Altered muscle activation patterns (AMAP): an analytical tool to compare muscle activity patterns of hemiparetic gait with a normative profile

Shraddha Srivastava, Carolynn Patten, Steven A Kautz, Shraddha Srivastava, Carolynn Patten, Steven A Kautz

Abstract

Background: Stroke survivors often have lower extremity sensorimotor impairments, resulting in an inability to sufficiently recruit muscle activity at appropriate times in a gait cycle. Currently there is a lack of a standardized method that allows comparison of muscle activation in hemiparetic gait post-stroke to a normative profile.

Methods: We developed a new tool to quantify altered muscle activation patterns (AMAP). AMAP accounts for spatiotemporal asymmetries in stroke gait by evaluating the deviations of muscle activation specific to each gait sub-phase. It also recognizes the characteristic variability within the healthy population. The inter-individual variability of normal electromyography (EMG) patterns within some sub-phases of the gait cycle is larger compared to others, therefore AMAP penalizes more for deviations in a gait sub-phase with a constant profile (absolute active or inactive) vs variable profile. EMG data were collected during treadmill walking, from eight leg muscles of 34 stroke survivors at self-selected speeds and 20 healthy controls at four different speeds. Stroke survivors' AMAP scores, for timing and amplitude variations, were computed in comparison to healthy controls walking at speeds matched to the stroke survivors' self-selected speeds.

Results: Altered EMG patterns in the stroke population quantified using AMAP agree with the previously reported EMG alterations in stroke gait that were identified using qualitative methods. We defined scores ranging between ±2.57 as "normal". Only 9% of healthy controls were outside "normal" window for timing and amplitude. Percentages of stroke subjects outside the "normal" window for each muscle were, Soleus = 79%; 73%, Medial Gastrocnemius = 62%; 79%, Tibialis Anterior = 62%; 59%, and Gluteus Medius = 48%; 51% for amplitude and timing component respectively, alterations were relatively smaller for the other four muscles. Paretic-propulsion was negatively correlated to AMAP scores for the timing component of Soleus. Stroke survivors' self-selected walking speed was negatively correlated with AMAP scores for amplitude and timing of Soleus but only amplitude of Medial gastrocnemius (p < 0.05).

Conclusions: Our results validate the ability of AMAP to identify alterations in the EMG patterns within the stroke population and its potential to be used to identify the gait phases that may require more attention when developing an optimal gait training paradigm.

Trial registration: ClinicalTrials.gov NCT00712179 , Registered July 3rd 2008.

Keywords: EMG assessment; Electromyography; Locomotion; Muscle activation patterns; Stroke.

Conflict of interest statement

Ethics approval and consent to participate

Written informed consent approved by the institutional review board at the University of Florida was obtained from all the subjects for publication of this study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Representative data from stroke survivors’ muscle activity patterns demonstrating the sensitivity of k-means cluster analysis to identify “on/off” periods. Each row presents EMG signals for a) soleus, b) tibialis anterior, and c) medial gastrocnemius from stroke survivor’ single gait cycle. Left panels present original EMG data and the right panels present the same representative data after it were high pass filtered (20 Hz) with a zero lag fourth-order Butterworth filter, demeaned, rectified, and smoothed with a zero lag fourth-order low-pass (25 Hz) Butterworth filter. The red solid lines represent k-means clusters
Fig. 2
Fig. 2
Left panel demonstrates the stroke survivors’ EMG activity amplitude during self-selected walking; the box plots indicate the range in the data, horizontal black line in center is the median, the upper and lower boundaries of the box indicating the upper and lower quartile respectively, and red markers represent extreme values. Right panel demonstrates AMAP scores of stroke survivors for the amplitude component of each muscle. The shaded gray area is the normal range of scores (±2.57). Each dot within a region of gait cycle represents score of a stroke survivor with solid red dots representing the subjects with scores outside the “normal” window of ±2.57. Positive scores, i.e. solid red dots above the “normal” window, represent EMG activation greater than “normal” and vice versa. For the clarity of data, we have adjusted the Y-axes scales on the right panel between ±5 and ± 11. The EMG data from each muscle were normalized to the averaged peak activation across all the steps taken by the subject
Fig. 3
Fig. 3
Left panel demonstrates the stroke survivors’ EMG activity timing during self-selected walking; the box plots indicate the range in the data, horizontal black line in center is the median, the upper and lower boundaries of the box indicating the upper and lower quartile respectively, and red marker represent extreme values. Right panel demonstrates AMAP scores of stroke survivors for the timing component of each muscle. The shaded gray area is the normal range of scores (±2.57). Each dot within a region of gait cycle represents score of a stroke survivor with solid red dots representing the subjects with scores outside the “normal” window of ±2.57. Positive scores represent duration of EMG activation longer than “normal” and vice versa. For the clarity of data, we have adjusted the Y-axes scales on the right panel between ±5 and ± 11. The EMG data from each muscle were normalized to the averaged peak activation across all the steps taken by the subject
Fig. 4
Fig. 4
Examples of altered EMG patterns in comparison to normal pattern are illustrated for EMG activity at self-selected walking speeds for all muscles. Black solid lines are the mean EMG activity of healthy controls and shaded grey area is the SD. Red solid lines are EMG activity of a representative stroke survivor with Table 3 representing the corresponding AMAP scores for the amplitude and timing components (values highlighted in red in the table represent scores outside the “normal” window of ±2.57). To clearly present the EMG activity, time is presented as percent of gait cycle
Fig. 5
Fig. 5
Correlations between Pp and the total AMAP scores for SO averaged across all regions of the timing component. The total AMAP scores were negatively associated (p < 0.05) with Pp. The red dots represent stroke subjects that had AMAP scores outside of the “normal” window of ±2.57
Fig. 6
Fig. 6
Correlations between self-selected walking speeds and total AMAP scores for the amplitude components (scores averaged across all regions of the amplitude component) of SO (left panel) and MG (right panel). The red dots represent stroke subjects that had AMAP scores outside of the “normal” window of ±2.57. The total AMAP scores of SO and MG for amplitude were negatively associated with the walking ability of stroke survivors (p 

References

    1. Erni T, Colombo G. Locomotor training in paraplegic patients: a new approach to assess changes in leg muscle EMG patterns. Electroencephalogr Clin Neurophysiol. 1998;109(2):135–139. doi: 10.1016/S0924-980X(98)00005-8.
    1. Ricamato AL, Hidler JM. Quantification of the dynamic properties of EMG patterns during gait. J Electromyogr Kinesiol. 2005;15(4):384–392. doi: 10.1016/j.jelekin.2004.10.003.
    1. Den Otter A, et al. Abnormalities in the temporal patterning of lower extremity muscle activity in hemiparetic gait. Gait Posture. 2007;25(3):342–352. doi: 10.1016/j.gaitpost.2006.04.007.
    1. Hof A, et al. Detection of non-standard EMG profiles in walking. Gait Posture. 2005;21(2):171–177. doi: 10.1016/j.gaitpost.2004.01.015.
    1. Fung J, Barbeau H. A dynamic EMG profile index to quantify muscular activation disorder in spastic paretic gait. Electroencephalogr Clin Neurophysiol. 1989;73(3):233–244. doi: 10.1016/0013-4694(89)90124-7.
    1. Shiavi R, Bugle H, Limbird T. Electromyographic gait assessment, part 2: preliminary assessment of hemiparetic synergy patterns. J Rehabil Res Dev. 1987;24(2):24–30.
    1. Burridge J, et al. Indices to describe different muscle activation patterns, identified during treadmill walking, in people with spastic drop-foot. Med Eng Phys. 2001;23(6):427–434. doi: 10.1016/S1350-4533(01)00061-3.
    1. Nadeau S, et al. Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clin Biomech. 1999;14(2):125–135. doi: 10.1016/S0268-0033(98)00062-X.
    1. Knutsson E, Richards C. Different types of disturbed motor control in gait of hemiparetic patients. Brain. 1979;102(2):405–430. doi: 10.1093/brain/102.2.405.
    1. Yelnik A, et al. A clinical guide to assess the role of lower limb extensor overactivity in hemiplegic gait disorders. Stroke. 1999;30(3):580–585. doi: 10.1161/01.STR.30.3.580.
    1. Higginson J, et al. Muscle contributions to support during gait in an individual with post-stroke hemiparesis. J Biomech. 2006;39(10):1769–1777. doi: 10.1016/j.jbiomech.2005.05.032.
    1. Lamontagne A, Richards CL, Malouin F. Coactivation during gait as an adaptive behavior after stroke. J Electromyogr Kinesiol. 2000;10(6):407–415. doi: 10.1016/S1050-6411(00)00028-6.
    1. Bowden MG, et al. Anterior-posterior ground reaction forces as a measure of paretic leg contribution in hemiparetic walking. Stroke. 2006;37(3):872–876. doi: 10.1161/01.STR.0000204063.75779.8d.
    1. Hall AL, et al. Relationships between muscle contributions to walking subtasks and functional walking status in persons with post-stroke hemiparesis. Clin Biomech. 2011;26(5):509–515. doi: 10.1016/j.clinbiomech.2010.12.010.
    1. Clark DJ, et al. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J Neurophysiol. 2010;103(2):844–857. doi: 10.1152/jn.00825.2009.
    1. Allen JL, Kautz SA, Neptune RR. The influence of merged muscle excitation modules on post-stroke hemiparetic walking performance. Clin Biomech. 2013;28(6):697–704. doi: 10.1016/j.clinbiomech.2013.06.003.
    1. Neptune RR, Clark DJ, Kautz SA. Modular control of human walking: a simulation study. J Biomech. 2009;42(9):1282–1287. doi: 10.1016/j.jbiomech.2009.03.009.
    1. McGowan CP, et al. Modular control of human walking: adaptations to altered mechanical demands. J Biomech. 2010;43(3):412–419. doi: 10.1016/j.jbiomech.2009.10.009.
    1. Zajac FE, Neptune RR, Kautz SA. Biomechanics and muscle coordination of human walking: part II: lessons from dynamical simulations and clinical implications. Gait Posture. 2003;17(1):1–17. doi: 10.1016/S0966-6362(02)00069-3.
    1. Di Fabio RP. Reliability of computerized surface electromyography for determining the onset of muscle activity. Phys Ther. 1987;67(1):43–48. doi: 10.1093/ptj/67.1.43.
    1. Hodges PW, Bui BH. A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalogr Clin Neurophysiol. 1996;101(6):511–519.
    1. Mulroy S, et al. Use of cluster analysis for gait pattern classification of patients in the early and late recovery phases following stroke. Gait Posture. 2003;18(1):114–125. doi: 10.1016/S0966-6362(02)00165-0.
    1. Shiavi R, et al. Variability of electromyographic patterns for level-surface walking through a range of self-selected speeds. Bull Prosthet Res. 1980;10:5–14.
    1. Wootten M, Kadaba M, Cochran G. Dynamic electromyography. II. Normal patterns during gait. J Orthop Res. 1990;8(2):259–265. doi: 10.1002/jor.1100080215.
    1. Arsenault A, Winter D, Marteniuk R. Is there a ‘normal’profile of EMG activity in gait? Med Biol Eng Comput. 1986;24(4):337–343. doi: 10.1007/BF02442685.
    1. Sibley KM, et al. Changes in spatiotemporal gait variables over time during a test of functional capacity after stroke. J Neuroeng Rehabil. 2009;6(1):27. doi: 10.1186/1743-0003-6-27.
    1. Den Otter A, et al. Gait recovery is not associated with changes in the temporal patterning of muscle activity during treadmill walking in patients with post-stroke hemiparesis. Clin Neurophysiol. 2006;117(1):4–15. doi: 10.1016/j.clinph.2005.08.014.
    1. Raja B, Neptune RR, Kautz SA. Coordination of the non-paretic leg during hemiparetic gait: expected and novel compensatory patterns. Clin Biomech. 2012;27(10):1023–1030. doi: 10.1016/j.clinbiomech.2012.08.005.
    1. Perry J, et al. Classification of walking handicap in the stroke population. Stroke. 1995;26(6):982–989. doi: 10.1161/01.STR.26.6.982.
    1. Kitatani R, et al. Ankle muscle coactivation during gait is decreased immediately after anterior weight shift practice in adults after stroke. Gait Posture. 2016;45:35–40. doi: 10.1016/j.gaitpost.2016.01.006.
    1. Dean JC, Kautz SA. Foot placement control and gait instability among people with stroke. J Rehabil Res Dev. 2015;52(5):577–590. doi: 10.1682/JRRD.2014.09.0207.
    1. Kirtley C, Whittle MW, Jefferson R. Influence of walking speed on gait parameters. J Biomed Eng. 1985;7(4):282–288. doi: 10.1016/0141-5425(85)90055-X.

Source: PubMed

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