Are biomechanical strategies to perform functional activities different between individuals with subacute and chronic stroke?

Abstract

OBJECTIVE:

To evaluate if the capacity to perform functional mobility activities change within the first year post-stroke using the Timed “Up and Go” Assessment of Biomechanical Strategies (TUG-ABS).

METHODS:

A cross-sectional study was conducted with thirty-eight stroke individuals. A motion analysis system was used during the Timed “Up and Go” (TUG) test to evaluate the following activities: sit-to-stand, gait, turn, and stand-to-sit. Kinematic variables related to each activity were obtained in addition to TUG-ABS scores. The ability to perform the activities was compared between subacute (up to 3 months post-stroke, n = 21) and chronic participants (4 to 12 months post-stroke, n = 17) using Mann-Whitney U tests (α= 5%).

RESULTS:

Results were expressed as median difference (MD) and 95% confidence intervals (95% CI). TUG-ABS scores: Sit-to-stand (MD = 0, 95% CI = 0.0 to 1), gait (MD = 0, 95% CI = 0.0 to 1), stand-to-sit (MD = 0, 95% CI = 0.0 to 1), and total score (MD = 2.0, 95% CI = 0.0 to 6) were not different between groups. Subacute participants presented significant better scores during turn activity (MD = 2.0, 95% CI 0.0 to 2.0). All kinematic variables were not different between participants.

CONCLUSIONS:

Capacity to perform functional activities was not different within the first year post-stroke, suggesting that biomechanical strategies are developed within the first three months following stroke.

Keywords

Walking disability evaluation neurological rehabilitation

1 Introduction

Stroke is the leading cause of disability worldwide (Johnson et al., 2019). Stroke survivors often experience motor deficits (i.e., loss of strength and coordination) and mobility limitations, which leading to functional dependence, falls, and poor perceived quality of life (Langhorne, Bernhardt &, Kwakkel, 2011; Faria et al., 2015).

Despite common motor deficits, recovery seems to initiate early after stroke. Motor recovery is more intense within the first three months (Langhorne, Bernhardt &, Kwakkel, 2011). The current understanding regarding brain repair suggests that acute (1–7 days post-stroke) and early subacute (7 days-3 months) periods are critical for neural plasticity post-stroke. In the late subacute (3–6 months) and chronic (>6 months) stages, recovery decreases progressively. Although behavioral changes are possible years post-stroke, most recoveries may occur within the first year (weeks-to-months) after the event (Bernhardt et al., 2017).

Motor recovery is mainly affected by lower limb weakness, which leading to biomechanical changes during functional activities. Such changes are evidenced during locomotion and may generate high energy demand and significant dynamic instability, resulting in impaired gait and functional mobility (Chen et al., 2003).

Gait after stroke is characterized by short steps, especially the paretic lower limb, to reduce single support time. Increased swing time is also observed due to inadequate propulsion of paretic hip and ankle flexors (Chen, Patten, Kothari, & Zajac, 2005). This asymmetric behavior between limbs promotes greater lateral displacement of the center of mass, increasing postural instability during walking (Clark, Williams, Fini, Moore, & Bryant, 2012).

The ability to turn and change direction is also affected after a stroke episode (Faria, Reis, Teixeira-Salmela, & Nadeau, 2009). Turning during walking requires complex gait pattern changes, such as programmed asymmetry between limbs for width and length steps (Sendgman, Goldie, & Lansek, 1994; Patla, Prentice, Robinson, & Neufeld, 1991). Such adaptations are not adequately performed after a stroke, leading to increased incidence of falls, particularly when turning is performed to the paretic side (Manaf, Justine, Omar, Isa, & Salleh, 2012).

Similarly, the ability to perform body transfer is impaired. To perform transfers from standing to sitting (stand-to-sit) and sitting to standing (sit-to-stand), lower limb strength must be synchronized and center of mass maintained within the base of support (Na, Hwang, & Woo, 2016). Although these activities require complex movements and knee and ankle joint stability, they are repeated four times per hour, on average. Hemiparetic individuals practice these activities at a lower frequency and with limited stability (Yang, 2016).

Given the deficits mentioned above, functional ability must be adequately assessed. The “Timed Up and Go” (TUG) test is commonly used because it represents functional mobility activities (Hafsteindóttir, Rensink, & Schuurmans, 2014). Although stroke individuals exhibit changes in biomechanical strategies during the TUG test, it analyzes only the time spent to complete the test, emphasizing the need for detailed analysis of other test components. For this, the “Timed Up and Go” Assessment of Biomechanical Strategies (TUG-ABS) tool was developed and demonstrated validity and reliability in individuals with hemiparesis after stroke (Faria, Teixeira-Salmela, & Nadeau, 2013a). This test evaluates movement strategies to perform activities (biomechanical strategies), which are important to guide clinical decision-making (Faria, Teixeira-Salmela, & Nadeau, 2013a). By applying the TUG-ABS, one can qualitatively and quantitatively analyze each TUG activity (i.e., sit-to-stand, gait, 180° turn, and stand-to-sit) (Faria et al., 2015).

Therefore, we aimed to investigate if the capacity to perform functional mobility activities differs within the first year post-stroke.

2 Method

2.1 Design

A cross-sectional study was conducted following the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement (von Elm et al., 2007).

2.2 Participants, therapists, and centers

Adult individuals with subacute and chronic stroke were recruited from neurological rehabilitation centers or after hospital discharge from reference hospitals in Natal/RN (Brazil). Data collection was performed in an outpatient rehabilitation setting (university research laboratory) by physiotherapy researchers. The study was conducted within the confines of the Declaration of Helsinki and approved by the research ethics committee of Federal University of Rio Grande do Norte (under protocol number 488.293/13).

The following inclusion criteria was established to ensure sample homogeneity regarding potential predictors of recovery: clinical diagnosis of first stroke episode resulting in gait deficits (i.e., gait speed < 0.9 m/s) (Fulk, He, Boyne, & Dunning, 2017) in a period up to one year, age 21 to 70 years, able to walk 10 m independently, able to stand up from a chair without arms or backrest, and capable of understanding simple motor commands. Those with adverse clinical conditions affecting gait or balance or both and pain or discomfort impeding the completion of the requested activities were excluded.

2.3 Outcome measures

Demographic data (age and gender) and type of stroke (ischemic or hemorrhagic) were collected. Neurological status, cognition, and gait ability were also obtained as sample characterization measures using the National Institute of Health Stroke Scale (NIHSS) (Cincura et al., 2009), Mini-Mental State Examination (MMSE) (Brucki, Nitrini, Caramelli, Bertolucci, & Okamoto, 2003), and Functional Ambulation Category (FAC) (Mehrholz, Wagner, Rutte, Meißner, & Pohl, 2007), respectively.

TUG-ABS test was the primary outcome measure (Faria et al., 2013a). This tool identifies biomechanical strategies analyzing movement parameters and strategies during functional activities. TUG-ABS test also presents suitable psychometric properties and good clinical value in post-stroke hemiparetic individuals (Faria, Teixeira-Salmela, & Nadeau, 2013a; Faria, Teixeira-Salmela, & Nadeau, 2013b). The final version of the TUG-ABS test comprises four items (activities) and 15 sub-items, with a total score of 45 points. TUG-ABS items consist of sit-to-stand (three sub-items), gait (five sub-items), turn (four sub-items), and stand-to-sit (three sub-items). Each sub-item can be scored from 1 (worst performance) to 3 (best performance) (Faria et al., 2015).

To reinforce biomechanical analysis, kinematic variables were obtained as secondary outcomes using a motion analysis system composed of eight cameras (Qualisys Motion Capture System, Qualisys Medical AB, Gothenburg, Sweden). This system is based on a three-dimensional reconstruction of passive reflective markers, which were positioned on 38 predefined bone prominences (Brasileiro et al., 2015).

After obtaining sample characteristics and positioning reflective markers, participants were asked to perform a modified TUG test. In the original TUG test, individuals should leave the sitting position with their backs on the chair, get up and walk three meters (as fast as possible), turn around, return towards the same chair, sit, and support their back on the chair (Podsiadlo & Richardson, 1991). In our study, participants were evaluated using a chair without arm support and backrest. Each participant was instructed to get up, walk 2 meters, turn around a cone (180° turn), walk back, and sit on the chair using the own comfortable and usual pace (Faria, Teixeira-Salmela, & Nadeau, 2013b). Participants were also informed that “turn around the cone” could be performed in any direction. Each individual performed three consecutive tasks with a 3-minute rest between trials.

Kinematic data were acquired at a frequency of 120 Hz using the Qualisys Track Manager 2.6 software (Qualisys Medical AB, Gothenburg, Sweden). Recordings were filtered using a low-pass Butterworth filter and cut-off frequency of 6 Hz. The second trial of all participants was retrieved for data analysis, exported to the Visual 3D processing software (Visual 3D Standard, C-Motion, Rockville, MD), and analyzed by an independent examiner. This trained examiner filled out the TUG-ABS test for each participant, considering up to three views for each trial. Although TUG-ABS test is applied using real-time observations, the motion system records allowed a detailed analysis of TUG test execution. We also highlight that kinematic analysis is not part of the standard TUG-ABS protocol (Faria, Teixeira-Salmela, & Nadeau, 2013a).

Events were defined in the Visual 3D software to identify the beginning and end of each activity (i.e., sit-to-stand, gait, turn, and stand-to-sit). The following kinematic variables were related to items/activities of the TUG-ABS test:

Hip range of motion (ROM) (°) and time (s) spent during transfer from sitting to standing;

Maximum hip extension (°), step length symmetry ratio (paretic step length/non-paretic step length), and double support time (s) during gait;

Stride length (m) and number of steps while turning;

Maximum knee flexion (°) and time (s) to perform stand-to-sit transfer.

2.3.1 Sample size

Sample size was determined based on a previous study (Almeida et al., 2017), which evaluated individuals with hemiparesis due to stroke and different functional mobility levels using TUG-ABS test. In this study, significant differences were observed according to mobility level in 26 participants. Therefore, a sample of 26 participants was established as the minimal sample size required, but it would be increased to ensure reliable results.

2.3.2 Data analysis

Data analysis was conducted using the SPSS software (SPSS, IBM®, USA, version 20.0). Two groups were stratified according to injury time: subacute (1 to 3 months post-stroke) and chronic (4 to 12 months post-stroke). Data normality was analyzed using the Shapiro-Wilk test and sample characteristics were expressed as frequencies (%) or percentiles. The Mann-Whitney U test was used to compare the following outcomes between groups: i) score of each TUG-ABS item, ii) TUG-ABS total score, and iii) all kinematic variables. Data from groups were expressed as median and 25^th–75^th percentiles. Median difference between groups and confidence intervals (95% CI) were calculated using Minitab® software, version 19.0. All inferential analyses considered α= 5% (two-tailed).

3 Results

3.1 Flow of participants and therapists

No concerns or withdraws were observed after inclusion criteria. Of the included participants, 20 individuals (15 from subacute and 5 from chronic group) reported no engagements in any regular physical activity or physical therapy. Demographic and clinical data are shown in Table 1. Three physical therapists previously trained for the study procedures (2 for data collection and 1 for TUG-ABS data analysis) were involved.

Table 1
Demographic and clinical data of participants in the subacute (n = 21) and chronic (n = 17) groups

Variable Subacute group Chronic group

Gender [male/female] 13 / 8 10 / 7

Stroke type [I / H] 17 / 4 15 / 2

Age [years] 58.0 (46.0–65.0) 58.0 (55.0–64.0)

FAC [score] 3.0 (3.0–4.0) 3.0 (3.0–4.0)

NIHSS [score] 2.0 (1.0–4.0) 3.0 (1.0–4.0)

MMSE [score] 24.0 (21.0–25.0) 24.0 (19.0–24.0)

Variable	Subacute group	Chronic group
Gender [male/female]	13 / 8	10 / 7
Stroke type [I / H]	17 / 4	15 / 2
Age [years]	58.0 (46.0–65.0)	58.0 (55.0–64.0)
FAC [score]	3.0 (3.0–4.0)	3.0 (3.0–4.0)
NIHSS [score]	2.0 (1.0–4.0)	3.0 (1.0–4.0)
MMSE [score]	24.0 (21.0–25.0)	24.0 (19.0–24.0)

Data of Gender and Stroke type are expressed as frequency of cases. Data of Age, FAC, NIHSS and MMSE are expressed as median (25th percentile –75th percentile). Abbreviations: I, Ischaemic; H, Haemorragic; FAC, Functional Ambulatory Category; NIHSS, National Institute of Health Stroke Scale; MMSE, Mini Mental State Examination.

3.2 Are biomechanical strategies used in functional mobility activities different between stroke individuals according to injury time?

Except for the “Turn” item, scores of TUG-ABS activities (items) were not significantly different between groups. TUG-ABS total score was also not different between groups (Table 2).

Table 2
Scores of the items of the “Timed Up and Go” Assessment of Biomechanical Strategies (TUG-ABS) test in the subacute (n = 21) and chronic (n = 17) groups

TUG -ABS items Subacute group median Chronic group median Difference between groups median P U Z

(25th–75th) (25th–75th) (95% CI)

Sit-to-stand [score] 9.0 (9.0–9.0) 9.0 (8.0–9.0) –0.0 (0.0 to 1) 0.098 130.5 1.717

Gait [score] 14.0 (13.0–15.0) 14.0 (12.5–15.0) 0.0 (0.0 to 1) 0.359 148.0 0.939

Turn [score] 10.0 (9.0–11.0) 8.0 (6.5–10.0) 2.0 (–0.0 to 2.0) 0.038 112.5 2.060

Stand-to-sit [score] 9.0 (7.5–9.0) 8.0 (7.0–9.0) –0.0 (0.0 to 1.0) 0.502 157.0 0.687

Total [score] 42.0 (37.5–44.0) 38.0 (35.0–42.5) 2.0 (–0.0 to 6.0) 0.142 128.5 1.483

TUG -ABS items	Subacute group median	Chronic group median	Difference between groups median	P	U	Z
Sit-to-stand [score]	9.0 (9.0–9.0)	9.0 (8.0–9.0)	–0.0 (0.0 to 1)	0.098	130.5	1.717
Gait [score]	14.0 (13.0–15.0)	14.0 (12.5–15.0)	0.0 (0.0 to 1)	0.359	148.0	0.939
Turn [score]	10.0 (9.0–11.0)	8.0 (6.5–10.0)	2.0 (–0.0 to 2.0)	0.038	112.5	2.060
Stand-to-sit [score]	9.0 (7.5–9.0)	8.0 (7.0–9.0)	–0.0 (0.0 to 1.0)	0.502	157.0	0.687
Total [score]	42.0 (37.5–44.0)	38.0 (35.0–42.5)	2.0 (–0.0 to 6.0)	0.142	128.5	1.483

Data of Groups are expressed as median (25th percentile –75th percentile). Data of Difference between groups are expressed as median (95% confidence interval). Values of P, U and z: Mann-Whitney U test. Abbreviations: TUG-ABS, “Timed Up and Go” Assessment of Biomechanical Strategies; CI, Confidence Interval.

No significant differences were observed between groups regarding kinematic variables (hip ROM, maximum hip extension, step length symmetry ratio, double support time, stride length, number of steps while turning, maximum knee flexion, and time to perform sit-to-stand and stand-to-sit transfers) (Table 3).

Table 3

Kinematic variables related to the activities of the “Timed Up and Go” Assessment of Biomechanical Strategies (TUG-ABS) test in the subacute (n = 21) and chronic (n = 17) groups

Kinematic variables	Subacute group median	Chronic group median	Difference between groups median	P	U	z
	(25th–75th)	(25th–75th)	(95% CI)
Sit-to Stand
Hip ROM (°)	48.2 (43.7–55.4)	50.1 (39.9–62.0)	–1.83 (–10.88 to 6.81)	0.780	169.0	0.279
Time spent (s)	1.55 (1.05–2.74)	1.35 (1.07–2.01)	0.02 (–0.36 to 0.64)	0.872	173.0	0.162
Gait
Maximum hip extension (°)	8.0 (0.4–14.6)	11.4 (3.8–16.5)	–3.11 (–9.80 to 4.67)	0.355	147.0	0.925
Step length symmetry	0.95 (0.84–1.22)	1.04 (0.87–1.43)	–0.08 (–0.27 to 0.16)	0.537	157.5	0.617
Double support time (s)	0.53 (0.44–0.86)	0.55 (0.44–0.75)	0.02 (–0.13 to 0.18)	0.769	168.5	0.294
Turn
Number of steps	5.0 (4.0–8.0)	5.0 (4.5–9.5)	–1.0 (–2.0 to 1.0)	0.362	148.0	0.911
Stride length (m)	0.69 (0.50–0.77)	0.58 (0.35–0.71)	0.09 (–0.05 to 0.23)	0.191	134.0	1.306
Stand-to-sit
Maximum knee flexion (°)	94.5 (89.6–103.0)	96.9 (85.6–109.2)	–2.18 (–12.11 to 7.68)	0.714	166.0	0.367
Time spent (s)	2.80 (2.05–4.60)	3.00 (1.90–4.05)	0.1 (–0.70 to 1.02)	0.769	168.5	0.294

4 Discussion

Functional mobility analysis of TUG-ABS test allowed identifying biomechanical strategies used and whether they would vary according to post-stroke time. Both groups were similar in terms of demographic (age and gender) and clinical characteristics (i.e., stroke type and severity, gait deficit, and cognition) at study entry. Also, strategies were similar between groups within the first year after stroke.

Both groups exhibited satisfactory performance during sit-to-stand activity. Most individuals stood up without supporting upper limbs and with little or no lateral trunk movement. Hip ROM during sitting-to-standing was suitable and the time spent to perform it was good enough for both groups. Acute stroke survivors may present an altered performance during stand-up and sit-down activities since individuals are still adapting to new locomotor strategies to compensate weight-bearing asymmetries and muscle weakness (Cheng et al., 1998). In our study, individuals with up to 3 months of injury seemed adapted to this activity, suggesting that adaptation to this movement may occur within the first months post-stroke.

Acceptable performance during sit-to-stand activity does not mean adequate body symmetry. Rocha et al. (2010) observed an altered symmetry in chronic stroke individuals during sit-to-stand and stand-to-sit activities and proposed non-paretic lower limb constraint during sit-to-stand. This constraint improved performance and lower limb symmetry, suggesting that adequate stimuli can improve performance and biomechanical efficiency even in the chronic phase.

Participants of both groups also performed a proper gait. Most individuals exhibited symmetric step length and adequate double support time. Participants initiated foot contact using the heel and presented adequate hip extension at the end of the stance phase. Most participants took their foot off the floor during the swing phase. In general, participants maintained a stable walking without atypical trunk movements; however, gait was not assessed at longer walking distances in the present study.

Even with upper limb paresis or paralysis, individuals may spontaneously recover trunk and lower limb strength in the first months after stroke, (Mercer, Freburger, Yin, & Preisser, 2014), which may explain gait performance of the participants. Gait strategies may also be developed in the first three months and maintained in the later stages after injury, given similar performance between groups. In this sense, early training should be emphasized to adapt to functional biomechanical strategies. Laufer et al. (2001) observed functional mobility improvements after treadmill training compared with over-ground ambulation in individuals with up to three months post-stroke. Although one can argue that motor recovery occurs more intensively in the acute phase (Mercer, Freburger, Yin, & Preisser, 2014), our results reinforce that additional gains can be acquired by applying the appropriate stimulus.

According to TUG-ABS results, turning performance was different between groups. During this activity, most individuals performed more than five steps to change direction completely, particularly those with 4 to 12 months post-stroke. However, similar number of steps and stride length were observed between groups.

Turning is a challenging task after stroke due to inter-limb asymmetry and difficulties in maintaining balance; thus, requiring strength and postural stability (Chen, Yang, Cheng, Chan, & Wang, 2014). Total turn time is also essential to promote functional and independent direction change (Na, Kim, & Lee, 2015). In the present study, both groups replaced the “spin strategy” (rotation around the own axis) by the “step strategy” (increased number of steps) during the task, increasing turning time. Furthermore, body rotation was inadequate in both groups (mainly in chronic participants), indicating that turning strategies are developed in the early phase and may worsen in the subsequent months after stroke.

Compensatory and mal-adaptive strategies can be developed while attempting to promote functional movements; thus, early rehabilitation must be encouraged to restore these movements. If rehabilitation onset is delayed, turn training may last longer until postural imbalance, asymmetries, and compensatory alterations are reduced (Podsiadlo & Richardson, 1991). Task-specific training should also be considered. Chen et al. (2014) trained chronic stroke individuals on a circular treadmill and observed improvements in turning speed, step length, and cadence, indicating that adequate stimulus promotes gains in the chronic phase.

Both groups showed “better performance” in the sit-to-stand activity and presented continuous movements and adequate balance during transfer. When sitting, participants maintained lower limbs aligned and parallel, demonstrating adequate muscle control. The time spent during this activity was also appropriate in both groups.

Mercer et al. (2014) observed that individuals with better paretic lower limb motor function during the first weeks after a stroke had faster walking speeds and better ability to load the limb during functional activities. Moreover, these advantages were still present six months post-stroke. Therefore, lower limb motor function recovery in the first months post-stroke may influence sit-to-stand, gait, and stand-to-sit performance. Once individuals perform these activities, practice helps maintaining biomechanical strategies in the subsequent months. Accordingly, if adequate rehabilitation is provided at an early stage, appropriate movement strategies can be developed and further strengthened, contributing to a better functional prognosis for these individuals.

Although the present study contributed to increasing the body of evidence regarding TUG-ABS test after stroke, external validity was probably a limitation due to sample. Further studies with greater sample size and other populations are suggested.

5 Conclusion

In conclusion, strategies used for functional mobility activities are similar within the first year after stroke, suggesting that biomechanical strategies are developed within the first three months after stroke (early subacute phase). Therefore, early rehabilitation must be emphasized to adequately restore abilities as sit-to-stand, gait, stand-to-sit and especially, turning.

Footnotes

Acknowledgments

The authors thank Probatus Academic Services for providing scientific language translation and editing.

Conflict of interest

This work was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) [Financial code 001]. The authors declare no competing financial interests or personal relationships influencing this paper.

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