motion during gait then men. An increase in frontal plane pelvic motion may be advantageous from an energy conserving point (Saunders, Inman, & Eberhart, 1953) but it may also be associated with increased lumbo-sacral motion and lower back pain (Smith et al., 2002). To date, no known studies exist studying gender effects on pelvis-fixed CoM motion. Whether the differences observed are partly attributable to the high frequency of females in the JIA participant group is unknown. Cadence and walking speed can also affect the CoM movement. The group with JIA in the present study has been previously reported to have a normalized walking speed before ICI
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treatment of 0.79 s 1 (normalized to height), a step length of 0.53 m, and a cadence of 125 steps/min (Brostro¨m, Hagelberg, et al., 2004) and the group of controls, a normalized walking speed of 0.93 s 1, a step length of 0.61 m, and a cadence of 129 steps/min (Gutierrez, 2003). As such, some of the observed trend in CoM vertical displacement may be attributable to the difference in walking speed, where higher walking speed and/or step length was expected to be associated with higher vertical CoM excursions. In general, the overall similarity of upper body and CoM motion during gait between the participants with JIA and the control group was unexpected. The ICI treatment, while positively affecting the lower limb movements and kinetics (Brostro¨m, Hagelberg, et al., 2004), had no significant effect on the upper body kinematics, which were albeit similar to the control group. The studied group of children was heterogeneous with respect to the location and degree of affected joints, which may have affected the likelihood of finding significantly altered gait strategies in the upper body and CoM movements – each participant may be optimizing her gait according to her own experience of pain and impairment. The results of our study could have several implications in clinical practice. With the knowledge that children with JIA are more posteriorly tilted in the trunk, and place their centers of mass off-centered, it might be possible to understand better how children with JIA compensate for pain and involvement in their gait strategies, and ultimately to plan treatment to improving their gait. A thorough understanding of gait deviations and the resulting compensatory mechanisms helps clinicians treat the primary cause of gait deviation, instead of the secondary deviation. References Andersson, G. B., Fasth, A., Andersson, J., Berglund, G., Ekstrom, H., Eriksson, M., et al. (1987). Incidence and prevalence of juvenile chronic arthritis: A population survey. Annals of the Rheumatic Diseases, 46, 277–281. Baker, R. (2001). Pelvic angles: A mathematically rigorous definition which is consistent with a conventional clinical understanding of the terms. Gait and Posture, 13, 1–6. Bartonek, A., Saraste, H., Eriksson, M., Knutson, L., & Cresswell, A. G. (2002). Upper body movement during walking in children with lumbo-sacral myelomeningocele. Gait and Posture, 15, 120–129. Brostro¨m, E., Hagelberg, S., & Haglund-Akerlind, Y. (2004). Effect of joint injections in children with juvenile idiopathic arthritis: evaluation by 3D-gait analysis. Acta Paediatrica, 7, 906–910. Brostro¨m, E., Haglund-Akerlind, Y., Hagelberg, S., & Cresswell, A. G. (2002). Gait in children with juvenile chronic arthritis. Timing and force parameters. Scandinavian Journal of Rheumatology, 31, 317–323. Brostro¨m, E., Nordlund, M. M., & Cresswell, A. G. (2004). Plantar- and dorsiflexor strength in prepubertal girls with juvenile idiopathic arthritis. Archive Physical Medicine and Rehabilitation, 85, 1224–1230. Cassidy, J. T., & Petty, R. E. (2002). Textbook of pediatric rheumatology (2nd ed.). New York: Churchill Livingstone Inc. Davis, R. B., Ounpuu, S., Tyberski, D., & Gage, J. R. (1991). A gait analysis data collection and reduction technique. Human Movement Science, 10, 575–587. Eames, M. H. A., Cosgrove, A., & Baker, R. (1999). Comparing methods of estimating the total body centre of mass in three-dimensions in normal and pathological gaits. Human Movement Science, 18, 637–646. Engsberg, J. R., Lenke, L. G., Uhrich, M. L., Ross, S. A., & Bridwell, K. H. (2003). Prospective comparison of gait and trunk range of motion in adolescents with idiopathic thoracic scoliosis undergoing anterior or posterior spinal fusion. Spine, 28, 1993–2000. Fairburn, P. S., Panagamuwa, B., Falkonakis, A., Osborne, S., Palmer, R., Johnson, B., et al. (2002). The use of multidisciplinary assessment and scientific measurement in advanced juvenile idiopathic arthritis can categorise gait deviations to guide treatment. Archive Physical Medicine and Rehabilitation, 87, 160–165. Frigo, C., Bardare, M., Corona, F., Casnaghi, D., Cimaz, R., Naj Fovino, P., et al. (1996). Gait alteration in patients with Juvenile idiopathic arthritis: A computerized analysis. Journal of Orthopaedic Rheumatolgy, 9, 82–90.
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