ORIGINAL ARTICLE
A Descriptive Study of Lower Limb Torsional Kinematic Profiles in Children With Spastic Diplegia Anne-Laure Simon, MD,* Brice Ilharreborde, MD, PhD,* Fabrice Megrot, PhD,w Cindy Mallet, MD,* Reza Azarpira, MD,z Keyvan Mazda, MD,* Ana Presedo, MD,* and Georges F. Pennec¸ot, MD*
Background: Lower limb rotational anomalies in spastic diplegic children with cerebral palsy (CP) are common and difficult to identify through physical examination alone. The identification and treatment of the overall rotational disorders must be considered to restore physiological lever-arms lengths and leverarms orientation. The aims of the study were to assess the prevalence of lower limb rotational malalignment and to describe the distribution of the different kinematic torsional profiles in children with spastic diplegia. Methods: Instrumented gait analysis data from 188 children with spastic diplegia were retrospectively reviewed. None of the patients had undergone surgery previously or received botulinum toxin treatment within 6 months before the review. Kinematic data, collected at the midstance phase, included: pelvic, hip, and ankle rotation and foot progression angle. Results: The prevalence of kinematic rotational deviations was 98.4%. Sixty-one percent of the children walked with an internal foot progression angle and 21% exhibited external alignment. The pelvis was internally rotated in 41% of the cases and externally in another 27%. Hip rotation was internal in 29% and external in 27% of the cases. Ankle rotation was internal in 55% and external in 16% of the cases. Lower limb rotational anomalies involved more than one level in 77% of the limbs. A kinematic compensatory deviation was identified in at least one level in 48% of the limbs. Conclusions: Kinematic rotational anomalies were identified in nearly all the 188 children in the study. The multilevel involvement of lower limb malalignment was not systematically associated with compensatory mechanisms between the levels. Ankle rotational anomalies were the most frequent cause of lower limb torsional deviations followed by pelvic malalignment. Level of Evidence: Level IV. Key Words: lower limb, transverse plane, kinematics, spastic diplegia, cerebral palsy (J Pediatr Orthop 2015;35:576–582) From the *Pediatric Orthopedics Department, Robert Debre´ Hospital, Paris; wBois-Larris Motion Analysis Laboratory, Centre of Functional Reeducation and Rehabilitation, Lamorlaye, France; and zPediatric Orthopedics Department, Namazi Hospital, Shiraz, Iran. None of the authors received financial support for this study. The authors declare no conflicts of interest. Reprints: Anne-Laure Simon, MD, Pediatric Orthopedics Department, Robert Debre´ Hospital, 48 Bd Serrurier, Paris 75019, France. E-mail: [email protected]. Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved.
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ower limb torsional anomalies are common in children with spastic diplegia and usually involve multiple levels (pelvis, hip, and ankle). The influence of torsional malalignment on gait kinetics and kinematics has been well documented. Transverse plane deviations change the orientation and the length of muscular lever-arm, thus contributing to abnormal moments.1,2 Although mechanisms and causes of lower limbs torsional profiles in children with cerebral palsy (CP) are well known, the assessment of kinematic prevalence and the description of lower limb transverse plane deviations in children with spastic diplegia have not been established. Numerous studies investigating rotational malalignment have been reported but studies are variable regarding CP type (data from hemiplegic, diplegic, and quadriplegic patients were analyzed collectively), are usually focused on specific lower limb levels, or take various kinematic plane deviations into considerations.3–7 Given that transverse plane abnormalities are not always recognizable through physical examination (static evaluation), instrumented gait analysis is a prerequisite for proper functional evaluation.8–10 Transverse plane kinematics provide reliable information to analyze the impact of torsional deviations on lower limb alignment and gait patterns.11,12 The aims of the present study were to assess the prevalence of lower limb rotational malalignment and to describe the distribution of the different kinematic torsional profiles in children with spastic diplegia.
METHODS Patients Following institutional review board approval, full 3-dimensional gait analyzes performed between 2007 and 2011 in 188 diplegic children with CP of type II (159/188, 85%) and III (29/188, 15%) according to the Gross Motor Function Classification System (GMFCS) were retrospectively reviewed. The average age of the patients was 11.7 ± 0.2 years (range, 4.25 to 25 y). Inclusion criteria were: a diagnosis of spastic diplegic CP, the ability to walk with or without assistive devices and a full-instrumented gait analysis recorded barefoot. Exclusion criteria were: previous surgical procedures and previous botulinum-toxin injection or cast within the 6 months before performing the instrumented gait analysis. J Pediatr Orthop
Volume 35, Number 6, September 2015
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J Pediatr Orthop
Volume 35, Number 6, September 2015
Gait Analysis Gait analysis data included videotaping, tri-dimensional kinematics and a physical examination. The motion of body segments was recorded in 3 dimensions with an 8-camera VICON MX system (Oxford Metrics Ltd., Oxford, UK) near-infra-red motion analysis system, at a sampling rate of 100 Hz. Fifteen passive reflecting markers were placed on anatomic landmarks, respecting the Helen Hayes protocol. The biomechanical model as described by Davis and Ounpuu (Plug-in Gait) was used in the study.13 To improve the consistency of the measures, the knee and the ankle flexion axis were calculated for each patient during the static phase, to improve the Plug-in Gait model: the Knee Alignment Device (KAD, Motion Labs Systems) was used and a medial ankle marker (MED protocol) was added. Data were filtered using a fourth-order zero-lag Butterworth low-pass-filter, with a 6 Hz cutoff frequency. The Euler angles for the hips, knees, and ankles were calculated. Datasets from multiple trials were collected as the child walked barefoot at a self-selected cadence along a walkway. One representative and regular stride was selected and analyzed by one senior orthopaedic surgeon qualified in instrumented gait analysis after reviewing both videotapes and transverse plane kinematic curves. Kinematic data from 376 lower limbs were collected. The following transverse plane parameters were analyzed: pelvis, hip and ankle kinematics, and foot progression angle. Data were collected at 30% of the gait cycle. All values within more or less 1 SD from the mean were considered normal.14 Accuracy and consistency of data quality were monitored with periodic testing measures of healthy subjects without lower limb torsional deviations. Normal values from the laboratory were 5 to 3 degrees for pelvic rotation, 9 to 4 degrees for hip rotation, 15 to 28 degrees for ankle rotation, and 4 to 15 degrees for foot progression angle. Negative and positive values corresponded respectively to internal and external rotation.
Statistical Analysis All quantitative data were reported as mean ± standard error of the mean (SEM) with reference to angle range of motion from kinematic data. All qualitative data were reported as percent.
RESULTS
Lower Limb Torsional Profiles in Spastic Diplegia
TABLE 1. Distribution of Torsional Anomalies Among the 376 Lower Limbs Foot progression angle Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Pelvis rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Hip rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Ankle rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.)
Internal
Normal
External
61 231 12.1 ± 0.7 [ 52; 3]
18 67 8.4 ± 0.5 [4; 15]
21 78 29.1 ± 1.3 [16; 68]
41 154 14.1 ± 1.3 [ 52; 6]
32 121 1.3 ± 0.22 [9; 4]
27 101 9.6 ± 0.5 [5; 28]
29 107 17.2 ± 0.7 [ 39; 10]
44 166 2.7 ± 0.3 [39; 10]
27 103 12 ± 0.6 [5; 30]
55 205 1.9 ± 0.6 [ 48; 14]
29 111 20.2 ± 0.4 [15; 28]
16 60 40.1 ± 1.4 [29; 74]
LL indicates lower limbs; SEM, standard error of the mean.
Given the wide range of rotational anomalies, data were classified according to the foot progression angle, which is widely considered as the result of overlying rotational anomalies and which can easily be identified on the videotapes.
Internal Foot Progression Angle Lower limbs were internally rotated at all levels in 3% of the children (Fig. 1). The remaining children showed combined anomalies between the levels resulting in an internal foot progression angle. A single level cause of internal foot progression angle was detected in 46.3% of the limbs. The level was identified at the pelvis in 10.8%, at the hip in 6.9%, and at the ankle in 28.6% of the limbs. Some cases of internal foot progression angle were identified even when the rotation of each level was within normal values. These results can be attributed to the fact that each rotation value was at the lower limit of the SD, with an internal foot progression gait pattern at the end.
Global Distribution
Normal Foot Progression Angle
Table 1 summarizes the distribution of torsional anomalies of foot progression angle and pelvic, hip, and ankle rotation. The prevalence of kinematic transverse plane deviation was 98.4%. Internal malalignment was the most frequent pattern for foot progression angle, pelvic, and ankle rotation. Normal alignment was the most frequent pattern for the hip. Lower limb rotational anomalies involved more than one level in 77% of the limbs. A kinematic compensatory deviation was identified in at least one level in 48% of the limbs. Twenty-seven percent of theses kinematic compensatory deviations occurred between the hip and the ipsilateral pelvis.
Nine percent of the lower limbs had no abnormal segmental rotation (Fig. 2). The remaining children had compensatory segmental torsional anomalies resulting in normal foot progression angle.
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External Foot Progression Angle Lower limbs were externally rotated at all levels in 4% of the children (Fig. 3). The remaining children had combined anomalies between the levels resulting in an external foot progression angle. A single level cause of external foot progression angle was detected in 46.2% of the limbs. The level was identified at the pelvis in 6.4%, at the hip in 10.3%, and at the ankle in 29.5% of the limbs. www.pedorthopaedics.com |
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PELVIC ROTATION
HIP ROTATION
48 NORMAL
32 EXTERNAL
25 INTERNAL
70 NORMAL
32 NORMAL
13 EXTERNAL
35 INTERNAL
63 EXTERNAL
Volume 35, Number 6, September 2015
ANKLE ROTATION
18 INTERNAL
98 INTERNAL
23 NORMAL
5 EXTERNAL
7 INTERNAL
3%
10 NORMAL
4.3%
1 EXTERNAL
0.4%
30 INTERNAL
13.0%
13 NORMAL
5.6%
5 EXTERNAL
2.0%
25 INTERNAL
10.8%
6 NORMAL
2.6%
1 EXTERNAL
0.4%
14 INTERNAL
6.0%
10 NORMAL
4.3%
1 EXTERNAL
0.4%
28 INTERNAL
12.0%
3 NORMAL
1.3%
1 EXTERNAL
0.4%
11 INTERNAL
4.8%
1 NORMAL
0.4%
1 EXTERNAL
0.4%
30 INTERNAL
13.0%
5 NORMAL
2.0%
0 EXTERNAL
0%
23 INTERNAL
10.0%
0 NORMAL
0%
0 EXTERNAL
0%
4 INTERNAL
1.7%
1 NORMAL
0.4%
0 EXTERNAL
0%
FIGURE 1. Distribution of torsional anomalies in the 231 lower limbs with internal foot progression angle.
Some cases of external foot progression angle were identified, although rotations at each level were within normal values. This follows the explanation given for internal foot progression angle.
DISCUSSION Prevalence of Transverse Plane Kinematic Deviations Mechanisms and consequences of lower limb rotational deviations on gait in children with cerebral palsy are well known.1,2,8,15,16 As would be expected from
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clinical experience, the current study in a large population of ambulatory children with spastic diplegia found a high prevalence of transverse plane kinematic anomalies. A previous study from Wren et al4 identified 14 specific gait anomalies in children with CP and their respective prevalence. However, these anomalies combined sagittal and transverse plane malalignment and a number of them were influenced by previous surgical procedures. Furthermore, in their study, rotational malalignment was exclusively defined as the association of external foot progression angle and internal hip rotation. Copyright
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J Pediatr Orthop
Volume 35, Number 6, September 2015
PELVIS ROTATION
HIP ROTATION
Lower Limb Torsional Profiles in Spastic Diplegia
ANKLE ROTATION
0 INTERNAL
4 INTERNAL
28 INTERNAL
10 NORMAL
3.0%
2 EXTERNAL
3.0%
3 INTERNAL
4.5%
5 NORMAL
7.5%
2 EXTERNAL
3.0%
5 INTERNAL
14 EXTERNAL
9 NORMAL 0 EXTERNAL 0 INTERNAL
3 INTERNAL
24 NORMAL
11 NORMAL
10 EXTERNAL
6 NORMAL
3 EXTERNAL
0% 0% 3.0%
1 EXTERNAL
1.5%
4 INTERNAL
6%
6 NORMAL
9.0%
1 EXTERNAL
1.5%
7 INTERNAL
10.0%
3 NORMAL
2 INTERNAL
15 EXTERNAL
7.5% 13.5%
2 NORMAL
0 EXTERNAL
6 INTERNAL
0%
2 NORMAL
4.5% 0% 3%
3 NORMAL
4.5%
1 EXTERNAL
1.5%
5 INTERNAL
7.5%
1 NORMAL
1.5%
0 EXTERNAL
0%
2 INTERNAL
3.0%
1 NORMAL
1.5%
0 EXTERNAL
0%
FIGURE 2. Distribution of torsional anomalies in the 67 lower limbs with normal foot progression angle.
The prevalence of kinematic deviations at each lower limb level was also assessed in the current study. As reported by Wren et al,4 internal foot progression angle was the most common pattern that was found. The high prevalence of hip rotation within normal values was consistent with the findings of O’Sullivan et al.7 Their results were higher (60%), influenced as much by the association of different types of CP (hemiplegia and diplegia), as by the large range of age (range, 3 to 50 y), which suggests potential issues regarding the previous surgical status. Pelvic and ankle internal rotational prevalence had not been assessed previously in the literature. O’Sullivan et al17 reported the prevalence of pelvic retraction (external pelvic rotation) to be 30.4% in diplegic children. Their remaining 69.6% were defined as “non-retracted pelvis,” which allowed no distinction between internal and normal pelvic rotation.
Transverse Plane Kinematic Deviations The current study showed a wide variety of lower limb rotational deformities. Much information was colCopyright
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lected (Figs. 1–3). There were different profiles of lower limb torsional associations, but the various patterns failed to suggest a classification scheme similar to that described in the sagittal plane.18,19 Lower limb transverse plane deviations were frequently multilevel with frequent compensatory directions. Therefore, identification of each individual rotational anomaly is essential to rectify foot progression angle and to avoid unsatisfactory results if surgical procedures are considered.20–22 If one rotational anomaly is undetected or not taken into account, a lever arm dysfunction will persist. Abnormal pelvic rotation was associated with abnormal foot progression angle in 68% of the cases. As demonstrate by Kawamura et al9 and Viehweger et al,10 physical examination fails to identify this particular transverse plane deviation. To properly diagnose abnormal pelvic rotation, kinematic data are essential. According to Chung et al, postoperative residual pelvic rotation depended on the extent of preoperative kinematics magnitude. However, the impact of pelvic rotation on the recurrence of lower limb rotational deviations recurrences is not assessed in the litwww.pedorthopaedics.com |
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PELVIC ROTATION
HIP ROTATION
11 NORMAL
10 EXTERNAL
4 INTERNAL
28 NORMAL
17 NORMAL
7 EXTERNAL
5 INTERNAL
22 EXTERNAL
Volume 35, Number 6, September 2015
ANKLE ROTATION
7 INTERNAL
28 INTERNAL
9 NORMAL
8 EXTERNAL
0 INTERNAL
0%
0 NORMAL
0%
7 EXTERNAL
9.0%
0 INTERNAL
0%
4 NORMAL
5.0%
7 EXTERNAL
9%
0 INTERNAL
0%
4 NORMAL
5.0%
6 EXTERNAL
8.0%
0 INTERNAL
0%
2 NORMAL
2.5%
2 EXTERNAL
2.5%
0 INTERNAL
0%
10 NORMAL
13.0%
7 EXTERNAL
9.0%
1 INTERNAL
1.5%
3 NORMAL
4.0%
3 EXTERNAL
4.0%
0 INTERNAL
0%
0 NORMAL
0%
5 EXTERNAL
6.5%
2 INTERNAL
2.5%
3 NORMAL
4%
4 EXTERNAL
5%
1 INTERNAL
1.5%
4 NORMAL
5.0%
3 EXTERNAL
4%
FIGURE 3. Distribution of torsional anomalies in the 78 lower limbs with external foot progression angle.
erature.23 As suggested by Aminian et al, each individual deviation should be taken into account for proper correction.24 This raises the question of the type of surgery to perform in cases of pelvic rotational anomalies. Do procedures at another level correct abnormal pelvic rotation? What about the contralateral side? Further investigation is needed to resolve these questions. The prevalence of hip/pelvis compensatory directions was similar to the results reported by De Luca et al.21–23 In their study, they assumed that external pelvic rotation could be a compensatory mechanism for excessive internal hip rotation, but no proof was reported.25 Pelvic rotation could as well be a primary deformity from the ipsilateral side or the contralateral side, compensated by excessive hip rotation. Ankle rotation anomalies were also extremely frequent and needed to be interpreted cautiously as discussed below. However, almost a quarter of foot
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progression deviations resulted from excessive ankle rotation. Ankle deviation as an isolated cause, allowed a straightforward surgical decision. For the remaining cases therapeutic decision to normalize foot progression angle should take into account overlying rotational anomalies identified by the instrumented gait analysis. The origin of lower limb rotational anomalies could not be determined by the current study. Mechanisms are multiple (including spasticity, contracture, and bone deformities) and their identification is based on clinical and on 3-dimensional gait analysis data (kinetics, dynamic electromyography).
Limitations The first limitation of the study was the use of transverse plane kinematics. Although several authors have emphasized its lack of reliability, neither clinical evaluation nor observational gait analysis are reliable Copyright
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J Pediatr Orthop
Volume 35, Number 6, September 2015
enough to detect these anomalies.10,11,26 To reduce the risk of errors, strict protocols (knee varus-valgus curves), and rigorous physical examination and markers placement performed by the same physician, were used.27,28 Furthermore, overall clinical and instrumented gait analysis data must be considered together. The second limitation to be considered was the use of the Plug-in Gait protocol. The effect of misalignment on knee/ankle joint center estimations, kinematics, and crosstalk have been well documented.28 To improve measures consistency, a modified version of the Plug-in gait model was used. The KAD and MED protocol were used. Thus, shank and thigh rotation offset were calculated by this model, which modified ankle and knee joint centers position in the dynamic trials and improved the consistency. Ankle rotation constituted the amount of anomalies of the tibia and fibula positions and of the hindfoot and forefoot deformities. Results from clinical examination (in static position and during gait) must be conscientiously considered for proper interpretation of the transverse plane kinematic data. However, using the KAD and the MED protocol in the static phase provided a direct measure of the ankle flexion axis and minimized the inherent errors of the nonmodified model. Knee rotation (movement of the tibia relative to the femur) was not assessed in the current study. It is clear that foot progression angle was influenced by tibial torsion and/or intra-articular knee rotation in children with a crouch gait at the midstance phase. Consistent data were not identified to reliably distinguish these 2 possible causes. Furthermore, measures occurred through knee movement, which cannot be calculated with the use of the Euler angles because knee movement combined rotation and translation movements. Improvement in the protocols could be made for a direct measurement of tibial torsion by adding markers on the tibial tuberosity and fibular head but these need to be assessed.29 The third limitation was the inclusion of children with GMFCS III, walking with assistive devices (K-walkers and crutches) during the 3-dimensional gait analysis. Assistive devices influence gait pattern and therefore transverse plane deviations. However, the aim of instrumented gait analysis is to assess functional deviations. Daily life use of assistive devices therefore reflected the functional gait of these children. The current study quantitatively assessed the high prevalence of lower limb rotational anomalies in spastic diplegic children with cerebral palsy and their multilevel localization. It also emphasized the necessity of 3D gait analysis to complete abnormal lower limb rotational analysis. Overall collected data are essential to identify each anomaly and the level where it occurs. Identification of these anomalies is fundamental if a surgical procedure is considered. No rotational deviation must be ignored to diminish the risk of unsatisfactory results. Moreover, few issues remain. The impact and management of excessive pelvic rotation, only assess by instrumented gait analysis, is still unresolved. Further investigation into Copyright
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Lower Limb Torsional Profiles in Spastic Diplegia
the primary deformity between the hip-pelvic complex is needed. REFERENCES 1. Gage JR, Schwartz MH. Pathological gait and lever arm dysfunction. The Treatment of Gait Problems in Cerebral Palsy. London: Mc Keith Press; 2004:99–119. 2. Rethlefsen SA, Kay RM. Transverse plane gait problems in children with cerebral palsy. J Pediatr Orthop. 2013;33:422–430. 3. De Morais Filho MC, Kawamura CM, Andrade PH, et al. Factors associated with pelvic asymmetry in transverse plane during gait in patients with cerebral palsy. J Pediatr Orthop B. 2009;18: 320–324. 4. Wren TAL, Rethlefsen S, Kay RM. Prevalence of specific gait abnormalities in children with cerebral palsy: influence of cerebral palsy subtype, age, and previous surgery. J Pediatr Orthop. 2005;25:79–83. 5. Rethlefsen SA, Healy BS, Wren TAL, et al. Causes of intoeing gait in children with cerebral palsy. J Bone Joint Surg Am. 2006;88: 2175–2180. 6. Gaston MS, Rutz E, Dreher T, et al. Transverse plane rotation of the foot and transverse hip and pelvic kinematics in diplegic cerebral palsy. Gait Posture. 2011;34:218–221. 7. O’Sullivan R, Walsh M, Hewart P, et al. Factors associated with internal hip rotation gait in patients with cerebral palsy. J Pediatr Orthop. 2006;26:537–541. 8. Aktas S, Aiona MD, Orendurff M. Evaluation of rotational gait abnormality in the patients cerebral palsy. J Pediatr Orthop. 2000; 20:217–220. 9. Kawamura CM, de Morais Filho MC, Barreto MM, et al. Comparison between visual and three-dimensional gait analysis in patients with spastic diplegic cerebral palsy. Gait Posture. 2007;25: 18–24. 10. Viehweger E, Zu¨rcher Pfund L, He´lix M, et al. Influence of clinical and gait analysis experience on reliability of observational gait analysis (Edinburgh Gait Score Reliability). Ann Phys Rehabil Med. 2010;53:535–546. 11. McGinley JL, Baker R, Wolfe R, et al. The reliability of threedimensional kinematic gait measurements: a systematic review. Gait Posture. 2009;29:360–369. 12. Song KM, Concha MC, Haideri NF. Effects of lower limb torsion on ankle kinematic data during gait analysis. J Pediatr Orthop. 2001;21:792–797. 13. Davis RB 3rd, Ounpuu S, Tyburski D. A gait data collection and reduction technique. Hum Mov Sci. 1991;10:575–587. 14. Schwartz MH, Trost JP, Wervey RA. Measurement and management of errors in quantitative gait data. Gait Posture. 2004;20: 196–203. 15. Pennec¸ot GF. Analyse des troubles de rotation et recherche de leur origin. [Lower limbe rotational anomalies and causes] French. Marche Pathologique de l’enfant Paralyse´ Ce´re´bral [Pathological gait of children with cerebral palsy]. Sauramps Me´dical; 2009: 117–128. French. 16. Perry J, Burnfield JM. Pathological gait. Gait Analysis Normal and Pathological Function. Thorofare, NJ: SLACK Incorporated; 1992:163–278. 17. O’Sullivan R, Walsh M, Jenkinson A, et al. Factors associated with pelvic retraction during gait in cerebral palsy. Gait Posture. 2007;25:425–431. 18. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;288:139–147. 19. Rodda JM, Graham HK, Carson L, et al. Sagittal gait patterns in spastic diplegia. J Bone Joint Surg Br. 2004;86:251–258. 20. Kim H, Aiona M, Sussman M. Recurrence after femoral derotational osteotomy in cerebral palsy. J Pediatr Orthop. 2005;25: 739–743. 21. Ounpuu S, DeLuca P, Davis R, et al. Long-term effects of femoral derotation osteotomies: an evaluation using three-dimensional gait analysis. J Pediatr Orthop. 2002;22:139–145.
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22. Lofterød B, Terjesen T. Changes in lower limb rotation after soft tissue surgery in spastic diplegia. Acta Orthop. 2010;81: 245–249. 23. Aminian A, Vankoski SJ, Dias L, et al. Spastic hemiplegic cerebral palsy and the femoral derotation osteotomy: effect at the pelvis and hip in the transverse plane during gait. J Pediatr Orthop. 2003;23: 314–320. 24. Chung CY, Lee SH, Choi IH, et al. Residual pelvic rotation after single-event multilevel surgery in spastic hemiplegia. J Bone Joint Surg Br. 2008;90:1234–1238. 25. DeLuca PA. Gait analysis in the treatment of the ambulatory child with cerebral palsy. Clin Orthop Relat Res. 1991;264:65–75.
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26. Toro B, Nester C, Farren P. A review of observational gait assessment in clinical practice. Physiother Theory Pract. 2003;19:137–149. 27. Leardini A, Chiari L, Della Croce U, et al. Human movement analysis using stereo photogrammetry. Part 3. Soft tissue artifact assessment and compensation. Gait Posture. 2005;21:212–225. 28. Della Croce U, Leardini A, Chiari L, et al. Human movement analysis using stereo photogrammetry. Part 4: assessment of anatomical landmark misplacement and its effects on joint kinematics. Gait Posture. 2005;21:226–237. 29. Davids JR, Davis RB. Tibial torsion: significance and measurement. Gait Posture. 2007;26:169–171.
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A Descriptive Study of Lower Limb Torsional Kinematic Profiles in Children With Spastic Diplegia Anne-Laure Simon, MD,* Brice Ilharreborde, MD, PhD,* Fabrice Megrot, PhD,w Cindy Mallet, MD,* Reza Azarpira, MD,z Keyvan Mazda, MD,* Ana Presedo, MD,* and Georges F. Pennec¸ot, MD*
Background: Lower limb rotational anomalies in spastic diplegic children with cerebral palsy (CP) are common and difficult to identify through physical examination alone. The identification and treatment of the overall rotational disorders must be considered to restore physiological lever-arms lengths and leverarms orientation. The aims of the study were to assess the prevalence of lower limb rotational malalignment and to describe the distribution of the different kinematic torsional profiles in children with spastic diplegia. Methods: Instrumented gait analysis data from 188 children with spastic diplegia were retrospectively reviewed. None of the patients had undergone surgery previously or received botulinum toxin treatment within 6 months before the review. Kinematic data, collected at the midstance phase, included: pelvic, hip, and ankle rotation and foot progression angle. Results: The prevalence of kinematic rotational deviations was 98.4%. Sixty-one percent of the children walked with an internal foot progression angle and 21% exhibited external alignment. The pelvis was internally rotated in 41% of the cases and externally in another 27%. Hip rotation was internal in 29% and external in 27% of the cases. Ankle rotation was internal in 55% and external in 16% of the cases. Lower limb rotational anomalies involved more than one level in 77% of the limbs. A kinematic compensatory deviation was identified in at least one level in 48% of the limbs. Conclusions: Kinematic rotational anomalies were identified in nearly all the 188 children in the study. The multilevel involvement of lower limb malalignment was not systematically associated with compensatory mechanisms between the levels. Ankle rotational anomalies were the most frequent cause of lower limb torsional deviations followed by pelvic malalignment. Level of Evidence: Level IV. Key Words: lower limb, transverse plane, kinematics, spastic diplegia, cerebral palsy (J Pediatr Orthop 2015;35:576–582) From the *Pediatric Orthopedics Department, Robert Debre´ Hospital, Paris; wBois-Larris Motion Analysis Laboratory, Centre of Functional Reeducation and Rehabilitation, Lamorlaye, France; and zPediatric Orthopedics Department, Namazi Hospital, Shiraz, Iran. None of the authors received financial support for this study. The authors declare no conflicts of interest. Reprints: Anne-Laure Simon, MD, Pediatric Orthopedics Department, Robert Debre´ Hospital, 48 Bd Serrurier, Paris 75019, France. E-mail: [email protected]. Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved.
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L
ower limb torsional anomalies are common in children with spastic diplegia and usually involve multiple levels (pelvis, hip, and ankle). The influence of torsional malalignment on gait kinetics and kinematics has been well documented. Transverse plane deviations change the orientation and the length of muscular lever-arm, thus contributing to abnormal moments.1,2 Although mechanisms and causes of lower limbs torsional profiles in children with cerebral palsy (CP) are well known, the assessment of kinematic prevalence and the description of lower limb transverse plane deviations in children with spastic diplegia have not been established. Numerous studies investigating rotational malalignment have been reported but studies are variable regarding CP type (data from hemiplegic, diplegic, and quadriplegic patients were analyzed collectively), are usually focused on specific lower limb levels, or take various kinematic plane deviations into considerations.3–7 Given that transverse plane abnormalities are not always recognizable through physical examination (static evaluation), instrumented gait analysis is a prerequisite for proper functional evaluation.8–10 Transverse plane kinematics provide reliable information to analyze the impact of torsional deviations on lower limb alignment and gait patterns.11,12 The aims of the present study were to assess the prevalence of lower limb rotational malalignment and to describe the distribution of the different kinematic torsional profiles in children with spastic diplegia.
METHODS Patients Following institutional review board approval, full 3-dimensional gait analyzes performed between 2007 and 2011 in 188 diplegic children with CP of type II (159/188, 85%) and III (29/188, 15%) according to the Gross Motor Function Classification System (GMFCS) were retrospectively reviewed. The average age of the patients was 11.7 ± 0.2 years (range, 4.25 to 25 y). Inclusion criteria were: a diagnosis of spastic diplegic CP, the ability to walk with or without assistive devices and a full-instrumented gait analysis recorded barefoot. Exclusion criteria were: previous surgical procedures and previous botulinum-toxin injection or cast within the 6 months before performing the instrumented gait analysis. J Pediatr Orthop
Volume 35, Number 6, September 2015
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J Pediatr Orthop
Volume 35, Number 6, September 2015
Gait Analysis Gait analysis data included videotaping, tri-dimensional kinematics and a physical examination. The motion of body segments was recorded in 3 dimensions with an 8-camera VICON MX system (Oxford Metrics Ltd., Oxford, UK) near-infra-red motion analysis system, at a sampling rate of 100 Hz. Fifteen passive reflecting markers were placed on anatomic landmarks, respecting the Helen Hayes protocol. The biomechanical model as described by Davis and Ounpuu (Plug-in Gait) was used in the study.13 To improve the consistency of the measures, the knee and the ankle flexion axis were calculated for each patient during the static phase, to improve the Plug-in Gait model: the Knee Alignment Device (KAD, Motion Labs Systems) was used and a medial ankle marker (MED protocol) was added. Data were filtered using a fourth-order zero-lag Butterworth low-pass-filter, with a 6 Hz cutoff frequency. The Euler angles for the hips, knees, and ankles were calculated. Datasets from multiple trials were collected as the child walked barefoot at a self-selected cadence along a walkway. One representative and regular stride was selected and analyzed by one senior orthopaedic surgeon qualified in instrumented gait analysis after reviewing both videotapes and transverse plane kinematic curves. Kinematic data from 376 lower limbs were collected. The following transverse plane parameters were analyzed: pelvis, hip and ankle kinematics, and foot progression angle. Data were collected at 30% of the gait cycle. All values within more or less 1 SD from the mean were considered normal.14 Accuracy and consistency of data quality were monitored with periodic testing measures of healthy subjects without lower limb torsional deviations. Normal values from the laboratory were 5 to 3 degrees for pelvic rotation, 9 to 4 degrees for hip rotation, 15 to 28 degrees for ankle rotation, and 4 to 15 degrees for foot progression angle. Negative and positive values corresponded respectively to internal and external rotation.
Statistical Analysis All quantitative data were reported as mean ± standard error of the mean (SEM) with reference to angle range of motion from kinematic data. All qualitative data were reported as percent.
RESULTS
Lower Limb Torsional Profiles in Spastic Diplegia
TABLE 1. Distribution of Torsional Anomalies Among the 376 Lower Limbs Foot progression angle Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Pelvis rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Hip rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.) Ankle rotation Percentage Number of LL Mean ± SEM (deg.) Range (deg.)
Internal
Normal
External
61 231 12.1 ± 0.7 [ 52; 3]
18 67 8.4 ± 0.5 [4; 15]
21 78 29.1 ± 1.3 [16; 68]
41 154 14.1 ± 1.3 [ 52; 6]
32 121 1.3 ± 0.22 [9; 4]
27 101 9.6 ± 0.5 [5; 28]
29 107 17.2 ± 0.7 [ 39; 10]
44 166 2.7 ± 0.3 [39; 10]
27 103 12 ± 0.6 [5; 30]
55 205 1.9 ± 0.6 [ 48; 14]
29 111 20.2 ± 0.4 [15; 28]
16 60 40.1 ± 1.4 [29; 74]
LL indicates lower limbs; SEM, standard error of the mean.
Given the wide range of rotational anomalies, data were classified according to the foot progression angle, which is widely considered as the result of overlying rotational anomalies and which can easily be identified on the videotapes.
Internal Foot Progression Angle Lower limbs were internally rotated at all levels in 3% of the children (Fig. 1). The remaining children showed combined anomalies between the levels resulting in an internal foot progression angle. A single level cause of internal foot progression angle was detected in 46.3% of the limbs. The level was identified at the pelvis in 10.8%, at the hip in 6.9%, and at the ankle in 28.6% of the limbs. Some cases of internal foot progression angle were identified even when the rotation of each level was within normal values. These results can be attributed to the fact that each rotation value was at the lower limit of the SD, with an internal foot progression gait pattern at the end.
Global Distribution
Normal Foot Progression Angle
Table 1 summarizes the distribution of torsional anomalies of foot progression angle and pelvic, hip, and ankle rotation. The prevalence of kinematic transverse plane deviation was 98.4%. Internal malalignment was the most frequent pattern for foot progression angle, pelvic, and ankle rotation. Normal alignment was the most frequent pattern for the hip. Lower limb rotational anomalies involved more than one level in 77% of the limbs. A kinematic compensatory deviation was identified in at least one level in 48% of the limbs. Twenty-seven percent of theses kinematic compensatory deviations occurred between the hip and the ipsilateral pelvis.
Nine percent of the lower limbs had no abnormal segmental rotation (Fig. 2). The remaining children had compensatory segmental torsional anomalies resulting in normal foot progression angle.
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External Foot Progression Angle Lower limbs were externally rotated at all levels in 4% of the children (Fig. 3). The remaining children had combined anomalies between the levels resulting in an external foot progression angle. A single level cause of external foot progression angle was detected in 46.2% of the limbs. The level was identified at the pelvis in 6.4%, at the hip in 10.3%, and at the ankle in 29.5% of the limbs. www.pedorthopaedics.com |
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PELVIC ROTATION
HIP ROTATION
48 NORMAL
32 EXTERNAL
25 INTERNAL
70 NORMAL
32 NORMAL
13 EXTERNAL
35 INTERNAL
63 EXTERNAL
Volume 35, Number 6, September 2015
ANKLE ROTATION
18 INTERNAL
98 INTERNAL
23 NORMAL
5 EXTERNAL
7 INTERNAL
3%
10 NORMAL
4.3%
1 EXTERNAL
0.4%
30 INTERNAL
13.0%
13 NORMAL
5.6%
5 EXTERNAL
2.0%
25 INTERNAL
10.8%
6 NORMAL
2.6%
1 EXTERNAL
0.4%
14 INTERNAL
6.0%
10 NORMAL
4.3%
1 EXTERNAL
0.4%
28 INTERNAL
12.0%
3 NORMAL
1.3%
1 EXTERNAL
0.4%
11 INTERNAL
4.8%
1 NORMAL
0.4%
1 EXTERNAL
0.4%
30 INTERNAL
13.0%
5 NORMAL
2.0%
0 EXTERNAL
0%
23 INTERNAL
10.0%
0 NORMAL
0%
0 EXTERNAL
0%
4 INTERNAL
1.7%
1 NORMAL
0.4%
0 EXTERNAL
0%
FIGURE 1. Distribution of torsional anomalies in the 231 lower limbs with internal foot progression angle.
Some cases of external foot progression angle were identified, although rotations at each level were within normal values. This follows the explanation given for internal foot progression angle.
DISCUSSION Prevalence of Transverse Plane Kinematic Deviations Mechanisms and consequences of lower limb rotational deviations on gait in children with cerebral palsy are well known.1,2,8,15,16 As would be expected from
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clinical experience, the current study in a large population of ambulatory children with spastic diplegia found a high prevalence of transverse plane kinematic anomalies. A previous study from Wren et al4 identified 14 specific gait anomalies in children with CP and their respective prevalence. However, these anomalies combined sagittal and transverse plane malalignment and a number of them were influenced by previous surgical procedures. Furthermore, in their study, rotational malalignment was exclusively defined as the association of external foot progression angle and internal hip rotation. Copyright
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J Pediatr Orthop
Volume 35, Number 6, September 2015
PELVIS ROTATION
HIP ROTATION
Lower Limb Torsional Profiles in Spastic Diplegia
ANKLE ROTATION
0 INTERNAL
4 INTERNAL
28 INTERNAL
10 NORMAL
3.0%
2 EXTERNAL
3.0%
3 INTERNAL
4.5%
5 NORMAL
7.5%
2 EXTERNAL
3.0%
5 INTERNAL
14 EXTERNAL
9 NORMAL 0 EXTERNAL 0 INTERNAL
3 INTERNAL
24 NORMAL
11 NORMAL
10 EXTERNAL
6 NORMAL
3 EXTERNAL
0% 0% 3.0%
1 EXTERNAL
1.5%
4 INTERNAL
6%
6 NORMAL
9.0%
1 EXTERNAL
1.5%
7 INTERNAL
10.0%
3 NORMAL
2 INTERNAL
15 EXTERNAL
7.5% 13.5%
2 NORMAL
0 EXTERNAL
6 INTERNAL
0%
2 NORMAL
4.5% 0% 3%
3 NORMAL
4.5%
1 EXTERNAL
1.5%
5 INTERNAL
7.5%
1 NORMAL
1.5%
0 EXTERNAL
0%
2 INTERNAL
3.0%
1 NORMAL
1.5%
0 EXTERNAL
0%
FIGURE 2. Distribution of torsional anomalies in the 67 lower limbs with normal foot progression angle.
The prevalence of kinematic deviations at each lower limb level was also assessed in the current study. As reported by Wren et al,4 internal foot progression angle was the most common pattern that was found. The high prevalence of hip rotation within normal values was consistent with the findings of O’Sullivan et al.7 Their results were higher (60%), influenced as much by the association of different types of CP (hemiplegia and diplegia), as by the large range of age (range, 3 to 50 y), which suggests potential issues regarding the previous surgical status. Pelvic and ankle internal rotational prevalence had not been assessed previously in the literature. O’Sullivan et al17 reported the prevalence of pelvic retraction (external pelvic rotation) to be 30.4% in diplegic children. Their remaining 69.6% were defined as “non-retracted pelvis,” which allowed no distinction between internal and normal pelvic rotation.
Transverse Plane Kinematic Deviations The current study showed a wide variety of lower limb rotational deformities. Much information was colCopyright
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lected (Figs. 1–3). There were different profiles of lower limb torsional associations, but the various patterns failed to suggest a classification scheme similar to that described in the sagittal plane.18,19 Lower limb transverse plane deviations were frequently multilevel with frequent compensatory directions. Therefore, identification of each individual rotational anomaly is essential to rectify foot progression angle and to avoid unsatisfactory results if surgical procedures are considered.20–22 If one rotational anomaly is undetected or not taken into account, a lever arm dysfunction will persist. Abnormal pelvic rotation was associated with abnormal foot progression angle in 68% of the cases. As demonstrate by Kawamura et al9 and Viehweger et al,10 physical examination fails to identify this particular transverse plane deviation. To properly diagnose abnormal pelvic rotation, kinematic data are essential. According to Chung et al, postoperative residual pelvic rotation depended on the extent of preoperative kinematics magnitude. However, the impact of pelvic rotation on the recurrence of lower limb rotational deviations recurrences is not assessed in the litwww.pedorthopaedics.com |
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PELVIC ROTATION
HIP ROTATION
11 NORMAL
10 EXTERNAL
4 INTERNAL
28 NORMAL
17 NORMAL
7 EXTERNAL
5 INTERNAL
22 EXTERNAL
Volume 35, Number 6, September 2015
ANKLE ROTATION
7 INTERNAL
28 INTERNAL
9 NORMAL
8 EXTERNAL
0 INTERNAL
0%
0 NORMAL
0%
7 EXTERNAL
9.0%
0 INTERNAL
0%
4 NORMAL
5.0%
7 EXTERNAL
9%
0 INTERNAL
0%
4 NORMAL
5.0%
6 EXTERNAL
8.0%
0 INTERNAL
0%
2 NORMAL
2.5%
2 EXTERNAL
2.5%
0 INTERNAL
0%
10 NORMAL
13.0%
7 EXTERNAL
9.0%
1 INTERNAL
1.5%
3 NORMAL
4.0%
3 EXTERNAL
4.0%
0 INTERNAL
0%
0 NORMAL
0%
5 EXTERNAL
6.5%
2 INTERNAL
2.5%
3 NORMAL
4%
4 EXTERNAL
5%
1 INTERNAL
1.5%
4 NORMAL
5.0%
3 EXTERNAL
4%
FIGURE 3. Distribution of torsional anomalies in the 78 lower limbs with external foot progression angle.
erature.23 As suggested by Aminian et al, each individual deviation should be taken into account for proper correction.24 This raises the question of the type of surgery to perform in cases of pelvic rotational anomalies. Do procedures at another level correct abnormal pelvic rotation? What about the contralateral side? Further investigation is needed to resolve these questions. The prevalence of hip/pelvis compensatory directions was similar to the results reported by De Luca et al.21–23 In their study, they assumed that external pelvic rotation could be a compensatory mechanism for excessive internal hip rotation, but no proof was reported.25 Pelvic rotation could as well be a primary deformity from the ipsilateral side or the contralateral side, compensated by excessive hip rotation. Ankle rotation anomalies were also extremely frequent and needed to be interpreted cautiously as discussed below. However, almost a quarter of foot
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progression deviations resulted from excessive ankle rotation. Ankle deviation as an isolated cause, allowed a straightforward surgical decision. For the remaining cases therapeutic decision to normalize foot progression angle should take into account overlying rotational anomalies identified by the instrumented gait analysis. The origin of lower limb rotational anomalies could not be determined by the current study. Mechanisms are multiple (including spasticity, contracture, and bone deformities) and their identification is based on clinical and on 3-dimensional gait analysis data (kinetics, dynamic electromyography).
Limitations The first limitation of the study was the use of transverse plane kinematics. Although several authors have emphasized its lack of reliability, neither clinical evaluation nor observational gait analysis are reliable Copyright
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J Pediatr Orthop
Volume 35, Number 6, September 2015
enough to detect these anomalies.10,11,26 To reduce the risk of errors, strict protocols (knee varus-valgus curves), and rigorous physical examination and markers placement performed by the same physician, were used.27,28 Furthermore, overall clinical and instrumented gait analysis data must be considered together. The second limitation to be considered was the use of the Plug-in Gait protocol. The effect of misalignment on knee/ankle joint center estimations, kinematics, and crosstalk have been well documented.28 To improve measures consistency, a modified version of the Plug-in gait model was used. The KAD and MED protocol were used. Thus, shank and thigh rotation offset were calculated by this model, which modified ankle and knee joint centers position in the dynamic trials and improved the consistency. Ankle rotation constituted the amount of anomalies of the tibia and fibula positions and of the hindfoot and forefoot deformities. Results from clinical examination (in static position and during gait) must be conscientiously considered for proper interpretation of the transverse plane kinematic data. However, using the KAD and the MED protocol in the static phase provided a direct measure of the ankle flexion axis and minimized the inherent errors of the nonmodified model. Knee rotation (movement of the tibia relative to the femur) was not assessed in the current study. It is clear that foot progression angle was influenced by tibial torsion and/or intra-articular knee rotation in children with a crouch gait at the midstance phase. Consistent data were not identified to reliably distinguish these 2 possible causes. Furthermore, measures occurred through knee movement, which cannot be calculated with the use of the Euler angles because knee movement combined rotation and translation movements. Improvement in the protocols could be made for a direct measurement of tibial torsion by adding markers on the tibial tuberosity and fibular head but these need to be assessed.29 The third limitation was the inclusion of children with GMFCS III, walking with assistive devices (K-walkers and crutches) during the 3-dimensional gait analysis. Assistive devices influence gait pattern and therefore transverse plane deviations. However, the aim of instrumented gait analysis is to assess functional deviations. Daily life use of assistive devices therefore reflected the functional gait of these children. The current study quantitatively assessed the high prevalence of lower limb rotational anomalies in spastic diplegic children with cerebral palsy and their multilevel localization. It also emphasized the necessity of 3D gait analysis to complete abnormal lower limb rotational analysis. Overall collected data are essential to identify each anomaly and the level where it occurs. Identification of these anomalies is fundamental if a surgical procedure is considered. No rotational deviation must be ignored to diminish the risk of unsatisfactory results. Moreover, few issues remain. The impact and management of excessive pelvic rotation, only assess by instrumented gait analysis, is still unresolved. Further investigation into Copyright
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Lower Limb Torsional Profiles in Spastic Diplegia
the primary deformity between the hip-pelvic complex is needed. REFERENCES 1. Gage JR, Schwartz MH. Pathological gait and lever arm dysfunction. The Treatment of Gait Problems in Cerebral Palsy. London: Mc Keith Press; 2004:99–119. 2. Rethlefsen SA, Kay RM. Transverse plane gait problems in children with cerebral palsy. J Pediatr Orthop. 2013;33:422–430. 3. De Morais Filho MC, Kawamura CM, Andrade PH, et al. Factors associated with pelvic asymmetry in transverse plane during gait in patients with cerebral palsy. J Pediatr Orthop B. 2009;18: 320–324. 4. Wren TAL, Rethlefsen S, Kay RM. Prevalence of specific gait abnormalities in children with cerebral palsy: influence of cerebral palsy subtype, age, and previous surgery. J Pediatr Orthop. 2005;25:79–83. 5. Rethlefsen SA, Healy BS, Wren TAL, et al. Causes of intoeing gait in children with cerebral palsy. J Bone Joint Surg Am. 2006;88: 2175–2180. 6. Gaston MS, Rutz E, Dreher T, et al. Transverse plane rotation of the foot and transverse hip and pelvic kinematics in diplegic cerebral palsy. Gait Posture. 2011;34:218–221. 7. O’Sullivan R, Walsh M, Hewart P, et al. Factors associated with internal hip rotation gait in patients with cerebral palsy. J Pediatr Orthop. 2006;26:537–541. 8. Aktas S, Aiona MD, Orendurff M. Evaluation of rotational gait abnormality in the patients cerebral palsy. J Pediatr Orthop. 2000; 20:217–220. 9. Kawamura CM, de Morais Filho MC, Barreto MM, et al. Comparison between visual and three-dimensional gait analysis in patients with spastic diplegic cerebral palsy. Gait Posture. 2007;25: 18–24. 10. Viehweger E, Zu¨rcher Pfund L, He´lix M, et al. Influence of clinical and gait analysis experience on reliability of observational gait analysis (Edinburgh Gait Score Reliability). Ann Phys Rehabil Med. 2010;53:535–546. 11. McGinley JL, Baker R, Wolfe R, et al. The reliability of threedimensional kinematic gait measurements: a systematic review. Gait Posture. 2009;29:360–369. 12. Song KM, Concha MC, Haideri NF. Effects of lower limb torsion on ankle kinematic data during gait analysis. J Pediatr Orthop. 2001;21:792–797. 13. Davis RB 3rd, Ounpuu S, Tyburski D. A gait data collection and reduction technique. Hum Mov Sci. 1991;10:575–587. 14. Schwartz MH, Trost JP, Wervey RA. Measurement and management of errors in quantitative gait data. Gait Posture. 2004;20: 196–203. 15. Pennec¸ot GF. Analyse des troubles de rotation et recherche de leur origin. [Lower limbe rotational anomalies and causes] French. Marche Pathologique de l’enfant Paralyse´ Ce´re´bral [Pathological gait of children with cerebral palsy]. Sauramps Me´dical; 2009: 117–128. French. 16. Perry J, Burnfield JM. Pathological gait. Gait Analysis Normal and Pathological Function. Thorofare, NJ: SLACK Incorporated; 1992:163–278. 17. O’Sullivan R, Walsh M, Jenkinson A, et al. Factors associated with pelvic retraction during gait in cerebral palsy. Gait Posture. 2007;25:425–431. 18. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;288:139–147. 19. Rodda JM, Graham HK, Carson L, et al. Sagittal gait patterns in spastic diplegia. J Bone Joint Surg Br. 2004;86:251–258. 20. Kim H, Aiona M, Sussman M. Recurrence after femoral derotational osteotomy in cerebral palsy. J Pediatr Orthop. 2005;25: 739–743. 21. Ounpuu S, DeLuca P, Davis R, et al. Long-term effects of femoral derotation osteotomies: an evaluation using three-dimensional gait analysis. J Pediatr Orthop. 2002;22:139–145.
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22. Lofterød B, Terjesen T. Changes in lower limb rotation after soft tissue surgery in spastic diplegia. Acta Orthop. 2010;81: 245–249. 23. Aminian A, Vankoski SJ, Dias L, et al. Spastic hemiplegic cerebral palsy and the femoral derotation osteotomy: effect at the pelvis and hip in the transverse plane during gait. J Pediatr Orthop. 2003;23: 314–320. 24. Chung CY, Lee SH, Choi IH, et al. Residual pelvic rotation after single-event multilevel surgery in spastic hemiplegia. J Bone Joint Surg Br. 2008;90:1234–1238. 25. DeLuca PA. Gait analysis in the treatment of the ambulatory child with cerebral palsy. Clin Orthop Relat Res. 1991;264:65–75.
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26. Toro B, Nester C, Farren P. A review of observational gait assessment in clinical practice. Physiother Theory Pract. 2003;19:137–149. 27. Leardini A, Chiari L, Della Croce U, et al. Human movement analysis using stereo photogrammetry. Part 3. Soft tissue artifact assessment and compensation. Gait Posture. 2005;21:212–225. 28. Della Croce U, Leardini A, Chiari L, et al. Human movement analysis using stereo photogrammetry. Part 4: assessment of anatomical landmark misplacement and its effects on joint kinematics. Gait Posture. 2005;21:226–237. 29. Davids JR, Davis RB. Tibial torsion: significance and measurement. Gait Posture. 2007;26:169–171.
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