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Joint moment contributions to swing knee extension acceleration during gait in individuals with spastic diplegic cerebral palsy
Gait & Posture 33 (2011) 66–70
Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Joint moment contributions to swing knee extension acceleration during gait in individuals with spastic diplegic cerebral palsy Evan J. Goldberg a, Philip S. Requejo b, Eileen G. Fowler a,* a b
Department of Orthopaedic Surgery, University of California at Los Angeles, Los Angeles, CA 90095, United States Rancho Los Amigos National Rehabilitation Center, Downey, CA 90242, United States
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2010 Received in revised form 17 August 2010 Accepted 24 September 2010
The mechanisms contributing to swing phase knee acceleration in individuals with spastic diplegic cerebral palsy (CP) are not well understood, but evidence suggests that selective voluntary motor control (SVMC) may play a role. The purpose of this study was to examine the relationship between lower limb SVMC, measured using Selective Control Assessment of the Lower Extremity (SCALE), and joint moment contributions to swing knee extension acceleration in participants with spastic diplegic CP. Eighteen participants were recruited (mean age = 13.8 years, range = 6–30 years, Gross Motor Function Classification System Levels I–III). Induced acceleration analysis was performed during the swing phase of gait. Average joint moment contributions to swing knee extension acceleration were calculated. Contributions from stance limb and swing limb joint moments were correlated with SCALE scores using Pearson’s correlations. A strong correlation was found (p < 0.0001, r = 0.85) between SCALE score and the total swing joint moment contributions to swing knee extension acceleration. As SCALE score increased, swing joint moments provided less resistance to knee extension acceleration. No relationship (p = 0.18) was found between stance moment contributions to swing knee acceleration and stance limb SCALE scores. Excessive contributions from swing limb joint moments appear to be the factor limiting swing knee extension in spastic diplegic CP gait. Interventions that address negative contributions due to spasticity may not be effective in patients who cannot generate adequate knee extension due to poor SVMC. ß 2010 Elsevier B.V. All rights reserved.
Keywords: Induced acceleration analysis Spastic diplegic cerebral palsy Gait Terminal-swing knee extension
1. Introduction Inadequate terminal-swing knee extension during gait is common in children with spastic diplegic cerebral palsy (CP) [1– 3], negatively influencing step length and walking speed. Research suggests that selective voluntary motor control (SVMC) plays an important role in achieving full knee extension when the hip is flexing in children with spastic diplegic CP [4]. Children with good SVMC were more capable of extending the knee while the hip was flexing during swing, as occurs in normal walking. In contrast, children with poor SVMC were less able to dissociate hip and knee movement often utilizing abnormal mass flexor/extensor synergy patterns. While spasticity may also limit knee extension [1,3,5], Rozumalski and Schwartz [6] reported that SVMC and strength had stronger associations with excessive knee flexion at initial contact. Since SVMC is an important factor in achieving terminal knee
* Corresponding author at: Department of Orthopaedic Surgery, 1000 Veteran Ave, 22-64 Rehabilitation Center, Los Angeles, CA 90095-1795 United States. Tel.: +1 310 825 4028; fax: +1 310 825 5290. E-mail address: [email protected] (E.G. Fowler). 0966-6362/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2010.09.026
extension, it should also influence mechanisms responsible for knee extension acceleration. In individuals without disability, swing knee extension is produced primarily by stance limb muscles [7] and eccentrically controlled by the swing knee flexors [8]. The vasti are normally inactive when swing knee extension acceleration occurs. Determining how muscle groups can accelerate a single joint is complex because muscles are capable of accelerating joints they do not span through intersegmental reaction forces [9]. Induced acceleration analysis (IAA) is a technique used to assess biomechanical interactions in multi-segment systems by determining the contributions of joint moments to joint accelerations. A study using IAA found that the primary contributors to swing knee extension acceleration were the stance limb hip muscles during normal gait [7]. Therefore, the authors suggested that stance limb weakness may lead to inadequate terminal-swing knee extension in CP. Recent examination of gait in individuals with hemiplegic CP suggest an alternative explanation. Despite differences in impairment between limbs, stance limb contributions to swing knee acceleration were similar [10]. On the hemiplegic side, swing limb joint moments decelerating knee extension were excessive resulting in lower average knee extension acceleration compared
[(Fig._1)TD$IG]
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to the non-hemiplegic limb. Exemplar data from this study suggests that lower limb SVMC may influence joint moment contributions to swing knee acceleration. Hemiplegic limbs with lower levels of SVMC demonstrated simultaneous hip and knee joint flexor moments, further reducing average knee extension acceleration. These patients exhibited a moderate amount of SVMC impairment on their hemiplegic limbs (SCALE range 4–7). Therefore, assessing these contributions in individuals with spastic diplegia provides greater insight into these mechanisms across a wider range of impairment. The purpose of this study was to examine the effect of lower limb SVMC on contributions to swing knee extension acceleration in participants with spastic diplegic CP with bilateral impairment. We hypothesized that a strong positive relationship exists between SVMC and swing limb contributions to swing knee acceleration. 2. Methods 2.1. Study population A convenience sample of eighteen individuals with spastic diplegic CP were recruited for this study from patients referred for a gait analysis (mean age standard deviation = 13.8 7.2 years, height = 1.4 0.2 m, weight = 39.5 19.9 kg). All participants were able to walk independently with or without assistive devices. Five participants were classified as Gross Motor Function Classification System (GMFCS) Level I, eight as Level II and five as Level III [11]. Exclusion criteria for all participants were: orthopedic or neurological surgery within the preceding 12 months; botulinum toxin injections or serial casting within the preceding three months; and muscle transfer surgery at the hip or knee. Informed consent and assent, approved by the Institutional Review Board Human Subject’s Protection Committee of our institution, were obtained for all participants. 2.2. Selective voluntary motor control assessment SVMC was assessed using a valid and reliable tool called Selective Control Assessment of the Lower Extremity (SCALE) [12]. The ability to perform isolated movement patterns at the hip, knee, ankle, subtalar and toe joints was assessed bilaterally. Hip flexion/extension with the knee extended was tested in side lying. The following tests were performed in sitting: knee extension/flexion, ankle dorsiflexion/plantar flexion with the knee extended, subtalar inversion/eversion, and toe flexion/extension. SVMC was graded at each joint as ‘‘Normal’’ (2 points), ‘‘Impaired’’ (1 point) or ‘‘Unable’’ (0 points). An overall SCALE score was calculated by summing the points assigned to each joint for a maximum of 10 points/limb. 2.3. Gait analysis Gait analysis was performed in the Kameron Gait and Motion Analysis Laboratory using an eight-camera system (Motion Analysis Corporation, Santa Rosa, CA). Two forceplates (Kistler Instrumentation Corporation, Amherst, NY) were concealed in the walkway to record ground reaction forces. Fifteen reflective markers were placed on the participants lower limbs using a modified Helen Hayes marker set [13]. Participants walked barefoot at a self-selected pace on a 25-foot walkway until at least 3 forceplate hits were recorded per limb. Each forceplate hit was checked visually to insure that the hit was isolated. Handheld assistance was provided for balance, if needed. Forceplate data was evaluated to insure that peak vertical forces reached body weight. These participants walked at speeds substantially slower than age-matched controls. As vertical ground reaction forces at slow speeds do not rise above body weight [14], full weight bearing was a reasonable assumption. If the peak vertical ground reaction force was less than body weight, trials were disregarded. Data were collected in Cortex 1.0 (Motion Analysis Corp., Santa Rosa, CA), sampled at 60 Hz and smoothed using a Butterworth filter at 6 Hz [15].
2.4. Induced acceleration analysis One representative trial per participant was selected and imported into Visual 3D Basic/RT (C-Motion, Inc., Germantown, MD). The contribution of each joint moment to swing knee acceleration was calculated using the IAA Module. Kinematic and kinetic data were calculated. The biomechanical model was described and validated by Kepple et al. [16] and has been used previously to assess energy flow through the lower extremity body segments in individuals without disability [17] and joint moment contributions to knee and hip joint accelerations in individuals with pathology [10,18,19]. The model had seven segments: a combined head, arms and trunk segment, and bilateral thighs, shanks and feet. The hip was modeled as a spherical joint allowing flexion/extension, abduction/adduction and internal/external rotation. The knee was a revolute joint allowing flexion/extension.
Fig. 1. Knee extension acceleration (KEA) during the swing phase of gait. The extension phase is defined as the period in which the knee acceleration is positive (extension), and the braking phase is defined as the period in which the knee is acceleration is negative (flexion). The arrows above indicate when the knee is flexing and extending based on kinematic data.
The ankle was a universal joint allowing dorsi/plantar flexion and inversion/ eversion. A constraint was placed on the foot that fixed it to the floor when flat, but allowed it to rotate about the center of pressure when in contact with the ground but not flat. IAA was performed as described previously [16]. The model was configured at each frame according to experimental data. Gravity and all joint moments were set to zero, and joint moments from gait analysis were entered into the model sequentially for each participant. The resulting swing knee acceleration was calculated for the input moment. The input moment was then set to zero, and all other joint moments were sequentially entered as the input in the model. This process was completed for each lower extremity joint moment at each frame during swing. The final output provided the knee angular acceleration generated by each joint moment. Contributions were averaged during the period in which the knee was accelerating toward extension (i.e., the extension phase) (Fig. 1). Contributions from stance and swing limb joint moments were correlated with SCALE scores using Pearson’s correlations (r). If a significant (p < 0.05) relationship was found for total stance or swing joint moment contributions, individual joint moment contributions were correlated with SCALE scores for the limb. Analysis was limited to the left limb swing phase mechanics. Swing limb contributions were correlated with left limb SCALE scores, and stance limb contributions were correlated with right limb SCALE scores. Pearson’s correlations were also used to examine the relationship between SCALE scores and terminal-swing knee extension.
3. Results A strong correlation (r = 0.85, p < 0.0001) was found between SCALE scores and total swing joint moment contributions to swing knee extension acceleration (Fig. 2A). As SCALE score increased, the swing joint moments provided less resistance to knee extension. No relationship (p = 0.18) was found between total stance moment contributions to swing knee acceleration and SCALE scores (Fig. 2B). Significant correlations were found between SCALE scores and swing hip and ankle contributions to swing knee extension acceleration (hip: r = 0.51, ankle: r = 0.52, p < 0.05) (Fig. 3A and C). A tendency toward significance was found for the relationship between SCALE scores and swing knee contributions to swing knee extension acceleration (r = 0.47, p = 0.051) (Fig. 3B). As SCALE score increased, the negative (flexor) contribution to swing knee extension acceleration decreased for the hip and knee. While most of the swing hip and knee joint moments accelerated the knee toward flexion on average during the extension phase, one participant (SCALE = 8) had hip flexion/extension moment that accelerated the knee toward extension, primarily due to a large hip extension moment at the end of the extension phase. Another participant (SCALE = 9) had a knee flexion/extension moment that accelerated the knee toward extension, primarily due to its extension moment at toe-off followed by a diminished flexor
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[(Fig._3)TD$IG]
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Fig. 2. Total contributions to swing knee extension acceleration from the (A) swing limb joint moments and (B) stance limb joint moments. Circles indicate that two data points overlap.
moment. In contrast to the hip and knee moments, the negative contribution from the ankle moment increased with increasing SCALE scores (Fig. 3C). While the regression results reported for swing limb hip and ankle moment contributions include moments in the frontal and transverse plane, these contributions were substantially smaller than the sagittal plane contributions, and no significant trends were found individually. A significant relationship was also found between SCALE scores and terminal-swing knee extension (r = 0.64, p < 0.005) indicating that knee extension increased with increasing levels of SVMC. When assessing the largest components of the swing limb contributions to swing knee acceleration (i.e., hip and knee flexion/ extension moment contributions), substantial differences were found across the spectrum of SCALE scores. Exemplar data from a participant with poor SVMC (SCALE = 2) shows that both the hip and knee moments simultaneously accelerated the knee toward flexion for most of the extension phase, resulting in diminished swing knee acceleration (Fig. 4A and E). This was also observed for a participant with fair SVMC (SCALE = 4); however, the magnitude of joint moment contribution accelerations were lower (Fig. 4B and F). These results were representative of most of the participants with SCALE scores of 4 or lower. For a participant with good SVMC (SCALE = 9), the knee moment accelerated the knee toward extension while the hip moment accelerated the knee toward flexion following toe-off (Fig. 4C and G). About halfway through the extension phase, the contributions of both the hip and knee moments were markedly reduced and slightly flexor. Toward the end of the extension phase, the knee moment accelerated the knee toward flexion to a greater degree while the hip moment accelerated the knee toward extension. These contributions were similar to those of an individual without disability (Fig. 4D and H) with the exception of the short period that simultaneous hip and knee contributions were negative.
Fig. 3. Total contributions to swing knee extension acceleration from the (A) swing hip moments, (B) swing knee moments and (C) swing ankle moments. Circles indicate that two data points overlap.
4. Discussion The strong relationship between total swing joint moment contributions to swing knee extension acceleration and SCALE scores supports our hypothesis. The findings verified previous suggestions that SVMC may be an important factor in achieving the knee extension acceleration necessary for adequate step length and, therefore, walking speed in individuals with spastic CP [10] and provides insight into these mechanisms across the spectrum of SCALE scores. Overall, stance limb joint moments tended to accelerate the swing knee toward extension while swing limb joint moments tended to accelerate the knee toward flexion, which agrees with previous IAA studies of individuals without disability [7]. In addition to influencing the coupled motion between the hip and knee during terminal swing [4], our results suggest that SVMC influenced hip and knee joint moment contributions to swing knee acceleration during early and mid-swing. In most participants with low SCALE scores (0–4), the swing hip and knee flexion/extension moments simultaneously accelerated the swing knee toward flexion for most of the extension phase resulting in diminished knee extension acceleration (Fig. 4A and B). In these participants, the knee moment contribution was most likely influenced by
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Fig. 4. Swing hip and knee flexion/extension moment contributions to swing knee acceleration, moments and angles for participants with (A), (E) and (I) poor SVMC; (B), (F) and (J) fair SVMC; (C), (G) and (K) good SVMC; and (D), (H) and (L) an individual without disability. The individual without disability was selected from our database and best represented the average of all of these participants. Positive indicates extension.
hamstring activity associated with a flexor synergy pattern. Inappropriate knee flexor activity has been confirmed during early swing in hemiplegic CP [20]. Hamstring spasticity and contractures most likely do not influence the negative contributions of the swing knee moment during this period because the knee is flexed and the hamstrings are not operating at a long length [21]. Hamstring spasticity and contractures were not likely factors in these participants as knee was relatively flexed throughout the extension phase (see Fig. 4I–L). These negative contributions are more important during mid- or late swing when the hip is fully flexed and the knee is rapidly extending. Participants with higher SCALE scores demonstrated a more non-synergistic action of swing hip and knee moments (Fig. 4C) similar to that of individuals without disability (Fig. 4D). While these individuals may demonstrate a short period in which both the hip and knee simultaneously accelerate the knee toward flexion (Fig. 4C), the length of this period is substantially shorter than those with poor SVMC. In contrast to hip and knee contributions, ankle contributions to swing knee acceleration decreased with increasing SCALE scores. Participants with good SVMC are able to dorsiflex the ankle while the knee is extending during swing, which is a non-synergistic movement. Dorsiflexion has been shown to accelerate the knee toward flexion during swing [7,22]. A score of ‘‘normal’’ SVMC at the ankle is less common in individuals with poor SVMC as greater distal SVMC impairment has been reported for individuals with spastic CP [23]. The magnitudes of the accelerations created by the swing ankle were substantially less than those from the swing hip and knee, so this trend had little influence on the total swing moment contribution. Arnold et al. [7] suggested that individuals with CP walked with inadequate terminal-swing knee extension due to stance limb muscle weakness. While those with poor SVMC walk with inadequate terminal-swing knee extension [4,6], no significant trend was found between level of impairment (SVMC) and stance
limb moment contributions to swing knee extension acceleration (Fig. 2B). During stance, lower extremity extensor moments add energy to the trunk [17] and accelerate the pelvis upward, creating reaction forces on the swing limb that accelerate the knee toward extension [7]. Therefore, mass extensor patterns exhibited by some participants with CP, including those with poor SVMC, during single limb support are capable of generating appropriate acceleration on the swing limb during the extension phase. The strongest correlation found was between SCALE scores and total swing limb joint moment contributions to swing knee extension acceleration (Fig. 2A), whereas correlations between SCALE scores and individual joint moment contributions on the swing limb were weaker (Fig. 3). Different walking strategies may explain the variability in the individual joint moment contributions. For example, two participants (Participant 1 and 2) had SCALE scores of 2, but Participant 1 functioned at a GMFCS level III while Participant 2 functioned at a GMFCS level I. Total swing joint moment contributions were similar ( 39518/s/s for Participant 1 vs. 45378/s/s for Participant 2, Fig. 2A); however, the magnitudes of the hip, knee and ankle contributions varied greatly (see Fig. 3). For Participant 1, hip and knee flexor moments that decelerated knee extension produced similar net accelerations over the extension phase, and swing ankle contributions were minimal. Participant 2 had a hip flexor moment that decelerated knee extension substantially more than the knee flexor moment and an ankle plantar flexion moment that accelerated the knee toward extension. Several limitations of this study, including the use of joint moments instead of muscle forces or muscle excitation patterns as the simulation input and not explicitly calculating contributions from the velocity-related forces, have been described previously [10]. In this study, the pelvis and trunk were modeled as a single segment; however, normative stance limb and swing limb contributions to swing knee acceleration were similar using the
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present model [10] to those found by Arnold et al. [7], who modeled the pelvis and trunk separately. The participants ranged widely in age; however, SVMC is reflective of perinatal brain damage, and we would not expect impairment severity to change across the age span used for this study. Future studies should assess how these contributions to swing knee extension acceleration change with increasing walking speed in CP. Arnold et al. [24] assessed these contributions in individuals without disability and found that velocity-related force contributions increased substantially with increasing speed and swing muscle flexor contributions decreased to a lesser degree at increasing speeds. It is unknown whether flexor contributions from the swing limb decrease at fast speeds in individuals with CP. Both SVMC and spasticity may be contributing factors. Individuals with poor SVMC who are able to increase walking speed may rely on velocity-related forces or stance limb muscles to increase knee extension acceleration. In summary, a strong relationship was found between SVMC and swing moment contributions to swing knee extension acceleration. Swing limb joint moments of participants with poor SVMC resisted knee extension to a larger extent than those of individuals with good SVMC. In contrast, stance moment contributions to swing knee extension acceleration appear to be independent of SVMC. These results should be considered when planning treatments for individuals with CP who exhibit inadequate terminal-swing knee extension. While strengthening stance limb muscles could potentially improve terminal-swing knee extension, this may not be the most efficient strategy. The limiting factor in spastic diplegic CP appears to be excessive contributions from the swing limb joint moments that inhibit swing knee extension. While addressing negative contributions due to spasticity or contractures is possible, SVMC is most likely stable for this age-group. Addressing negative contributions in patients with sufficient SVMC through treatments that decrease spasticity or eliminate contractures, such as botulinum toxin injections, intrathecal baclofen or muscle lengthenings, may provide a more efficient means for patients to improve terminalswing knee extension, thus increasing step length and walking speed. Acknowledgements The authors gratefully acknowledge Marcia Greenberg and Loretta Staudt for their assistance with data collection and the support of the Lena Longo Foundation. Conflict of interest None declared.
References [1] Crenna P. Spasticity and ‘spastic’ gait in children with cerebral palsy. Neurosci Biobehav Rev 1998;22:571–8. [2] Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res 1993;139–47. [3] Tuzson AE, Granata KP, Abel MF. Spastic velocity threshold constrains functional performance in cerebral palsy. Arch Phys Med Rehabil 2003;84:1363–8. [4] Fowler EG, Goldberg EJ. The effect of lower extremity selective voluntary motor control on interjoint coordination during gait in children with spastic diplegic cerebral palsy. Gait Posture 2009;29:102–7. [5] Baumann JU, Ruetsch H, Schurmann K. Distal hamstring lengthening in cerebral palsy. An evaluation by gait analysis. Int Orthop 1980;3:305–9. [6] Rozumalski A, Schwartz MH. Crouch gait patterns defined using k-means cluster analysis are related to underlying clinical pathology. Gait Posture 2009;30:155–60. [7] Arnold AS, Thelen DG, Schwartz MH, Anderson FC, Delp SL. Muscular coordination of knee motion during the terminal-swing phase of normal gait. J Biomech 2007;40:3314–24. [8] Davis RB, Ounpuu S. Kinetics of normal gait. In: Gage JR, editor. The Treatment of Gait Problems in Cerebral Palsy. London: Mac Keith Press; 2004. p. 120–33. [9] Zajac FE, Gordon ME. Determining muscle’s force and action in multi-articular movement. Exerc Sport Sci Rev 1989;17:187–230. [10] Goldberg EJ, Requejo PS, Fowler EG. Joint moment contributions to swing knee extension acceleration during gait in children with spastic hemiplegic cerebral palsy. J Biomech 2010;43:893–9. [11] Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214–23. [12] Fowler EG, Staudt LA, Greenberg MB, Oppenheim WL. Selective Control Assessment of the Lower Extremity (SCALE): development, validation, and interrater reliability of a clinical tool for patients with cerebral palsy. Dev Med Child Neurol 2009;51:607–14. [13] Davis III RB, Ounpuu S, Tyburski D, Gage JR. A gait analysis data collection and reduction technique. Human Movement Sci 1991;10:575–87. [14] Schwartz MH, Rozumalski A, Trost JP. The effect of walking speed on the gait of typically developing children. J Biomech 2008;41:1639–50. [15] Kidder SM, Abuzzahab Jr FS, Harris GF, Johnson JE. A system for the analysis of foot and ankle kinematics during gait. IEEE Trans Rehabil Eng 1996;4:25–32. [16] Kepple TM, Siegel KL, Stanhope SJ. Relative contributions of the lower extremity joint moments to forward progression and support during gait. Gait Posture 1997;6:1–8. [17] Siegel KL, Kepple TM, Stanhope SJ. Joint moment control of mechanical energy flow during normal gait. Gait Posture 2004;19:69–75. [18] Siegel KL, Kepple TM, Stanhope SJ. Using induced accelerations to understand knee stability during gait of individuals with muscle weakness. Gait Posture 2006;23:435–40. [19] Siegel KL, Kepple TM, Stanhope SJ. A case study of gait compensations for hip muscle weakness in idiopathic inflammatory myopathy. Clin Biomech (Bristol Avon) 2007;22:319–26. [20] Patikas D, Wolf S, Doderlein L. Electromyographic evaluation of the sound and involved side during gait of spastic hemiplegic children with cerebral palsy. Eur J Neurol 2005;12:691–9. [21] Arnold AS, Liu MQ, Schwartz MH, Ounpuu S, Delp SL. The role of estimating muscle-tendon lengths and velocities of the hamstrings in the evaluation and treatment of crouch gait. Gait Posture 2006;23:273–81. [22] Anderson FC, Goldberg SR, Pandy MG, Delp SL. Contributions of muscle forces and toe-off kinematics to peak knee flexion during the swing phase of normal gait: an induced position analysis. J Biomech 2004;37:731–7. [23] Fowler EG, Staudt LA, Greenberg MB. Lower-extremity selective voluntary motor control in patients with spastic cerebral palsy: increased distal motor impairment. Dev Med Child Neurol 2010;52:264–9. [24] Arnold AS, Schwartz MH, Thelen DG, Delp SL. Contributions of muscles to terminal-swing knee motions vary with walking speed. J Biomech 2007;40: 3660–71.
Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Joint moment contributions to swing knee extension acceleration during gait in individuals with spastic diplegic cerebral palsy Evan J. Goldberg a, Philip S. Requejo b, Eileen G. Fowler a,* a b
Department of Orthopaedic Surgery, University of California at Los Angeles, Los Angeles, CA 90095, United States Rancho Los Amigos National Rehabilitation Center, Downey, CA 90242, United States
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2010 Received in revised form 17 August 2010 Accepted 24 September 2010
The mechanisms contributing to swing phase knee acceleration in individuals with spastic diplegic cerebral palsy (CP) are not well understood, but evidence suggests that selective voluntary motor control (SVMC) may play a role. The purpose of this study was to examine the relationship between lower limb SVMC, measured using Selective Control Assessment of the Lower Extremity (SCALE), and joint moment contributions to swing knee extension acceleration in participants with spastic diplegic CP. Eighteen participants were recruited (mean age = 13.8 years, range = 6–30 years, Gross Motor Function Classification System Levels I–III). Induced acceleration analysis was performed during the swing phase of gait. Average joint moment contributions to swing knee extension acceleration were calculated. Contributions from stance limb and swing limb joint moments were correlated with SCALE scores using Pearson’s correlations. A strong correlation was found (p < 0.0001, r = 0.85) between SCALE score and the total swing joint moment contributions to swing knee extension acceleration. As SCALE score increased, swing joint moments provided less resistance to knee extension acceleration. No relationship (p = 0.18) was found between stance moment contributions to swing knee acceleration and stance limb SCALE scores. Excessive contributions from swing limb joint moments appear to be the factor limiting swing knee extension in spastic diplegic CP gait. Interventions that address negative contributions due to spasticity may not be effective in patients who cannot generate adequate knee extension due to poor SVMC. ß 2010 Elsevier B.V. All rights reserved.
Keywords: Induced acceleration analysis Spastic diplegic cerebral palsy Gait Terminal-swing knee extension
1. Introduction Inadequate terminal-swing knee extension during gait is common in children with spastic diplegic cerebral palsy (CP) [1– 3], negatively influencing step length and walking speed. Research suggests that selective voluntary motor control (SVMC) plays an important role in achieving full knee extension when the hip is flexing in children with spastic diplegic CP [4]. Children with good SVMC were more capable of extending the knee while the hip was flexing during swing, as occurs in normal walking. In contrast, children with poor SVMC were less able to dissociate hip and knee movement often utilizing abnormal mass flexor/extensor synergy patterns. While spasticity may also limit knee extension [1,3,5], Rozumalski and Schwartz [6] reported that SVMC and strength had stronger associations with excessive knee flexion at initial contact. Since SVMC is an important factor in achieving terminal knee
* Corresponding author at: Department of Orthopaedic Surgery, 1000 Veteran Ave, 22-64 Rehabilitation Center, Los Angeles, CA 90095-1795 United States. Tel.: +1 310 825 4028; fax: +1 310 825 5290. E-mail address: [email protected] (E.G. Fowler). 0966-6362/$ – see front matter ß 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2010.09.026
extension, it should also influence mechanisms responsible for knee extension acceleration. In individuals without disability, swing knee extension is produced primarily by stance limb muscles [7] and eccentrically controlled by the swing knee flexors [8]. The vasti are normally inactive when swing knee extension acceleration occurs. Determining how muscle groups can accelerate a single joint is complex because muscles are capable of accelerating joints they do not span through intersegmental reaction forces [9]. Induced acceleration analysis (IAA) is a technique used to assess biomechanical interactions in multi-segment systems by determining the contributions of joint moments to joint accelerations. A study using IAA found that the primary contributors to swing knee extension acceleration were the stance limb hip muscles during normal gait [7]. Therefore, the authors suggested that stance limb weakness may lead to inadequate terminal-swing knee extension in CP. Recent examination of gait in individuals with hemiplegic CP suggest an alternative explanation. Despite differences in impairment between limbs, stance limb contributions to swing knee acceleration were similar [10]. On the hemiplegic side, swing limb joint moments decelerating knee extension were excessive resulting in lower average knee extension acceleration compared
[(Fig._1)TD$IG]
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to the non-hemiplegic limb. Exemplar data from this study suggests that lower limb SVMC may influence joint moment contributions to swing knee acceleration. Hemiplegic limbs with lower levels of SVMC demonstrated simultaneous hip and knee joint flexor moments, further reducing average knee extension acceleration. These patients exhibited a moderate amount of SVMC impairment on their hemiplegic limbs (SCALE range 4–7). Therefore, assessing these contributions in individuals with spastic diplegia provides greater insight into these mechanisms across a wider range of impairment. The purpose of this study was to examine the effect of lower limb SVMC on contributions to swing knee extension acceleration in participants with spastic diplegic CP with bilateral impairment. We hypothesized that a strong positive relationship exists between SVMC and swing limb contributions to swing knee acceleration. 2. Methods 2.1. Study population A convenience sample of eighteen individuals with spastic diplegic CP were recruited for this study from patients referred for a gait analysis (mean age standard deviation = 13.8 7.2 years, height = 1.4 0.2 m, weight = 39.5 19.9 kg). All participants were able to walk independently with or without assistive devices. Five participants were classified as Gross Motor Function Classification System (GMFCS) Level I, eight as Level II and five as Level III [11]. Exclusion criteria for all participants were: orthopedic or neurological surgery within the preceding 12 months; botulinum toxin injections or serial casting within the preceding three months; and muscle transfer surgery at the hip or knee. Informed consent and assent, approved by the Institutional Review Board Human Subject’s Protection Committee of our institution, were obtained for all participants. 2.2. Selective voluntary motor control assessment SVMC was assessed using a valid and reliable tool called Selective Control Assessment of the Lower Extremity (SCALE) [12]. The ability to perform isolated movement patterns at the hip, knee, ankle, subtalar and toe joints was assessed bilaterally. Hip flexion/extension with the knee extended was tested in side lying. The following tests were performed in sitting: knee extension/flexion, ankle dorsiflexion/plantar flexion with the knee extended, subtalar inversion/eversion, and toe flexion/extension. SVMC was graded at each joint as ‘‘Normal’’ (2 points), ‘‘Impaired’’ (1 point) or ‘‘Unable’’ (0 points). An overall SCALE score was calculated by summing the points assigned to each joint for a maximum of 10 points/limb. 2.3. Gait analysis Gait analysis was performed in the Kameron Gait and Motion Analysis Laboratory using an eight-camera system (Motion Analysis Corporation, Santa Rosa, CA). Two forceplates (Kistler Instrumentation Corporation, Amherst, NY) were concealed in the walkway to record ground reaction forces. Fifteen reflective markers were placed on the participants lower limbs using a modified Helen Hayes marker set [13]. Participants walked barefoot at a self-selected pace on a 25-foot walkway until at least 3 forceplate hits were recorded per limb. Each forceplate hit was checked visually to insure that the hit was isolated. Handheld assistance was provided for balance, if needed. Forceplate data was evaluated to insure that peak vertical forces reached body weight. These participants walked at speeds substantially slower than age-matched controls. As vertical ground reaction forces at slow speeds do not rise above body weight [14], full weight bearing was a reasonable assumption. If the peak vertical ground reaction force was less than body weight, trials were disregarded. Data were collected in Cortex 1.0 (Motion Analysis Corp., Santa Rosa, CA), sampled at 60 Hz and smoothed using a Butterworth filter at 6 Hz [15].
2.4. Induced acceleration analysis One representative trial per participant was selected and imported into Visual 3D Basic/RT (C-Motion, Inc., Germantown, MD). The contribution of each joint moment to swing knee acceleration was calculated using the IAA Module. Kinematic and kinetic data were calculated. The biomechanical model was described and validated by Kepple et al. [16] and has been used previously to assess energy flow through the lower extremity body segments in individuals without disability [17] and joint moment contributions to knee and hip joint accelerations in individuals with pathology [10,18,19]. The model had seven segments: a combined head, arms and trunk segment, and bilateral thighs, shanks and feet. The hip was modeled as a spherical joint allowing flexion/extension, abduction/adduction and internal/external rotation. The knee was a revolute joint allowing flexion/extension.
Fig. 1. Knee extension acceleration (KEA) during the swing phase of gait. The extension phase is defined as the period in which the knee acceleration is positive (extension), and the braking phase is defined as the period in which the knee is acceleration is negative (flexion). The arrows above indicate when the knee is flexing and extending based on kinematic data.
The ankle was a universal joint allowing dorsi/plantar flexion and inversion/ eversion. A constraint was placed on the foot that fixed it to the floor when flat, but allowed it to rotate about the center of pressure when in contact with the ground but not flat. IAA was performed as described previously [16]. The model was configured at each frame according to experimental data. Gravity and all joint moments were set to zero, and joint moments from gait analysis were entered into the model sequentially for each participant. The resulting swing knee acceleration was calculated for the input moment. The input moment was then set to zero, and all other joint moments were sequentially entered as the input in the model. This process was completed for each lower extremity joint moment at each frame during swing. The final output provided the knee angular acceleration generated by each joint moment. Contributions were averaged during the period in which the knee was accelerating toward extension (i.e., the extension phase) (Fig. 1). Contributions from stance and swing limb joint moments were correlated with SCALE scores using Pearson’s correlations (r). If a significant (p < 0.05) relationship was found for total stance or swing joint moment contributions, individual joint moment contributions were correlated with SCALE scores for the limb. Analysis was limited to the left limb swing phase mechanics. Swing limb contributions were correlated with left limb SCALE scores, and stance limb contributions were correlated with right limb SCALE scores. Pearson’s correlations were also used to examine the relationship between SCALE scores and terminal-swing knee extension.
3. Results A strong correlation (r = 0.85, p < 0.0001) was found between SCALE scores and total swing joint moment contributions to swing knee extension acceleration (Fig. 2A). As SCALE score increased, the swing joint moments provided less resistance to knee extension. No relationship (p = 0.18) was found between total stance moment contributions to swing knee acceleration and SCALE scores (Fig. 2B). Significant correlations were found between SCALE scores and swing hip and ankle contributions to swing knee extension acceleration (hip: r = 0.51, ankle: r = 0.52, p < 0.05) (Fig. 3A and C). A tendency toward significance was found for the relationship between SCALE scores and swing knee contributions to swing knee extension acceleration (r = 0.47, p = 0.051) (Fig. 3B). As SCALE score increased, the negative (flexor) contribution to swing knee extension acceleration decreased for the hip and knee. While most of the swing hip and knee joint moments accelerated the knee toward flexion on average during the extension phase, one participant (SCALE = 8) had hip flexion/extension moment that accelerated the knee toward extension, primarily due to a large hip extension moment at the end of the extension phase. Another participant (SCALE = 9) had a knee flexion/extension moment that accelerated the knee toward extension, primarily due to its extension moment at toe-off followed by a diminished flexor
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Fig. 2. Total contributions to swing knee extension acceleration from the (A) swing limb joint moments and (B) stance limb joint moments. Circles indicate that two data points overlap.
moment. In contrast to the hip and knee moments, the negative contribution from the ankle moment increased with increasing SCALE scores (Fig. 3C). While the regression results reported for swing limb hip and ankle moment contributions include moments in the frontal and transverse plane, these contributions were substantially smaller than the sagittal plane contributions, and no significant trends were found individually. A significant relationship was also found between SCALE scores and terminal-swing knee extension (r = 0.64, p < 0.005) indicating that knee extension increased with increasing levels of SVMC. When assessing the largest components of the swing limb contributions to swing knee acceleration (i.e., hip and knee flexion/ extension moment contributions), substantial differences were found across the spectrum of SCALE scores. Exemplar data from a participant with poor SVMC (SCALE = 2) shows that both the hip and knee moments simultaneously accelerated the knee toward flexion for most of the extension phase, resulting in diminished swing knee acceleration (Fig. 4A and E). This was also observed for a participant with fair SVMC (SCALE = 4); however, the magnitude of joint moment contribution accelerations were lower (Fig. 4B and F). These results were representative of most of the participants with SCALE scores of 4 or lower. For a participant with good SVMC (SCALE = 9), the knee moment accelerated the knee toward extension while the hip moment accelerated the knee toward flexion following toe-off (Fig. 4C and G). About halfway through the extension phase, the contributions of both the hip and knee moments were markedly reduced and slightly flexor. Toward the end of the extension phase, the knee moment accelerated the knee toward flexion to a greater degree while the hip moment accelerated the knee toward extension. These contributions were similar to those of an individual without disability (Fig. 4D and H) with the exception of the short period that simultaneous hip and knee contributions were negative.
Fig. 3. Total contributions to swing knee extension acceleration from the (A) swing hip moments, (B) swing knee moments and (C) swing ankle moments. Circles indicate that two data points overlap.
4. Discussion The strong relationship between total swing joint moment contributions to swing knee extension acceleration and SCALE scores supports our hypothesis. The findings verified previous suggestions that SVMC may be an important factor in achieving the knee extension acceleration necessary for adequate step length and, therefore, walking speed in individuals with spastic CP [10] and provides insight into these mechanisms across the spectrum of SCALE scores. Overall, stance limb joint moments tended to accelerate the swing knee toward extension while swing limb joint moments tended to accelerate the knee toward flexion, which agrees with previous IAA studies of individuals without disability [7]. In addition to influencing the coupled motion between the hip and knee during terminal swing [4], our results suggest that SVMC influenced hip and knee joint moment contributions to swing knee acceleration during early and mid-swing. In most participants with low SCALE scores (0–4), the swing hip and knee flexion/extension moments simultaneously accelerated the swing knee toward flexion for most of the extension phase resulting in diminished knee extension acceleration (Fig. 4A and B). In these participants, the knee moment contribution was most likely influenced by
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Fig. 4. Swing hip and knee flexion/extension moment contributions to swing knee acceleration, moments and angles for participants with (A), (E) and (I) poor SVMC; (B), (F) and (J) fair SVMC; (C), (G) and (K) good SVMC; and (D), (H) and (L) an individual without disability. The individual without disability was selected from our database and best represented the average of all of these participants. Positive indicates extension.
hamstring activity associated with a flexor synergy pattern. Inappropriate knee flexor activity has been confirmed during early swing in hemiplegic CP [20]. Hamstring spasticity and contractures most likely do not influence the negative contributions of the swing knee moment during this period because the knee is flexed and the hamstrings are not operating at a long length [21]. Hamstring spasticity and contractures were not likely factors in these participants as knee was relatively flexed throughout the extension phase (see Fig. 4I–L). These negative contributions are more important during mid- or late swing when the hip is fully flexed and the knee is rapidly extending. Participants with higher SCALE scores demonstrated a more non-synergistic action of swing hip and knee moments (Fig. 4C) similar to that of individuals without disability (Fig. 4D). While these individuals may demonstrate a short period in which both the hip and knee simultaneously accelerate the knee toward flexion (Fig. 4C), the length of this period is substantially shorter than those with poor SVMC. In contrast to hip and knee contributions, ankle contributions to swing knee acceleration decreased with increasing SCALE scores. Participants with good SVMC are able to dorsiflex the ankle while the knee is extending during swing, which is a non-synergistic movement. Dorsiflexion has been shown to accelerate the knee toward flexion during swing [7,22]. A score of ‘‘normal’’ SVMC at the ankle is less common in individuals with poor SVMC as greater distal SVMC impairment has been reported for individuals with spastic CP [23]. The magnitudes of the accelerations created by the swing ankle were substantially less than those from the swing hip and knee, so this trend had little influence on the total swing moment contribution. Arnold et al. [7] suggested that individuals with CP walked with inadequate terminal-swing knee extension due to stance limb muscle weakness. While those with poor SVMC walk with inadequate terminal-swing knee extension [4,6], no significant trend was found between level of impairment (SVMC) and stance
limb moment contributions to swing knee extension acceleration (Fig. 2B). During stance, lower extremity extensor moments add energy to the trunk [17] and accelerate the pelvis upward, creating reaction forces on the swing limb that accelerate the knee toward extension [7]. Therefore, mass extensor patterns exhibited by some participants with CP, including those with poor SVMC, during single limb support are capable of generating appropriate acceleration on the swing limb during the extension phase. The strongest correlation found was between SCALE scores and total swing limb joint moment contributions to swing knee extension acceleration (Fig. 2A), whereas correlations between SCALE scores and individual joint moment contributions on the swing limb were weaker (Fig. 3). Different walking strategies may explain the variability in the individual joint moment contributions. For example, two participants (Participant 1 and 2) had SCALE scores of 2, but Participant 1 functioned at a GMFCS level III while Participant 2 functioned at a GMFCS level I. Total swing joint moment contributions were similar ( 39518/s/s for Participant 1 vs. 45378/s/s for Participant 2, Fig. 2A); however, the magnitudes of the hip, knee and ankle contributions varied greatly (see Fig. 3). For Participant 1, hip and knee flexor moments that decelerated knee extension produced similar net accelerations over the extension phase, and swing ankle contributions were minimal. Participant 2 had a hip flexor moment that decelerated knee extension substantially more than the knee flexor moment and an ankle plantar flexion moment that accelerated the knee toward extension. Several limitations of this study, including the use of joint moments instead of muscle forces or muscle excitation patterns as the simulation input and not explicitly calculating contributions from the velocity-related forces, have been described previously [10]. In this study, the pelvis and trunk were modeled as a single segment; however, normative stance limb and swing limb contributions to swing knee acceleration were similar using the
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present model [10] to those found by Arnold et al. [7], who modeled the pelvis and trunk separately. The participants ranged widely in age; however, SVMC is reflective of perinatal brain damage, and we would not expect impairment severity to change across the age span used for this study. Future studies should assess how these contributions to swing knee extension acceleration change with increasing walking speed in CP. Arnold et al. [24] assessed these contributions in individuals without disability and found that velocity-related force contributions increased substantially with increasing speed and swing muscle flexor contributions decreased to a lesser degree at increasing speeds. It is unknown whether flexor contributions from the swing limb decrease at fast speeds in individuals with CP. Both SVMC and spasticity may be contributing factors. Individuals with poor SVMC who are able to increase walking speed may rely on velocity-related forces or stance limb muscles to increase knee extension acceleration. In summary, a strong relationship was found between SVMC and swing moment contributions to swing knee extension acceleration. Swing limb joint moments of participants with poor SVMC resisted knee extension to a larger extent than those of individuals with good SVMC. In contrast, stance moment contributions to swing knee extension acceleration appear to be independent of SVMC. These results should be considered when planning treatments for individuals with CP who exhibit inadequate terminal-swing knee extension. While strengthening stance limb muscles could potentially improve terminal-swing knee extension, this may not be the most efficient strategy. The limiting factor in spastic diplegic CP appears to be excessive contributions from the swing limb joint moments that inhibit swing knee extension. While addressing negative contributions due to spasticity or contractures is possible, SVMC is most likely stable for this age-group. Addressing negative contributions in patients with sufficient SVMC through treatments that decrease spasticity or eliminate contractures, such as botulinum toxin injections, intrathecal baclofen or muscle lengthenings, may provide a more efficient means for patients to improve terminalswing knee extension, thus increasing step length and walking speed. Acknowledgements The authors gratefully acknowledge Marcia Greenberg and Loretta Staudt for their assistance with data collection and the support of the Lena Longo Foundation. Conflict of interest None declared.
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