Delay in Initiation and Termination of Tibialis Anterior Contraction in Lower-Limb Hemiparesis: Relationship to Lower-Limb Motor Impairment and Mobility

Article Outline

• Abstract
• Methods
  • Participants
  • Electromyographic Measurements
  • Lower-Limb Motor Impairment and Mobility Assessment
  • Analysis
• Results
  • Participant Characteristics
  • Electromyographic Parameters
  • Electromyographic Parameters and Clinical Measures
• Discussion
• Conclusions
• References
• Copyright

Abstract 

Chae J, Quinn A, El-Hayek K, Santing J, Berezovski R, Harley M. Delay in initiation and termination of tibialis anterior contraction in lower-limb hemiparesis: relationship to lower-limb motor impairment and mobility.

Objective

To assess the relationship between delays in initiation and termination of tibialis anterior contraction in the hemiplegic lower limb and clinical measures of lower-limb motor impairment and mobility.

Design

Cross-sectional correlational study.

Setting

Outpatient rehabilitation clinic of an academic medical center.

Participants

Convenience sample of 22 chronic stroke survivors with lower-limb hemiparesis.

Interventions

Not applicable.

Main Outcome Measures

Delays in initiation and termination of tibialis anterior electromyographic activity during isometric contraction, lower-limb Fugl-Meyer Assessment (FMA), and Modified Emory Functional Ambulation Profile (mEFAP).

Results

The affected lower limb exhibited significantly longer delays in initiation and termination of tibialis anterior contraction relative to the unaffected limb. Delay in termination of 3-second tibialis anterior contraction of the affected limb correlated significantly with the FMA and mEFAP. However, delay in initiation of tibialis anterior contraction did not correlate with clinical measures.

Conclusions

Delay in termination of muscle activity in the hemiparetic lower limb may have important clinical implications, but delay in initiation did not correlate with clinical measures. Controlled, interventional trials are needed to demonstrate a cause and effect relationship.

Key Words:  Electromyography , Hemiparesis , Motor skills disorders , Rehabilitation

STROKE IS A LEADING CAUSE of disability among older adults. More than 700,000 strokes occur annually in the United States, with a prevalence of approximately 4 million.¹ Nearly one third of all stroke survivors will have significant residual disability, with older people generally experiencing slower functional recovery.², ³ Hemiparesis may be a consequence of stroke, and significant hemiparesis is often the primary indication for intensive stroke rehabilitation.⁴

To expand treatment strategies, the nature of hemiparesis and its relationship to clinical outcomes must be further elucidated using quantifiable methods. Prior electromyographic studies among stroke survivors demonstrated significant delays in initiation⁵, ⁶, ⁷, ⁸ and termination of muscle contraction,⁵, ⁶, ⁸ gaps in electromyographic interference patterns,⁹ abnormal co-contraction of agonist and antagonist muscles,¹⁰, ¹¹ and abnormal co-activation of synergistic muscles.¹² We recently demonstrated a strong correlation between electromyographic activation patterns and clinical measures of upper-limb motor function.¹³, ¹⁴ However, similar relationships in the lower limb have not been demonstrated.

The purpose of this study was to describe the relationship between delays in initiation and termination of muscle contraction in the lower limb of hemiparetic participants and clinical measures of motor impairment and mobility. Abnormalities that correlate with clinical measures may be targets for interventions. For example, delay in initiation may be addressed with functional electric stimulation.¹⁵ Similarly, delay in termination may be addressed via antispasticity pharmacologic interventions¹⁶ or novel techniques that electrically block unwanted muscle activity.¹⁷ Electromyographic parameters that correlate with clinical measures may also be used as outcome measures to localize the locus of the intervention. Because delays in initiation and termination of muscle contraction are likely centrally mediated, an intervention that improves these measures in parallel with clinical improvements would suggest a central mechanism rather than peripheral.

We tested 3 hypotheses. First, to confirm the findings of prior reports, we tested the hypothesis that a significant difference exists in delays in initiation and termination of muscle contraction between the affected and unaffected lower limbs of stroke survivors. Second, we tested the hypothesis that the degree of delays in initiation and termination of muscle contraction in the affected lower limb correlates significantly with clinical measures of motor impairment and mobility. Finally, we tested the hypothesis that electromyographic activation patterns correlate with a wide range of lower-limb mobility tasks.

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Methods 

Participants 

We recruited a convenience sample of stroke survivors from an outpatient stroke rehabilitation clinic of an academic medical center. Inclusion criteria included first clinical hemorrhagic or nonhemorrhagic stroke, time from stroke onset to study entry of greater than 6 months, age greater than 18 years old, ability to follow 3-stage commands, and medical stability. We made a concerted effort to recruit subjects with a wide range of lower-limb motor impairment from severe to mild based on the Fugl-Meyer Assessment (FMA). Subjects with a history of prior stroke involving the opposite hemisphere, coexisting neurologic condition involving the lower limbs, uncompensated hemineglect, uncompensated homonymous hemianopia, and absent sensation were excluded. Subjects were characterized with respect to age, sex, stroke type (hemorrhagic, nonhemorrhagic), stroke level (cortical, subcortical), and side of hemiparesis. Stroke type and stroke level were determined by interviewing the subject and reviewing the subject’s medical records, radiology reports, and clinical manifestations. The study protocol was approved by the institutional review board.

Electromyographic Measurements 

We measured delays in initiation and termination of tibialis anterior electromyographic activity during isometric contraction. Subjects were seated on an isokinetic dynamometer^a with seat back tilted to 75°, knee flexed to 30°, and ankle plantar-flexed to 30°. The tibialis anterior was selected based on its essential function in dorsiflexing the ankle during the swing phase of gait. We elected not to force the neutral ankle position, in order to minimize baseline electromyographic activity in subjects with hypertonia of the gastrocnemius muscle. Electromyographic activity was recorded via conductive solid-gel electrocardiogram neonatal/pediatric disposable Ag-AgCl transcutaneous recording electrodes^b placed over the motor point of the tibialis anterior. The active electrode was placed over the muscle belly and the reference electrode over the muscle tendon.

We instructed the subjects to dorsiflex the ankle as forcefully and quickly as possible against the confinement of the ankle apparatus in response to an audible beep, and to relax the muscle as quickly as possible as soon as the beep terminated. Subjects were asked to respond to 6 audible beeps consisting of 3 trials of 3-second contractions and 3 trials of 5-second contractions. The trials were presented in a balanced random order to minimize subject anticipation. “Start times” of 0.5, 1.0, and 1.5 seconds prior to each beep were also randomized to minimize anticipation. Both the hemiparetic and uninvolved limbs were tested.

We defined delay in initiation of the electromyographic signal as the time interval between onset of the audible beep and onset of the electromyographic signal.¹⁴ Delay in termination of the electromyographic signal was defined as the time interval between termination of the audible beep and termination of the electromyographic signal.¹⁴ The onset of electromyographic activity was defined visually on the basis of the earliest rise in electromyographic activity beyond the steady state. Each tracing was displayed in random order without reference to subject, start of movement, or side of the body in order to reduce bias. The method correlates very highly with various computer-based onset determination techniques (r=.999, P<.001), but exhibits significantly higher reliability.¹⁸ The same method was used for determining offset. Although comparisons with computer-based determination techniques and relevant psychometrics have not been reported, there is no theoretical basis for doubting the method’s applicability to offset determination.

Data acquisition hardware included amplifiers^c and a data acquisition board (model 6052E)^d interfaced with a Pentium III desktop computer. Data was processed with LabView.^d Amplifier gain was set at 3300 with bandpass filter frequencies set at 10 and 1000Hz. A sampling frequency of 2500Hz was used.

Lower-Limb Motor Impairment and Mobility Assessment 

We administered all lower-limb motor impairment and mobility measures on the same day as the electromyographic assessments. Hemiparetic lower-limb motor impairment was assessed with the FMA.¹⁹ The FMA’s battery of tests measures poststroke impairment including upper- and lower-limb motor impairment, range of motion, pain, reflexes, sensation, and balance. For the purpose of this study, only the lower-limb motor impairment component of the FMA was used. The specific items in the lower-limb motor impairment component were derived from the Brunnstrom stages of poststroke motor recovery,²⁰ although specific stages are not used. The measure takes into account evolving synergy patterns as well as isolated strength, coordination, and hypertonia. Each task is graded on a 3-point ordinal scale (0, cannot perform; 1, perform partially; 2, perform fully) and summed to provide a lower-limb maximum score of 34. The reliability and validity of the FMA have been documented.²¹

We assessed the ability of a hemiparetic lower limb to execute specific mobility tasks using the Modified Emory Functional Ambulation Profile (mEFAP). The mEFAP measures the time to ambulate through 5 common environmental terrains with or without an assistive device or manual assistance. Specific tasks include (1) a 5-m walk on a hard floor; (2) a 5-m walk on a carpeted surface; (3) rising from a chair, a 3-m walk, and return to a seated position (timed up and go); (4) traversing a standardized obstacle course; and (5) ascending and descending 5 stairs. Subjects were tested without their ankle-foot orthoses, but were allowed to use their other assistive devices. Subjects performed the ambulation task under supervision and if necessary with physical assistance. The adjusted scores which take into account assistive devices were used for the study. The reliability and validity of the mEFAP have been demonstrated.²²

Analysis 

We compared the differences in delay of initiation and termination of electromyographic signal between the affected and unaffected lower limbs using the paired t test. To assess the relationship between electromyographic timing parameters and clinical measures, delays in initiation and termination of the affected limb were normalized with respect to the unaffected limb. Specifically, normalized delay in the affected limb was defined as: (delay in the affected limb – delay in the unaffected limb)/delay in the unaffected limb. The relationship between the electromyographic timing parameters and clinical measures was assessed using the Pearson correlation coefficient. A P value of .05 was selected as the level of significance. Impaired cognition, aphasia, and side of hemiparesis may influence the relationship between electromyographic parameters and clinical measures. Therefore, linear regression models were also generated to explore this possibility. The independent and dependent variables for each regression model are shown in table 1. All statistical analyses were performed using SPSS^e for Windows.

Table 1. Independent and Dependent Variables for Linear Regression Analyses

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Results 

Participant Characteristics 

A total of 22 chronic stroke survivors participated in the study. The mean age ± standard deviation (SD) of subjects was 57.7±15.6 years (range, 33.8–87.6y). Sixteen (73%) subjects were men. The mean time from stroke onset to study evaluation was 4.2±2.6 years (range, 0.7–12.4y). Nineteen (86%) subjects had nonhemorrhagic strokes and 3 had hemorrhagic strokes. Among subjects with nonhemorrhagic stroke, 9 (47%) were due to embolism, 5 (26%) were due to lacunar infarcts, 2 (11%) were due to thrombotic infarcts, and 3 (16%) were due to unknown etiology. Eleven (50%) subjects had right hemiparesis. Six (27%) subjects had aphasia, 5 (23%) had cognitive impairments, and 5 (23%) had sensory impairments. None of the subjects had hemineglect. All subjects completed the electromyography and FMA and mEFAP assessments. Only 1 subject required minimal assistance for negotiating the stairs component of the mEFAP. FMA and mEFAP scores are shown in table 2.

Table 2. FMA and mEFAP Scores

Measures	Mean ± SD (s)
FMA total	21.9±5.1
mEFAP
Floor	32.8±34.2
Carpet	31.3±31.7
Timed up and go	75.0±75.6
Obstacle	128.3±144.0
Stairs	29.7±24.0
Total	303.0±307.1

Electromyographic Parameters 

The mean and SD of delays in initiation and termination of electromyographic activity between the affected and unaffected limbs are shown in table 3. Delays in initiation of electromyographic activity were significantly longer for the affected limb compared with the unaffected limb for both 3- and 5-second contraction durations (P<.05). Similarly, delays in termination of electromyographic activity were significantly longer for the affected limb compared with the unaffected limb for both 3- and 5-second contraction durations (P<.05).

Table 3. Delays in Initiation and Termination of Tibialis Anterior Contraction of the Affected and Unaffected Limbs

Delay	Affected	Unaffected	Difference (95% CI)	P
Delay in initiation (ms)
3-s contraction	293±136	240±97	53(7–99)	.027
5-s contraction	307±238	209±60	98(1–194)	.048
Delay in termination (ms)
3-s contraction	1047±629	709±334	337(64–611)	.018
5-s contraction	866±587	545±233	321(67–578)	.016

NOTE. Values are mean ± SD.

Abbreviation: CI, confidence interval.

Electromyographic Parameters and Clinical Measures 

Pearson correlation coefficients relating electromyographic parameters and clinical measures are shown in table 4. There were significant correlations between delay in termination during 3-second contraction and FMA total and mEFAP total. Delay in termination of 3-second contraction correlated significantly with all components of the mEFAP. The carpet component exhibited the highest correlation. This was followed by floor, timed up and go, obstacle course, and then stairs. Scatter diagrams relating delay in termination during 3-second contraction to FMA total and mEFAP total are shown in figure 1. Correlations between delay in termination during 5-second contraction and clinical measures were not significant. Similarly, none of the correlations relating delay in initiation and clinical measures were significant. Linear regression models that account for cognition, aphasia, and side of hemiparesis also showed significant association between delay in termination of 3-second contraction and FMA total (F=4.6, P=.01) and mEFAP total (F=6.9, P=.002). However, none of the other models were significant.

Table 4. Pearson Correlation Coefficients Relating Electromyographic Parameters and Clinical Measures

Clinical Measures	3-Second Contraction		5-Second Contraction
	Initiation	Termination	Initiation	Termination
FMA total	−.24	−.64‡	−.35	−.21
mEFAP
5-m walk: hard floor	.18	.66‡	.25	.24
5-m walk: carpet	.21	.71‡	.26	.34
Timed up and go	.20	.64‡	.25	.27
Obstacle course	.16	.55†	.18	.20
Stairs	.36	.46⁎	.19	.22
Total	.21	.63†	.22	.27

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• Fig 1. 

  Scatter diagram showing relationship between delay in termination of contraction during 3-second tibialis contraction and (A) lower-extremity FMA total score and (B) mEFAP total score. Delay in termination of contraction was defined as (delay in termination of the affected limb – delay in termination of the unaffected limb)/delay in termination of the unaffected limb.

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Discussion 

The principal findings of this study are: (1) there is a significant difference in the delay in initiation and termination of tibialis anterior contraction between the affected and unaffected lower limbs of chronic stroke survivors, (2) delay in termination of tibialis anterior, but not delay in initiation, correlates significantly with lower-limb motor impairment, and mobility, and (3) delay in termination correlates with a wide range of lower-limb mobility tasks.

Consistent with our earlier study in the hemiparetic upper limb¹⁴ and those of others⁵, ⁷, ⁸ we found a significant delay in initiation of tibialis anterior contraction of the hemiparetic lower limb compared with the unaffected limb. The task required of subjects in this study represents a “simple reaction time.” Delay in simple reaction time can be attributed to lesions causing specific impairments in processing and efferent mechanisms. Motor processing is mediated by the posterior parietal cortex and premotor areas, whereas selection of motor strategy and motor execution are mediated by the primary motor and premotor areas.²³ However, the final motor output among stroke survivors can be modulated by changes in descending and propriospinal excitatory and inhibitory inputs into the spinal interneurons and alpha motoneurons²⁴ as well as neuroplastic changes consequent to brain injury.²⁵

We observed a difference of approximately 75ms in the delay in initiation of tibialis anterior contraction between the affected and unaffected limbs. How much of this difference was due to impairment in the motor processing rather than efferent mechanism is difficult to assess. Heald et al²⁶ reported difference in latency of no more than 10ms between paretic and nonparetic upper limbs after activating the motor cortex with transcortical magnetic stimulation and recording thenar muscle responses. Dewald et al⁸ reported that the difference in delay in the reflex response between paretic and nonparetic limbs ranged between 10 and 40ms. This delay, which is attributable to deficits in the efferent mechanism, would account for only a small portion of the delay observed in this study, suggesting motor processing contributes substantially to the delay in initiation of motor activation in hemiparetic muscles.

Consistent with our earlier study in the hemiparetic upper limb¹⁴ and those of others,⁵, ⁶, ¹² we found a significant delay in termination of tibialis anterior contraction of the affected limb relative to the unaffected limb. Possible mechanisms include increased alpha motoneuron excitability,²⁷ loss of supraspinal inhibitory influences on normal interneuronal pool,²⁸ increased and decreased Renshaw’s inhibition,²⁷ reduction in corticospinal input resulting in increased dependence on undamaged vestibulospinal, reticulospinal, and tectospinal pathways,⁸, ¹², ²⁹ and redistribution of cortical pathways to spinal segmental circuits leading to more unfocused descending inputs.¹¹ Whether any or all of these mechanisms are responsible for the prolonged delay in termination of muscle contraction in the paretic limb observed in this study remains to be elucidated.

The second and third objectives of this study were to describe the statistical relationship between fundamental neural deficits manifested by delay in initiation and termination of tibialis anterior contraction and clinical measures of lower-limb motor impairment and mobility. We found significant correlations between delay in termination of tibialis anterior contraction during 3-second contraction and clinical measures. Because specific tasks in the FMA and mEFAP are multiphasic, appropriate termination of muscle activity in between phases is required to successfully complete the tasks. Thus, correlation between delay in termination of tibialis contraction and clinical measures may reflect a mechanistic or cause and effect relationship. If this is the case, interventions that facilitate termination of muscle contraction might lead to improved functional ability. Possible interventions include intrathecal baclofen,¹⁶ oral spasticity medications,³⁰ and high-frequency electric stimulation block.¹⁷

However, correlation indicates only association and it is possible that delays in termination of muscle contraction are simply reflective of the constellation of other “positive signs” that a stroke survivor may already exhibit. It is possible that subjects with more prolonged delays in termination of muscle contraction also have greater degree of abnormal co-contraction of agonist and antagonist muscles, abnormal co-activation of synergistic muscles, and spasticity, all of which may have significant impact on functional activity. While correlational studies may provide insights into mechanisms for functional deficits and potential interventions, cause and effect relationships can only be demonstrated by prospectively introducing specific interventions to address specific motor abnormalities in a controlled manner with assessment of functional outcomes.

Contrary to our earlier work in the upper limb, delays in initiation did not correlate with clinical measures. It is possible that the timing of initiation of tibialis anterior contraction is not critical to the completion of lower-limb tasks. It is also possible that lower-limb tasks require minimal motor processing. If delay in initiation reflects motor processing and lower-limb tasks require minimal motor processing, then one would anticipate a lack of correlation. Finally, it is possible that the lack of correlation is an artifact of methodology. Electromyographic patterns were measured while subjects were seated. Thus, electromyographic activation patterns may not reflect actual delays in initiation and termination of muscle activity during lower-limb tasks.

The observation that there was a significant correlation between clinical measures and delay in termination of tibialis contraction during 3-second contraction trials but not during 5-second contraction trials deserves additional comment. It may be that 3-second contractions are more representative of duration of muscle contractions utilized to complete tasks in the FMA and mEFAP. Clearly, none of the tasks in the clinical measures require 5 seconds of contraction. In fact, delay in termination may have been more pronounced if the durations of contractions were shorter and more representative of contractions utilized in the tasks in the clinical measures.

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Conclusions 

This study demonstrated significant differences in the delay in initiation and termination of tibialis anterior contraction between the affected and unaffected limbs, but only delay in termination correlated with clinical measures. The delay in termination correlated with a wide range of lower-limb functional tasks. The lack of correlation between delay in initiation of tibialis anterior contraction and clinical measures suggests that the former has limited clinical relevance. The clinical relevance of delay in termination of tibialis anterior will need to be confirmed by an interventional clinical trial that reduces the delay in tibialis anterior contraction and assesses clinical outcomes. The measure may also be used as an outcome measure to localize the locus of effect of an intervention to the central nervous system.

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