Toe walking: Muscular demands at the ankle and knee

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Toe Walking: Muscular Demands at the Ankle and Knee Jacquelin Perry, MD, ScD, Judith M. Burnfield, PT, JoAnne K. Gronley, DPT, Sara J. Mulroy, PhD, PT ABSTRACT. Perry J, Burnfield JM, Gronley JK, Mulroy SJ. Toe walking: muscular demands at the ankle and knee. Arch Phys Med Rehabil 2003;84:7-16. Objective: To compare the relationship between electromyographic activity and internal moment in heel-toe and toe walking. Design: Simultaneous recording of stride characteristics and kinematic, kinetic, and intramuscular electromyographic data; paired t tests identified significant between-condition differences. Setting: Gait laboratory. Participants: Ten able-bodied subjects. Interventions: Not applicable. Main Outcome Measures: Kinematic, moment, power, and electromyographic variables (ankle, knee). Results: Compared with heel-toe walking, toe walking showed greater plantarflexion during stance (P⬍.001), higher plantarflexor moments (peak, mean) during loading response (P⬍.001) and midstance (P⬍.001), lower mean plantarflexor moments during terminal stance (P⫽.002), premature soleus (P⫽.001) and gastrocnemius (P⬍.001) activity, and higher levels of mean soleus and gastrocnemius activity during stance. During toe walking, the peak internal knee extensor moment was lower in midstance (P⫽.002), and power absorption was reduced in loading response; however, vastus intermedius electromyographic activity was not reduced. Conclusions: During toe walking, terminal stance soleus and gastrocnemius activity was greater, despite a lower mean internal plantarflexor moment. The dichotomy between internal moments and muscle effort (ie, electromyographic activity) was consistent with the reduction in force-generation capacity of the calf muscles when the ankle was in a plantarflexed position. Key Words: Biomechanics; Electromyography; Gait; Rehabilitation; Torque. © 2003 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation OE WALKING IS A COMMON GAIT deviation that most often is related to spastic paralysis. Failure to contact T the floor with the heel at the onset of stance frequently is observed in persons with cerebral palsy (CP),1-3 traumatic brain injury,4 and stroke5 and in children diagnosed with idiopathic toe walking.1,3

From the Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center, Downey, CA. Presented in part at the Gait and Clinical Movement Analysis Society’s annual meetings, April 2000, Rochester, MN, and April 2001, Sacramento, CA. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Jacquelin Perry, MD, Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center, 7601 E Imperial Hwy, Downey, CA 90242, e-mail: [email protected]. 0003-9993/03/8401-6990$35.00/0 doi:10.1053/apmr.2003.50057

Functionally, toe walking has been associated with premature and prolonged electromyographic activity of the ankle plantarflexors,2,4,6,7 plantarflexor spasticity,2,8 and plantarflexor contractures.2,9-11 Stance stability is compromised as a result of the reduced portion of the foot in contact with the ground.1,3,4,8,11,12 These functional limitations often result in reduced velocity and shorter stride length.1,3,8 Recently, it has been suggested that toe walking may provide compensatory advantages for persons with upper motoneuron lesions when compared with normal heel-toe walking. Kerrigan et al13 recorded motion and force platform data in 17 able-bodied subjects during heel-toe walking and toe walking. From these data, they calculated the internal moments generated at the ankle and knee. They identified significant reductions in the peak internal moments of force at the ankle and knee with toe walking. Both ankle plantarflexor moment and power generation were reduced during terminal stance and preswing, whereas in loading response, the moments of the ankle dorsiflexors and knee extensors were absent. From these findings, Kerrigan proposed that toe walking required less ankle plantarflexor, ankle dorsiflexor, and knee extensor muscle strength than heel-toe walking and hence might provide potential compensatory advantages. They noted, however, that 1 limitation in their study was their lack of direct muscle measurement (ie, electromyograms [EMGs]) to support this premise. Other investigators,4,14,15 however, have suggested that toe walking may require more effort from the muscles at the ankle, knee, and hip than heel-toe walking requires. Rose et al14 used surface electromyography to compare muscle activity patterns during heel-toe (10 subjects without pathology) and toe walking (8 subjects with CP). They divided the reference limb gait cycle (representing a single stride) into percentage points with 0% of the gait cycle representing initial contact and 100% representing the next initial contact. During toe walking, premature gastrocnemius activity during the preceding swing (91% gait cycle) and onset during early stance (9% gait cycle) were recorded. Additionally, prolonged quadriceps activity with cessation in terminal stance (38% gait cycle) versus midstance (15% gait cycle) and prolonged tibialis anterior activity were recorded during toe walking. These findings suggest that, in addition to altering calf muscle demand, toe walking also may increase the effort expended by knee extensors and ankle dorsiflexors. A possible explanation for the apparent contradiction in findings between derived internal moments and recorded electromyographic activity at the ankle and knee during toe walking may be the differences in study populations, that is, spastic CP versus subjects without pathology. Spastic paralysis introduces the potential complications of increased muscle action due to exaggerated reflexes and the dominance of primitive locomotor patterns. Further resolution of this conceptual conflict was not possible, because there were no common data. Rose14 did not record mechanical moments, and Kerrigan13 did not report electromyographic activity. A biomechanical explanation for the differences could be the influence of joint position on both the active force generation of muscles16 and the passive force production of the surrounding ligaments, tendons, and aponeurosis.17 Gordon et al16 found Arch Phys Med Rehabil Vol 84, January 2003

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MUSCULAR DEMANDS OF TOE WALKING, Perry

that muscle force production varied with the magnitude of overlap between the actin and myosin filaments within the sarcomere (ie, the sarcomere length-tension curve). Specifically, muscle fibers have an ideal length at which maximum force can be produced, and an overly shortened position significantly reduces the muscle’s force capability due to inefficient filament alignment within the sarcomere. Additionally, joint position also alters the passive contributions of ligaments, soft tissue, and muscles to the internal moment.17 In particular, Siegler et al17 noted a progressively increasing passive plantarflexor moment as ankle dorsiflexion increased. The significance of changes in EMGs and mechanical moment as joint position is altered during walking is critical. Inferences that therapeutic efforts to reduce equinus may not be as necessary, as is the clinical custom, could have a notable effect on patient care in today’s climate of minimizing medical costs.13 A search of the literature showed no study that used simultaneously recorded kinematic, kinetic, and electromyographic data to compare mechanical moments and muscular responses during toe walking versus heel-toe walking. Therefore, the purpose of this study was to clarify the relationship between electromyographic activity and internal moment in toe walking and heel-toe walking by measuring these factors in a common population. Specifically, the hypotheses to be tested were the following: (1) during toe walking, the peak internal plantarflexor moment would be lower, but the mean amplitude and duration of plantarflexor electromyographic activity would be greater, than those values in heel-toe walking and (2) during toe walking, the peak internal knee extensor moment would be lower, but the mean amplitude and duration of knee extensor electromyographic activity would be greater, than those values in heel-toe walking. METHODS Because they have the physical capacity to perform heel-toe walking as well as toe walking, we tested able-bodied subjects. To identify most accurately the relationships among joint position, internal mechanical moments, and muscular responses to moment demands, we simultaneously recorded kinematic, kinetic, and electromyographic data. Participants Ten subjects over the age of 18 years comprised the study group (8 women, 2 men; mean age ⫾ standard deviation [SD], 36.9⫾11.2y; mean height, 171.7⫾8.3cm; mean mass, 67.2⫾12.4kg). Subjects were screened for musculoskeletal and neurologic impairments and were free from any conditions that would affect their gait. All subjects ambulated at a community level, and none used an assistive device. Each subject signed informed consent and was provided with the Bill of Rights of Human Subjects. All testing was conducted at the Pathokinesiology Laboratory at Rancho Los Amigos National Rehabilitation Center, in Downey, CA. Instrumentation To eliminate the effect of acceleration and deceleration, a comprehensive gait analysis of each subject was conducted along a 10-m walkway, with the middle 6m designated for data collection. A Stride Analyzera was used to measure foot-floor contact patterns, to calculate stride characteristics, and to delineate the phasing of electromyographic activity. This system consisted of an insole containing compression closing switches (with a sensitivity of .02mPa) in the area of the heel, first and fifth metatarsals, and great toe. FM-FM telemetryb was used to Arch Phys Med Rehabil Vol 84, January 2003

transmit signals from the Stride Analyzer package to a DEC 11/73 computer.c A VICON motion analysis systemd was used to define the 3-dimensional motion of the lower limbs and pelvis. This system included 6 charge-coupled cameras with strobed infrared light-emitting diodes and retroreflective markers (diameter, 17mm) taped to the subject’s skin at overlying specified anatomic landmarks.18 Motion data were sampled at a rate of 50Hz, filtered at 6Hz (by use of a Butterworth digital filter), and recorded on a DEC PDP 11/83 computer.c A Kistler piezoelectric forceplatee (410⫻610mm) recorded the ground reaction forces. The plate was concealed in the center of a 10-m walkway (to avoid targeting). Forceplate data were sampled at 2500Hz on the DEC 11/73 computer, which also recorded the VICON frame signal for temporal synchronization of the motion and force data. Intramuscular electromyography, with bipolar wire electrodes (50-␮m Ni-Cr alloy wire in a 25-gauge needle), recorded the timing and intensity of muscle activity. An FM-FM telemetry systemb transmitted the electromyography signals from the subject to the DEC 11/73 computer. All electromyographic data were filtered over a system bandwidth of 150 to 1000Hz, with an overall gain of 1000, and recorded digitally at a sampling rate of 2500Hz per channel. Procedures Before gait analysis, the subject’s age, height, weight, and lower-extremity anthropometric data were recorded. To determine stride characteristics and to identify phases of the gait cycle, a pair of insole foot switchesa were taped to the bottom of each subject’s feet. To determine sagittal plane lowerextremity kinematics, VICON reflective markers were placed over the sacrum, anterior superior iliac spine (bilaterally), greater trochanter, anterior thigh, medial and lateral femoral condyles, anterior tibia, medial and lateral malleoli, dorsum of the foot, first and fifth metatarsal heads, and posterior heel.18,19 To quantify muscular responses during heel-toe and toe walking conditions, fine-wire electrodes were inserted according to Basmajian and DeLuca’s technique20 into the muscle bellies of the soleus, medial gastrocnemius, anterior tibialis, and vastus intermedius. Electrode placement was confirmed by palpation of the tendon and muscle belly during mild electric stimulation through the inserted wires and by recording the electromyography signal during maximum voluntary isometric muscle contraction. Manual muscle tests were performed in standard positions described in the Daniel and Worthingham muscle-testing manual.21 The functional electromyographic data for each study muscle were normalized to its electromyography signal acquired during the maximal isometric muscle test (MMT) to allow for comparison of electromyographic intensity between muscles and to control for the variability of electrode placement. For each condition (toe walking, heel-toe walking), stride characteristics, kinematics, ground reaction forces, and EMGs were recorded simultaneously. Subjects were provided with an opportunity to practice toe walking until they achieved a consistent toe-walking pattern. Next, 2 trials of walking on the toes (forefoot only) at a self-selected speed were recorded, followed by 2 trials of walking in a heel-toe manner at a speed approximating (⫾5%) that obtained during toe walking. A successful trial was defined as a trial in which an isolated step by the tested foot landed fully on the forceplate. Following gait analysis, end muscle tests were recorded to confirm continued insertion into the desired muscles.

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MUSCULAR DEMANDS OF TOE WALKING, Perry

Data Management Stride characteristics and foot-floor contact patterns were defined by using foot-switch data. To eliminate the effects of gender on stride characteristics, these data were expressed as a percentage of normal (%N) for the corresponding gender. Normative stride characteristic information was derived from Stride Analyzer and foot-switch data recorded from 420 healthy subjects at the pathokinesiology laboratory.12,22 Footswitch data were used to define the phasing of all gait data. Each stride was time-normalized, with initial contact defined as 0% of the gait cycle and the end of swing as 100%.12,22 For each stride, stance was defined as the period during which the reference limb was in contact with the ground, whereas swing was defined as the period when the reference limb was not in contact with the ground. To allow EMGs, kinetics, and kinematics to be averaged across multiple subjects, data were normalized to a stance duration of 62% of the gait cycle. This value is considered to be representative of normal walking12 and was consistent with the average stance phase shown by subjects. Stance phase was further subdivided into 5 subphases based on the foot-switch pattern recorded during stance, and swing was divided into 3 equal intervals.12 VICON motion data were processed with AMASS softwaref to produce 3-dimensional trajectories for each marker. The position and orientation of the pelvis, thigh, shank, and foot segments in the laboratory coordinate system were obtained, and computer algorithms, using Euler embedded coordinates, determined lower-extremity joint angles for each percentage of the gait cycle. The magnitude and timing of peak joint angle values during each phase of the gait cycle were identified. For subsequent use in the kinetic analysis, body segment velocities and accelerations were calculated by direct differentiation of the displacement data. The magnitude, orientation, and point of application (center of pressure) of the resultant ground reaction force were determined from forceplate data. We used measured body-segment parameters in conjunction with empirical relationships derived from cadaver studies to estimate the mass, center of mass, and moments of inertia of body segments.23,24 Joint and body segment kinematic information were combined with ground reaction force data to obtain ankle and knee joint moments by using the standard 3-dimensional inverse dynamics approach described by Meglan and Todd.25 Joint moments were normalized to body weight and leg length. Ankle and knee joint powers were determined by the product of joint moment and joint angular velocity. Digitally acquired electromyographic data were full-wave rectified and integrated over .01-second intervals for the stride corresponding with the force data. Intensities were reported as a percentage of the MMT recorded according to standard positions described by the Daniel and Worthingham muscletesting manual.21 The timing of electromyography was assessed with the EMG Analyzer software.a The EMG Analyzer determined onsets and cessations for all envelopes of EMGs (ie, clusters of action potentials) that exceeded an amplitude of 5% MMT. Envelopes of EMGs separated by short-duration gaps (⬍5% of the gait cycle) were combined into larger packets for analysis.26,27 Mean onset and cessation times were then calculated, and a time-adjusted mean profile for each muscle was obtained for both the toe-walking and the heel-toe–walking conditions. All electromyographic onsets and cessations were reported as a percentage of the gait cycle. The EMG Analyzer program also was used to determine the mean and peak amplitude of electromyographic activity for each muscle

throughout the gait cycle and during each phase of the gait cycle (loading response through terminal swing).12,26,27 Intrasubject repeatability of ankle and knee motion, moment, and power intercycle patterns for both the toe-walking and heel-toe gait trials were evaluated statistically by using the coefficient of multiple correlation (CMC).28 Within each subject, a highly consistent intercycle pattern was identified for motion, moment, and power variables, as evidenced by the moderately high to high CMCs (range, .849 –.999). Mean intrasubject CMCs were also calculated across subjects for ankle motion (toe⫽.930, heel-toe⫽.973), moment (toe⫽.991, heeltoe⫽.993), and power (toe⫽.967, heel-toe⫽.970), as well as for knee motion (toe⫽.984, heel-toe⫽.995), moment (toe⫽.933, heel-toe⫽.960), and power (toe⫽.931, heeltoe⫽.927). These data suggest that the limited number of walking trials measured in this study provided a reliable representation of the data. To identify differences between heel-toe–walking (normal) and toe-walking (simulated equinus) conditions, paired t tests were used to compare stride characteristics, foot-floor contact patterns, peak ankle and knee joint angles, mean and peak ankle and knee joint moments and power during each phase of stance, and mean and peak electromyographic activity for each muscle. We performed Bonferroni adjustments to account for multiple comparisons within a priori selected motion (P⬍.0031), moment (P⬍.0027), power (P⬍.0032), and electromyographic (P⬍.020) data. Statistical significance was defined as P⬍.05/n (where n is the number of variables analyzed within each data type). All data were analyzed with SPSS, version 10.0,g statistical software. RESULTS Stride Characteristics Consistent with the design of the study, subjects walked at similar speeds during toe walking (84.6%N) and heel-toe walking (83.4%N). During toe walking, significant reductions in stride length (83.0%N vs 90.9%N, P⬍.001) and increases in cadence (102.2%N vs 91.3%N, P⫽.001) were recorded when compared with heel-toe walking. Kinematics A comparison of ankle position showed significantly greater plantarflexion at each of the stance subphases during toe walking versus heel-toe walking (P⬍.001; fig 1). During toe walking, the ankle was at 24.3° of plantarflexion at the time of initial floor contact. Loading the limb then reduced the ankle angle to 9.8°—a motion of relative dorsiflexion. This finding was in sharp contrast to the small arc of increasing plantarflexion (from 1.1° to 4.5°) recorded during heel-toe weight acceptance. The contrast in ankle positions of the 2 gaits increased in both midstance and early terminal stance: toe walking continued in equinus, whereas progressive dorsiflexion was the motion pattern for heel-toe walking. The peak ankle position in terminal stance during toe walking was 12.0° of ankle plantarflexion, whereas heel-toe walking moved the ankle into 12.7° of dorsiflexion. No significant differences in knee position were recorded throughout the stance phases of the gait cycle, with the exception of preswing (fig 2). In preswing, the knee was flexed 28.2°, on average, during toe walking compared with 37.7° with heel-toe walking (P⫽.002). Kinetics The 2 modes of walking registered significantly different internal moment patterns at the ankle during the first half of Arch Phys Med Rehabil Vol 84, January 2003

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Fig 1. Mean ankle motion (degrees) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). Abbreviations: ISw, initial swing; LR, loading response; MSt, midstance; MSw, midswing; PSw, preswing; TSt, terminal stance; TSw, terminal swing. *Significantly greater plantarflexion during toe walking compared with heel-toe walking during each stance phase (P<.001).

stance (fig 3). In response to heel strike, heel-toe gait generated a small internal dorsiflexion moment (⫺.10N䡠m/kg䡠m at 5% gait cycle), which then quickly reversed into an increasing plantarflexor moment. This pattern did not occur with toe walking; instead, limb loading began with a plantarflexor moment (⫹.15N䡠m/kg䡠m), which rapidly increased (table 1). As a result of this diverse onset, toe walking generated significantly higher peak plantarflexor moments during loading response (1.32 vs .18N䡠m/kg䡠m, P⬍.001) and midstance (1.22 vs .74N䡠m/kg䡠m, P⬍.001) compared with heel-toe walking. During terminal stance, which is a period of heel rise with heel-toe gait, there was no significant difference between the

Fig 3. Mean internal ankle moments (N䡠m/kg䡠m) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). *Significantly higher peak and mean plantarflexor moments during loading response and midstance for toe walking compared with heel-toe walking (P<.001). †Significantly lower peak plantarflexor moment during terminal stance for toe walking compared with heel-toe walking (Pⴝ.002).

peak plantarflexor moments for toe walking and heel-toe walking (1.26 vs 1.48N䡠m/kg䡠m). Timing of the peak plantarflexor torques also was similar (48% gait cycle). Similar to the peak moments at the ankle, mean moments also showed a pattern of significant differences. During toe walking, significantly more positive mean ankle moments were recorded in loading response (.93 vs .01N䡠m/kg䡠m, P⬍.001) and midstance (.84 vs .45N䡠m/kg䡠m, P⬍.001), reflecting a greater plantarflexor moment. In contrast, the mean ankle moment for toe walking was significantly less than heel-toe walking during terminal stance (.97 vs 1.19N䡠m/kg䡠m, P⫽.002). At the knee, both modes of walking began with a brief internal flexor moment of similar magnitude (⫺.20N䡠m/kg䡠m at 1% gait cycle; fig 4). These quickly reversed to an extensor moment, which peaked at the transition between loading response and midstance (14% gait cycle). The peak internal extensor moment during toe walking was approximately 65% lower in loading response (.18 vs .52N䡠m/kg䡠m, P⫽.004) and

Table 1: Comparison of Internal Ankle Moments (N䡠m/kg䡠m) Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Loading response, peak dorsiflexor Loading response, peak plantarflexor Midstance, peak plantarflexor Terminal stance, peak plantarflexor Preswing, peak plantarflexor Loading response, mean Midstance, mean Terminal stance, mean Preswing, mean Fig 2. Mean knee motion (degrees) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). *Significantly reduced knee flexion during toe walking compared with heel-toe walking during preswing (Pⴝ.002).

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Toe

Heel-Toe

.15⫾.05 ⫺.10⫾.10

P

⬍.001*

1.32⫾.30 .18⫾.15 ⬍.001* 1.22⫾.32 .74⫾.16 ⬍.001* 1.26⫾.38 1.48⫾0.46 .044 1.18⫾.37 1.44⫾0.42 .016 .93⫾.20 .01⫾.10 ⬍.001* .84⫾.17 .45⫾.16 ⬍.001* .97⫾.26 1.19⫾0.30 .002* .54⫾.17 .73⫾.26 .007

NOTE. Values are mean ⫾ SD. ⫹ values, plantarflexor moments; ⫺ values, dorsiflexor moments. * Statistically significant, P⬍.0027 (.05/18).

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Fig 4. Mean internal knee moments (N䡠m/kg䡠m) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). *During toe walking, the peak internal extensor moment was significantly lower during midstance (Pⴝ.002) compared with heel-toe walking. †During toe walking, the mean flexor moment was significantly lower during terminal stance compared with heel-toe walking (Pⴝ.002).

midstance (.17 vs .50N䡠m/kg䡠m, P⫽.002) compared with heeltoe walking (table 2). At the knee, the apparent difference in mean moments did not reach statistical significance during loading response or midstance. In terminal stance, toe walking registered a significantly lower negative mean moment compared with heel-toe walking (⫺.07 vs ⫺.22N䡠m/kg䡠m, P⫽.002). Power During heel-toe gait, the mean ankle power curve for stance was characterized by a negatively sloping period of absorption from loading response through the beginning of terminal stance, followed by a large positive power generation burst during late terminal stance and preswing. In contrast, during toe walking, the mean ankle power curve during stance was characterized by 4 alternating periods of power absorption and power generation (fig 5).

Table 2: Comparison of Internal Knee Moments (N䡠m/kg䡠m) Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Toe

Heel-Toe

P

Loading response, peak flexor Loading response, peak extensor Midstance, peak extensor Terminal stance, peak extensor Preswing, peak extensor Loading response, mean Midstance, mean Terminal stance, mean Preswing, mean

⫺.30⫾.11 .18⫾.26 .17⫾.14 .05⫾.14 .19⫾.12 ⫺.03⫾.21 .02⫾.13 ⫺.07⫾.18 .12⫾.10

⫺.32⫾.24 .52⫾.18 .50⫾.21 ⫺.05⫾.18 .15⫾.12 .20⫾.17 .21⫾.14 ⫺.22⫾.23 .04⫾.12

.800 .004 .002* .009 .285 .025 .006 .002* .040

NOTE. Values are mean ⫾ SD. ⫹ values, extensor moments; ⫺ values, flexor moments. * Statistically significant, P⬍.0027 (.05/18).

Fig 5. Mean ankle power (W/kg䡠m) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). *Significant differences in peak ankle power absorption and mean ankle power during loading response for toe walking compared with heel-toe walking (P<.001). †Significant differences in peak ankle power generation (Pⴝ.001) and mean ankle power during midstance for toe walking compared with heel-toe walking.

During loading response, toe walking registered a significantly larger peak ankle power absorption burst compared with heel-toe walking (⫺2.50 vs ⫺.26W/kg䡠m, P⬍.001; table 3). Then, during midstance, a significant peak ankle power generation burst was recorded with toe walking, whereas power absorption occurred with heel-toe walking (1.08 vs ⫺.11W/ kg䡠m, P⫽.001). Similar to the pattern of peak powers at the ankle, the mean powers at the ankle showed a pattern of significant differences. Mean ankle power profiles during loading response showed significantly greater power absorption during toe walking compared with heel-toe walking (⫺1.18 vs ⫺.07W/kg䡠m, P⬍.001). Throughout midstance, significantly greater power generation

Table 3: Comparison of Ankle Power (W/kg䡠m) Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Toe

Loading response, minimum ⫺2.50⫾.73 Midstance, maximum 1.08⫾.71 Terminal stance, minimum ⫺.66⫾.44 Preswing, maximum 2.52⫾1.27 Loading response, mean ⫺1.18⫾.60 Midstance, mean .53⫾.43 Terminal stance, mean ⫺.11⫾.37 Preswing, mean 1.24⫾.59

Heel-Toe

P

⫺.26⫾.13 ⫺.11⫾.09 ⫺.69⫾.45 3.29⫾1.70 ⫺.07⫾.06 ⫺.26⫾.11 ⫺.18⫾.28 1.75⫾1.08

⬍.001* .001* .874 .045 ⬍.001* ⬍.001* .618 .059

NOTE. Values are mean ⫾ SD. ⫹ values, power generation; ⫺ values, power absorption. * Statistically significant, P⬍.0032 (.05/16).

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Fig 6. Mean knee power (W/kg䡠m) recorded throughout the gait cycle for toe walking versus heel-toe walking (nⴝ10). *Significant differences in peak knee power absorption during loading response for toe walking compared with heel-toe walking (P<.001).

occurred during toe walking compared with heel-toe walking (.53 vs ⫺.26W/kg䡠m, P⬍.001). At the knee, both modes of walking began with a period of power generation (fig 6). However, during the remainder of the loading response, toe walking was characterized by a decline in peak power generation, whereas heel-toe walking showed a burst of power absorption (⫺.11 vs ⫺.59W/kg䡠m, P⬍.001; table 4). This pattern resulted in a significant difference in mean power during loading response between the 2 modes of walking, with toe walking reflecting a net requirement for power generation and heel-toe walking reflecting a net requirement for power absorption (.28 vs ⫺.04W/kg䡠m, P⫽.005). Throughout the remainder of stance, both modes of walking showed similar power patterns, with peaks in power generation occurring in midstance and late terminal stance and a peak in power absorption occurring in preswing (see fig 6, table 4). Electromyography The timing of muscle activity did not differ significantly between the 2 modes of walking, except for the onset of soleus and medial gastrocnemius activity and the cessation of anterior tibialis activity (fig 7). During toe walking, subjects’ electromyographic profiles (fig 7) showed that (1) the soleus electromyographic activity began much earlier (ie, in the preceding midswing phase; 82% gait cycle), whereas with the heel-toe gait the onset of soleus activity was just after heel strike (1.5% gait cycle, P⫽.001); (2) the medial gastrocnemius began much earlier (ie, in the previous initial swing phase; 71% gait cycle) compared with heel-toe gait (loading response, 7% gait cycle, P⬍.001); and (3) the anterior tibialis electromyographic activity ceased much earlier (ie, in the preceding terminal swing; 88% gait cycle) compared with heel-toe gait (loading response, 10% gait cycle; P⬍.001). Arch Phys Med Rehabil Vol 84, January 2003

In addition to the temporal variations in electromyographic activity between the 2 modes of walking, differences in the relative intensity of muscle activity were recorded between toe walking and heel-toe walking. Toe walking led to diminished electromyographic activity in the anterior tibialis and significantly greater electromyographic activity in the extensor muscles of the ankle compared with that registered during heel-toe walking (table 5). During loading response, the mean EMG recorded from the anterior tibialis with toe walking (1.8% MMT) was only 12% of that recorded with heel-toe walking (14.8% MMT). Also, the duration of anterior tibialis activity was decreased during toe walking (39% gait cycle) when compared with heel-toe walking (50% gait cycle). Both the soleus and gastrocnemius consistently displayed higher levels of mean electromyographic activity throughout stance during toe walking than occurred with heel-toe walking. These differences were greatest in the loading response, at which time the soleus intensity was 4-fold higher with toe walking (88.3% vs 22.1% MMT). The gastrocnemius difference was even further magnified (78.3% vs 2.9% MMT). The greater intensity of soleus and gastrocnemius muscle activity persisted through midstance and terminal stance. During terminal stance, toe-walking soleus activity was increased by 75% (105.8% vs 60.3% MMT) compared with heel-toe walking, whereas gastrocnemius activity was increased by 83% (71.3% vs 38.9% MMT). At the knee, the mean electromyographic activity of the vastus intermedius during limb loading did not differ significantly between the 2 modes of walking (table 6). During toe walking, the apparent increase in vastus intermedius activity in both midstance (18.4% vs 3.5% MMT) and terminal stance (13.0% vs 2.4% MMT) did not reach statistical significance. Additionally, the onset and cessation of vastus intermedius electromyographic activity did not differ significantly between the 2 modes of walking (fig 7). DISCUSSION Toe walking is an obligated gait for persons with calf muscle spasticity or primitive control that prevents heel contact with the ground. On the basis of experience and gait studies of patients impaired by CP or stroke-induced hemiplegia, most clinicians have concluded that restoration of a heel-toe gait improves the patient’s function. A recent study,13 which focused solely on the mechanical moment generated during toe walking, identified that the equinus foot posture reduced the peak plantarflexor and knee extensor moments. This was interpreted as the equinus foot providing a “compensatory ad-

Table 4: Comparison of Knee Power (W/kg䡠m) Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Toe

Heel-Toe

P

Loading response, minimum Midstance, maximum Terminal stance, maximum Preswing, minimum Loading response, mean Midstance, mean Terminal stance, mean Preswing, mean

⫺.11⫾.17 .22⫾.22 .16⫾.22 ⫺.62⫾.38 .28⫾.09 .03⫾.12 .00⫾.04 ⫺.35⫾.27

⫺.59⫾.27 .39⫾.25 .30⫾.31 ⫺.56⫾.38 ⫺.04⫾.18 .15⫾.12 .02⫾.08 ⫺.19⫾.33

⬍.001* .090 .026 .604 .005 .053 .394 .191

NOTE. Values are mean ⫾ SD. ⫹ values, power generation; ⫺ values, power absorption. * Statistically significant, P⬍.0032 (.05/16).

MUSCULAR DEMANDS OF TOE WALKING, Perry

13

Fig 7. Mean rectified and integrated electromyographic profiles (expressed as percentage of MMT) for toe walking versus heel-toe walking (nⴝ10). *During toe walking, the onset of soleus electromyographic activity was significantly earlier compared with heel-toe walking (Pⴝ.001). †During toe walking, the onset of medial gastrocnemius activity was significantly earlier compared with heel-toe walking (P<.001). ‡During toe walking, the cessation of anterior tibialis activity was significantly earlier compared with heel-toe walking (P<.001). 储During toe walking, mean soleus electromyographic activity was significantly greater during loading response (Pⴝ.001) compared with heel-toe walking. During toe walking, mean medial gastrocnemius activity was significantly greater during loading response (P<.001) and terminal stance (P<.001) compared with heel-toe walking.

vantage,” which reduced the demand for muscle strength. The clinical interpretation would be to preserve the equinus posture. The findings from our duplication of the equinus moment study with the addition of simultaneous dynamic electromyographic activity contradict the assumption that a reduced plantarflexor moment during toe walking would be associated with decreased plantarflexor muscle activity.13 Muscle demand was not reduced by the lesser moments of an equinus gait. On the contrary, muscle intensity was increased. During heel-toe gait, the peak plantarflexion torque occurred in terminal stance (1.48N䡠m/kg䡠m). This was accompanied by moderately intense plantarflexor muscle activity (soleus⫽60.3% MMT; gastrocnemius⫽38.9% MMT). Toe walking reduced the plantarflexion mo-

ment by 15% (1.26N䡠m/kg䡠m), but the muscle intensity was nearly doubled (soleus⫽105.8% MMT; gastrocnemius⫽71.3% MMT). A pertinent factor was the difference in ankle position. Heel-toe gait placed the ankle in 12.7° of dorsiflexion, whereas the equinus of toe walking positioned the ankle in 12° of plantarflexion. Nistor et al29 investigated the torque-producing capability of the ankle at angles similar to those used in this study and reported that the maximal isometric torque with the ankle in 15° of plantarflexion was only 62% of that with the ankle in 15° of dorsiflexion. Similarly, Gravel et al30 reported that the maximum isometric plantarflexor force production in 10° of plantarflexion was only 75% of that produced when the ankle was in 10° of dorsiflexion. Arch Phys Med Rehabil Vol 84, January 2003

14

MUSCULAR DEMANDS OF TOE WALKING, Perry

Table 5: Comparison of Anterior Tibialis, Soleus, and Medial Gastrocnemius Mean Electromyographic Activity Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Toe

Heel-Toe

P

Soleus, loading response 88.3⫾39.7 22.1⫾21.8 .001* Soleus, midstance 73.2⫾34.6 36.6⫾12.5 .003 Soleus, terminal stance 105.8⫾47.0 60.3⫾27.7 .006 Soleus, preswing 15.1⫾23.1 5.4⫾6.3 .162 Gastrocnemius, loading response 78.3⫾16.9 2.9⫾3.6 ⬍.001* Gastrocnemius, midstance 57.0⫾16.5 32.2⫾8.1 .005 Gastrocnemius, terminal stance 71.3⫾20.0 38.9⫾18.6 ⬍.001* Gastrocnemius, preswing 1.8⫾3.8 0.3⫾0.7 .285 Anterior tibialis, loading response 1.8⫾3.5 14.8⫾15.8 .017 Anterior tibialis, midstance 1.0⫾2.7 2.8⫾6.1 .455 Anterior tibialis, terminal stance 1.2⫾3.3 0.8⫾1.3 .654 Anterior tibialis, preswing 16.2⫾11.3 9.0⫾4.7 .026 NOTE. Values are mean ⫾ SD. Electromyographic data are expressed as percentage of MMT. * Statistically significant, P⬍.0020 (.05/24).

In a separate study, Herman31 measured both maximum voluntary isometric plantarflexor muscle strength and gastrocsoleus electromyographic activity in a series of ankle positions between 30° of plantarflexion and 15° of dorsiflexion. They showed a linear increase in strength as the ankle moved from plantarflexion to dorsiflexion. The 2 experimental ankle angles (10° plantarflexion, 15° dorsiflexion) that most closely approximated the data in the current equinus gait study (12° plantarflexion, 12.7° dorsiflexion) showed that calf muscle strength in the plantarflexed position was approximately two thirds (71%) of that available with the ankle dorsiflexed. Additionally, to maintain a given magnitude of maximum voluntary isometric contraction, a greater amount of soleus and medial gastrocnemius electromyographic activity was required when the ankle was plantarflexed than when it was dorsiflexed. Because terminal stance is a period of relative isometric muscle activity,12 the Herman31 findings can serve as a basis for understanding the findings of the current equinus study. Despite a lower mean plantarflexor moment during terminal stance toe walking compared with heel-toe walking, the mean electromyographic activity of the gastrocnemius and soleus was higher to provide stability for the plantarflexed ankle. The anatomic basis for this strength difference is explained, primarily, by the length-tension relationship within the sarcomere, the force-generating unit of muscle.16 Gordon et al16 showed that muscle fiber tension was proportional to the number of cross-bridges between the thin (actin) and thick (myosin) filaments. Both shortening and lengthening of the sarcomere beyond the optimum length reduced the available force. Additionally, the contribution of ligaments, tendons, and aponeuroses to the passive internal ankle joint moment was influenced by joint position. Siegler et al17 reported that the passive internal plantarflexor moment increased as the ankle moved from 20° of plantarflexion to 14° of dorsiflexion and calculated that, during the heel-toe–walking terminal stance, passive forces would contribute approximately 6% of the total plantarflexor moment. The finding by Herman31 that maximum plantarflexor strength occurred at 10° of dorsiflexion implies that this position provides the optimum combination of actin-myosin filament cross-bridge formation and passive tension development for the plantarflexors, because the moment arm of the Arch Phys Med Rehabil Vol 84, January 2003

triceps surae is reduced from its peak length by approximately 15% in 10° of ankle dorsiflexion.32,33 A similar relationship between ankle position and plantarflexor muscle strength was identified by mathematical modeling.34 Integration of muscle and tendon geometry and the force-producing qualities of the plantarflexor muscles (fiber length, physiologic cross-section, tendon stress) at selected positions in the range of ankle joint motion showed that maximum isometric muscle torque was produced when the ankle was slightly dorsiflexed.34 This position corresponds to the posture of the ankle during terminal stance (10° dorsiflexion), the gait phase when the internal plantarflexor moment demand reaches its peak.12 These findings suggest that the most probable reason for increased terminal stance electromyographic activity in the presence of decreased internal moment demands during toe walking was the influence of joint position and muscle length on active and passive force production. Shortening of the muscles during toe walking markedly reduced the strength of the ankle plantarflexors and diminished passive contributions from the surrounding anatomic structures. Failure to realize a reduction in terminal stance plantarflexor moment during toe walking comparable to that reported by Kerrigan et al13 merely indicates that our subjects did not walk in as much equinus. Although ankle motion was not reported in the previous study, an extrapolation of this value from their torque data suggests that their subjects were in greater plantarflexion during terminal stance compared with the 13° recorded for our subjects. This difference reflects the choice of test subjects. In the previous study, 9 of the 17 subjects were ballet dancers, trained in “demi-point” walking, and the other 8 subject were reported to have walked in a similar manner.13 Our subjects had no ballet experience, but their moderate equinus (13°) is more comparable to that of spastic patients. In this study, the increased loading response activity of the soleus and gastrocnemius during toe walking compared with heel-toe walking was present, in part, to meet the increased plantarflexor moment demands. Compared with heel-toe walking, the more plantarflexed ankle position inherent in toe walking impeded efficient cross-bridge formation and necessitated greater electromyographic activity for force production. Similarly, during the midstance phase of toe walking, both the mean and peak plantarflexor moments were higher (65% and 87%, respectively) compared with the moments recorded during heel-toe walking. Kinematic data, however, showed that the soleus was undergoing a concentric contraction during toe walking (ie, the ankle plantarflexion angle increased), in contrast to the eccentric contraction occurring during heel-toe walking. The 2-fold increase in soleus activity (73.2% vs 36.6% MMT) was present during the midstance phase of toe walking to meet both the increased plantarflexor moment and to compensate for the reduced electromyographic activity– force efficiency of a concentric versus eccentric contraction.35

Table 6: Comparison of Vastus Intermedius Mean Electromyographic Activity Between Toe Walking and Heel-Toe Walking (nⴝ10) Variable

Vastus Vastus Vastus Vastus

intermedius, intermedius, intermedius, intermedius,

Toe

Heel-Toe

P

loading response 26.9⫾16.0 25.1⫾16.0 .726 midstance 18.4⫾13.1 3.5⫾4.2 .003 terminal stance 13.0⫾11.5 2.4⫾3.7 .008 preswing 6.8⫾13.3 4.4⫾6.6 .546

NOTE. Values are mean ⫾ SD. Electromyographic data are expressed as percentage of MMT.

MUSCULAR DEMANDS OF TOE WALKING, Perry

In addition to the amplitude of muscle activity during toe walking, a second important factor is the duration of intense soleus and gastrocnemius activity. The maximum intensity of both plantarflexor muscles was recorded during loading response (88% and 78% MMT, respectively), and high levels continued through midstance. Hence, the electromyographic activity–time integrals were significantly higher for toe walking. Muscle overuse would lead to early fatigue and, hence, to limited endurance. At the knee, toe walking created a similar biomechanical dichotomy. Torques were lower and power absorption was less, findings that were not reflected in decreased quadriceps (vastus intermedius) electromyographic activity. Initial floor contact by the toe or the heel created the same arc of knee flexion during loading response (toe⫽7°–17.9°, heel-toe⫽3.7°–16.7°), but differences in the alignment of the ground reaction force during toe walking reduced the recorded torque (.18N䡠m/kg䡠m for toe vs .52N䡠m/kg䡠m for heel-toe) and power absorption (⫺.11W/kg䡠m for toe vs ⫺.59W/kg䡠m for heel-toe) compared with heel-toe walking. The similarity of vastus intermedius electromyographic activity (27% and 25% MMT) during the 2 gaits indicated that knee position, rather than the recorded internal torque and power, was the stimulus for muscle intensity. CONCLUSIONS The reduction in internal plantarflexor moments in terminal stance during toe walking was not accompanied by a decrease in plantarflexor electromyographic activity. On the contrary, the reduced moments were accompanied by an increase in both mean and peak electromyographic activity of the soleus and medial gastrocnemius. These findings suggest that clinical decisions concerning the necessity of therapeutic interventions to reduce equinus should consider not only the effect on internal moments, but also the anticipated changes to the muscles’ active and passive forcegenerating capability.

10. 11. 12. 13. 14.

15. 16. 17. 18.

19. 20. 21. 22.

Acknowledgments: We thank Kevin Grant for his valuable contributions to this study during data collection and processing.

23.

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Arch Phys Med Rehabil Vol 84, January 2003

Suppliers a. B&L Engineering, 3002 Dow Ave, Ste 416, Tustin, CA 92780. b. Biosentry Telemetry Inc, 207-20G Earl St, Torrance, CA 90503. c. Digital Equipment Corp, 1 Kendall Sq, Cambridge, MA 02139. d. Vicon Motion Systems, 14 Minns Business Pk, West Way, Oxford OX2 0JB, UK. e. Kistler Instrument Corp, 75 John Glenn Dr, Amherst, NY 142282171. f. Adtech Inc, 3465 Waialae Ave, Ste 200, Honolulu, HI 96816. g. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.