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Dynamic spasticity determines hamstring length and knee flexion angle during gait in children with spastic cerebral palsy
Gait & Posture 64 (2018) 255–259
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Dynamic spasticity determines hamstring length and knee flexion angle during gait in children with spastic cerebral palsy Ja Young Choia, Eun Sook Parkb, Dongho Parkb, Dong-wook Rhab, a b
T
⁎
Department of Physical Medicine & Rehabilitation, Eulji University Hospital, Eulji University College of Medicine, Daejeon, Republic of Korea Department of Rehabilitation Medicine, Severance Hospital, Research Institute of Rehabilitation Medicine, Yonsei University College of Medicine, Seoul, Republic of Korea
A R T I C LE I N FO
A B S T R A C T
Keywords: Cerebral palsy Spasticity Tardieu scale Knee angle Muscle length
Background: Previous researchers reported that popliteal angle did not correlate well with knee angle during gait in individuals with spastic cerebral palsy (CP). Research question: To determine if hamstring spasticity, as measured by Modified Tardieu Scale (MTS) at rest, is associated with knee flexion angle at initial contact and midstance during gait. Methods: Thirty ambulatory children (mean age 8.7 ± 2.4 years) diagnosed with spastic CP participated. The hamstrings’ spasticity was assessed in the supine position with the MTS, measuring R1 (muscle reaction to passive fast stretch), R2 (passive range of motion), and R2-R1 (dynamic component of spasticity). We conducted 3-dimensional computerized gait analysis and calculated semimembranosus muscle-tendon length and lengthening velocity during gait using musculoskeletal modeling and inverse kinematic analysis by OpenSim. Pearson correlation coefficients were calculated to estimate the association of MTS with biomechanical parameters during gait. Results: Knee flexion angle at initial contact and maximal knee extension angle during stance phase significantly positively correlated with both R1 and ㅣR2 - R1ㅣ of MTS, but not with R2 angle. The length of semimembranosus at initial contact, end of swing, and minimal length during stance phase were strongly negatively associated with R1, rather than R2 or ㅣR2 - R1ㅣ angles. Significance: The R1 angle of MTS (muscle reaction to passive fast stretch) is more relevant correlate of knee flexion angle during gait than the R2 (passive range of motion).
1. Introduction Flexed knee gait is one of the most common gait abnormalities in children with cerebral palsy (CP) and its frequency occurs as age increases [1]. The etiology of flexed knee gait is multi-factorial, short and spastic hamstrings are considered to be the main cause of this gait abnormality [2]. Although many authors have reported that hamstring lengthening is an effective treatment for improving flexed knee gait [3,4], some previous studies have shown that hamstring lengths are not actually shorter than usual in CP patients with flexed knee gait [5,6]. Measurement of the popliteal angle is a widely used clinical means of assessing hamstring length in the supine position. However, the popliteal angle did not correlate well with the knee angle during gait in individuals with CP in several previous studies [5,7–9]. Assessment of the popliteal angle is a static measurement in the supine position only; therefore, it could be difficult to reflect the dynamic range of the knee
angle and hamstring length during gait. The medial hamstring muscle is a biarticulate muscle that acts as both a hip extensor and a knee flexor, and so it has a tremendous effect on the complex interaction of hip and knee joints during gait. Spasticity is commonly defined as a velocity dependent increase in tonic stretch reflexes due to hyper‐excitability [10], while stiffness is a mechanical resistance of the myotendinous tissue, as it is passively lengthened. The Modified Tardieu Scale (MTS) is a clinical tool for assessing spasticity that includes quantitative measurement [11]. Passive movements of MTS are tested at two speeds: as slow as possible (R2), and as fast as possible (R1). As for knee flexor muscle, the R2 angle of MTS is equal to the popliteal angle. Although several studies have investigated the correlation between popliteal angle and kinematic parameter of the knee joint during gait [5,7], there is a lack of research on the relationship between dynamic assessment of spasticity using MTS and gait analysis parameters.
Abbreviations: CP, cerebral palsy; MTS, modified Tardieu scale; ROM, range of motion; 3D, 3-dimensional ⁎ Corresponding author at: Department of Rehabilitation Medicine, Severance Hospital, Research Institute of Rehabilitation Medicine, Yonsei University College of Medicine, 50 Yonseiro, Seodaemun-gu, Seoul, 03722, Republic of Korea. E-mail address: [email protected] (D.-w. Rha). https://doi.org/10.1016/j.gaitpost.2018.06.163 Received 6 April 2018; Received in revised form 1 June 2018; Accepted 24 June 2018 0966-6362/ © 2018 Elsevier B.V. All rights reserved.
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2.2.3. Muscle-tendon length We determined the muscle-tendon lengths and velocities of the semimembranosus for each subject. The muscle-tendon length was estimated using a 3D computer model of the lower extremity (Lower Limb Extremity Model 2010) [12]. We conducted inverse kinematic analysis of motion capture data with this model using OpenSim, an open source biomechanics simulation application [13]. In order to measure the changes of muscle-tendon length during gait, we used the least-squares formulation [14] to compute a set of desired joint angles for tracking based on the marker trajectories from the gait analysis. We normalized the muscle-tendon lengths based on the lengths when the hip and knee were in the anatomic position, with all joint angles set at zero [6]. We averaged data for three steps from a multi-step trial to analyze the muscle-tendon length. We estimated muscle–tendon lengthening velocity by computing the numerical derivative of the muscle–tendon length data with respect to time. We analyzed peak lengthening velocity during mid to end swing.
Therefore, the aim of this study was to investigate whether the use of the MTS in children with CP to determine both dynamic spasticity and mechanical resistance of hamstring muscles is associated with hamstring length and knee flexion angle during gait. 2. Methods This was a retrospective study conducted in a university-affiliated, tertiary-care teaching hospital. Ethical approval was granted by the institutional review board and ethics committee of our hospital (42014-0516). 2.1. Participants For this study, the medical records of children with CP, who were referred to our motion analysis laboratory between December 2012 and November 2014, were retrospectively reviewed. Inclusion criteria were as follows: (1) able to walk independently without assistance (Gross Motor Function Classification System [GMFCS] level I-II), (2) Modified Ashworth Scale (MAS) at knee flexors ≥ 1+ with R2 − R1 angle of MTS > 15 °, and (3) age 5–15 years. Exclusion criteria were as follows: (1) chemodenervation therapy within the past 6 months, (2) previous selective rhizotomy, intrathecal baclofen pump and orthopedic surgery, (3) previous history of peripheral neuropathy or myopathy. In the case of bilateral CP, we selected the more affected limb based on the MTS score. Accordingly, we analyzed 30 limbs of 30 children with CP in this study.
2.3. Statistical analysis Statistical analysis was performed using the Statistical Package for the Social Sciences for Windows (SPSS version 23.0, IBM SPSS Incorporated, Chicago, IL, USA). Descriptive statistics, such as mean and standard deviation (SD), were used to summarize patient demographics. Pearson correlation coefficients for parametric data and Spearman’s rank correlation coefficients for nonparametric data were computed to estimate the association of MTS with biomechanical parameters. The level of significance was set to p-value < 0.05.
2.2. Assessments
3. Results
2.2.1. Clinical measures of hamstring spasticity The muscle tone of the hamstring was assessed with the MTS [11]. During the MTS, children were asked to relax in the supine position, with the hip joint of the contralateral leg in a flexed position to eliminate residual anterior pelvic tilt [12,13]. The study leg was positioned to 90-degree hip flexion with full-degree knee flexion. Then, the knee was passively extended twice: the first time very slowly (> 5 s for the entire range of motion), and the second time as fast as possible (< 1 s). Two levels of the popliteal angle were measured by manual goniometry referring to R2 and R1 angles, respectively. All clinical measures were routinely recorded as part of the gait analysis by two experienced physiatrists. The angle of muscle reaction (R1) referred to the point in the range of motion (ROM) where a catch was first felt during a quick, passive extension of the knee joint. By contrast, full range of motion (R2) referred to the popliteal angle measured at the end of the movement. The absolute difference between the two angles ( R2 − R1 ) represented the dynamic components of spasticity [11]. Therefore, R2 represented only the mechanical resistance of hamstrings, whereas R1 was the summation of both mechanical resistance and the dynamic spasticity of hamstrings.
In total, 30 ambulatory children with spastic cerebral palsy (18 unilateral and 12 bilateral; 16 boys and 14 girls), aged from 5 to 15 years (mean age of the children was 8.7 ± 2.4 years), whose GMFCS level was I or II (GMFCS level I/II: 19/11) participated in this study. The characteristics of the subjects are described in Table 1. 3.1. Correlation between MTS and the kinematic data during gait Positive values of kinematic data indicate pelvic anterior tilt and knee flexion, while negative values indicate pelvic posterior tilt and knee extension. Table 2 shows the correlation coefficients between the MTS and the sagittal knee angle on gait analysis. The absolute value of R2 - R1 (ㅣR2 - R1ㅣ) of MTS moderately positively correlated with the knee angle at initial contact (r = 0.482; p < 0.01), and knee angle at end swing (r = 0.543; p < 0.01), and weakly correlated with maximal knee extension during stance phase (rs = 0.387; p < 0.05). R1 of MTS also showed a moderate positive correlation with the knee angle at initial contact (r = 0.490; p < 0.01) and end swing (r = 0.582; Table 1 Participant characteristics.
2.2.2. Gait kinematics Gait analysis was performed using a computerized 3D motion analysis (VICON MX-T10 Motion Analysis System, Oxford Metrics Inc., Oxford, UK) to measure kinematic data during the gait cycle. Subjects were instrumented with 16 passive reflective markers according to Helen Hayes marker set. Six digital videos were recorded simultaneously, from each video on the front and rear, and four videos on the side, while the child walked barefoot on an 8 m pathway. Data from three trials at a self-selected walking speed were collected for each subject at a sampling rate of 100 Hz. We captured all data based on the VICON Plug-in-Gait model; then we used NEXUS software version 1.8.5 to calculate joint kinematics, based on an average of three representative trials.
Characteristic
No./Valuea
No. of participants No. of legs Most affected side, right/left Gender, male/female Age at gait analysis, years GMFCS level, I / II Type of cerebral palsy, unilateral/ bilateral Modified Tardieu scale of knee flexor R1 angle, degrees R2 angle, degrees ㅣR2 - R1ㅣangle, degrees
30 30 11 / 19 16 / 14 8.7 ± 2.4 (5–15) 19 / 11 18 / 12
GMFCS: Gross motor functional classification system. a Values are mean ± standard deviation (range). 256
65.00 ± 20.55 (20–110) 36.83 ± 13.68 (5–60) 28.17 ± 12.21 (15–70)
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Table 2 correlation coefficients between knee flexor Modified Tardieu Scale and kinematic data of sagittal plane. Knee angle Parameters
R1 of MTS Correlation p-value R2 of MTS Correlation p-value ㅣR2 - R1ㅣ of MTS Correlation p-value
Pelvis angle
Initial contact
Max Ext stance
Max Fl swing
End swing
Anterior tilting at initial contact
Maximal anterior tilting
Anterior tilting at End swing
.490b .006
.387a .034
.069 .719
.582b .001
−.282 .131
−.175 .354
−.311 .094
.306 .100
.160 .398
.073 .703
.390a .033
−.054 .778
−.007 .972
−.104 .584
.482b .007
.387c .035
.034 .858
.543b .002
−.415a .023
−.288 .123
−.408a .025
MTS, modified Tardieu scale; Max, maximal; Ext, extension; Fl, flexion. Positive values of kinematic data indicate pelvic anterior tilt and knee flexion, while negative values indicate pelvic posterior tilt and knee extension. a Correlation is significant at the 0.05 level by Pearson’s correlation coefficient. b Correlation is significant at the 0.01 level by Pearson’s correlation coefficient. c Correlation is significant at the 0.05 level by Spearman’s rank correlation coefficient.
= -0.443; p < 0.05), while R2 showed only a weak negative correlation at end swing (r = −0.386; p < 0.05). By contrast, ㅣR2 - R1ㅣ of MTS demonstrated a moderate negative correlation with the semimembranosus muscle length at only minimal stance phase (r = -0.430; p < 0.05). In addition, the lengthening velocity of semimembranosus during the swing phase did not significantly correlate with the MTS of the hamstring.
p < 0.01), and a weak positive correlation with maximal knee extension during stance phase (r = 0.387; p < 0.05). R2 only weakly positively correlated with the knee flexion angle at end swing (r = 0.390; p < 0.05). Maximal knee flexion angle during the swing phase did not correlate with MTS. For pelvic kinematics, ㅣR2 - R1ㅣ negatively correlated with the pelvic anterior tilting at initial contact (r = -0.415; p < 0.05) and end swing (r = −0.408; p < 0.05). This result indicates that a higher dynamic spasticity of hamstring was related to more posterior pelvic tilt (Table 2). A scatterplot showing the significant relationship between the R1 of MTS and the knee angle at initial contact with a regression line is shown in Fig. 1.
4. Discussion This study demonstrated that the R1 or R2 - R1 of the hamstring MTS, which represent the dynamic component of spasticity, significantly correlated with knee angle and hamstring length during gait, unlike the R2, which represents the passive range of motion at the knee joint. We tested the MTS of the hamstring with the hip in the 90-degree flexed position, placing the hamstrings at their maximal stretch across the hip and knee [15]. The spasticity is activated when the muscle is stretched to the R1 position; and then the viscoelasticity of the soft tissues and joints and the component of contracture may have come into play until the muscle is stretched to the R2 position [16]. Thus, the
3.2. Correlation between MTS and the muscle-tendon length during gait As for semimembranosus, R1 had the highest correlation with muscle length, compared to R2 or R2 - R1 (Table 3). R1 of MTS showed a moderate negative correlation with the muscle length of semimembranosus at initial contact (r = -0.405; p < 0.05) (Fig. 1), and minimal length during stance phase (r = −0.494; p < 0.05) and end swing (r
Fig. 1. Correlation between the R1 angle of the Modified Tardieu Scale and the knee flexion angle (A) and semimembranosus length (B) at initial contact. Knee flexion angle and semimembranosus length at initial contact were significantly correlated with the R1 angle. 257
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gait than static contracture. The hamstring is a biarticular muscle that affect both the knee and hip joints. In addition, the hip angle itself can have important modulating effects on hamstring stretch reflexes [22]. Therefore, we assessed the pelvic angle during gait and only the absolute value of R2 R1 negatively correlated with the pelvic angle in the sagittal pelvic kinematic analysis, meaning the dynamic spasticity of hamstrings promoted posterior pelvic tilting, especially at initial contact and end swing.
Table 3 correlation coefficients between knee flexor Modified Tardieu Scale and the length of semimembranosus. Semimembranosus length Parameters
R1 of MTS Correlation p-value R2 of MTS Correlation p-value ㅣR2 - R1ㅣ of MTS Correlation p-value
Initial contact
Min stance
End swing
Lengthening velocity during end swing
−.405a .026
−.494b .006
−.443a .014
−.060 .753
−.340 .066
−.358 .052
−.386a .035
.041 .830
−.178 .346
−.430a .018
−.178 .348
−.190 .315
4.2. Correlation between MTS and the muscle-tendon length during gait In the muscle-tendon length study, the R1 angle of MTS showed a moderate negative correlation with semimembranosus length at both the stance and swing phase. This means that muscle reaction to exaggerated stretch reflexes is associated with a short hamstring length during gait. In contrast, the popliteal angle, R2 of MTS, only weakly correlated with semimembranosus length, and only at the end swing. There is a paucity of studies on the correlation between popliteal angle and hamstring length during gait. Delp et al. [5] concluded that the popliteal angle was not a valid indicator of maximum hamstring length during the gait cycle, whereas Thompson et al. [7] showed that the popliteal angle significantly correlated with maximal hamstring length during gait, but only when performed by the most reliable examiner and when using a modified method. In their study, the modified popliteal angle of > 40° used by the most reliable examiner may indicate that the medial hamstrings are short. Our study is different because: (1) the sample size was more than two times greater; (2) we used the modified method assessing the popliteal angle by a reliable examiner. In the modified method, the contralateral hip is flexed to eliminate anterior pelvic tilt caused by hip flexor tightness [7]. Although the modified method of measuring the popliteal angle is the more reliable technique to reflect hamstring length, most previous studies used the conventional method to measure the popliteal angle, with the contralateral hip in a neutral position [9] or not mentioned at all [8,17]. The hamstring muscle is stretched to its maximal length at initial contact and the terminal swing phase. This may be the reason that the popliteal angle showed a weak correlation with hamstring length at only the end swing in our study. During the swing phase of normal gait, the hamstring muscles are rapidly stretched, through the combined action of knee extension and hip flexion. Hamstring muscles were reported to lengthen slowly in the second half of the swing phase in the children with CP, and it may be caused by their shortening or spasticity [23]. However, in our study there was no significant correlation between MTS and the peak lengthening velocity of semimembranosus during the swing phase. This means that the lengthening velocity is related not only to dynamic spasticity and muscle contracture, but also to other factors, including co-contraction or selective motor control. Selective motor control is required, especially during the terminal swing, when the combination of hip flexion and knee extension motion is needed [24]. Impaired selective motor control was reported to influence knee position at initial contact, which is associated with decreased knee extension during the swing phase [25]. Additionally, the popliteal angle did not show a significant correlation with hamstring length during the stance phase in our study. Hoffinger et al. [6] found that the hamstring lengths during the stance phase in most patients with crouch gait were longer than the resting length and that hamstrings functioned as hip extensors during a significant portion of the stance phase. This issue of the impact of hamstring lengthening on knee flexion during stance is very much debated [3,4]. Previous studies show that many children with flexed knee gait do not have shortened hamstrings, and our study findings also support this statement [5]. This study indicates that a neural component of spasticity, other than static shortening or contracture, plays critical role in knee angle and hamstring length during the gait. In the same context, a child with
MTS, modified Tardieu scale. Min stance, minimal length during stance. a Correlation is significant at the 0.05 level by Pearson’s correlation coefficient. b Correlation is significant at the 0.01 level by Pearson’s correlation coefficient.
R2 - R1 represents the dynamic spasticity and R1 represents the summation of both mechanical resistance and the dynamic spasticity of hamstrings. 4.1. Correlation between MTS and the kinematic data during gait This study found no significant correlation between the popliteal angle and the knee flexion angle during stance phase, and only a weak correlation was noted at the end swing. Although most previous studies showed no significant correlation between the popliteal angle and the knee angle during the gait cycle [8,9], some studies still suggest that such a relationship does exist. Desloovere et al. [17] showed a negative correlation between the popliteal angle and maximal knee extension in the stance phase, but the correlation was weak (r = -0.28, P < 0.01). Faber et al. [18], by contrast, showed that the popliteal angle (R2), not the stretch restricted angle (R1), was strongly associated with the maximum knee extension at the end swing, suggesting that mechanical resistance of the hamstrings is more important for knee angle during gait. This result partly agreed with our finding of a weak correlation between the popliteal angle (R2) and the knee flexion angle only at end swing phase. However, R1 and R2 - R1 showed a higher correlation with knee flexion angles during the gait than R2 did in our study. Previous studies measured clinical parameters similar to R1, named “initial” or “first” popliteal angle [9,19]. These terms were defined as the muscle reaction during stretch; however, the stretch velocity was not as fast as the R1 we measured in this study. McMulkin et al. [9] investigated the correlation between initial and final popliteal angles and knee flexion angle in the stance phase, revealing a Pearson’s correlation coefficient of −0.49. Whereas Cooney et al. [19] declared the initial popliteal angle was significantly correlated with knee extension at the terminal swing. The Cooney et al. study partially supports our findings, although the first resistance point in their study was not equal to the R1 of MTS in our study. Spastic hamstrings have been found to have lower activation thresholds during passive stretch [20]. Perry and Newsam [21] showed that patients with a flexed knee gait exhibit premature firing of the hamstrings during the swing phase. This premature activation of the hamstring is related to R1 of the MTS and is a dynamic component of spasticity. Reduced knee extension at the terminal swing might be explained by a premature onset of the hamstring activity due to exaggerated stretch reflexes. This study is the first to report the significant correlation of R2 - R1, a dynamic component of MTS, with the knee flexion angle. Our study revealed that dynamic spasticity had a stronger correlation with knee kinematics during the 258
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a dynamic but not yet static hamstring contracture may be better treated with chemodenervation, including botulinum toxin or intrathecal baclofen, rather than orthopedic surgery, to improve knee extension at the end swing and the concatenate initial contact [26]. We need further studies with more subjects to confirm the effects of hamstring muscle botulinum toxin injection on gait functions of children with spastic CP.
[4] P.A. DeLuca, S. Ounpuu, R.B. Davis, J.H. Walsh, Effect of hamstring and psoas lengthening on pelvic tilt in patients with spastic diplegic cerebral palsy, J. Pediatr. Orthop. 18 (6) (1998) 712–718. [5] S.L. Delp, A.S. Arnold, R.A. Speers, C.A. Moore, Hamstrings and psoas lengths during normal and crouch gait: implications for muscle-tendon surgery, J. Orthop. Res. 14 (1) (1996) 144–151. [6] S.A. Hoffinger, G.T. Rab, H. Abou-Ghaida, Hamstrings in cerebral palsy crouch gait, J. Pediatr. Orthop. 13 (6) (1993) 722–726. [7] N.S. Thompson, R.J. Baker, A.P. Cosgrove, J.L. Saunders, T.C. Taylor, Relevance of the popliteal angle to hamstring length in cerebral palsy crouch gait, J. Pediatr. Orthop. 21 (3) (2001) 383–387. [8] M.S. Orendurff, J.S. Chung, R.A. Pierce, Limits to passive range of joint motion and the effect on crouch gait in children with cerebral palsy, Gait Posture 7 (2) (1998) 165. [9] M.L. McMulkin, J.J. Gulliford, R.V. Williamson, R.L. Ferguson, Correlation of static to dynamic measures of lower extremity range of motion in cerebral palsy and control populations, J. Pediatr. Orthop. 20 (3) (2000) 366–369. [10] J.W. Lance, The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture, Neurology 30 (12) (1980) 1303–1313. [11] R.N. Boyd, H.K. Graham, Objective measurement of clinical findings in the use of botulinum toxin type a for the management of children with cerebral palsy, Eur. J. Neurol. 6 (S4) (1999) s23–s35. [12] E.M. Arnold, S.R. Ward, R.L. Lieber, S.L. Delp, A model of the lower limb for analysis of human movement, Ann. Biomed. Eng. 38 (2) (2010) 269–279. [13] S.L. Delp, F.C. Anderson, A.S. Arnold, P. Loan, A. Habib, C.T. John, et al., OpenSim: open-source software to create and analyze dynamic simulations of movement, IEEE Trans. Biomed. Eng. 54 (11) (2007) 1940–1950. [14] T.W. Lu, J.J. O’Connor, Bone position estimation from skin marker co-ordinates using global optimisation with joint constraints, J. Biomech. 32 (2) (1999) 129–134. [15] J.L. Young, J. Rodda, P. Selber, E. Rutz, H.K. Graham, Management of the knee in spastic diplegia: what is the dose? Orthop. Clin. North. Am. 41 (4) (2010) 561–577. [16] W.K. Yam, M.S. Leung, Interrater reliability of modified ashworth scale and modified tardieu scale in children with spastic cerebral palsy, J. Child Neurol. 21 (12) (2006) 1031–1035. [17] K. Desloovere, G. Molenaers, H. Feys, C. Huenaerts, B. Callewaert, P. Van de Walle, Do dynamic and static clinical measurements correlate with gait analysis parameters in children with cerebral palsy? Gait Posture 24 (3) (2006) 302–313. [18] I.R. Faber, B. Nienhuis, N.P. Rijs, A.C. Geurts, J. Duysens, Is the modified tardieu scale in semi-standing position better associated with knee extension and hamstring activity in terminal swing than the supine Tardieu? Dev. Med. Child Neurol. 50 (5) (2008) 382–387. [19] K.M. Cooney, J.O. Sanders, M.C. Concha, F.L. Buczek, Novel biomechanics demonstrate gait dysfunction due to hamstring tightness, Clin. Biomech. (Bristol, Avon) 21 (1) (2006) 59–66. [20] L. Bar-On, E. Aertbelien, G. Molenaers, K. Desloovere, Muscle activation patterns when passively stretching spastic lower limb muscles of children with cerebral palsy, PLoS One 9 (3) (2014) e91759. [21] J. Perry, C. Newsam, Function of the hamstrings in cerebral palsy, in: Sussman (Ed.), The Diplegic Child: Evaluation and Management, American Academy of Orthopaedic Surgeons, Rosemont, IL, 1992, pp. 299–307. [22] J.J. Visser, J.E. Hoogkamer, M.F. Bobbert, P.A. Huijing, Length and moment arm of human leg muscles as a function of knee and hip-joint angles, Eur. J. Appl. Physiol. Occup. Physiol. 61 (5-6) (1990) 453–4560. [23] P. Crenna, Spasticity and ‘spastic’ gait in children with cerebral palsy, Neurosci. Biobehav. Rev. 22 (4) (1998) 571–578. [24] E.G. Fowler, E.J. Goldberg, The effect of lower extremity selective voluntary motor control on interjoint coordination during gait in children with spastic diplegic cerebral palsy, Gait Posture 29 (1) (2009) 102–107. [25] D.W. Rha, K. Cahill-Rowley, J. Young, L. Torburn, K. Stephenson, J. Rose, Biomechanical and clinical correlates of stance-phase knee flexion in persons with spastic cerebral palsy, PMR (2015), http://dx.doi.org/10.1016/j.pmrj.2015.06.003. [26] D.L. Damiano, Rehabilitative therapies in cerebral palsy: the good, the not as good, and the possible, J. Child Neurol. 24 (9) (2009) 1200–1204. [27] J.M. Gracies, K. Burke, N.J. Clegg, R. Browne, C. Rushing, D. Fehlings, et al., Reliability of the Tardieu Scale for assessing spasticity in children with cerebral palsy, Arch. Phys. Med. Rehabil. 91 (3) (2010) 421–428. [28] L. Bar-On, E. Aertbelien, H. Wambacq, D. Severijns, K. Lambrecht, B. Dan, et al., A clinical measurement to quantify spasticity in children with cerebral palsy by integration of multidimensional signals, Gait Posture 38 (1) (2013) 141–147.
4.3. Limitations There are several limitations of this study. First, some children with CP have bone deformities, but the musculoskeletal model used to estimate the hamstring lengths in this study didn’t consider the effects of variable bone deformities in each child on alteration of moment arm and length of hamstring muscle. Future studies should develop the musculoskeletal model to reflect these skeletal deformities. Another limitation of our study is the standardization of the MTS. Although reliable hamstring MTS in children with CP have been reported [27], it can be difficult to determine the accurate angle of catch in R1 measurements. Recently, instrumented clinical tests have been developed to analyze biomechanical and electrophysiological muscle responses during passive stretch [28]. However, our study is meaningful to the clinician in an office setting who wishes to estimate the biomechanical changes during gait based on the more feasible grading of MTS. 5. Conclusion The popliteal angle (R2 of MTS) did not significantly correlate with the knee flexion angle or with hamstring length during stance phase, and only weakly correlated at the end swing. By contrast, the muscle reaction angle to exaggerated stretch reflexes (R1 of MTS) is a more relevant parameter with the knee flexion angle during gait than passive ROM of R2. In addition, the dynamic component of spasticity (R2 - R1) is associated with the knee flexion and pelvic tilting angles during gait. Conflict of interest The authors declare no conflict of interest. Acknowledgements This study was supported by a faculty research grant of Yonsei University College of Medicine for 2014 (6-2014-0065). References [1] G.E. Rose, K.A. Lightbody, R.G. Ferguson, J.C. Walsh, J.E. Robb, Natural history of flexed knee gait in diplegic cerebral palsy evaluated by gait analysis in children who have not had surgery, Gait Posture 31 (3) (2010) 351–354. [2] S.H. Dhawlikar, L. Root, R.L. Mann, Distal lengthening of the hamstrings in patients who have cerebral palsy. Long-term retrospective analysis, J. Bone Jt. Surg. Am. 74 (9) (1992) 1385–1391. [3] W.N. Chang, A.I. Tsirikos, F. Miller, N. Lennon, J. Schuyler, L. Kerstetter, et al., Distal hamstring lengthening in ambulatory children with cerebral palsy: primary versus revision procedures, Gait Posture 19 (3) (2004) 298–304.
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Full length article
Dynamic spasticity determines hamstring length and knee flexion angle during gait in children with spastic cerebral palsy Ja Young Choia, Eun Sook Parkb, Dongho Parkb, Dong-wook Rhab, a b
T
⁎
Department of Physical Medicine & Rehabilitation, Eulji University Hospital, Eulji University College of Medicine, Daejeon, Republic of Korea Department of Rehabilitation Medicine, Severance Hospital, Research Institute of Rehabilitation Medicine, Yonsei University College of Medicine, Seoul, Republic of Korea
A R T I C LE I N FO
A B S T R A C T
Keywords: Cerebral palsy Spasticity Tardieu scale Knee angle Muscle length
Background: Previous researchers reported that popliteal angle did not correlate well with knee angle during gait in individuals with spastic cerebral palsy (CP). Research question: To determine if hamstring spasticity, as measured by Modified Tardieu Scale (MTS) at rest, is associated with knee flexion angle at initial contact and midstance during gait. Methods: Thirty ambulatory children (mean age 8.7 ± 2.4 years) diagnosed with spastic CP participated. The hamstrings’ spasticity was assessed in the supine position with the MTS, measuring R1 (muscle reaction to passive fast stretch), R2 (passive range of motion), and R2-R1 (dynamic component of spasticity). We conducted 3-dimensional computerized gait analysis and calculated semimembranosus muscle-tendon length and lengthening velocity during gait using musculoskeletal modeling and inverse kinematic analysis by OpenSim. Pearson correlation coefficients were calculated to estimate the association of MTS with biomechanical parameters during gait. Results: Knee flexion angle at initial contact and maximal knee extension angle during stance phase significantly positively correlated with both R1 and ㅣR2 - R1ㅣ of MTS, but not with R2 angle. The length of semimembranosus at initial contact, end of swing, and minimal length during stance phase were strongly negatively associated with R1, rather than R2 or ㅣR2 - R1ㅣ angles. Significance: The R1 angle of MTS (muscle reaction to passive fast stretch) is more relevant correlate of knee flexion angle during gait than the R2 (passive range of motion).
1. Introduction Flexed knee gait is one of the most common gait abnormalities in children with cerebral palsy (CP) and its frequency occurs as age increases [1]. The etiology of flexed knee gait is multi-factorial, short and spastic hamstrings are considered to be the main cause of this gait abnormality [2]. Although many authors have reported that hamstring lengthening is an effective treatment for improving flexed knee gait [3,4], some previous studies have shown that hamstring lengths are not actually shorter than usual in CP patients with flexed knee gait [5,6]. Measurement of the popliteal angle is a widely used clinical means of assessing hamstring length in the supine position. However, the popliteal angle did not correlate well with the knee angle during gait in individuals with CP in several previous studies [5,7–9]. Assessment of the popliteal angle is a static measurement in the supine position only; therefore, it could be difficult to reflect the dynamic range of the knee
angle and hamstring length during gait. The medial hamstring muscle is a biarticulate muscle that acts as both a hip extensor and a knee flexor, and so it has a tremendous effect on the complex interaction of hip and knee joints during gait. Spasticity is commonly defined as a velocity dependent increase in tonic stretch reflexes due to hyper‐excitability [10], while stiffness is a mechanical resistance of the myotendinous tissue, as it is passively lengthened. The Modified Tardieu Scale (MTS) is a clinical tool for assessing spasticity that includes quantitative measurement [11]. Passive movements of MTS are tested at two speeds: as slow as possible (R2), and as fast as possible (R1). As for knee flexor muscle, the R2 angle of MTS is equal to the popliteal angle. Although several studies have investigated the correlation between popliteal angle and kinematic parameter of the knee joint during gait [5,7], there is a lack of research on the relationship between dynamic assessment of spasticity using MTS and gait analysis parameters.
Abbreviations: CP, cerebral palsy; MTS, modified Tardieu scale; ROM, range of motion; 3D, 3-dimensional ⁎ Corresponding author at: Department of Rehabilitation Medicine, Severance Hospital, Research Institute of Rehabilitation Medicine, Yonsei University College of Medicine, 50 Yonseiro, Seodaemun-gu, Seoul, 03722, Republic of Korea. E-mail address: [email protected] (D.-w. Rha). https://doi.org/10.1016/j.gaitpost.2018.06.163 Received 6 April 2018; Received in revised form 1 June 2018; Accepted 24 June 2018 0966-6362/ © 2018 Elsevier B.V. All rights reserved.
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2.2.3. Muscle-tendon length We determined the muscle-tendon lengths and velocities of the semimembranosus for each subject. The muscle-tendon length was estimated using a 3D computer model of the lower extremity (Lower Limb Extremity Model 2010) [12]. We conducted inverse kinematic analysis of motion capture data with this model using OpenSim, an open source biomechanics simulation application [13]. In order to measure the changes of muscle-tendon length during gait, we used the least-squares formulation [14] to compute a set of desired joint angles for tracking based on the marker trajectories from the gait analysis. We normalized the muscle-tendon lengths based on the lengths when the hip and knee were in the anatomic position, with all joint angles set at zero [6]. We averaged data for three steps from a multi-step trial to analyze the muscle-tendon length. We estimated muscle–tendon lengthening velocity by computing the numerical derivative of the muscle–tendon length data with respect to time. We analyzed peak lengthening velocity during mid to end swing.
Therefore, the aim of this study was to investigate whether the use of the MTS in children with CP to determine both dynamic spasticity and mechanical resistance of hamstring muscles is associated with hamstring length and knee flexion angle during gait. 2. Methods This was a retrospective study conducted in a university-affiliated, tertiary-care teaching hospital. Ethical approval was granted by the institutional review board and ethics committee of our hospital (42014-0516). 2.1. Participants For this study, the medical records of children with CP, who were referred to our motion analysis laboratory between December 2012 and November 2014, were retrospectively reviewed. Inclusion criteria were as follows: (1) able to walk independently without assistance (Gross Motor Function Classification System [GMFCS] level I-II), (2) Modified Ashworth Scale (MAS) at knee flexors ≥ 1+ with R2 − R1 angle of MTS > 15 °, and (3) age 5–15 years. Exclusion criteria were as follows: (1) chemodenervation therapy within the past 6 months, (2) previous selective rhizotomy, intrathecal baclofen pump and orthopedic surgery, (3) previous history of peripheral neuropathy or myopathy. In the case of bilateral CP, we selected the more affected limb based on the MTS score. Accordingly, we analyzed 30 limbs of 30 children with CP in this study.
2.3. Statistical analysis Statistical analysis was performed using the Statistical Package for the Social Sciences for Windows (SPSS version 23.0, IBM SPSS Incorporated, Chicago, IL, USA). Descriptive statistics, such as mean and standard deviation (SD), were used to summarize patient demographics. Pearson correlation coefficients for parametric data and Spearman’s rank correlation coefficients for nonparametric data were computed to estimate the association of MTS with biomechanical parameters. The level of significance was set to p-value < 0.05.
2.2. Assessments
3. Results
2.2.1. Clinical measures of hamstring spasticity The muscle tone of the hamstring was assessed with the MTS [11]. During the MTS, children were asked to relax in the supine position, with the hip joint of the contralateral leg in a flexed position to eliminate residual anterior pelvic tilt [12,13]. The study leg was positioned to 90-degree hip flexion with full-degree knee flexion. Then, the knee was passively extended twice: the first time very slowly (> 5 s for the entire range of motion), and the second time as fast as possible (< 1 s). Two levels of the popliteal angle were measured by manual goniometry referring to R2 and R1 angles, respectively. All clinical measures were routinely recorded as part of the gait analysis by two experienced physiatrists. The angle of muscle reaction (R1) referred to the point in the range of motion (ROM) where a catch was first felt during a quick, passive extension of the knee joint. By contrast, full range of motion (R2) referred to the popliteal angle measured at the end of the movement. The absolute difference between the two angles ( R2 − R1 ) represented the dynamic components of spasticity [11]. Therefore, R2 represented only the mechanical resistance of hamstrings, whereas R1 was the summation of both mechanical resistance and the dynamic spasticity of hamstrings.
In total, 30 ambulatory children with spastic cerebral palsy (18 unilateral and 12 bilateral; 16 boys and 14 girls), aged from 5 to 15 years (mean age of the children was 8.7 ± 2.4 years), whose GMFCS level was I or II (GMFCS level I/II: 19/11) participated in this study. The characteristics of the subjects are described in Table 1. 3.1. Correlation between MTS and the kinematic data during gait Positive values of kinematic data indicate pelvic anterior tilt and knee flexion, while negative values indicate pelvic posterior tilt and knee extension. Table 2 shows the correlation coefficients between the MTS and the sagittal knee angle on gait analysis. The absolute value of R2 - R1 (ㅣR2 - R1ㅣ) of MTS moderately positively correlated with the knee angle at initial contact (r = 0.482; p < 0.01), and knee angle at end swing (r = 0.543; p < 0.01), and weakly correlated with maximal knee extension during stance phase (rs = 0.387; p < 0.05). R1 of MTS also showed a moderate positive correlation with the knee angle at initial contact (r = 0.490; p < 0.01) and end swing (r = 0.582; Table 1 Participant characteristics.
2.2.2. Gait kinematics Gait analysis was performed using a computerized 3D motion analysis (VICON MX-T10 Motion Analysis System, Oxford Metrics Inc., Oxford, UK) to measure kinematic data during the gait cycle. Subjects were instrumented with 16 passive reflective markers according to Helen Hayes marker set. Six digital videos were recorded simultaneously, from each video on the front and rear, and four videos on the side, while the child walked barefoot on an 8 m pathway. Data from three trials at a self-selected walking speed were collected for each subject at a sampling rate of 100 Hz. We captured all data based on the VICON Plug-in-Gait model; then we used NEXUS software version 1.8.5 to calculate joint kinematics, based on an average of three representative trials.
Characteristic
No./Valuea
No. of participants No. of legs Most affected side, right/left Gender, male/female Age at gait analysis, years GMFCS level, I / II Type of cerebral palsy, unilateral/ bilateral Modified Tardieu scale of knee flexor R1 angle, degrees R2 angle, degrees ㅣR2 - R1ㅣangle, degrees
30 30 11 / 19 16 / 14 8.7 ± 2.4 (5–15) 19 / 11 18 / 12
GMFCS: Gross motor functional classification system. a Values are mean ± standard deviation (range). 256
65.00 ± 20.55 (20–110) 36.83 ± 13.68 (5–60) 28.17 ± 12.21 (15–70)
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Table 2 correlation coefficients between knee flexor Modified Tardieu Scale and kinematic data of sagittal plane. Knee angle Parameters
R1 of MTS Correlation p-value R2 of MTS Correlation p-value ㅣR2 - R1ㅣ of MTS Correlation p-value
Pelvis angle
Initial contact
Max Ext stance
Max Fl swing
End swing
Anterior tilting at initial contact
Maximal anterior tilting
Anterior tilting at End swing
.490b .006
.387a .034
.069 .719
.582b .001
−.282 .131
−.175 .354
−.311 .094
.306 .100
.160 .398
.073 .703
.390a .033
−.054 .778
−.007 .972
−.104 .584
.482b .007
.387c .035
.034 .858
.543b .002
−.415a .023
−.288 .123
−.408a .025
MTS, modified Tardieu scale; Max, maximal; Ext, extension; Fl, flexion. Positive values of kinematic data indicate pelvic anterior tilt and knee flexion, while negative values indicate pelvic posterior tilt and knee extension. a Correlation is significant at the 0.05 level by Pearson’s correlation coefficient. b Correlation is significant at the 0.01 level by Pearson’s correlation coefficient. c Correlation is significant at the 0.05 level by Spearman’s rank correlation coefficient.
= -0.443; p < 0.05), while R2 showed only a weak negative correlation at end swing (r = −0.386; p < 0.05). By contrast, ㅣR2 - R1ㅣ of MTS demonstrated a moderate negative correlation with the semimembranosus muscle length at only minimal stance phase (r = -0.430; p < 0.05). In addition, the lengthening velocity of semimembranosus during the swing phase did not significantly correlate with the MTS of the hamstring.
p < 0.01), and a weak positive correlation with maximal knee extension during stance phase (r = 0.387; p < 0.05). R2 only weakly positively correlated with the knee flexion angle at end swing (r = 0.390; p < 0.05). Maximal knee flexion angle during the swing phase did not correlate with MTS. For pelvic kinematics, ㅣR2 - R1ㅣ negatively correlated with the pelvic anterior tilting at initial contact (r = -0.415; p < 0.05) and end swing (r = −0.408; p < 0.05). This result indicates that a higher dynamic spasticity of hamstring was related to more posterior pelvic tilt (Table 2). A scatterplot showing the significant relationship between the R1 of MTS and the knee angle at initial contact with a regression line is shown in Fig. 1.
4. Discussion This study demonstrated that the R1 or R2 - R1 of the hamstring MTS, which represent the dynamic component of spasticity, significantly correlated with knee angle and hamstring length during gait, unlike the R2, which represents the passive range of motion at the knee joint. We tested the MTS of the hamstring with the hip in the 90-degree flexed position, placing the hamstrings at their maximal stretch across the hip and knee [15]. The spasticity is activated when the muscle is stretched to the R1 position; and then the viscoelasticity of the soft tissues and joints and the component of contracture may have come into play until the muscle is stretched to the R2 position [16]. Thus, the
3.2. Correlation between MTS and the muscle-tendon length during gait As for semimembranosus, R1 had the highest correlation with muscle length, compared to R2 or R2 - R1 (Table 3). R1 of MTS showed a moderate negative correlation with the muscle length of semimembranosus at initial contact (r = -0.405; p < 0.05) (Fig. 1), and minimal length during stance phase (r = −0.494; p < 0.05) and end swing (r
Fig. 1. Correlation between the R1 angle of the Modified Tardieu Scale and the knee flexion angle (A) and semimembranosus length (B) at initial contact. Knee flexion angle and semimembranosus length at initial contact were significantly correlated with the R1 angle. 257
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gait than static contracture. The hamstring is a biarticular muscle that affect both the knee and hip joints. In addition, the hip angle itself can have important modulating effects on hamstring stretch reflexes [22]. Therefore, we assessed the pelvic angle during gait and only the absolute value of R2 R1 negatively correlated with the pelvic angle in the sagittal pelvic kinematic analysis, meaning the dynamic spasticity of hamstrings promoted posterior pelvic tilting, especially at initial contact and end swing.
Table 3 correlation coefficients between knee flexor Modified Tardieu Scale and the length of semimembranosus. Semimembranosus length Parameters
R1 of MTS Correlation p-value R2 of MTS Correlation p-value ㅣR2 - R1ㅣ of MTS Correlation p-value
Initial contact
Min stance
End swing
Lengthening velocity during end swing
−.405a .026
−.494b .006
−.443a .014
−.060 .753
−.340 .066
−.358 .052
−.386a .035
.041 .830
−.178 .346
−.430a .018
−.178 .348
−.190 .315
4.2. Correlation between MTS and the muscle-tendon length during gait In the muscle-tendon length study, the R1 angle of MTS showed a moderate negative correlation with semimembranosus length at both the stance and swing phase. This means that muscle reaction to exaggerated stretch reflexes is associated with a short hamstring length during gait. In contrast, the popliteal angle, R2 of MTS, only weakly correlated with semimembranosus length, and only at the end swing. There is a paucity of studies on the correlation between popliteal angle and hamstring length during gait. Delp et al. [5] concluded that the popliteal angle was not a valid indicator of maximum hamstring length during the gait cycle, whereas Thompson et al. [7] showed that the popliteal angle significantly correlated with maximal hamstring length during gait, but only when performed by the most reliable examiner and when using a modified method. In their study, the modified popliteal angle of > 40° used by the most reliable examiner may indicate that the medial hamstrings are short. Our study is different because: (1) the sample size was more than two times greater; (2) we used the modified method assessing the popliteal angle by a reliable examiner. In the modified method, the contralateral hip is flexed to eliminate anterior pelvic tilt caused by hip flexor tightness [7]. Although the modified method of measuring the popliteal angle is the more reliable technique to reflect hamstring length, most previous studies used the conventional method to measure the popliteal angle, with the contralateral hip in a neutral position [9] or not mentioned at all [8,17]. The hamstring muscle is stretched to its maximal length at initial contact and the terminal swing phase. This may be the reason that the popliteal angle showed a weak correlation with hamstring length at only the end swing in our study. During the swing phase of normal gait, the hamstring muscles are rapidly stretched, through the combined action of knee extension and hip flexion. Hamstring muscles were reported to lengthen slowly in the second half of the swing phase in the children with CP, and it may be caused by their shortening or spasticity [23]. However, in our study there was no significant correlation between MTS and the peak lengthening velocity of semimembranosus during the swing phase. This means that the lengthening velocity is related not only to dynamic spasticity and muscle contracture, but also to other factors, including co-contraction or selective motor control. Selective motor control is required, especially during the terminal swing, when the combination of hip flexion and knee extension motion is needed [24]. Impaired selective motor control was reported to influence knee position at initial contact, which is associated with decreased knee extension during the swing phase [25]. Additionally, the popliteal angle did not show a significant correlation with hamstring length during the stance phase in our study. Hoffinger et al. [6] found that the hamstring lengths during the stance phase in most patients with crouch gait were longer than the resting length and that hamstrings functioned as hip extensors during a significant portion of the stance phase. This issue of the impact of hamstring lengthening on knee flexion during stance is very much debated [3,4]. Previous studies show that many children with flexed knee gait do not have shortened hamstrings, and our study findings also support this statement [5]. This study indicates that a neural component of spasticity, other than static shortening or contracture, plays critical role in knee angle and hamstring length during the gait. In the same context, a child with
MTS, modified Tardieu scale. Min stance, minimal length during stance. a Correlation is significant at the 0.05 level by Pearson’s correlation coefficient. b Correlation is significant at the 0.01 level by Pearson’s correlation coefficient.
R2 - R1 represents the dynamic spasticity and R1 represents the summation of both mechanical resistance and the dynamic spasticity of hamstrings. 4.1. Correlation between MTS and the kinematic data during gait This study found no significant correlation between the popliteal angle and the knee flexion angle during stance phase, and only a weak correlation was noted at the end swing. Although most previous studies showed no significant correlation between the popliteal angle and the knee angle during the gait cycle [8,9], some studies still suggest that such a relationship does exist. Desloovere et al. [17] showed a negative correlation between the popliteal angle and maximal knee extension in the stance phase, but the correlation was weak (r = -0.28, P < 0.01). Faber et al. [18], by contrast, showed that the popliteal angle (R2), not the stretch restricted angle (R1), was strongly associated with the maximum knee extension at the end swing, suggesting that mechanical resistance of the hamstrings is more important for knee angle during gait. This result partly agreed with our finding of a weak correlation between the popliteal angle (R2) and the knee flexion angle only at end swing phase. However, R1 and R2 - R1 showed a higher correlation with knee flexion angles during the gait than R2 did in our study. Previous studies measured clinical parameters similar to R1, named “initial” or “first” popliteal angle [9,19]. These terms were defined as the muscle reaction during stretch; however, the stretch velocity was not as fast as the R1 we measured in this study. McMulkin et al. [9] investigated the correlation between initial and final popliteal angles and knee flexion angle in the stance phase, revealing a Pearson’s correlation coefficient of −0.49. Whereas Cooney et al. [19] declared the initial popliteal angle was significantly correlated with knee extension at the terminal swing. The Cooney et al. study partially supports our findings, although the first resistance point in their study was not equal to the R1 of MTS in our study. Spastic hamstrings have been found to have lower activation thresholds during passive stretch [20]. Perry and Newsam [21] showed that patients with a flexed knee gait exhibit premature firing of the hamstrings during the swing phase. This premature activation of the hamstring is related to R1 of the MTS and is a dynamic component of spasticity. Reduced knee extension at the terminal swing might be explained by a premature onset of the hamstring activity due to exaggerated stretch reflexes. This study is the first to report the significant correlation of R2 - R1, a dynamic component of MTS, with the knee flexion angle. Our study revealed that dynamic spasticity had a stronger correlation with knee kinematics during the 258
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a dynamic but not yet static hamstring contracture may be better treated with chemodenervation, including botulinum toxin or intrathecal baclofen, rather than orthopedic surgery, to improve knee extension at the end swing and the concatenate initial contact [26]. We need further studies with more subjects to confirm the effects of hamstring muscle botulinum toxin injection on gait functions of children with spastic CP.
[4] P.A. DeLuca, S. Ounpuu, R.B. Davis, J.H. Walsh, Effect of hamstring and psoas lengthening on pelvic tilt in patients with spastic diplegic cerebral palsy, J. Pediatr. Orthop. 18 (6) (1998) 712–718. [5] S.L. Delp, A.S. Arnold, R.A. Speers, C.A. Moore, Hamstrings and psoas lengths during normal and crouch gait: implications for muscle-tendon surgery, J. Orthop. Res. 14 (1) (1996) 144–151. [6] S.A. Hoffinger, G.T. Rab, H. Abou-Ghaida, Hamstrings in cerebral palsy crouch gait, J. Pediatr. Orthop. 13 (6) (1993) 722–726. [7] N.S. Thompson, R.J. Baker, A.P. Cosgrove, J.L. Saunders, T.C. Taylor, Relevance of the popliteal angle to hamstring length in cerebral palsy crouch gait, J. Pediatr. Orthop. 21 (3) (2001) 383–387. [8] M.S. Orendurff, J.S. Chung, R.A. Pierce, Limits to passive range of joint motion and the effect on crouch gait in children with cerebral palsy, Gait Posture 7 (2) (1998) 165. [9] M.L. McMulkin, J.J. Gulliford, R.V. Williamson, R.L. Ferguson, Correlation of static to dynamic measures of lower extremity range of motion in cerebral palsy and control populations, J. Pediatr. Orthop. 20 (3) (2000) 366–369. [10] J.W. Lance, The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture, Neurology 30 (12) (1980) 1303–1313. [11] R.N. Boyd, H.K. Graham, Objective measurement of clinical findings in the use of botulinum toxin type a for the management of children with cerebral palsy, Eur. J. Neurol. 6 (S4) (1999) s23–s35. [12] E.M. Arnold, S.R. Ward, R.L. Lieber, S.L. Delp, A model of the lower limb for analysis of human movement, Ann. Biomed. Eng. 38 (2) (2010) 269–279. [13] S.L. Delp, F.C. Anderson, A.S. Arnold, P. Loan, A. Habib, C.T. John, et al., OpenSim: open-source software to create and analyze dynamic simulations of movement, IEEE Trans. Biomed. Eng. 54 (11) (2007) 1940–1950. [14] T.W. Lu, J.J. O’Connor, Bone position estimation from skin marker co-ordinates using global optimisation with joint constraints, J. Biomech. 32 (2) (1999) 129–134. [15] J.L. Young, J. Rodda, P. Selber, E. Rutz, H.K. Graham, Management of the knee in spastic diplegia: what is the dose? Orthop. Clin. North. Am. 41 (4) (2010) 561–577. [16] W.K. Yam, M.S. Leung, Interrater reliability of modified ashworth scale and modified tardieu scale in children with spastic cerebral palsy, J. Child Neurol. 21 (12) (2006) 1031–1035. [17] K. Desloovere, G. Molenaers, H. Feys, C. Huenaerts, B. Callewaert, P. Van de Walle, Do dynamic and static clinical measurements correlate with gait analysis parameters in children with cerebral palsy? Gait Posture 24 (3) (2006) 302–313. [18] I.R. Faber, B. Nienhuis, N.P. Rijs, A.C. Geurts, J. Duysens, Is the modified tardieu scale in semi-standing position better associated with knee extension and hamstring activity in terminal swing than the supine Tardieu? Dev. Med. Child Neurol. 50 (5) (2008) 382–387. [19] K.M. Cooney, J.O. Sanders, M.C. Concha, F.L. Buczek, Novel biomechanics demonstrate gait dysfunction due to hamstring tightness, Clin. Biomech. (Bristol, Avon) 21 (1) (2006) 59–66. [20] L. Bar-On, E. Aertbelien, G. Molenaers, K. Desloovere, Muscle activation patterns when passively stretching spastic lower limb muscles of children with cerebral palsy, PLoS One 9 (3) (2014) e91759. [21] J. Perry, C. Newsam, Function of the hamstrings in cerebral palsy, in: Sussman (Ed.), The Diplegic Child: Evaluation and Management, American Academy of Orthopaedic Surgeons, Rosemont, IL, 1992, pp. 299–307. [22] J.J. Visser, J.E. Hoogkamer, M.F. Bobbert, P.A. Huijing, Length and moment arm of human leg muscles as a function of knee and hip-joint angles, Eur. J. Appl. Physiol. Occup. Physiol. 61 (5-6) (1990) 453–4560. [23] P. Crenna, Spasticity and ‘spastic’ gait in children with cerebral palsy, Neurosci. Biobehav. Rev. 22 (4) (1998) 571–578. [24] E.G. Fowler, E.J. Goldberg, The effect of lower extremity selective voluntary motor control on interjoint coordination during gait in children with spastic diplegic cerebral palsy, Gait Posture 29 (1) (2009) 102–107. [25] D.W. Rha, K. Cahill-Rowley, J. Young, L. Torburn, K. Stephenson, J. Rose, Biomechanical and clinical correlates of stance-phase knee flexion in persons with spastic cerebral palsy, PMR (2015), http://dx.doi.org/10.1016/j.pmrj.2015.06.003. [26] D.L. Damiano, Rehabilitative therapies in cerebral palsy: the good, the not as good, and the possible, J. Child Neurol. 24 (9) (2009) 1200–1204. [27] J.M. Gracies, K. Burke, N.J. Clegg, R. Browne, C. Rushing, D. Fehlings, et al., Reliability of the Tardieu Scale for assessing spasticity in children with cerebral palsy, Arch. Phys. Med. Rehabil. 91 (3) (2010) 421–428. [28] L. Bar-On, E. Aertbelien, H. Wambacq, D. Severijns, K. Lambrecht, B. Dan, et al., A clinical measurement to quantify spasticity in children with cerebral palsy by integration of multidimensional signals, Gait Posture 38 (1) (2013) 141–147.
4.3. Limitations There are several limitations of this study. First, some children with CP have bone deformities, but the musculoskeletal model used to estimate the hamstring lengths in this study didn’t consider the effects of variable bone deformities in each child on alteration of moment arm and length of hamstring muscle. Future studies should develop the musculoskeletal model to reflect these skeletal deformities. Another limitation of our study is the standardization of the MTS. Although reliable hamstring MTS in children with CP have been reported [27], it can be difficult to determine the accurate angle of catch in R1 measurements. Recently, instrumented clinical tests have been developed to analyze biomechanical and electrophysiological muscle responses during passive stretch [28]. However, our study is meaningful to the clinician in an office setting who wishes to estimate the biomechanical changes during gait based on the more feasible grading of MTS. 5. Conclusion The popliteal angle (R2 of MTS) did not significantly correlate with the knee flexion angle or with hamstring length during stance phase, and only weakly correlated at the end swing. By contrast, the muscle reaction angle to exaggerated stretch reflexes (R1 of MTS) is a more relevant parameter with the knee flexion angle during gait than passive ROM of R2. In addition, the dynamic component of spasticity (R2 - R1) is associated with the knee flexion and pelvic tilting angles during gait. Conflict of interest The authors declare no conflict of interest. Acknowledgements This study was supported by a faculty research grant of Yonsei University College of Medicine for 2014 (6-2014-0065). References [1] G.E. Rose, K.A. Lightbody, R.G. Ferguson, J.C. Walsh, J.E. Robb, Natural history of flexed knee gait in diplegic cerebral palsy evaluated by gait analysis in children who have not had surgery, Gait Posture 31 (3) (2010) 351–354. [2] S.H. Dhawlikar, L. Root, R.L. Mann, Distal lengthening of the hamstrings in patients who have cerebral palsy. Long-term retrospective analysis, J. Bone Jt. Surg. Am. 74 (9) (1992) 1385–1391. [3] W.N. Chang, A.I. Tsirikos, F. Miller, N. Lennon, J. Schuyler, L. Kerstetter, et al., Distal hamstring lengthening in ambulatory children with cerebral palsy: primary versus revision procedures, Gait Posture 19 (3) (2004) 298–304.
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